sign in sign up
<<
Home , Acidimicrobium, Actinomycetales, Alkaliphile, Brevibacterium, Deinococcus murrayi, Hydrogenobacter

FEMS Reviews 25 (2001) 175^243 www.fems-microbiology.org

Energetics of overall metabolic reactions of thermophilic and hyperthermophilic and

Jan P. Amend *, Everett L. Shock

Department of and Planetary Sciences, Washington University, CB 1169 St. Louis, MO 63130, USA

Received 1 February 2000; received in revised form 1 June 2000; accepted 1 November 2000

Abstract

Thermophilic and hyperthermophilic Archaea and Bacteria have been isolated from marine hydrothermal systems, heated sediments, continental solfataras, hot springs, water heaters, and industrial waste. They catalyze a tremendous array of widely varying metabolic processes. As determined in the laboratory, electron donors in thermophilic and hyperthermophilic microbial reactions include H2, 2‡ 23 23 Fe ,H2S, S, S2O3 ,S4O6 , sulfide minerals, CH4, various mono-, di-, and hydroxy-carboxylic acids, , amino acids, and complex 3‡ 3 3 23 23 23 organic substrates; electron acceptors include O2,Fe ,CO2, CO, NO3 ,NO2 , NO, N2O, SO4 ,SO3 ,S2O3 , and S. Although many assimilatory and dissimilatory metabolic reactions have been identified for these groups of , little attention has been paid to 0 the energetics of these reactions. In this review, standard molal Gibbs free energies (vGr ) as a function of temperature to 200³C are tabulated for 370 organic and inorganic redox, disproportionation, dissociation, hydrolysis, and solubility reactions directly or indirectly 0 involved in microbial . To calculate values of vGr for these and countless other reactions, the apparent standard molal Gibbs free energies of formation (vG0) at temperatures to 200³C are given for 307 solids, liquids, gases, and aqueous solutes. It is shown that 0 values of vGr for many microbially mediated reactions are highly temperature dependent, and that adopting values determined at 25³C for systems at elevated temperatures introduces significant and unnecessary errors. The metabolic processes considered here involve compounds that belong to the following chemical systems: H^O, H^O^N, H^O^S, H^O^N^S, H^O^Cinorganic, H^O^C, H^O^N^C, H^O^S^C, H^O^ N^S^Camino acids, H^O^S^C^metals/minerals, and H^O^P. For four metabolic reactions of particular interest in thermophily and hyperthermophily (knallgas reaction, anaerobic and reduction, and autotrophic ), values of the overall Gibbs free energy (vGr) as a function of temperature are calculated for a wide range of chemical compositions likely to be present in near-surface and deep hydrothermal and geothermal systems. ß 2001 Federation of European Microbiological Societies. Published by Elsevier Science B.V. All rights reserved.

Keywords: Metabolic reaction; Energetics; ; ; ; High temperature

Contents

1. Introduction ...... 176 2. and ...... 177 2.1. at high temperature ...... 177 2.2. Natural host environments ...... 177 2.3. Deep biosphere ...... 177 3. Metabolism of thermophiles and hyperthermophiles ...... 178 3.1. Energy-yielding substrates for and ...... 178 3.2. Comparisons with ...... 183 4. Thermodynamic framework ...... 183 4.1. Energetics of metabolic reactions at 25³C and 1 bar ...... 183 4.2. Internally consistent thermodynamic data at elevated temperatures and pressures . . . 183 4.3. Gas solubilities ...... 184 4.4. Neutrality ...... 184

4.5. pKa values ...... 185

* Corresponding author. Tel.: +1 (314) 935 8651; Fax: +1 (314) 935-7361; E-mail: [email protected]

0168-6445 / 01 / $20.00 ß 2001 Federation of European Microbiological Societies. Published by Elsevier Science B.V. All rights reserved. PII: S0168-6445(00)00062-0

FEMSRE 711 7-3-01 176 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

4.6. Pressure e¡ects ...... 186 4.7. Moving out of the conventional bioenergetic reference frame ...... 187 4.8. Coupled and linked redox reactions ...... 189 5. Energetics of microbial metabolic reactions ...... 190 5.1. The H^O system ...... 191 5.2. The H^O^N system ...... 192 5.3. The H^O^S system ...... 194 5.4. The H^O^N^S system ...... 195

5.5. The H^O^Cinorganic system ...... 196 5.6. The H^O^C, H^O^N^C, H^O^S^C, and H^O^N^S^Camino acid systems ...... 197 5.7. The H^O^S^C^metals/minerals system ...... 199 5.8. The H^O^P system ...... 203 6. Concluding remarks ...... 204

Acknowledgements ...... 205

Appendix ...... 205 0 00 A.1. Interconversion of vGr and vGr ...... 206 A.2. Relationship between Gibbs free energies and electrode potentials ...... 207 A.3. Calculating activities from concentrations ...... 207 A.4. Review of the revised HKF equations of state ...... 210 A.5. Gas solubility reactions ...... 213 A.6. Dissociation reactions ...... 213 A.7. Auxiliary redox, disproportionation, and hydrolysis reactions ...... 215 A.8. Microbially mediated Cl redox reactions ...... 215 A.9. Mineral redox and hydrolysis and cation hydrolysis reactions ...... 217

References ...... 218

1. Introduction Archaea domains. It follows that the origin and evolution of many metabolic reactions and pathways may be rooted In the late 1970s, with the discovery of the Archaea, in thermophiles. At the same time, discoveries about ther- Woese and coworkers rang in the most recent biological mophiles are continuously being made and many reactions revolution by proposing that gene sequences could be used known only from mesophiles at present may also be con- to divide all life on Earth into three distinct groups which ducted by unknown thermophiles. are taxonomically above the level of . These Perhaps the most fundamental characteristic dictating groups later became known as domains and include the the progression of a metabolic reaction, in fact any chem- Eucarya, Bacteria (formerly Eubacteria), and Archaea ical reaction, is the amount of energy required or released. (formerly Archaebacteria) [1]. Partial ribosomal RNA se- A quantitative assessment of the energy budget at the quences from countless organisms have now been deter- appropriate temperature, pressure, and chemical composi- mined and employed to establish phylogenetic relation- tion of the system of interest is an essential prerequisite for ships. In addition, approximately 30 complete , determining which of a large array of metabolic reactions including those of several Archaea, have been deciphered, may be energy-yielding (exergonic). Energy conservation and having as many as 100 microbial genomes in the very in microorganisms living at ambient conditions (meso- near future no longer seems unrealistic [2]. Although phy- philes) is well documented [6], but the counterpart for logenetic trees built upon this ever-increasing wealth of organisms at elevated temperatures is not. The purpose partial and complete genomic data may di¡er, in some of this study is to calculate the energetics as a function cases signi¢cantly [3], these data provide the cornerstone of temperature and pressure for numerous known meta- for investigating life's phylogenetic diversity, the Earth's bolic reactions and determine which of these may provide evolutionary history, and the universal ancestor [4]. an energetic drive for thermophilic microorganisms. For Beyond genetic relations, molecular phylogeny can also reasons discussed below, the emphasis is placed on overall be used to interpret the evolutionary progression of meta- metabolic reactions rather than the stepwise reactions bolic and consequently microbial diversity [5]. A striking which constitute assimilatory processes. These overall re- feature of global phylogenetic trees that cannot be over- actions, such as the reduction of elemental sulfur by H2 to looked is that thermophiles, organisms that favor elevated yield H2S, or the oxidation of (CH4)byO2 to temperatures, represent the deepest and shortest branches yield CO2 and H2O, generally consist of several electron of these trees, both in the Bacteria and particularly the transfer steps, each of which may be catalyzed by a di¡er-

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 177 ent . Therefore, the organism containing the appro- organism if it catalyzes the reaction. Therefore, at high priate is viewed as mediating the sum of stepwise temperatures, it is the rapid unassisted approach to equi- reactions in overall metabolic processes. librium that places a limit on life and not temperature itself.

2. Thermophiles and hyperthermophiles 2.2. Natural host environments

2.1. Life at high temperature Easily accessible natural biotopes of thermophilic mi- crobes include shallow and deep marine hydrothermal An alkaline in the Lower Basin of vent environments, heated beach sediments, continental Yellowstone National Park, USA hosts Thermocrinis ru- solfataric areas, and hot springs. The in situ temperatures ber, an aerobic, facultatively chemolithotrophic Bacterium and pressures of these vary considerably, but that grows in the laboratory between 44 and 89³C by more than cover the range to which known organisms oxidizing , elemental sulfur, thiosulfate, formate, have adapted. The majority of these systems are charac- or formamide. Deep-sea hydrothermal systems at a depth terized by extremely low concentrations. Conse- of 2600 m near 21³N on the East Paci¢c Rise support quently, most of the known of thermophiles are anaerobic autotrophic such as Methanococ- classi¢ed as obligate or facultative anaerobes, though cus jannaschii which grows optimally in the laboratory at aerobic and microaerophilic isolates are also known. As V85³C. Meanwhile, acid solutions generated by the inter- noted by Brock [24], the majority of continental hot spring action of volcanic gases and seawater at Vulcano in the £uids exhibit a bimodal distribution with respect to pH Aeolian Islands and the solfatara ¢elds of Naples, Italy with average values either in the acidic region (pH 1^3) are the habitats of acidophilic Archaea, including Acidia- or near neutral to slightly alkaline (pH 7^9). It should thus nus infernus, , and Metallosphaera come as no surprise that a preponderance of thermophiles sedula, which grow optimally at a pH near 2. The enor- is either acidophilic or neutrophilic. mous genetic and metabolic diversity present in high tem- Although many thermophile biotopes have in situ pres- perature environments re£ect the ranges of pH, oxidation/ sures signi¢cantly greater than atmospheric, researchers reduction states, solute concentrations, gas compositions, are only starting to realize the e¡ects of pressure on and mineralogy that characterize these environments. growth. For example, the survival of the deep-sea hyper- Microorganisms which inhabit these high temperature thermophile strain ES4 at super-optimal tem- environments are de¢ned as thermophilic if their optimum peratures was enhanced by elevated pressure (220 bar) rel- growth temperatures are s 45³C [7]. If an organism has ative to low pressure (30 bar) [25]. On the other hand, the optimum and maximum growth temperatures of at least hyperthermophile isolated from a depth 80 and 90³C, respectively, it is further de¢ned as a hyper- of 3650 m from a hydrothermally heated black smoker thermophile [8]. The current maximum growth tempera- fragment at the Mid Atlantic Ridge showed no growth ture of a pure isolate is 113³C [9], but microbiologists are enhancement when incubated at 250 bar relative to experi- willing to speculate that the upper temperature limit for ments at 3 bar [9]. In contrast, earlier experiments on life may be closer to 150³C [10,11]. Circumstantial evi- M. jannaschii, an autotrophic from submarine dence obtained from mixed culture experiments [12], par- hydrothermal systems, showed a decrease in doubling time ticulate DNA concentrations in black smoker £uids from 83 min at 86³C and 7.8 bar to 18 min at the same [13,14], direct cell counts on sediment samples [15], and temperature but 750 bar [26]. At 90³C, in the same study, £uid inclusion studies [16] suggests that even this estimate the doubling time of M. jannaschii decreased from 160 min appears conservative. Regardless of what the maximum at 7.8 bar to 50 min at 750 bar. Owing to the wide range growth temperature of life on Earth may be ^ if such a of temperature, pressure, £uid chemistry, and mineralogy temperature does in fact exist ^ it is safe to say that it of host environments, the metabolic strategies of thermo- remains unknown. philes are, accordingly, highly diverse. Although extreme temperatures attract considerable at- tention in the discussion of hyperthermophiles [10,11], bi- 2.3. Deep biosphere omolecule stability [17^20], and the universal ancestor [21^ 23], they are less relevant than the availability of energy. It is increasingly apparent that surface thermal features All chemosynthetic organisms gain energy by catalyzing and the organisms they support are giving researchers a oxidation/reduction (redox) reactions that are slow to glimpse of what life may be like in the deep subsurface equilibrate on their own. These reactions have to be ther- [27,28]. Indeed, numerous studies have shown that a sub- modynamically favored but kinetically inhibited to serve surface biosphere exists in coastal plain sediments, sedi- as energy sources. As temperature increases, reaction rates mentary basins, and granitic and basaltic (see also increase, and at some elevated temperature, abiotic Table 1). For example, autotrophic methanogens and 23 3‡ reaction rates are so fast that there is no bene¢t to an SO4 and Fe reducers have been identi¢ed at depths

FEMSRE 711 7-3-01 178 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

Table 1 Direct observations of microorganisms in the deep subsurface

Location Rock or £uid type Max. depth TMAX Laboratory metabolism References (m) (³C)

23 Cerro Negro, NM, USA Sandstone, shale 247 Heterotrophy, SO4 reduction, [163] Savannah River, Aiken, SC, USA Sediments of sand 260 Aerobic and anaerobic heterotrophy, [164,165] 23 and clay SO4 reduction, methanogenesis, nitri¢cation, N2-¢xation Rainier Mesa, NV, USA Volcanic ashfall tu¡ 400 18 Aerobic chemoheterotrophy [166,167] 3‡ 23 Lac du Bonnet batholith, Man., Granite 420 Fe and SO4 reduction, [168,169] Canada Fe2‡ oxidation a 23 b Japan Sea, Peru Margin, Eastern Marine sediments 518 80 SO4 -reducing methanotrophy , [28,39] 3 23 equatorial Paci¢c, Juan de Fuca Ridge, NO3 and SO4 reduction, obligate Lau Basin, Philippine Trench, and facultative barophily Kermadec-Tonga Trench, Soenda Deep, Weber Deep ë 3‡ 23 Aspo«, Granite 860 20.5 Heterotrophic Fe and SO4 [40^43] reduction, autotrophic methanogenesis and acetogenesis Great Artesian Basin, Australia Thermal 914 88 Heterotrophic and autotrophic [170^172] 23 SO4 reduction Stripa mine, Sweden Granite 1240 26 Heterotrophy and autotrophy [173] Hanford Reservation, Washington, Basalt 1300 Autotrophic methanogenesis, [29,30] 23 3‡ USA SO4 and Fe reduction 23 Madison Formation, MT, USA Aquifers in dolomitic 1800 50 SO4 reduction, methanogenesis [174] limestone Piceance Basin, CO, USA Sandstone and shale 2100 85 Heterotrophic and autotrophic [175,176] Fe3‡ reduction 23 Paris Basin, France Oil ¢eld brine, 2500 85 Heterotrophic and autotrophic SO4 [35,38,177,178] geothermal water reduction, autotrophic methanogenesis 23 Taylorsville Basin, VA, USA Siltstone and shale 2800 85 Heterotrophic SO4 and [175,179] Fe3‡ reduction 3‡ 4‡ 3 Witwatersrand, South Africa Carbonate, sandstone, 3200 60 Heterotrophic Fe ,Mn ,S,NO3 , [31,32,173] shale O2 reduction Gravberg, , Sweden Granite 3500 60 Heterotrophy [33,34] 23 23 23 Northsea oil ¢elds: Statfjord and Oil ¢eld waters 4000 110 Heterotrophic SO4 ,SO3 ,S2O3 , [36,37,180,181] 23 Beatrice ¢elds, East Shetland basin and S reduction, autotrophic SO4 reduction, Heterotrophic Mn4‡, 3‡ 3 Fe , and NO3 reduction aThis refers to the depth below the sediment^water interface, not the depth below sea level. b 23 Although able to use SO4 as their have not been isolated, other lines of evidence strongly suggest their existence. up to 1300 m in basaltic rock in Washington, USA [29,30]. trophs that use organic compounds in sediments that are In addition, sedimentary rocks, such as sandstone, shale, the residue of photosynthetic organisms, or they can be and limestone at depths up to 3200 m and temperatures completely independent of , as in the case s 80³C are hosts to a variety of autotrophs and hetero- of autotrophs that gain energy and ¢x by reacting 23 3‡ 4‡ trophs, including aerobes and SO4 ,S,Fe ,Mn , and CO2 and H2 provided by geologic processes [30,44,45]. 3 NO3 reducers [31,32]. In the granitic aquifers at Grav- These observations lead inescapably to the proposition berg, Sweden, heterotrophic metabolism has been docu- that microorganisms can live in the subsurface wherever mented at a depth of 3500 m at 60³C [33,34]. Furthermore, there are sources of geochemical energy and where the thermophiles and hyperthermophiles have been cultured at system is open to mass exchange on at least the timescale temperatures up to V100³C from oil ¢eld waters in the of microbial processes. Paris Basin and the North Sea [35^38], and obligate and facultative barophiles (organisms that favor elevated pres- sures) thrive in marine sediments hundreds of meters be- 3. Metabolism of thermophiles and hyperthermophiles low the sediment^water interface [28,39]. The metabolic diversity already examined in the deep 3.1. Energy-yielding substrates for autotrophs and biosphere shows that chemosynthetic organisms can take heterotrophs advantage of many forms of energy that are su¤cient to support life [40^43]. These energy sources can be linked to More than 200 species of thermophiles and hyperther- photosynthesis at the surface, as in the case of hetero- mophiles belonging to circa 100 genera (Table 2) are cur-

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 179

Table 2 and metabolic features of thermophiles and hyperthermophiles

Genus Species TMAX (³C) Hetero/auto Aerobe/anaerobe References Thermophilic Bacteria Acidimicrobium ferrooxidans 57 FA FAN [182,183] Alicyclobacillus acidocaldarius 70 H AE [184^186] acidoterrestris 60 H AE [184] cycloheptanicus 53 H AE [184] Ammonifex degensii 77 FA AN [187] Anaerobranca horikoshii 66 H AN [188] infernus 61 H AN [116] schlegelii 79 FA AE [189] thermoantarcticus 65 H AE [190,191] thermoleovorans 78 H FAN [192] thermosphaericus 64 H AE [193] tusciae 55a FA AE [194] Calderobacterium hydrogenophilum 82 A AE [195] Caldicellulosiruptor lactoaceticus 78 H AN [196] owensensis 80 H AN [197] saccharolyticus 80 H AN [198] Caloramator indicus 75 H AN [199] proteoclasticus 68 H AN [200] Chloro£exus aurantiacus 65 H FAN [201] paradoxim 63 H AN [202] thermosuccinogenes 65 H AN [203] Coprothermobacter proteolyticus 75 H AN [204] Deferribacter thermophilus 65 H AN [181] geothermalis 55 H AE [205] murrayi 52 H AE [205] Desulfacinum infernum 65 FA AN [206] australicum 74 FA AN [170] geothermicum 57 FA AN [35] kuznetsovi 85 FA AN [207] luciae 70 FA AN [175,208] nigri¢cans ssp. salinus 70 H AN [209] putei 65 FA AN [175] thermoacetoxidans 65 FA AN [210] thermobenzoicum 70 H AN [211] thermocisternum 75 FA AN [180] thermosapovorans 60 FA AN [212] Desulfurella acetivorans 70 H AN [213] kamchatkensis 70 FA AN [214] multipotens 77 FA AN [215] propionica 63 FA AN [214] Desulfurobacterium thermolithotrophum 75 A AN [216] Dictyoglomus turgidus 86 H AN [217] Fervidobacterium islandicum 80 H AN [218] nodosum 79 H AN [219] pennavorans 80 H AN [220] Flexistipes sinusarabici 53 H AN [221] Geotoga petraea 55 H AN [222] subterranea 60 H AN [222] Halothermothrix orenii 68 H AN [223] acidophilus 65 A AE [224] halophilus 75 A AE [225] thermophilus 79 A AE [226,227] Hydrogenophilus thermoluteolus 52 FA AE [228,229] Isosphaera pallida 55 H AE [230] Meiothermus cerbereus 60 H AE [231] chliarophilus 60 H AE [232] ruber 65 H AE [232] silvanus 65 H AE [232] Methylococcus thermophilus 62 H AE [233] Moorella glycerini 65 H AN [234] thermoaceticum 65 H AN [235,236]

FEMSRE 711 7-3-01 180 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

Table 2 (continued)

Genus Species TMAX (³C) Hetero/auto Aerobe/anaerobe References Petrotoga miotherma 65 H AN [222] mobilis 65 H AN [237] Rhodothermus marinus 77 H AE [238] obamesis 85 H AE [239] Rubrobacter xylanophilus 70 H AE [240] radiotolerans 48a H AE [241] Sphaerobacter thermophilus 60 H AE [242] Spirochaeta caldaria 52a H AN [243] thermophila 73 H AN [244] acidophilus 50 FA FAN [183,245] thermosul¢dooxidans 55 FA FAN [183,246,247] Thermaerobacter marianensis 80 H AE [248] Thermoanaerobacter acetoethylicus 79 H AN [204,249] brockii 85 H AN [250^252] ethanolicus 78 H AN [252,253] kivui 72 FA AN [236,254] mathranii 75 H AN [255] sulfurophilus 75 H AN [256] thermohydrosulfuricus 78 H AN [252] wiegelii 78 H AN [257] Thermoanaerobacterium aotearoense 66 H AN [258] saccharolyticum 70 H AN [252] thermosulfurigenes 75 H AN [252] xylanolyticum 70 H AN [252] Thermoanaerobium lactoethylicum 75 H AN [259] Thermobrachium celere 75 H AN [260] Thermocrinis ruber 89 FA AE [261] Thermocrispum agreste 62 H AE [262] municipale 62 H AE [262] Thermodesulfobacterium commune 85 H AN [263] mobile 85 H AN [264,265] Thermodesulforhabdus norvegicus 74 H AN [266] Thermodesulfovibrio yellowstonii 70 H AN [267] Thermohalobacter berrensis 65 H AN [268] Thermohydrogenium kirishiense 75 H AN [269] Thermoleophilum album 70 H AE [270] Thermomicrobium roseum 85 H AE [271] Thermonema rossianum 65 H AE [272] Thermosipho africanus 77 H AN [273] Thermosyntropha lipolytica 70 H AN [274] Thermoterrabacterium ferrireducens 74 H AN [275] azorensis 87 A AE [276] thioparus 77 FA FAN [277,278] el¢i 72 H AN [279] hypogea 90 H AN [280] subterranea 75 H AN [281] thermarum 84 H AN [282] aquaticus 79 H AE [283] oshimai 70 H AE [284] thermophilus 85 H AE [285] Thiobacillus thermophilica 80 A AE [286] Hyperthermophilic Bacteria pyrophilus 95 A FAN [82] 90 H AN [287] neapolitana 90 H AN [288] Thermophilic Archaea Acidianus ambivalens 87 A FAN [289^291] brierleyi 75 FA FAN [292^294] lithotrophicus 89 A AN [37] vene¢cus 85 FA AN [295] Metallosphaera prunae 80 FA AE [296] sedula 80 FA AE [293,297]

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 181

Table 2 (continued)

Genus Species TMAX (³C) Hetero/auto Aerobe/anaerobe References de£uvii 65 A AN [298] thermoaggregans 75 A AN [299] thermoalcaliphilum 69 A AN [300] thermophilum 57 A AN [301] thermo£exum 70 A AN [298] thermolithotrophicus 70 A AN [302] vulcanius 89 A AN [303] Methanoculleus thermophilicum 60 H AN [304] evestigatus 60 H AN [305] thermophila 50 H AN [128] Methanothermobacter thermoautotrophicus 75 A AN [306] wolfeii 74 A AN [307] Methanothrix thermophila 60a H AN [308] Palaeococcus ferrophilus 88 H AN [309] Picrophilus oshimae 65 H AE [310,311] torridus 65 H AE [310,311] Stygiolobus azoricus 89 A AN [312] acidocaldarius 80 FA FAN [293,313^315] hakonensis 80 FA AE [316] metallicus 75 A AE [317] shibatae 86 FA AE [293,318,319] solfataricus 87 FA AE [293,320] Sulfurococcus mirabilis 86 FA AE [321] yellowstonii 80 FA AE [322] modestius 82 H FAN [259] Thermococcus zilligii 85 H AN [323,324] Thermoplasma acidophilum 63 H FAN [325,326] volcanium 67 H FAN [325] Hyperthermophilic Archaea Acidianus infernus 96 A FAN [292,293] 100 H AE [327] Archaeoglobus fulgidus 95 FA AN [328^330] profundus 90 A AN [331] Caldivirga maquilingensis 92 H FAN [332] Caldococcus litoralis 100 H AN [333] noboribetus 96 H AN [334,335] Desulfurococcus amylolyticus 97 H AN [336] mobilis 97 H AN [337] mucosus 97 H AN [337] Ferroglobus placidus 95 FA AN [84] Hyperthermus butylicus 108 H AN [338] Methanococcus fervens 92 A AN [303,339] igneus 91 A AN [340] infernus 91 A AN [341] jannaschii 94 A AN [126,304] kandleri 110 A AN [94,342] fervidus 97 A AN [343] sociabilis 97 A AN [344] Pyrobaculum aerophilum 104 FA FAN [345] islandicum 102 FA AN [346] organotrophum 102 H AN [346] 108 H AN [347] endeavori (ES4) 110 H AN [348] furiosus 103 H AN [349] horikoshii 102 H AN [350] woesei 104 H AN [351] Pyrodictium abyssi 110 H AN [347] brockii 110 A AN [352,353] occultum 110 A AN [352,353] Pyrolobus fumarii 113 A FAN [9] marinus 98 H AN [354] Stetteria hydrogenophila 102 H AN [355] Sulfophobococcus zilligii 95 H AN [356]

FEMSRE 711 7-3-01 182 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

Table 2 (continued)

Genus Species TMAX (³C) Hetero/auto Aerobe/anaerobe References Sulfurisphaera ohwakuensis 92 H FAN [357] Thermococcus acidaminovorans 93 H AN [358] aggregans 94 H AN [359] alcaliphilus 90 H AN [360] barophilus 100 H AN [361] barossi 92 H AN [362] celer 93 H AN [363] chitonophagus 93 H AN [364] fumicolans 103 H AN [365] gorgonarius 95 H AN [366] guaymasensis 90 H AN [359] hydrothermalis 100 H AN [367] litoralis 98 H AN [368,369] paci¢cus 95 H AN [366] peptonophilus 100 H AN [370] profundus 90 H AN [371] siculi 93 H AN [372] stetterib 98 H AN [373] maritimus 98 H/Ac AN [374,375] Thermo¢lum pendens 100 H AN [376] Thermoproteus neutrophilus 85a A AN [375] tenax 96 FA AN [375,377] uzoniensis 102 H AN [378] Thermosphaera aggregans 90 H AN [261] A: ; H: ; FA: facultative autotroph (or facultative heterotroph); AN: anaerobe; AE: aerobe; FAN: facultative anaerobe (or fac- ultative aerobe). aThis represents the optimum growth temperature; the maximum growth temperature is not given. bSome strains are thermophilic with a temperature optimum of 73^77³C and a maximum of 94³C, but others are hyperthermophilic with optimum and maximum growth temperatures equal to 88 and 98³C, respectively [373]. cFischer et al. (1983) [375] describe Thermodiscus maritimus as an obligate autotroph, but Stetter et al. (1990) [374] list it as a heterotroph.

rently known. These microorganisms can carry out a wide heterotrophs in natural are generally not re- variety of metabolic processes featuring a multitude of solved [46]. electron donors and acceptors. To date, 12 genera are In addition, all hyperthermophiles and many species of known within the Archaea, both aerobes and anaerobes, thermophiles are chemosynthetic rather than photosyn- autotrophs as well as heterotrophs, which catalyze meta- thetic, deriving energy by the oxidation or reduction of bolic reactions at temperatures v100³C. Although the dissolved organic and inorganic compounds rather than metabolic pathways used by thermophiles and hyperther- by harnessing solar energy. This fact also correlates di- mophiles are still largely unresolved, several dominant rectly with the geochemistry and geophysics of high tem- characteristics of energy-yielding redox reactions are ap- perature ecosystems. These environments are almost exclu- parent. Only approximately 25 known genera of thermo- sively at depths greater than those penetrable by . philes and hyperthermophiles contain obligate aerobes; Finally, the majority of thermophiles and hyperthermo- most are obligate anaerobes, but some are facultative an- philes in culture take advantage of electron transfer aerobes. Therefore, the common electron acceptors used among species in the sulfur redox system. Anaerobes com- by these organisms include, for example, sulfate, nitrate, monly reduce sulfate, sul¢te, thiosulfate, or elemental sul- , and ferric rather than oxygen. This fur to sul¢de, while aerobes may oxidize sul¢de or elemen- directly re£ects the geochemical nature of the biotopes tal sulfur to sulfate. Of these, perhaps the most common discussed above. energy-yielding process used by hyperthermophiles is the Furthermore, the majority of known thermophiles and reduction of elemental sulfur represented by: hyperthermophiles are obligately heterotrophic, preferen- H g†‡Sulfur ! H S g† 1† tially using complex mixtures of polypeptides and/or car- 2 2 bohydrates as energy and carbon sources in laboratory This experimentally-veri¢ed reaction [47] is believed to be growth experiments. Others are strict autotrophs that as- the sole energy-yielding process in numerous autotrophs, similate CO2, and yet others are able to grow hetero- or although it has been shown [48] that the energy release in autotrophically depending on the availability of carbon hot spring systems is rather moderate relative to other sources. It should be noted that the actual carbon com- known autotrophic and heterotrophic metabolic reac- pounds metabolized by thermophilic or hyperthermophilic tions.

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 183

3.2. Comparisons with mesophiles accurate thermodynamic properties at this temperature and pressure. Recent developments of theoretical equa- Thermophiles, and in particular hyperthermophiles, are tions of state permit the calculation of standard partial relatively recent discoveries in microbiology. If the volume molal thermodynamic properties of aqueous, liquid, solid, of Earth where life may exist is indeed as vast as recently and gaseous organic and inorganic compounds over wide estimated [27], most of the habitable subsurface can only ranges of temperature and pressure. In the present study, be inhabited by thermophiles and hyperthermophiles. we evaluated standard state1 thermodynamic properties at Although considerable progress has already been made temperatures up to 200³C, which is well within the range in identifying their required substrates for growth in the of temperature covered by experimental data and equa- laboratory, signi¢cant gaps still exist in (1) understanding tions of state, and should be su¤cient for metabolic en- the actual carbon sources of thermophilic heterotrophs in ergy calculations for even the most optimistic microbiolo- natural biotopes, (2) evaluating the impact of solid phases gists. on metabolism, both as substrates and products, (3) elu- cidating the pathways of intracellular anabolism and ca- 4.2. Internally consistent thermodynamic data at elevated tabolism, and (4) quantifying the energetics of metabolic temperatures and pressures reactions at the temperature, pressure, and chemical com- position of natural systems. In all four cases, the plethora There is always uncertainty in thermodynamic calcula- of information and data gathered from studies of meso- tions, but some sources can be minimized or even elimi- philic organisms may provide some useful constraints. nated. Systematic and experimental uncertainties can not It is the objective of this study to calculate the energetics be overcome through data interpretation. Mixing of ther- as functions of temperature and pressure of `overall' met- modynamic data from various sources can introduce in- abolic reactions known to be mediated by thermophiles consistencies that can cripple the accuracy of calculations. and hyperthermophiles. We have included reactions that On the other hand, inconsistencies among various sets of are unfamiliar to thermophily if they are experimentally thermodynamic data can be resolved by careful analysis. veri¢ed energy-yielding processes in mesophiles. In addi- The result is usually called an internally consistent data- tion, we supply thermodynamic properties of 307 individ- base, which means that thermodynamic properties of a ual aqueous solutes, gases, liquids, and minerals, which network of reactions have been used to extract corre- permit calculations for thousands of additional reactions sponding properties of individual compounds. The data that may be of interest as research progresses. Calculations and equations used in this study represent one of the of this sort may aid in identifying likely thermophilic and most comprehensive internally consistent data sets avail- hyperthermophilic not yet observed, as well able for biochemical and geochemical calculations. as in the selection of potential habitats for discovering The revised Helgeson^Kirkham^Flowers (HKF) equa- novel isolates. In a step toward reaching these goals, we tions of state have been combined with experimental cal- present a thermodynamic approach to evaluate quantita- orimetric, densimetric, and sound velocity measurements tively the energetics of overall metabolic reactions in mi- as well as solubility and dissociation data available in the croorganisms as functions of temperature and pressure. literature to generate parameters required to calculate standard molal thermodynamic properties at elevated tem- peratures and pressures for hundreds of aqueous com- 4. Thermodynamic framework pounds. The classes of compounds for which internally consistent thermodynamic data are now available include 4.1. Energetics of metabolic reactions at 25³C and 1 bar aqueous inorganic ions and neutral solutes [49^56], aque- ous organic compounds including , carbox- Prior to the discovery of thermophiles, energetic calcu- ylic acids, ketones, alcohols, aldehydes, amines, amides, lations at 25³C and 1 bar for metabolic reactions were chlorinated compounds, amino acids, and peptides [57^ su¤cient for most applications in microbiology. It can 67], and metal^organic complexes [68^70]. Discussions of be seen in tables and ¢gures presented here that the ener- the theoretical foundation for the HKF equations in their getics of the chemical reactions of interest show very little original form are given by Helgeson et al. (1981) [71], and change over a narrow temperature range near 25³C. In in their revised forms by Tanger and Helgeson [72], Shock other words, applying a thermodynamic value for a spe- and Helgeson [49,57], Shock et al. (1989, 1992) [50,51], ci¢c reaction at 25³C to the same reaction at 15 or 37³C Johnson et al. (1992) [73], and Sverjensky et al. (1997) introduces only minimal error. Thauer et al. (1977) [6] published a compilation of thermodynamic calculations at 25³C for energy conservation in chemotrophic anaer- 1 Standard states used in these calculations are as follows: for solids and water, unit activity of the pure compound at any temperature and pres- obes that is still useful today. However, accurately deter- sure; for gases, unit fugacity of the pure gas at any temperature and 1 bar; mining the energetics of metabolic reactions carried out, and for aqueous solutes, unit activity of a hypothetical 1 molal solution for example, by P. fumarii at 113³C and 250 bar requires referenced to in¢nite dilution at any temperature and pressure.

FEMSRE 711 7-3-01 184 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

minimizes at a temperature well above 100³C. In fact, the

solubility at PSAT of CO2(g) is nearly eight times higher near 0³C than at 200³C.

CH4 serves as a carbon source for methanotrophs, but it is metabolically produced by methanogens. Its solubility at

PSAT is quite temperature dependent at low temperature, but only moderately so above V50³C. It can be seen in

Fig. 1 that the values of log K for the CH4 solubility reaction minimize at V100³C and PSAT, and that CH4(g) is approximately twice as soluble at 2 and 200³C than at 100³C. Many hyperthermophilic heterotrophs currently in cul-

ture depend on the reduction of sulfur to H2S for opti- mum growth [8]. Therefore, the solubility of H2Sasa Fig. 1. Log K plotted against temperature at PSAT for the solubility of function of temperature may be useful for understanding gaseous H2S (reaction G8), CO2 (reaction G9), CH4 (reaction G10), their metabolisms. Not unlike that of CO2 discussed and H2 (reaction G1). above, the solubility of H2S decreases signi¢cantly with [55], and relevant equations are presented in the Appendix. increasing temperature. This can be interpreted from the

In addition, internally consistent data for solid, liquid, and values of log K for the H2S solubility reaction shown in gaseous organic compounds [74,75] and numerous inor- Fig. 1. In fact, like CO2, the solubility of H2S(g) at PSAT is ganic gases and rock-forming minerals [56,76] can be in- approximately eight times higher near 0³C than at 200³C. cluded in these calculations. To underscore the variability of thermodynamic data as functions of temperature and 4.4. Neutrality pressure, it seems appropriate to show a few examples of the e¡ects of temperature and pressure on the thermody- The temperature and pH dependencies of dissociation namic behavior of gases and aqueous species involved in reactions a¡ect many microbial metabolic processes. microbial metabolic reactions. Many bioenergetic calculations are carried out at pH = 7 (see below), because this denotes neutrality at 25³C and 4.3. Gas solubilities 1 bar. However, because neutrality is de¢ned as the pH where activities of H‡ and OH3 are equal, and the disso-

Molecular hydrogen (H2) is a common ciation constant for H2O is temperature dependent, the (reductant) in thermophilic and hyperthermophilic metab- pH representing neutrality also varies with temperature. olism. Therefore, the equilibrium constant for H2 dissolu- It can be seen in Fig. 2 that neutral pH, depicted by the tion in water as a function of temperature, shown in Fig. curve, decreases at PSAT from V7.4 at 0³C to V5.6 at 1, is of direct signi¢cance2. It can be seen in this ¢gure that 200³C. A pH of 7 carries no special signi¢cance at temper- the logarithm of the equilibrium constant (K) for the H2(g) atures and pressures other than 25³C and 1 bar. The con- dissolution reaction minimizes with increasing temperature sequences of this fact can not be ignored when describing 3 at constant pressure, (PSAT) . The key point to note is that metabolic reactions written in terms of species such as 23 the solubility of H2(g) is moderately temperature depen- CO2,H2S, SO4 ,NH3, and organic acids. dent. In fact, at PSAT,H2(g) is more than twice as soluble At neutral pH, as shown by the dashed curve in Fig. 3a, at 200³C than at 50³C. dissolved CO2 is the dominant species in the carbonic acid The solubility of CO2 plays an important role in the system only above V80³C; below this temperature, 3 4 metabolism of autotrophs that use it as a carbon source, HCO3 dominates at neutrality . It can be inferred from 23 as well as heterotrophs that produce it as a metabolite. this ¢gure that the equilibrium concentration of CO3 is Values of log K for the CO2(g) solubility reaction are only signi¢cant in highly alkaline solutions, regardless of also shown in Fig. 1. In contrast to H2, log K for CO2 the temperature. Note in Fig. 3b that at neutral pH the 3 activity of H2S exceeds that of HS to an increasing de- gree with increasing temperature. In the sys- 2 There are many ways to write this reaction and to describe its ther- tem (Fig. 3c), SO23 is the dominant species at alkaline and modynamic properties. The dissolution equilibrium refers to the reac- 4 tion H2(g) = H2(aq), and the corresponding equilibrium constant is given by K = a /f where a and f refer to activity and fugacity, re- H2 aq† H2 g† 4 spectively. Therefore, K is related to the Henry's constant KH, which Although carbonic acid is often represented as H2CO3, this molecule is refers to the reaction H (aq) = H (g) by K = a /K X , because only present as a reactive intermediate between HCO3 and dissolved CO . 2 2 H2 aq† H H2 aq† 3 2 K = f /X where X stands for mol fraction. The latter is the molecular form that s 99% of carbonic acid takes at pH H H2 g† H2 aq† values 6 pK1, and H2CO3 is a conventional species with properties equal 3 PSAT is used in this study to denote saturation pressures for H2O, in to the sum of the properties of H2O and CO2(aq) [77]. Therefore, we do other words the P^T boiling curve for water. not use H2CO3 in our calculations, tables, or ¢gures.

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 185

values for inorganic and organic acids involved in micro- bial metabolism, as illustrated with the examples shown in Fig. 4. In some cases, these changes are dramatic, and, as a result, the speciation of metabolites di¡ers considerably between environments at various temperatures even though pH values may be quite similar. For example, at neutral pH, will dominate the speciation of solutions at all temperatures from 0 to 200³C as shown in Fig. 4a. On the other hand, acetic acid acting as a bu¡er can hold the pH between 4.8 and 5.5 over this temperature range. Speciation of (Fig. 4b) is dominated by succinate23 at neutral pH and temperatures 6 V110³C, and by the monovalent anion, H^succinate3, at neutral pH and higher temperatures. Aspartic acid (Fig.

4c) exhibits only the slightest variation in pKa from 0 to Fig. 2. Neutral pH depicted by the curve as a function of temperature 200³C, and that of lysine (Fig. 4d) is not signi¢cantly more at P . SAT pronounced. In the three dissociation reactions of phos- phoric acid (Fig. 4e), the pH values of the equal activity neutral and well into the acid region over the entire curves vary only slightly as functions of temperature. 3 23 temperature range considered here. However, with increas- H2PO4 dominates at and near-neutral pH, and HPO4 33 ing temperature in highly acid environments, the activity dominates at slightly alkaline pH. H3PO4 and PO4 are 3 23 of HSO4 may rival and even surpass that of SO4 . In the only signi¢cant in highly acidic ( 6 V2) or highly alkaline ‡ system (Fig. 3d), NH4 is the dominant species at ( s V12) solutions, respectively. The speciation of vanadic neutral pH between 0 and 200³C, although to a lesser acid (Fig. 4f) shows ¢ve di¡erent protonated and depro- 3 degree with increasing temperature. tonated forms with H2VO4 being the dominant one at neutral pH over the entire temperature range.

4.5. pKa values The variations in speciation shown in Fig. 4 help to explain why various solutes behave di¡erently in natural

Changes in temperature have variable e¡ects on pKa high temperature environments. As an example, in one

3 Fig. 3. Temperature^pH diagrams at PSAT for the dissociation of (a) CO2(aq) (reactions H9 and H10); (b) H2S(aq) (reaction H8); (c) HSO4 (reaction ‡ H7); (d) NH4 (reaction H2). The solid curves represent equal activities of the species that predominate on either side of the curves. The dashed lines depict neutral pH (see Fig. 2).

FEMSRE 711 7-3-01 186 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

Fig. 4. Temperature^pH diagrams at PSAT for the dissociation of (a) acetic acid (reaction H12); (b) succinic acid (reactions H23 and H24); (c) aspartic ‡ ‡ acid (reaction H28); (d) lysine (reaction H31); (e) H3PO4 (reactions H45-H47); (f) VO2 (reactions H32^H35). The solid curves represent equal activ- ities of the species that predominate on either side of the curves. The dashed lines depict neutral pH (see Fig. 2). out£ow channel of Octopus Spring at Yellowstone Na- trate this point, values of vG0 of aqueous glycine are plot- tional Park, populated by T. ruber, the pH is 7.88 at ted in Fig. 5 as a function of temperature at various pres-

88³C [78]. In contrast, we measured pH as low as 2.12 sures from PSAT to 5 kbar (depicted as contours). It can be at only slightly lower temperature in thermal waters from Pozzo Vasca at Vulcano in the Aeolian Islands, southern Italy. At Octopus Spring, the predominant forms of the compounds shown in Fig. 4 would be acetate3, 23 3 23 23 succinate , aspartate , lysine, H2PO4 , and HVO4 , while at Vulcano, the speciation would be dominated by ‡ acetic acid, succinic acid, aspartic acid, lysine ,H3PO4, ‡ and VO2 .

4.6. Pressure e¡ects

Many thermophiles and hyperthermophiles are also bar- ophiles and may employ metabolic processes that are af- fected by pressure. In general, the e¡ect of pressure on values of the standard molal Gibbs free energy of forma- 0 tion (vG ) between P and 1 kbar is signi¢cantly less 0 SAT Fig. 5. vG of aqueous glycine plotted against temperature at PSAT and than the e¡ect of temperature from 0 to 100³C. To illus- constant pressure (labeled in kbar).

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 187 seen in this ¢gure that at constant temperature and dissociation change by V1.5 and V1.0 kJ mol31, respec- 0 pressures between PSAT and 1 kbar, values of vG di¡er tively. by 6 5kJmol31. Conversely, at constant pressure and This set of examples is included here to emphasize the temperatures between 0 and 100³C, vG0 decreases by point that the e¡ects of temperature and, to a lesser de- V17 kJ mol31. A change of this magnitude in vG0 for gree, pressure on the thermodynamic behavior of com- aqueous glycine would require a decrease in pressure from pounds involved in metabolic processes are often consid-

4 kbar to PSAT at constant temperature. In other words, at erable. Calculating the energetics of metabolic processes most conditions of biological interest, the e¡ect of pres- such as methanogenesis, sulfur reduction, and acetic acid sure on vG0 is secondary to that of temperature. There- catabolism, to name only a few, can be accomplished with fore, most thermodynamic properties tabulated in the the standard molal thermodynamic properties of all reac- present communication are calculated as a function of tants and products at the temperature and pressure of temperature at PSAT rather than as a function of pressure. interest, together with their activities in natural or labora- Nevertheless, in certain environments, the e¡ect of pres- tory systems. Traditionally, bioenergetic calculations are sure should not be ignored. Indeed, there is no need to conducted at reference conditions which are misleading make assumptions about pressure e¡ects on the thermo- at best when attempting to evaluate reaction energetics dynamic properties of aqueous species or reactions be- in high temperature/pressure systems. cause they can be calculated explicitly with the revised HKF equations of state by integrating the volume with 4.7. Moving out of the conventional bioenergetic reference respect to pressure (see below). frame Some further examples of the e¡ects of pressure are shown in Fig. 6 for reactions that are introduced above. Many bioenergetic calculations are carried out with It can be seen in Fig. 6a that increasing pressure to 1000 thermodynamic data at reference conditions of 1 atmos- bar (approximately equal to the pressure at a depth of 10 phere (atm), 25³C, and with the additional constraint that km in seawater) has a slight e¡ect on the pH of neutrality. pH = 7. Although few organisms actually require these en- At 100³C, neutral pH decreases from just above 6.1 to just vironmental conditions, these data are useful when consid- below 6.0 as pressure increases from 1 to 1000 bar. At ering the metabolic energy demands of organisms living in 0 100³C, values of vGr for the CO2 solubility reaction near-surface environments where no pressure extrapola- (Fig. 6b) change by V3 kJ mol31 over this same pressure tion is required, where the variability of temperature has range; those for H2S (Fig. 6c) and acetic acid (Fig. 6d) a minimal e¡ect on standard thermodynamic properties,

0 Fig. 6. vGr (or pH) plotted against pressure at 0, 100, and 200³C for the dissociation of H2O, H2S, and acetic acid as well as for the solubility of CO2(g).

FEMSRE 711 7-3-01 188 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 and where near-neutral pH can often be assumed for in- requires accounting for the stoichiometry of H‡ in the tracellular £uids owing to homeostasis. On the other hand, reaction (eH‡ ). A sample calculation of the interconver- acidophilic, barophilic, and thermophilic microorganisms sion from the standard state adopted in this study and require low pH or high pressures or high temperatures, its biological counterpart is presented in the Appendix. and some require combinations of these factors. From a Another problem which plagues bioenergetic calcula- geochemical, ecological, or environmental perspective, the tions does not involve the adoption of standard states, conventional biological reference frame for energetic cal- but rather confusion about the di¡erence between stan- culations can inhibit meaningful insights into how these dard state properties and the overall thermodynamic prop- organisms live. erties of reactions. It appears to be fairly common practice The problems introduced by the conventional bioener- to use standard state Gibbs free energies to argue whether getic reference frame are far from trivial. As shown above, a reaction can provide energy without bringing in any direct application of 25³C data to the elevated tempera- other environmental constraints. These arguments contra- tures that many microorganisms require can introduce vene thermodynamics. It is impossible to tell from the sign 0 enormous errors. In addition, many bioenergetic calcula- of vGr which way a reaction will proceed, unless all of the tions also convert the standard partial molal Gibbs free chemical species in the chemical process of interest are 0 energy of reaction (vGr ) into a revised version at pH = 7, already in their standard states. This can be the case for 0 indicated as vGr P. This is done by removing the hydrogen pure solids, but is generally not the case for aqueous sol- ion (H‡) from the standard state adopted for all other utes or gases. The direction in which a reaction involving aqueous species in the calculation (corresponding to unit aqueous solutes or gases will proceed can only be deter- activity in a hypothetical 1 molal solution referenced to mined from the overall Gibbs free energy after evaluating in¢nite dilution) and evaluating the free energy contribu- the activities of all of the chemical species in the reaction. tion of H‡ at an activity of 1037. This conversion is useful If this was not the case, then there would be no need to for studying processes inside mammalian cells, as well as make chemical analyses of natural or laboratory aqueous comparative studies based on well-controlled laboratory systems. The overall Gibbs free energy of a reaction (vGr) conditions. Arguments in defense of this approach are can be calculated from the familiar expression: presented by other investigators [79,80]. However, the vG ˆ vG0 ‡ RT ln Q 5† adoption of the revised biologic standard state unneces- r r r 0 sarily complicates thermodynamic evaluation of the e¡ects where vGr is as de¢ned above, R and T represent the gas of existing natural or laboratory constraints on the bioen- constant and temperature (K), respectively, and Qr de- ergetics of microorganisms. Furthermore, as illustrated notes the activity product. Values of Qr required to eval- above, the pH which corresponds to neutrality depends uate vGr with Eq. 5 can be determined from the relation: on pressure and temperature. Therefore, although neutral- Y e i;r ity may be a useful constraint for applying thermodynamic Qr ˆ ai 6† data in bioenergetic calculations, pH = 7 is not.

Values of neutral pH as a function of temperature are where ai stands for the activity of the ith species, and ei;r determined from values of the equilibrium constant (K) for represents the stoichiometric reaction coe¤cient of the ith the reaction: species in reaction r, which is negative for reactants and

‡ 3 positive for products. In the case of gases, activity is re- H2O l†HH ‡ OH 2† placed by fugacity of the species, fi. which in turn are calculated with the relation: It is the term on the left hand side of Eq. 5, vGr, which determines how a reaction will proceed. Indeed, relying on vG0 ˆ 32:303RT log K 3† r the sign of the ¢rst term on the right hand side of this 0 0 Values of vG2 and neutral pH as a function of temper- expression, vGr , can be very misleading as illustrated by ature are given in Table 3. To facilitate the conversion the example of anaerobic acetic acid oxidation represented 0 0 from vGr to vGr P and vice versa, the contribution of by: 0 a ‡ to vG (denoted as G ) as a function of temperature H r n CH COOH aq†‡2H O l†!2CO g†‡4H g† 7† is explicitly listed in Table 3. This conversion, expressed 3 2 2 2 0 as: At 100³C and PSAT, vG7 is positive, and equal to 35.9 kJ mol31. In shallow hot spring systems, such as those in the 00 0 vGr ˆ vGr ‡ e H‡ Gn 4† Aeolian Islands of Italy, the activity product, Q7, at the

Table 3 0 ‡ 3 The values of vGr ,pHneutral, and Gn for the water dissociation reaction H2O(l) = H +OH T (³C) 2 18 25 37 45 55 70 85 100 115 150 200

0 vGr 78.25 79.34 79.89 80.90 81.63 82.59 84.13 85.78 87.55 89.42 94.22 102.21 pHneutral 7.43 7.12 7.00 6.82 6.70 6.58 6.41 6.26 6.13 6.02 5.82 5.64 Gn 339.13 339.67 339.95 340.45 340.82 341.30 342.07 342.89 343.78 344.71 347.11 351.11

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 189 prevailing environmental conditions (a =3U1036 ; case by combining Reaction 9 with: CH3COOH f = 2.8U1032 ; f = 4.8U1035 [46,81]) is equal to CO2 H2 ‡ 3 315 0 H2 aq†!2H ‡ 2e 10† 1.39U10 . These values of vG7 and Q7 combined in Eq. 5 yield a negative value of vG7 equal to 370.2 kJ to yield: 31 mol . Therefore, at the actual environmental condi- NO3 ‡ H aq†!NO3 ‡ H O l† 11† tions, Reaction 7 is energy-yielding (exergonic); i.e., the 3 2 2 2 0 value of vG7 is negative, even though that of vG7 is pos- Reaction 11 represents the coupled process of nitrate re- itive. duction to and H2 oxidation to water, and does not The energetics of overall autotrophic and heterotrophic explicitly involve electrons even though electrons are reactions discussed below are grouped by chemical system transferred in the actual overall reaction. starting with simple systems such as H^O and H^O^N and This sort of representation is particularly useful because proceeding to more complex systems involving organic the source of electrons in microbial reactions may or may compounds, metal ions, minerals, and multiple oxidation not be known. For example, in the case of an autotroph states of sulfur. In each system, we tabulate values of vG0 that gains energy from the knallgas reaction: at various temperatures (T) for individual solids, gases, H aq†‡0:5O aq†!H O l† 12† and aqueous species, which are calculated from: 2 2 2

0 0 0 H2 is the source of electrons used to reduce O2 to water. vG ˆ vG 3S T3T r† f TrPr However, in the case of a heterotroph, it may only be

Z T Z T Z P known that the organism reduces nitrate to nitrite with 0 0 0 ‡ CPdT3T CPdln T ‡ V dP 8† electrons provided by the oxidation of uncharacterized T r T r Pr organic compounds in organic matter (either occurring 0 where vGf stands for the standard partial molal Gibbs naturally or from yeast extract or other commonly used free energy of formation from the elements at the reference constituents of laboratory media). In this case, it may still temperature (Tr) and pressure (Pr) of 298.15 K and 1 bar, be useful to consider the energetics of nitrate reduction S0 represents the standard partial molal entropy at the using Reaction 11 despite the fact that the source of the TrPr 0 0 reference conditions, and CP and V designate the stan- H2 is unknown. In fact, H2 may be a proxy for hydrogen dard partial molal isobaric heat capacity and volume, re- obtained from organic compounds or, for that matter, spectively. Evaluating the integrals in Eq. 8 is accom- electrons obtained through partial or complete oxidation plished with the revised-HKF equation of state (see of organic carbon. If the involved is Appendix). The advantage of this approach is that values known, then the coupled organic oxidation and nitrate 0 0 of vG can be summed directly to obtain vGr without reduction reactions can be obtained by combining Reac- having to evaluate thermodynamic properties of the ele- tion 11 with the H2-balanced organic oxidation reaction. ments as functions of temperature and pressure (besides, As an example, oxidation of carbon in to they cancel across any balanced ). CO2 : HCOOH aq†!CO aq†‡H aq† 13† 4.8. Coupled and linked redox reactions 2 2 can be combined with Reaction 11 to yield: Microorganisms have developed the means to take ad- HCOOH aq†‡NO3 ! NO3 ‡ CO aq†‡H O l† 14† vantage of an enormous variety of redox energy sources. 3 2 2 2 As a result, almost every conceivable combination of re- Note that this representation of the linked overall redox duced and oxidized compounds are linked by organisms in process of formic acid oxidation and nitrate reduction overall metabolic processes. Although the biochemical does not involve H2(aq) or electrons. Nevertheless, the pathways of electron transfer can be quite complicated, mechanisms of actual biochemical redox pathways may 3 mediated by enzymes, and are in many cases unknown, use H2,e , or both. it is useful to break down overall reactions into their con- In our treatment of coupled and linked redox reactions, stituent redox steps. This can be illustrated by writing we have chosen to tabulate standard Gibbs free energies half-cell reactions that explicitly include electrons (e3) for reactions that are identi¢ed with the metabolism of such as: speci¢c microorganisms. If the actual stoichiometry of the reaction has been demonstrated, or is certain for NO3 ‡ 2H‡ ‡ 2e3 ! NO3 ‡ H O l† 9† 3 2 2 that organism based on the description in the original which is a suitable thermodynamic representation of ni- literature, those reactions are indicated `as written'. `In- trate reduction to nitrite. This expression would be partic- ferred' is used in cases where there is some ambiguity ularly useful when considering the process going on at an but a reasonable interpretation of the text leads to the electrode (a cathode) where nitrate is reduced as electrons conclusion that the reaction is appropriate. Finally, we enter a solution. Half-cell reactions can be combined into also list organisms as using `hydrogen from an organic coupled redox reactions by conserving electrons; in this source' if it is apparent that the source of reductant is

FEMSRE 711 7-3-01 190 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

Table 4.1 0 31 Values of vG (kJ mol )atPSAT as a function of temperature for compounds in the system H^O Compounds T (³C) 218253745557085100115150200

O2(g) 4.69 1.44 0 32.47 34.12 36.20 39.33 312.48 315.64 318.83 326.33 337.20 O2(aq) 18.82 17.28 16.54 15.18 14.21 12.95 10.95 8.81 6.56 4.19 31.74 311.17 H2O2(aq) 3130.74 3133.01 3134.02 3135.75 3136.93 3138.40 3140.64 3142.91 3145.21 3147.54 3153.10 3161.31 3 HO2 366.61 367.14 367.32 367.57 367.71 367.84 367.96 368.02 367.99 367.91 367.40 365.88 H2O(l) 3235.64 3236.70 3237.18 3238.04 3238.63 3239.39 3240.57 3241.81 3243.08 3244.41 3247.66 3252.69 H2O(g) 3223.86 3226.82 3228.13 3230.39 3231.90 3233.81 3236.69 3239.59 3243.12 3246.07 3253.04 3263.16 OH3 3157.39 3157.36 3157.30 3157.14 3157.00 3156.80 3156.44 3156.02 3155.54 3154.99 3153.44 3150.48 H‡ 000000000000

H2(g) 2.98 0.91 0 31.57 32.63 33.96 35.97 38.00 310.05 312.12 317.00 324.12 H2(aq) 18.89 18.11 17.72 16.99 16.46 15.76 14.62 13.39 12.08 10.68 7.11 1.33

chosen to be H2 for convenience. These designations apply and a temperature at which many thermodynamic proper- to coupled reactions involving H2, such as Reaction 11, ties are measured; 45, 55, and 70³C, three representative rather than fully linked redox reactions. growth temperatures in thermophiles; 85, 100, and 115³C, three representative growth temperatures in hyperthermo- philes, the last being near the current upper temperature 5. Energetics of microbial metabolic reactions limit for a pure isolate in the laboratory; 150 and 200³C, two temperatures at which hyperthermophilic life may be

Is methanotrophy (the consumption of CH4) or meth- thriving, although clear laboratory results have yet to con- 5 0 0 anogenesis (the production of CH4) a viable mode of me- ¢rm this . Values of vG or vGr at temperatures other tabolism in a particular environment? When attempting to than those listed in the present tables can be readily de- isolate from a solfatara a that uses elemen- termined to high precision by interpolation. Using ¢nite tal sulfur, is one likely to ¢nd one that oxidizes sulfur to di¡erence derivatives between the two points on either side sulfate or one that reduces it to sul¢de? In microbial me- of the desired temperature will introduce errors in vG0 on tabolism, acetate is commonly produced as a metabolite, the order of 250 J mol31 or less, which is well within the but also consumed as a carbon source; which of these uncertainties of the accepted values (see also Fig. 5). Ex- processes is energy-yielding in a particular biotope or trapolation below 2³C or above 200³C should be avoided, growth experiment? In order to answer questions of this however, as it may yield values of vG0 that di¡er signi¢- type, the overall Gibbs free energies of the appropriate cantly from those computed with revised HKF equations reactions need to be calculated at the temperature, pres- of state. Thermodynamic calculations at temperatures 6 2 sure, and chemical composition that obtain in the system or s 200³C can be carried out with the software package of interest. In this section, we present and discuss the stan- SUPCRT92 [73] or ORGANOBIOGEOTHERM6. dard and overall Gibbs free energies of compounds and This section is further divided into subsections. We start reactions in autotrophic and heterotrophic microbial me- with the energetics of overall metabolic processes in the tabolism. Because some prefer to think of reaction ener- chemical system H^O and note some of the microbes getics in terms of standard potentials, relations between known to catalyze these speci¢c processes (Section 5.1). standard Gibbs free energies and standard potentials for Section 5.2 deals with compounds and reactions in the oxidation^reduction reactions are also discussed (see Ap- chemical system H^O^N, followed sequentially in further pendix). The focus in this study is on thermophilic Ar- subsections by the systems H^O^S, H^O^N^S, H^O^ chaea and Bacteria, and thus the thermodynamic proper- Cinorganic, H^O^C, H^O^N^C, H^O^S^C, H^O^N^S^ ties are computed as a function of temperature. Although Camino acid, and H^O^S^C^metals/minerals. Section 5.8 the thermodynamic properties for all compounds and re- covers the inorganic aqueous chemistry in the H^O^P sys- actions given in this review can also be calculated as func- tem and demonstrates the need for thermodynamic data as tions of pressure, those included here are limited to PSAT, a function of temperature for organo- com- unless mentioned otherwise. pounds. Finally, although various microorganisms gain In ¢gures depicting solubility and dissociation reactions, metabolic energy from Cl-redox reactions, we decided temperature is continuous from 0^200³C. However, in not to include a discussion in the main body of the text, most ¢gures and tables, we report values of vG0 and vG0 at representative temperatures, which were chosen r 5 as follows: 2³C, the average temperature of the world's Calculations above 100³C are conducted at PSAT, which for 115, 150, and 200³C correspond to 1.70, 4.76, and 15.54 bar, respectively. oceans; 18³C, the average temperature of surface ocean waters; 25³C, the accepted standard reference tempera- 6 Both of these codes are available from Prof. Harold Helgeson at U.C. ture; 37³C, the average body temperature of humans Berkeley.

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 191

Table 4.2 on H2 and O2 allow evaluation of vGr for Reaction A1. If Hydrogen and oxygen metabolic reactions 0 these data are from the gas phase, then values of vGr for A1 H2(aq)+0.5O2(aq)HH2O(l) the reaction involving gases will need to be calculated A2 H2O2(aq)+H2(aq)H2H2O(l) 0 from data in Table 4.1, or values of vGr for the solubility reactions for H2 and O2 from Tables A.3 and A.4 in the 0 because there are currently no known thermophiles that Appendix will need to be included with the values of vGr mediate these processes (J.D. Coates, 1999, personal com- for Reaction A1 in Table 4.3. munication). Instead, we provide standard Gibbs free en- The following example should help to illustrate this 0 ergies for Cl-containing (and other halogen-containing) point, which may be useful for converting values of vGr compounds and redox reactions, and identify mesophilic listed in these tables to values appropriate for a speci¢c 0 microorganisms responsible for their catalysis, in the Ap- application. Converting vGr from Table 4.3 for Reaction pendix. A1: 0:5O aq†‡H aq†HH O l† A1† 5.1. The H^O system 2 2 2 to that for: Aquifex pyrophilus, a hyperthermophile isolated from 0:5O g†‡H g†HH O l† 17† hot marine sediments at the Kolbeinsey Ridge, Iceland 2 2 2 1 0 [82], and other species among the Aqui¢cales gain meta- is accomplished by adding 2vGr for: bolic energy by reducing oxygen (or oxidizing hydrogen) O g†HO aq† G2† and forming water via: 2 2 0 and vGr for: H2 ‡ 0:5O2 ! H2O 15† H g†HH aq† G1† 0 2 2 Values of vGr for this reaction can be calculated from 0 those of vG for O2,H2 and H2O listed in Table 4.1 from Table A.4 in the Appendix. Therefore, using values 0 consistent with: of vGr from the tables in this review: X 0 0 0 0 1 0 0 vGr ˆ e i;rvG 16† vG17 ˆ vGA1 ‡ 2vGG2 ‡ vGG1 18† i 0 31 At 100³C, vGA1 from Table 4.3 is 3258.44 kJ mol , 0 The value of vGr will depend on whether the reaction is those for Reactions G2 and G1 from Table A.4 are 31 31 written to include gases (H2(g), O2(g)) or aqueous species 22.13 kJ mol and 22.20 kJ mol , respectively, and the 31 (H2(aq), O2(aq)), liquid H2O(H2O(l)), or water vapor corresponding value for Reaction 17 is 3225.2 kJ mol , 0 (H2O(v)). Values of vG for all of these chemical species which can also be calculated directly with the values in are given in Table 4.1. Other values of vG0 from Table 4.1 Table 4.1 (thereby illustrating a point about internal con- 0 allow evaluation of vGr with Eq. 16 for the dissociation of sistency of data). 7 H2O (Reaction 2), as well as reactions (A1) and (A2) in In continental or shallow submarine hot springs where Table 4.2, and other reactions that may be of interest in species of Aquifex are found, concentrations of H2(aq) and 0 . Values of vGr for the reactions in O2(aq) can be at or below the equilibrium saturation val- Table 4.2, calculated with Eq. 16 and consistent with data ues8. Activities consistent with these concentrations in in Table 4.1 are listed in Table 4.3. These are followed, in near-surface environments are likely to fall in the ranges Table 4.4, with an inventory of the microorganisms which used to construct the plots in Fig. 7, which show contours are known to use these reactions in their overall metabolic of the overall Gibbs free energy for Reaction A1 (vGA1)at processes. For example, besides A. pyrophilus, at least two 25, 55, 100, and 150³C. The slopes of these contours are dozen other species of microorganisms are known to gain dictated by the stoichiometry of Reaction A1. By compar- metabolic energy by mediating Reaction 15. ing these four plots it can be seen that the value of vGA1 0 Combining values of vGr from Table 4.3 with those of becomes less negative with increasing temperature if the 9 Qr, calculated with compositional constraints on the reac- activities of H2 and O2 are held constant . tants and products from natural systems or laboratory As an example, we can calculate the value of vGA1 with experiments, allows evaluation of vGr in accord with Eq. Eq. 5 for a shallow hot spring in the Baia di Levante on 5, which corresponds to the amount of energy available the island of Vulcano, Italy, close to the site of isolation from the environment for the overall reaction used in me- tabolism. In the case of A. pyrophilus, concentration data 8 In some cases supersaturation of aqueous solutions with gases is possi- ble if they are rapidly cooled, but nucleation of gas bubbles is a relatively 7 Two di¡erent numbering systems for reactions are used throughout this rapid process in natural systems. review. Arabic numerals are used to denote reactions introduced in the text, and capital letters followed by Arabic numerals represent reactions 9 Methods for calculating activities from concentration data are summa- listed in tables. rized in the Appendix.

FEMSRE 711 7-3-01 192 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

Table 4.3 0 31 Values of vGr (kJ mol )atPSAT as a function of temperature for reactions given in Table 4.2 Reaction T (³C) 2 18 25 37 45 55 70 85 100 115 150 200 A1 3263.94 3263.45 3263.17 3262.62 3262.20 3261.63 3260.67 3259.60 3258.44 3257.18 3253.90 3248.44 A2 3359.43 3358.50 3358.07 3357.31 3356.80 3356.14 3355.13 3354.10 3353.03 3351.95 3349.34 3345.40 for [83]. The reported temperature and system on the island of Vulcano, Italy, catalyzes the con- partial pressure of hydrogen gas (P ) of this spring are version of NO3 to NO3 (Reaction B1) and NO3 to NO H2 3 2 2 98³C and 4.8U1035 bar, respectively [81]. The correspond- (Reaction B5) [84]. Several other microbes responsible for 38 ing activity of H2 (3.80U10 ), required to evaluate QA1, mediating the reactions given in Table 5.2 are listed in was computed from the equilibrium constant at 98³C and Table 5.4.

1 bar of the H2 dissolution Reaction G1; the activity of Analogous to the approach described for the H^O sys- 34 O2 (1.64U10 ) was assumed to be in equilibrium with tem above, values of vGr in the H^O^N system can be 9 0 O2(g) in the . The value of QA1 (2.05U10 ) evaluated by combining values of vGr from Table 5.3 with determined with Eq. 6 was combined in Eq. 5 with the those of Qr calculated with compositional data on the 0 31 value of vGA1 (3258.60 kJ mol ) at 98³C and 1 bar to reactants and products in the geochemical or laboratory 31 3 3 yield vGA1 (3192.44 kJ mol ). This calculation shows environment of interest. Activities of NO3 ,NO2 , and H2 that 192.44 kJ per mol of H2(g) consumed is the maximum likely to be encountered in hot springs where A. pyrophilus amount of energy available to A. aeolicus or any other and F. placidus can be found are in the ranges depicted in hyperthermophile catalyzing the knallgas reaction in this Figs. 9^11. In order to accommodate the three composi- 3 3 hot spring on Vulcano. tional variables (H2,NO3 , and NO2 ) in two-dimensional plots, three sets of ¢gures at four temperatures (25, 55, 5.2. The H^O^N system 100, and 150³C) were constructed, each set evaluated at 33 35 a di¡erent value of H2 activity (10 in Fig. 9, 10 in Fig. 37 In the absence of su¤cient free oxygen, denitri¢ers, in- 10, and 10 in Fig. 11). In these ¢gures, values of vGB1 at cluding the thermophiles A. pyrophilus, Thermothrix thio- the four temperatures are shown as contours. As in the para, and Pyrobaculum aerophilum, as well as other groups example for the knallgas reaction discussed above, the of facultative anaerobes may switch from aerobic to an- slopes of the contour lines in Figs. 9^11 are set by the 3 aerobic respiration using NO3 as the terminal electron stoichiometry of reaction (B1). It can be seen in these 3 acceptor. Other microbes carrying out NO3 reduction ¢gures that vGB1 increases with increasing temperature 3 3 are obligate anaerobes, unable to pursue aerobic respira- at constant activities of NO3 ,NO2 , and H2. 3 tion. However, NO3 is not the only N-bearing compound The reactions listed in Table 5.2 are limited to those that involved in microbial metabolism. The biochemical cycling can be linked to speci¢c microorganisms. Thus, this table of nitrogen among its various inorganic forms involves +5, is limited by our ignorance about novel metabolic path- +3, +2, +1, 0, and 33 oxidation states more familiar as ways rather than by reactions that are thermodynamically 3 3 0 NO3 ,NO2 , NO, N2O, N2, and NH3. Values of vG at and geochemically plausible as energy sources for thermo- various temperatures between 0 and 200³C for these com- philes and hyperthermophiles. As an example, many hot pounds as gases or dissolved ions and associated forms, as springs have concentrations of ammonium and nitrate that appropriate, are listed in Table 5.1. Eleven reactions known to be involved in microbial metabolism are listed in Table 5.2, and the locations of each of these reactions in Table 4.4 Microorganisms that use the hydrogen and oxygen reactions speci¢ed in the of nitrogen are shown in Fig. 8. Table 4.2 It can be seen in this ¢gure that ¢ve of the overall reac- Reac- tions (B1, B4, B5, B7, and B8) involve the transfer of only tion one or two electrons, but the others involve the transfer of A1 Acidovorax dela¢eldii, Acidovorax facilis, Alcaligenes as many as three (Reactions B6, B9, and B11), ¢ve (Re- xylosoxidans, Ancylobacter aquaticus, Hydrogenophaga palleronii, action B2), six (Reaction B10), and even eight electrons hydrogenovora, Xanthobacter autotrophicus [379], 0 P. fumarii [9] Sulfolobus acidocaldarius, , (Reaction B3). Values of vGr as a function of temperature for these reactions are listed in Table 5.3. Sulfolobus shibatae, A. brierleyi, A. infernus, M. sedula [293] Among the thermophilic microbes, A. pyrophilus, which Bacillus schlegelii [189] Hydrogenobacter halophilus [225] Hydrogenophilus thermoluteolus [228,229] Calderobacterium can gain metabolic energy from the knallgas reaction as hydrogenophilum [195], M. prunae [296], Hydrogenobacter 3 discussed above, also mediates the reduction of NO3 and thermophilus [226], P. aerophilum [345], A. pyrophilus [82], 3 Hydrogenobacter acidophilus [224], Sulfurospirillum arcachonense NO2 represented by Reactions (B1), (B2), and (B6) [82]. Similarly, the anaerobic hyperthermophile Ferroglobus [380] placidus, isolated from a shallow submarine hydrothermal A2 Acetobacter peroxidans [381]

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 193

Fig. 7. Plots of vG (represented as solid contours) at P and 25, 55, 100, and 150³C for Reaction A1 as a function of log a and log a . The ac- r SAT O2 H2 tivity of H2O(l) is taken to be unity. are out of equilibrium with respect to the reaction: that can obtain metabolic energy by combining ammo- nium and nitrate to form nitrogen. If so, this metabolism ‡ 3 ‡ 1:25NH4 ‡ 0:75NO3 ! N2 aq†‡0:5H ‡ 2:25H2O l† would also tend to acidify the environment, or be a¡ected 19† by changes in pH brought about by other coexisting or- ganisms. In fact, Reaction 19 was proposed more than two It follows that it is plausible that an organism may exist decades ago as a metabolic process in chemosynthetic mi-

Table 5.1 0 31 Values of vG (kJ mol )atPSAT as a function of temperature for compounds in the system H^O^N Compounds T (³C) 218253745557085100115150200

3 NO3 3107.45 3109.87 3110.91 3112.66 3113.81 3115.24 3117.35 3119.44 3121.49 3123.52 3128.14 3134.30 HNO3(aq) 399.44 3102.23 3103.47 3105.64 3107.10 3108.94 3111.75 3114.61 3117.52 3120.47 3127.53 3138.03 3 NO2 329.28 331.35 332.22 333.67 334.62 335.79 337.49 339.15 340.77 342.35 345.84 350.29 HNO2(aq) 347.53 349.68 350.63 352.26 353.36 354.74 356.84 358.95 361.09 363.26 368.40 375.98 NO(g)a 91.39 88.04 86.57 84.03 82.33 80.20 76.99 73.75 70.50 67.23 59.53 48.38 NO(aq)b 104.56 102.87 102.06 100.58 99.53 98.15 95.98 93.67 91.25 88.72 82.46 72.77 a N2O(g) 109.22 105.73 104.20 101.55 99.78 97.55 94.18 90.78 87.36 83.91 75.78 63.94 c N2O(aq) 115.84 114.18 113.38 111.90 110.86 109.48 107.27 104.91 102.41 99.78 93.20 82.83 N2(g) 4.38 1.34 0 32.31 33.85 35.79 38.72 311.66 314.63 317.61 324.63 334.82 N2(aq) 20.15 18.84 18.18 16.98 16.12 14.99 13.18 11.24 9.19 7.02 1.55 37.19 NH3(g) 312.06 315.11 316.45 318.77 320.33 322.28 325.23 328.20 331.20 334.23 341.36 351.76 NH3(aq) 324.30 325.96 326.71 328.02 328.92 330.06 331.82 333.63 335.50 337.42 342.08 349.17 ‡ NH4 376.96 378.68 379.45 380.81 381.72 382.89 384.68 386.50 388.37 390.28 394.86 3101.70 aSee Table A.2 in the Appendix for thermodynamic properties. b 0 0 Obtained using the vGr values for NO(g)HNO(aq) from Plyasunov et al. (2000) [382] together with the value of vG for NO(g) tabulated here. c 0 0 Obtained using the vGr values for N2O(g)HN2O(aq) from Plyasunov et al. (2000) [382] together with the value of vG for N2O(g) tabulated here.

FEMSRE 711 7-3-01 194 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

Table 5.2 Inorganic nitrogen metabolic reactions

3 3 B1 NO3 +H2(aq)HNO2 +H2O(l) 3 ‡ B2 NO3 +2.5H2(aq)+H H0.5N2(aq)+3H2O(l) 3 ‡ B3 NO3 +4H2(aq)+H HNH3(aq)+3H2O(l) 3 3 B4 NO2 +0.5O2(aq)HNO3 3 ‡ B5 NO2 +0.5H2(aq)+H HNO(aq)+H2O(l) 3 ‡ B6 NO2 +1.5H2(aq)+H H0.5N2(aq)+2H2O(l) B7 NO(aq)+0.5H2(aq)H0.5N2O(aq)+0.5H2O(l) B8 0.5N2O(aq)+0.5H2(aq)H0.5N2(aq)+0.5H2O(l) B9 0.5N2(aq)+1.5H2(aq)HNH3(aq) a ‡ 3 B10 NH3(aq)+1.5O2(aq)HH +NO2 +H2O(l) 3 ‡ B11 NH3(aq)+NO2 +H HN2(aq)+2H2O(l) a Drozd (1976) [383] and Suzuki et al. (1974) [384] note that NH3, rather ‡ than NH4 , may be the substrate transferred across the cellular mem- branes. crobes [85], but it has never been observed. Recently, Strous et al. (1999) [86], described the cultivation of an organism able to metabolize a process very similar to Re- action 19, namely the anaerobic oxidation of ammonia to nitrogen using nitrite as the electron acceptor (reaction B11). This reaction too had been expected but went un- detected for decades. Fig. 8. Schematic of the microbial nitrogen redox cycle. The numbers in parentheses next to the species represent the oxidation state of N; the 5.3. The H^O^S system labels next to the reaction arrows denote the reaction listed in Table 5.2 and the number of electrons transferred in the process. The ghastly stench of hydrogen sul¢de is instantly fa- 23 23 23 miliar to anyone who has ever stepped foot on the island (Sox = +7), S2O6 (Sox = +5), S2O5 (Sox = +4), S3O6 1 23 23 1 23 of Vulcano, north of Sicily or visited the Phlegrean solfa- (Sox =+33), S2O4 (Sox = +3), S4O6 (Sox =+22), S2O3 23 23 2 23 tara near Naples, Italy. It is also unforgettable to anyone (Sox = +2), S5O6 (Sox = +2), S5 (Sox = 35), S4 1 23 2 23 who has ever cultured a sulfur reducer such as Pyrodicti- (Sox = 32), S3 (Sox = 33), S2 (Sox = 31). This wealth of um, Acidianus, Thermococcus, Pyrococcus,orDesulfuro- oxidation state possibilities is represented by the 27 sulfur 0 , to name only a few. H2S, in which sulfur is in compounds for which values of vG are listed in Table 6.1, the 32 oxidation state (Sox), is only one of several familiar and leads to a complex inorganic much of 23 23 forms of inorganic sulfur. The others include SO4 ,SO3 , which is mediated by microbes. As an example, 22 reac- and S, in which Sox equals +6, +4, and 0, respectively. In tions known to be conducted by microbes are listed in 0 addition, less common sulfur compounds exhibit a wide Table 6.2, and corresponding values of vGr are given in variety of other oxidation states. Of note in this regard are Table 6.3. It should be recognized that hundreds of other sulfur compounds with two or more S atoms, some of sulfur redox reactions are possible. which have fractional nominal oxidation states. These In addition to simple redox reactions among pairs of compounds include the following, in decreasing order of compounds, several of the reactions listed in Table 6.2 23 Sox, as well as their associated protonated forms: S2O8 involve disproportionation of sulfur among various oxida-

Table 5.3 0 31 Values of vGr (kJ mol )atPSAT as a function of temperature for reactions given in Table 5.2 Reaction T (³C) 218253745557085100115150200 B1 3176.36 3176.29 3176.21 3176.05 3175.90 3175.70 3175.34 3174.92 3174.44 3173.91 3172.49 3170.01 B2 3636.62 3636.09 3635.85 3635.45 3635.18 3634.84 3634.34 3633.84 3633.35 3632.88 3631.86 3630.69 B3 3699.32 3698.63 3698.23 3697.44 3696.85 3696.03 3694.68 3693.18 3691.56 3689.82 3685.39 3678.26 B4 387.58 387.17 386.96 386.57 386.30 385.92 385.33 384.68 384.00 383.27 381.42 378.43 B5 3111.24 3111.53 3111.76 3112.28 3112.71 3113.33 3114.41 3115.68 3117.10 3118.68 3122.92 3130.30 B6 3460.25 3459.80 3459.64 3459.40 3459.27 3459.14 3459.00 3458.92 3458.91 3458.97 3459.37 3460.68 B7 3173.90 3173.19 3172.82 3172.15 3171.65 3170.98 3169.95 3168.82 3167.63 3166.37 3163.25 3158.36 B8 3175.11 3175.08 3175.05 3174.98 3174.92 3174.82 3174.65 3174.44 3174.19 3173.92 3173.21 3172.02 B9 362.70 362.55 362.38 361.99 361.67 361.19 360.34 359.34 358.21 356.94 353.53 347.57 B10 3268.85 3268.01 3267.50 3266.46 3265.66 3264.55 3262.66 3260.54 3258.19 3255.63 3248.81 3237.06 B11 3397.55 3397.25 3397.25 3397.40 3397.60 3397.95 3398.66 3399.58 3400.71 3402.03 3405.85 3413.11

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 195

Table 5.4 vante on Vulcano, Italy [47]. P. occultum was the ¢rst Microorganisms that use the nitrogen reactions speci¢ed in Table 5.2 organism in pure culture able to grow at temperatures Reac- above 100³C, gaining metabolic energy by reducing ele- tion mental sulfur with H2 and producing H2S (Reaction B1 As written: F. placidus [84], A. pyrophilus [82], C19). Several other genera of thermophiles and hyperther- Veillonella alcalescens, Micrococcus denitri¢cans, mophiles (see Table 6.4), both autotrophic and heterotro- Thiobacillus denitri¢cans [6] phic, include species that are known to catalyze this re- Inferred: B. schlegelii [189] C. hydrogenophilum [195] Hydrogen from an organic source: Pseudomonas strain MT-1 duction reaction, including Acidianus, Thermococcus, [385], Silicibacter lacuscaerulensis [386], P. aerophilum [345], Pyrococcus, Hyperthermus, Pyrobaculum, Thermoplasma, Thermothrix thioparus [277,278], Clostridium perfringens, and Staphylothermus. Aerobacter aerogenes, , Pseudomonas aeruginosa, Values of vG as functions of a and a represen- C19 H2 H2S Pseudomonas denitri¢cans, Spirillum itersoni, tative of many hydrothermal systems are shown in Fig. 12. Selenomonas ruminantium [6] B2 As written: A. pyrophilus [82], M. denitri¢cans, These values were calculated at 25, 55, 100, and 150³C T. denitri¢cans [6] with Eq. 5 as described above. It can be seen in Fig. 12 Hydrogen from an organic source: P. aerophilum [345], that at constant values of a , values of vG decrease H2S C19 T. thioparus [277,278], C. perfringens, P. aeruginosa, with increasing values of a at any temperature investi- H2 P. denitri¢cans [6] gated; the decrease of vG is more precipitous at high B3 As written: Ammonifex degensii [187], P. fumarii C19 ([9], V. alcalescens [6] rather than at low temperatures. In other words, values of B4 As written: , Nitrospina, Nitrococcus [387] vGC19 increase with increasing temperature at low values B5 As written: F. placidus [84], M. denitri¢cans, T. denitri¢cans [6] of a , but decrease with increasing temperature at higher H2 Hydrogen from an organic source: T. thioparus [277,278], values of a . Conversely, at constant values of a , values H2 H2 C. perfringens, P. aeruginosa, P. denitri¢cans [6] of vG increase with increasing values of a at any B6 As written: A. pyrophilus [82], M. denitri¢cans, C19 H2S T. denitri¢cans [6], temperature investigated, increasing more dramatically at Hydrogen from an organic source: T. thioparus [277,278], high than at low temperatures. The net e¡ect of the com- C. perfringens, P. aeruginosa, P. denitri¢cans [6] plex dependence of vG on temperature, a , and a is C19 H2 H2S B7 As written: M. denitri¢cans, T. denitri¢cans [6] that organisms such as P. occultum can obtain the most Hydrogen from an organic source: T. thioparus [277,278], metabolic energy from Reaction (C19) at high tempera- C. perfringens, P. aeruginosa, P. denitri¢cans [6] B8 As written: M. denitri¢cans, T. denitri¢cans [6] tures, high activities of H2, and low activities of H2S. Hydrogen from an organic source: T. thioparus [277,278], The lowest amount of energy is available at high temper- C. perfringens, P. aeruginosa, P. denitri¢cans [6] atures, high activities of H2S, and low activities of H2. B9 As written: Methanosarcina barkeri [388], gigas, Observations of this type, coupled with appropriate chem- Desulfovibrio vulgaris, Desulfovibrio desulfuricans, ical analyses, should help to explain the occurrence of P. Desulfovibrio salexigens [389], Desulfovibrio africanus [389,390], Desulfovibrio baculatus [390] occultum in some hydrothermal systems but not in others. B10 As written: Nitrosococcus, , Nitrosospira, Nitrosovibrio [387], Nitrosolobus [391] 5.4. The H^O^N^S system B11 As written: Planctomycete [85,86,392] Metabolic processes are discussed above in which the

reduction (by H2) and oxidation (by O2) of various nitro- 23 tion states. As an example, thiosulfate, S2O3 , can dispro- gen (Table 5.2) or sulfur compounds (Table 6.2) provide 23 portionate to SO4 and H2S (reaction C8). As long as the energy for microorganisms. Additional metabolic process- products are produced in equal proportions, the overall es are known in which the oxidation of sulfur is coupled to oxidation state of sulfur does not change during the reac- the reduction of nitrogen. Five such reactions in which 3 tion. However, the nominal oxidation state of each of the NO3 serves as the electron acceptor and thiosulfate, sul- 23 23 sulfur atoms in S2O3 (Sox = +2) changes to +6 (SO4 )or fur, or sul¢de as the electron donor are listed in Table 6.5; 0 32(H2S) as the reaction proceeds. Although Reaction the corresponding values of vGr as a function of temper- (C8) does not contain H2 or O2, both reduction and oxi- ature are reported in Table 6.6. All ¢ve of these reactions dation occur as the reaction proceeds. Other sulfur dispro- are known to be carried out by thermophiles or hyper- portionation reactions listed in Table 6.2 include (C2), thermophiles, including, for example, T. thiopara, a facul- (C4), (C6), (C7), (C9), (C11), (C13), and (C17). Many of tatively anaerobic facultative chemolithoautotroph iso- the microorganisms known to catalyze the reactions listed lated from a pH-neutral, sul¢de-rich, 74³C hot spring in in Table 6.2 are given in Table 6.4. New Mexico. In the laboratory under anaerobic condi- As noted above, numerous thermophiles and hyperther- tions at temperatures between 62 and 77³C, T. thiopara mophiles gain metabolic energy by oxidizing or reducing can gain metabolic energy from Reactions (C23) and sulfur compounds. One of these is Pyrodictium occultum,a (C25)^(C27). Other microbes experimentally veri¢ed to hyperthermophilic chemolithoautotrophic Archaeon iso- mediate the sulfur^nitrogen redox couples shown in Table lated from shallow marine hot springs in the Baia di Le- 6.5 are listed in Table 6.7, including the hyperthermophiles

FEMSRE 711 7-3-01 196 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

Fig. 9. Plots of vGr (represented as solid contours) at PSAT and 25, 55, 100, and 150³C for Reaction (B1) as a function of log aNO3 and log aNO3 . The 2 3 33 activity of H2(aq) is set at 10 , and the activity of H2O(l) is taken to be unity.

Pyrobaculum, Aquifex, and Ferroglobus. Given the sub- Some Thiobacillus thioparus and Paracoccus strains oxidize stantial variety in oxidation states of inorganic sulfur organosulfur compounds such as carbonyl sul¢de or thio- and nitrogen compounds, it is very likely that the reactions cyanate to sulfate and CO2 (Reactions D2 and D7, respec- listed in Table 6.5 are only a subset of the sulfur^nitrogen tively) to gain metabolic energy [87]. These strains can also redox reactions used by microorganisms. hydrolyze carbonyl sul¢de (Reaction D3) and thiocyanate 3 (Reaction D8) yielding H2S and either CO2 or OCN , 0 5.5. The H^O^Cinorganic system respectively [87]. It should be noted that values of vGr over the temperature range considered here (Table 7.3) For the purpose of this review, we have grouped several for the two hydrolysis Reactions are much greater (less carbon compounds that can have abiotic sources in the H^ negative or even positive) than those of their oxidation

O^Cinorganic system including CH4 and hydrogen cyanide counterparts. (HCN). Values of vG0 as a function of temperature for Of the reactions listed in Table 7.2, autotrophic meth-

`inorganic' carbon species, including several containing N anogenesis from CO2 and H2 (Reaction D1) is by far the or S, are given in Table 7.1. Nine Reactions among these most common and also one of the best characterized of all molecules known to be mediated by microorganisms and metabolic processes in thermophiles [8,88^93]. Species be- 0 values of vGr as a function of temperature for these Re- longing to at least six genera are able to carry out this actions are given in Tables 7.2 and 7.3, respectively. mode of autotrophic methanogenesis, including a signi¢-

Under aerobic conditions, CO and CH4 can be oxidized cant number of thermophiles and hyperthermophiles. As to CO2 (reactions D4 and D9, respectively) by a variety of an example, Methanopyrus kandleri, isolated from heated organisms including members of the genera Bacillus, Pseu- deep sea sediments in the Guaymas Basin and from a domonas, Alcaligenes, and Methylococcus. Reduction (re- shallow marine hydrothermal system on Iceland [94], action D6) and disproportionation (Reaction D5) of CO grows on metabolic energy gained from reaction (D1) at producing CH4 can be mediated by Methanobacterium. temperatures up to 110³C. Many microorganisms respon-

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 197

35 Fig. 10. Same as for Fig. 9, except that the activity of H2(aq) is set at 10 . sible for conducting the reactions given in Table 7.2 are 5.6. The H^O^C, H^O^N^C, H^O^S^C, listed in Table 7.4. and H^O^N^S^Camino acid systems Values of the overall Gibbs free energy for autotrophic methanogenesis from CO2 (vGD1) were calculated in ac- In laboratory growth studies, thermophilic heterotrophs cord with Eq. 5 at 25, 55, 100, and 150³C and are shown commonly utilize complex organic molecules such as pro- in Figs. 13^15. In these ¢gures, constructed for activities teinaceous materials and as carbon and en- 33 35 37 of H2 equal to 10 (Fig. 13), 10 (Fig. 14), and 10 ergy sources. In nature, however, the molecular identities (Fig. 15), values of vGD1 are depicted as contours relative of the requisite organic compounds remain obscure. Ow- 310 to the activities of CH4 and CO2 that range from 10 to ing to an incomplete data set for the thermodynamic prop- 0. It can be seen in these ¢gures that vGD1 is negative at erties of aqueous sugars, peptides, nucleic acid bases, and most conditions considered here, increasing towards less vitamins at elevated temperatures, together with an alarm- exergonic values with increasing temperature at constant ing shortage of organic analyses from hydrothermal sys- activities of H2,CO2, and CH4. Reaction (D1) is ender- tems where heterotrophic thermophiles are known to gonic only at elevated temperatures in combination with thrive, only a limited number of heterotrophic metabolic high activities of CH4 or low activities of CO2 and H2. For reaction types could be included in this study. It may seem example, at representative activities of CH4,H2, and CO2 at ¢rst glance that the plethora of organic compounds in hydrothermal systems equal to 1036,1035, and 1034, listed in Table 8.1 would be su¤cient to characterize a respectively, and at a temperature of 100³C (see Fig. 14), signi¢cant fraction of overall heterotrophic metabolisms. close to the optimum laboratory growth temperature of This is not the case. Because of the dearth of thermody- 31 M. kandleri, vGD1 is equal to 355 kJ mol . Although namic and compositional data, we are limited to evaluat- 0 numerous obligately autotrophic thermophiles, including ing vGr for heterotrophic reactions which involve predom- M. kandleri, have been isolated from hydrothermal ecosys- inantly organic acids, alcohols, or amino acids. The 0 tems, the majority of thermophiles currently in culture are reactions and values of vGr as a function of temperature obligate heterotrophs [8]. in the system H^O^C are given in Tables 8.2 and 8.3,

FEMSRE 711 7-3-01 198 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

37 Fig. 11. Same as for Fig. 9, except that the activity of H2(aq) is set at 10 . respectively. Analogous data are also given for the systems The energetics of redox reactions involving organic car- H^O^N^C (Tables 8.5 and 8.6), H^O^S^C (Tables 8.8 and bon depend signi¢cantly on the type and amount of the

8.9), and H^O^N^S^Camino acid (Tables 8.11 and 8.12). Or- organic species as well as the type and amount of the ganisms known to carry out the reactions listed in Tables electron acceptor. To demonstrate this point, we compare,

8.2, 8.5, 8.8 and 8.11 are listed in Tables 8.4, 8.7, 8.10 and as examples, values of vGr at 100³C for all known hetero- 8.13, respectively. trophic metabolic reactions in Table 8.8 in which sulfate is

Of the Reactions included in this section, only a few reduced to sul¢de, and CO2 is the resultant oxidized car- have been experimentally veri¢ed as overall metabolic pro- bon compound (Reactions E27, E28, E32, E36, E43, E51, cesses in hyperthermophiles. For example, Methanococcus E57, E60, E63, E67, E74, E82, E88, E91^E96). To com- thermolithotrophicus is a methanogen able to dispropor- pute values of the activity product, Qr, in these model 23 tionate formic acid to CH4 and CO2 (Reaction E2). P. calculations, the activities of SO4 and H2S are chosen 34 36 aerophilum can oxidize various carboxylic acids with O2 to be 10 and 10 , respectively, the activities of CO2 as the electron acceptor under aerobic conditions (Reac- and each organic compound are 1034, and the pH is set 3 tions E3 and E5) or with NO3 under anaerobic conditions equal to 6. Values of vGr for all of these reactions were (Reactions E14, E15, E16, and E18). Several species of calculated with Eq. 5 using these activities along with ap- 0 Archaeoglobus gain metabolic energy by catalyzing the ox- propriate values of vGr given in Table 8.9. The temper- idation of formic acid (Reactions E28-E30), acetic acid ature and activities chosen here are not meant to represent (Reaction E33), and (Reactions E43, E45, and a speci¢c type of (although they are E47) in the presence of sulfate or sul¢te. Archaeoglobus reasonable values for some hot springs), but rather these vene¢cus can also metabolize with sul¢te as the values are used to permit evaluation of vGr and to show electron acceptor (Reaction E69). The facultative auto- the direct e¡ect of the speci¢c organic substrate on vGr at troph Thermoproteus tenax can grow heterotrophically isochemical, isothermal, and isobaric conditions. 0 by using elemental sulfur to oxidize formic acid (Reaction Values of vGr and vGr at 100³C and the geochemical E31), (Reaction E66), or ethanol (Reaction conditions noted above are given in Table 8.14 for a sub- E73). set of coupled organic carbon/inorganic sulfur redox reac-

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 199

Table 6.1 0 31 Values of vG (kJ mol )atPSAT as a function of temperature for compounds in the system H^O^S Compound T (³C) 2 18 25 37 45 55 70 85 100 115 150 200

23 SO4 3743.74 3744.30 3744.46 3744.63 3744.68 3744.68 3744.56 3744.32 3743.94 3743.44 3741.72 3737.75 3 HSO4 3752.89 3754.88 3755.76 3757.27 3758.29 3759.56 3761.49 3763.43 3765.38 3767.33 3771.89 3778.22 23 SO3 3486.98 3486.78 3486.60 3486.18 3485.84 3485.35 3484.48 3483.47 3482.30 3481.00 3477.35 3470.48 3 HSO3 3524.50 3526.75 3527.73 3529.41 3530.52 3531.92 3534.02 3536.12 3538.21 3540.31 3545.13 3551.79 SO2(aq) 3297.64 3300.05 3301.17 3303.16 3304.53 3306.29 3309.03 3311.88 3314.83 3317.88 3325.32 3336.72 SO2(g) 3294.52 3298.46 3300.19 3303.18 3305.19 3307.70 3311.49 3315.32 3319.17 3323.05 3332.19 3345.49 23 S2O3 3520.79 3522.10 3522.59 3523.33 3523.78 3524.28 3524.92 3525.44 3525.83 3526.10 3526.21 3524.89 3 HS2O3 3529.28 3531.31 3532.21 3533.74 3534.77 3536.06 3538.01 3539.97 3541.93 3543.89 3548.46 3554.80 H2S2O3(aq) 3531.33 3534.25 3535.56 3537.84 3539.39 3541.37 3544.38 3547.47 3550.61 3553.83 3561.55 3573.14 23 S2O4 3598.07 3599.74 3600.41 3601.46 3602.12 3602.89 3603.96 3604.91 3605.76 3606.49 3607.74 3608.17 3 HS2O4 3611.17 3613.57 3614.63 3616.48 3617.73 3619.29 3621.68 3624.10 3626.54 3629.01 3634.80 3643.04 H2S2O4(aq) 3611.97 3615.24 3616.73 3619.32 3621.09 3623.34 3626.80 3630.34 3633.97 3637.68 3646.64 3660.13 23 S2O5 3788.16 3790.03 3790.78 3791.99 3792.75 3793.65 3794.91 3796.07 3797.13 3798.07 3799.83 3801.01 23 S2O6 3963.42 3965.61 3966.51 3967.97 3968.91 3970.03 3971.62 3973.12 3974.52 3975.82 3978.41 3980.85 23 S2O8 31109.30 31113.30 31115.00 31118.00 31119.90 31122.20 31125.80 31129.20 31132.60 31135.90 31143.40 31153.20 23 S3O6 3954.77 3957.16 3958.14 3959.76 3960.79 3962.04 3963.84 3965.54 3967.15 3968.66 3971.76 3974.96 23 S4O6 31034.50 31038.80 31040.60 31043.60 31045.70 31048.10 31051.80 31055.50 31059.10 31062.60 31070.50 31080.90 23 S5O6 3954.12 3956.96 3958.14 3960.11 3961.39 3962.95 3965.21 3967.39 3969.48 3971.48 3975.77 3980.73 S(s) 0.71 0.22 0 30.39 30.65 30.99 31.51 32.04 32.59 33.17 34.70 37.08 HS3 13.63 12.45 11.97 11.17 10.66 10.04 9.16 8.33 7.55 6.82 5.33 3.85

H2S(aq) 325.21 327.06 327.92 329.47 330.55 331.94 334.12 336.39 338.76 341.23 347.30 356.69 H2S(g) 328.86 332.12 333.56 336.04 337.70 339.79 342.93 346.10 349.30 352.51 360.10 371.12 S2(g) 84.52 80.89 79.30 76.55 74.71 72.40 68.92 65.42 61.90 58.35 50.00 37.90 23 S2 80.43 79.72 79.50 79.22 79.09 79.00 78.99 79.12 79.38 79.78 81.30 85.08 23 S3 75.41 74.12 73.63 72.90 72.46 71.97 71.35 70.85 70.47 70.22 70.16 71.56 23 S4 71.63 69.77 69.03 67.84 67.09 66.21 64.98 63.86 62.85 61.96 60.33 59.37 23 S5 69.11 66.68 65.68 64.04 62.98 61.71 59.87 58.13 56.49 54.94 51.76 48.44 tions. Each reaction is of the type pound, which is propanol with an average nominal oxida- tion state of each carbon equal to 32; similarly, that the aC ‡ bSO23 ‡ cH‡ ˆ dCO ‡ eH S ‡ f H O 20† org 4 2 2 2 lowest energy yield is for the oxidation of the least reduced where a, b, c, d, e, and f represent the stoichiometric re- species, which is lactic acid with an average nominal oxi- action coe¤cients for the balanced chemical reaction, and dation state of each carbon equal to 0. This, however, is

Corg stands for any organic compound of interest. It can incorrect. The oxidations of these three compounds, rep- be seen in Table 8.14 that the amount of metabolic energy resented by Reactions (E36), (E43), and (E74), respec-

(vGr) released by these di¡erent heterotrophic reactions tively, yield 3208.50, 3258.72, and 3280.69 kJ per mol varies tremendously among the di¡erent organic sub- of carbon substrate. The oxidation of propanoic acid with strates. Per mol of organic carbon species metabolized, an average nominal oxidation state of each carbon equal values of vGr at 100³C range from 360.15 kJ for the to 32/3, intermediate to propanol and lactic acid, yields oxidation of aqueous formic acid (Reaction E28) to the lowest amount of energy. It follows that propanoic 31392.50 kJ for the oxidation of liquid hexadecane (Re- acid is less unstable than the other compounds and may action E95). Per mol of sulfate reduced, values of vGr at be more likely to be metastably preserved. This may ex- 100³C range from 363.05 kJ for the oxidation of CH4 plain the common occurrence of propanoic acid rather (Reaction E27) to 3240.59 kJ for the oxidation of formic than lactic acid or propanol in geologic £uids [95^97]. It acid (Reaction E28). Note that Reaction (E28) yields the should be emphasized that the relative positions with re- lowest amount of energy per mol of carbon species oxi- spect to energy yield of these three reactions, and in fact dized but the highest amount of energy per mol of sulfate all reactions considered here, may change considerably as reduced. It should perhaps be noted that environmental temperature, pressure, and the chemical composition of constraints determine the limiting reactants. the system change. It may be useful to compare the energy yield from the oxidation of di¡erent organic species with the same num- 5.7. The H^O^S^C^metals/minerals system ber of carbon atoms such as, for example, propanoic acid, lactic acid, and propanol, each of which is a three-carbon Sluggish redox reactions involving a host of other ele- compound. One might be tempted to assume that the en- ments can serve as sources of energy for thermophiles and ergy yield is highest for oxidizing the most reduced com- hyperthermophiles, and these reactions are often coupled

FEMSRE 711 7-3-01 200 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

Table 6.2 levels that are economically viable. As a consequence, Inorganic sulfur metabolic reactions there is an enormous scienti¢c literature on geochemical 23 ‡ C1 SO4 +4H2(aq)+2H HH2S(aq)+4H2O(l) processes involving oxidation, reduction, transport, and C2 4SO23+2H‡H3SO23+H S(aq) 3 4 2 deposition of these elements, and numerous experimental C3 SO23+3H (aq)+2H‡HH S(aq)+3H O(l) 3 2 2 2 investigations of phase equilibria, calorimetry, solubility, C4 SO2(aq)+H2O(l)+S(s)HH2S2O3(aq) 23 23 ‡ dissolution kinetics, crystal chemistry, aqueous speciation, C5 S2O3 +2O2(aq)+H2O(l)H2SO4 +2H 23 23 23 C6 6S2O3 +5O2(aq)H4SO4 +2S4O6 adsorption, and ion exchange. As a result, there are ther- 23 23 ‡ C7 5S2O3 +H2O(l)+4O2(aq)H6SO4 +2H +4S(s) modynamic data for numerous oxide, sul¢de, carbonate, C8 S O23+H O(l)HSO23+H S(aq) 2 3 2 4 2 and silicate minerals containing these elements, as well as 23 23 C9 S2O3 HSO3 +S(s) 23 ‡ for their aqueous ions, hydrolysis products, and com- C10 S2O3 +2H +4H2(aq)H2H2S(aq)+3H2O(l) 23 23 ‡ plexes. C11 4S2O4 +4H2O(l)H3H2S(aq)+5SO4 +2H 23 23 ‡ C12 S3O6 +2O2(aq)+2H2O(l)H3SO4 +4H Standard Gibbs free energies for minerals and aqueous 23 23 23 ‡ C13 S3O6 +H2O(l) = SO4 +S2O3 +2H solutes containing these elements are listed in Table 9.1. C14 2S O23+6H O(l)+7O (aq)H8SO23+12H‡ 4 6 2 2 4 An enormous number of reactions can be written involv- 23 23 ‡ C15 S4O6 +H2(aq)H2S2O3 +2H 23 ‡ ing these minerals and aqueous species, but we have se- C16 S(s)+1.5O2(aq)+H2O(l)HSO4 +2H 23 ‡ lected reactions that microorganisms have been shown to C17 4S(s)+4H2O(l)HSO4 +3H2S(aq)+2H ‡ 3 C18 S(s)+O2(aq)+H2O(l)HH +HSO3 conduct, or which can be inferred from reports in the C19 S(s)+H2(aq)HH2S(aq) literature. Inorganic reactions are listed in Table 9.2, and C20 H S(aq)+2O (aq)HSO23+2H‡ 0 2 2 4 corresponding values of vG are given in Table 9.3. Many C21 2H S(aq)+2O (aq)HS O23+H O(l)+2H‡ r 2 2 2 3 2 microbes known to catalyze the reactions in Table 9.2 are C22 H S(aq)+0.5O (aq)HS(s)+H O(l) 2 2 2 listed in Table 9.4. Reactions involving these metals or minerals and organic compounds are listed in Table 9.5, 0 with redox reactions in the H^O^N^S^C system. Reac- with values of vGr given in Table 9.6. Microbes associated tions involving iron and are the most familiar, in the literature with the metabolic processes represented but natural redox disequilibria occur in geochemical pro- in Table 9.5 are listed in Table 9.7. The following exam- cesses involving V, Cr, Cu, As, Se, Ag, W, Mo, Au, Hg, ples should help to illustrate the various types of processes and U as well. These elements are typically present at low involving these elements. In some cases, the distinctions concentrations in most natural settings, and locations between these processes are rather subtle. where they are concentrated tend to be ore deposits. Re- Pyrite (FeS2) oxidation is an energy-yielding process dox disequilibria are a large part of the explanation for conducted by several species of aerobic thermophiles, why these elements are concentrated in ore deposits to with a subtle distinction of whether both the sulfur and

Table 6.3 0 31 Values of vGr (kJ mol )atPSAT as a function of temperature for reactions given in Table 6.2 Reaction T (³C) 218253745557085100115150200 C1 3299.58 3302.00 3303.08 3304.96 3306.24 3307.85 3310.33 3312.86 3315.46 3318.13 3324.67 3335.03 C2 3308.53 3312.86 3314.91 3318.62 3321.21 3324.58 3329.89 3335.49 3341.39 3347.55 3363.05 3388.02 C3 3301.82 3304.71 3306.04 3308.38 3309.98 3312.04 3315.22 3318.52 3321.94 3325.48 3334.27 3348.28 C4 1.23 2.28 2.79 3.74 4.42 5.31 6.73 8.26 9.90 11.63 16.13 23.35 C5 3768.68 3764.38 3762.23 3758.24 3755.38 3751.59 3745.53 3739.02 3732.09 3724.75 3706.09 3675.58 C6 32013.30 32008.60 32006.20 32001.70 31998.40 31994.10 31987.10 31979.70 31971.70 31963.30 31941.90 31907.60 C7 31695.30 31686.90 31682.80 31675.30 31670.00 31663.10 31652.00 31640.30 31628.00 31615.20 31583.50 31533.00 C8 312.52 312.57 312.61 312.72 312.82 312.95 313.19 313.47 313.80 314.16 315.15 316.87 C9 34.53 35.53 35.98 36.76 37.28 37.94 38.93 39.93 40.93 41.93 44.15 47.33 C10 3312.10 3314.57 3315.70 3317.69 3319.06 3320.80 3323.52 3326.33 3329.26 3332.29 3339.82 3351.90 C11 3459.50 3456.93 3455.71 3453.53 3452.01 3450.07 3447.05 3443.91 3440.65 3437.28 3428.89 3415.39 C12 3842.80 3836.93 3833.95 3828.40 3824.41 3819.11 3810.60 3801.42 3791.63 3781.22 3754.59 3710.57 C13 374.12 372.54 371.72 370.17 369.03 367.52 365.07 362.41 359.54 356.47 348.51 334.99 C14 32598.70 32577.70 32567.20 32547.80 32533.80 32515.50 32486.00 32454.40 32420.80 32385.30 32294.60 32145.90 C15 325.94 323.55 322.32 320.03 318.37 316.17 312.62 38.78 34.68 30.30 10.97 29.78 C16 3537.03 3533.75 3532.09 3528.97 3526.72 3523.73 3518.90 3513.69 3508.10 3502.14 3486.75 3461.23 C17 120.37 120.44 120.51 120.67 120.82 121.03 121.41 121.89 122.47 123.20 125.84 131.23 C18 3308.39 3307.55 3307.09 3306.16 3305.46 3304.49 3302.88 3301.08 3299.09 3296.91 3291.03 3280.86 C19 344.81 345.39 345.64 346.07 346.35 346.71 347.23 347.74 348.25 348.73 349.71 350.95 C20 3756.16 3751.81 3749.62 3745.51 3742.56 3738.64 3732.34 3725.54 3718.29 3710.59 3690.94 3658.72 C21 3743.64 3739.24 3737.00 3732.79 3729.74 3725.69 3719.15 3712.07 3704.49 3696.43 3675.79 3641.85 C22 3219.13 3218.06 3217.53 3216.55 3215.84 3214.92 3213.44 3211.86 3210.19 3208.45 3204.20 3197.48

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 201

Table 6.4 Table 6.4 (continued) Microorganisms that use the sulfur reactions speci¢ed in Table 6.2 Reac- Reac- tion tion C17 As written: D. sulfoexigens [399], D. thiozymogenes, C1 As written: Archaeoglobus lithotrophicus [37], Desulfotomaculum Desulfobulbus propionicus [400] auripigmentum [393], Desulfacinum infernum [206], C18 As written: T. thiooxidans, T. thioparus [381] Desulfonatronum lacustre [394], Thermodesulfobacterium mobile C19 As written: P. occultum, P. brockii [353], A. infernus, A. brierleyi [265], Thermodesulfobacterium commune [263], Desulfotomaculum [292], A. degensii [187], T. tenax [375,377], Thermoproteus putei [175], Desulfotomaculum luciae [175,208], Archaeoglobus neutrophilus, T. maritimus [375], P. islandicum [346], profundus [331], Thermodesulfovibrio yellowstonii [267], A. pyrophilus [82], A. ambivalens [289^291], Desulfurella Desulfotomaculum kuznetsovii [207], Desulfotomaculum kamchatkensis, Desulfurella propionica [214], geothermicum [35], Desulfonatronovibrio hydrogenovorans [395], D. thermolithotrophum [216], Hyperthermus butylicus [338], Desulfotomaculum thermocisternum [180], Desulfotomaculum Stetteria hydrogenophila [355] Stygiolobus azoricus [312], thermosapovorans [212], A. degensii [187], Desulfotomaculum S. arcachonense [380] australicum [170], Desulfotomaculum halophilum [178], Hydrogen from an organic source: Thermococcus litoralis Desulfobulbus rhabdoformis [396], D. desulfuricans [381], [368,369], Thermococcus zilligii [323,324], Thermococcus Desulfotomaculum thermoacetoxidans [210] alcaliphilus [360], Pyrobaculum organotrophum [346], Hydrogen from an organic source: Archaeoglobus fulgidus Thermoproteus uzoniensis [378], Thermoplasma acidophilum, [328^330], Thermocladium modestius [259] T. volcanium [325], Thermo¢lum pendens [376], C2 As written: Desulfovibrio sulfodismutans [397,398], Desulfocapsa [351], Thermococcus profundus [371], [363], sulfoexigens [399], Desulfocapsa thiozymogenes [400] Desulfurococcus mucosus, Desulfurococcus mobilis [337], C3 As written: D. desulfuricans [381], D. infernum [206], D. lacustre Thermococcus stetteri [373], Pyrococcus abyssi [347], Pyrococcus [394], A. vene¢cus [295], D. putei [175], A. profundus [331], furiosus [349], [350], P. abyssi [352], T. yellowstonii [267], D. kuznetsovii [207], D. hydrogenovorans T. modestius [259], Thermococcus acidaminovorans [358], [395], D. thermocisternum [180], D. thermosapovorans [212], Thermococcus guaymasensis, Thermococcus aggregans [359], D. halophilum [178], D. rhabdoformis [396], Desulfurobacterium Thermococcus chitonophagus [364], Thermococcus barossii [362], thermolithotrophum [216], Pyrodictium brockii [352] Thermococcus fumicolans [365], Thermococcus gorgonarius [366], Hydrogen from an organic source: A. fulgidus [328^330], Thermococcus hydrothermalis [367], Thermococcus paci¢cus [214], Pyrobaculum islandicum [346] Thermococcus siculi [372], Thermosipho africanus [273], C4 As written: Thiobacillus thiooxidans, T. thioparus [381] T. maritima [287], [288], Desulfurococcus C5 As written: Thiobacillus novellus [381], A. pyrophilus [82], amylolyticus [336], Staphylothermus marinus [354] P. aerophilum [345], Thermothrix azorensis [276], T. thiopara C20 As written: Thiovulum, [409], T. chilensis [403], [277,278], Thiobacillus hydrothermalis [401], Thiomicrospira T. hydrothermalis [401], Thiobacillus propserus [406], crunogena [402], Thiomicrospira chilensis [403] T. crunogena [402], T. azorensis [276], S. hakonensis [316], C6 As written: Thiobacillus neapolitanus [381] T. thioparus [410] C7 As written: T. thioparus [381] C21 As written: T. thioparus [410] C8 As written: D. sulfodismutans [397,398], D. sulfoexigens [399], C22 As written: T. thioparus [410], Thiovulum [409], D. thiozymogenes [400], D. hydrogenovorans [395] Beggiatoa [407^409] C9 As written: purple and green photosynthetic Bacteria [404] C10 As written: A. fulgidus [329], D. infernum [206], F. placidus [84], D. lacustre [394], P. occultum [352], A. vene¢cus [295], D. putei iron are oxidized as in: [175], D. luciae [175,208], A. profundus [331],T. yellowstonii [267], D. kuznetsovii [207], D. thermocisternum [180], 2FeS ‡ 7:5O aq†‡H O l†!2Fe3‡ ‡ 4SO23 ‡ 2H‡ D. thermosapovorans [212], D. thermolithotrophum [216], 2 2 2 4 D. australicum [178], D. rhabdoformis [396], Thermotoga F5† subterranea [281] Hydrogen from an organic source: T. modestius [259], or whether only the sulfur is oxidized as in: P. islandicum [346], Pyrodictium abyssi [352], Thermotoga el¢i [279], Thermotoga hypogea [280] 2‡ 23 ‡ FeS2 ‡ 3:5O2 aq†‡H2O l†!Fe ‡ 2SO ‡ 2H C11 As written: D. sulfodismutans [397,398] 4 C12 As written: Thiobacillus tepidarius, T. neapolitanus [87] F6† C13 As written: T. tepidarius, T. neapolitanus [87] C14 As written: T. neapolitanus [381], T. chilensis [403], In both cases, pyrite oxidation yields sulfate and T. hydrothermalis [401], T. azorensis [276], Sulfolobus hakonensis which are capable of dissolving minerals and leaching [316], T. tepidarius [87] many other elements from pyrite-containing rocks. In C15 Hydrogen from an organic source: Bacterium paratyphosum B [405] C16 As written: T. thioparus [381], T. thiooxidans, T. ferrooxidans the case of the former reaction, the ferric ions produced [387], A. pyrophilus [82], A. infernus, A. brierleyi [292], Acidianus are likely to precipitate as ferric hydroxide, oxide, or oxy- ambivalens [289^291], M. sedula [297], M. prunae [296], S. hydroxide phases, and the variable thermodynamic prop- acidocaldarius [313], S. solfataricus [320], S. metallicus [317], erties of these possible products will in£uence the total Sulfolobacillus thermosul¢dooxidans [246], Sulfobacillus amount of energy available. acidophilus [245], S. shibatae [318,319], S. hakonensis [316], S. yellowstonii [322], Sulfurococcus mirabilis [321], T. thiopara Thiobacillus ferrooxidans has been shown to use Reac- [277,278], T. azorensis [276], T. prosperus [406], tion (F5) to completely oxidize the sulfur and iron in pyrite, T. hydrothermalis [401], T. chilensis [403], T. crunogena [402], as implied by its name. Other organisms such as M. sedula Beggiatoa [407^409], Thiovulum [409] and Metallosphaera prunae and are

FEMSRE 711 7-3-01 202 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

Fig. 12. Plots of vG (represented as solid contours) at P and 25, 55, 100, and 150³C for Reaction (C19) as a function of log a and log a . The r SAT H2 S H2 activity of H2O(l) is taken to be unity. all known to use reaction Reaction (F6), and have not ianus brierleyi. Chalcopyrite (CuFeS2) oxidation, corre- been shown to oxidize iron in pyrite. On the other hand, sponding to Reaction (F8), requires the consumption of Sulfurococcus yellowstonii, Thiobacillus prosperus, and H‡. Many organisms capable of other sul¢de oxidation Sulfobacillus thermosul¢dooxidans will use either reaction reactions are capable of oxidizing chalcopyrite. Because Reaction (F5) or Reaction (F6) as energy sources. All of this reaction has H‡ as a reactant, it would be enhanced these organisms, and no doubt many others, are likely to by the simultaneous oxidation of pyrite in which H‡ is a be the agents of pyrite oxidation and acid generation that product. leads to metal leaching and contamination of ground The heterotrophic reactions in Table 9.5, in which or- water near mine dumps and tailings piles [98^102]. This ganic compounds and metals or semi-metals are coupled, same microbially driven leaching process is also the foun- all involve reduction of the inorganic compounds. Inor- dation of modern methods to extract copper and other ganic redox couples for which speci¢c heterotrophic Re- metals from ore which is subsequently removed from so- actions are identi¢ed include FeIII^FeII,CoIII^CoII,AsV^ lution through electrolysis in an overall process that is AsIII,SeVI^Se0,SeVI^SeIV,SeIV^Se0, and UVI^UIV, but considerably less costly economically and environmentally inferences about many other couples including VV^VIII, than smelting [103,104]. CrVI^CrIII,MnVI^MnIII,MnIII^MnII,CuII^CuI,CuII^ In contrast to pyrite oxidation, several other microbially Cu0,AgI^Ag0, and AuIII^Au0, can be drawn from the mediated sul¢de oxidation reactions are either pH inde- microbiological and geochemical literature [105^115]. pendent or proceed with the consumption of H‡. Reac- tions (F7), (F9), (F10), and (F11) are examples of the Table 6.5 oxidation of pyrrhotite (FeS), covellite (CuS), sphalerite Mixed metabolic reactions involving S, N, H and O compounds

(ZnS), and galena (PbS) in which the sul¢de is oxidized 23 3 23 ‡ C23 5S2O3 +8NO3 +H2O(l)H10SO4 +4N2(aq)+2H to sulfate without generation of sulfuric acid. Members of 3 23 ‡ C24 5S(s)+6NO3 +2H2O(l)H5SO4 +3N2(aq)+4H 3 3 the thermophilic genera Sulfolobus, Metallosphaera, Sul- C25 NO3 +H2S(aq)HNO2 +H2O(l)+S(s) 3 ‡ furococcus, Sulfolobacillus, and Thiobacillus conduct these C26 2NO3 +5H2S(aq)+2H HN2(aq)+5S(s)+6H2O(l) C27 8NO3+5H S(aq)H4N (aq)+5SO23+4H O(l)+2H‡ reactions, and reaction (F10) can also be inferred for Acid- 3 2 2 4 2

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 203

Table 6.6 0 31 Values of vGr (kJ mol )atPSAT as a function of temperature for reactions given in Table 6.5 Reaction T (³C) 218253745557085100115150200 C23 33657.59 33641.55 33634.49 33622.38 33614.29 33604.17 33588.98 33573.76 33558.52 33543.23 33507.25 33454.68 C24 32545.80 32533.47 32527.93 32518.22 32511.64 32503.29 32490.51 32477.45 32464.06 32450.32 32416.33 32363.73 C25 3131.56 3130.90 3130.57 3129.98 3129.55 3128.99 3128.11 3127.17 3126.19 3125.18 3122.78 3119.06 C26 31049.22 31045.22 31043.48 31040.52 31038.60 31036.14 31032.50 31028.97 31025.48 31022.12 31015.15 31006.61 C27 33595.02 33578.69 33571.40 33558.75 33550.24 33539.43 33523.02 33506.42 33489.54 33472.43 33431.48 33370.35

Among the organisms that mediate the reactions listed in 5.8. The H^O^P system Table 9.5 only Bacillus infernus is a thermophile, able to grow in the laboratory between 45 and 60³C. B. infernus, Phosphorus is an essential nutrient not only in microbial isolated from V2700 m below the surface in the Taylors- metabolism, but in the metabolic processes of all life. ville Triassic Basin, VA, USA [116], is a strict anaerobe However, the P involved in metabolic reactions generally that can grow by mediating reactions (F14) and (F20). does not undergo oxidation or reduction; by far the most The other Reactions are known from mesophiles, but dominant redox state of P in organic and inorganic phos- there is no obvious thermodynamic reason that precludes phorus-containing compounds is +5, as in phosphate and thermophiles from their use. We have included these reac- pyrophosphate. Perhaps because make up the 0 tions and their values of vGr in Table 9.6 in the hope that majority of phosphorus-containing compounds in meta- these data may help in the design of growth media for bolic reactions, the thermodynamic properties of phospho- isolating thermophilic heterotrophs that use these energy rus molecules in other redox states have not received much sources in natural systems. Recent work from Hot Creek, attention. In addition to the various protonated and California [117] suggests that microbial oxidation deprotonated forms of phosphate and pyrophosphate, val- 0 0 occurs at elevated temperatures, and vGr values for reac- ues of vG as a function of temperature can be calculated tions such as (F22), (F23), and (F28) at high temperatures only for a few P-compounds in which P is in the +3 or may help to design media for isolating these organisms. It +1 oxidation state, as in phosphite and hypophosphite should be noted that combining data from Tables 8.1 and (Table 9.8). 0 9.1 allows calculation of vGr for thousands of heterotro- Thermodynamic properties at elevated temperatures of phic reactions involving inorganic redox couples. organo-phosphates are extremely sparse although these Also listed in Table 9.1 are data for aqueous species and compounds are central to numerous metabolic pathways, minerals containing Mg, Ca, Co, Ni, Zn, and Pb, which including known and proposed pathways in thermophiles are involved in reactions that can a¡ect microbial ener- and hyperthermophiles. For example, glucose 6-phos- getics although these elements do not exhibit redox phate, glyceraldehyde 3-phosphate, and phosphoenolpyru- changes in natural processes. For example, the availability vate are merely three of the numerous P-containing inter- 3 of HCO3 in a natural environment is often a function of mediates in the Entner^Doudoro¡ pathway in carbonate equilibria involving calcite (CaCO3) and other [123] and in the Embden^Meyerhof pathway in the anaer- carbonate minerals, through reactions such as: obic hyperthermophilic Bacterium Thermotoga maritima [124]. 2-Phosphoglycerate, phosphoenolpyruvate, and ace- Ca2‡ ‡ HCO3 ! calcite ‡ H‡ 21† 3 tyl-CoA are P-containing intermediates in the proposed 3 Autotrophic reactions dependent on HCO3 or CO2(aq) pyrosaccharolytic pathway of metabolism may be regulated by the presence of carbonate minerals, in hyperthermophilic Archaea [8]. In the oxidative and 3 and heterotrophic reactions that produce HCO3 or reductive tricarboxylic (or citric) acid (TCA) cycle used CO2(aq) can be responsible for the precipitation of these by heterotrophic and autotrophic microbes, respectively, minerals. Indeed, there are numerous examples of carbo- nate minerals in sedimentary rocks with carbon isotopic compositions indicative of an organic source for the car- Table 6.7 Microorganisms that use the reactions speci¢ed in Table 6.5 bon [118^122]. The extent to which this oxidation of car- bon is microbially mediated is typically unknown. As an- Reac- tion other example, the concentration of Pb in a solution will a¡ect the availability of energy from the dissolution of C23 T. denitri¢cans [381], P. aerophilum [345], A. pyrophilus [82], T. thioparus [277,278] galena (PbS) C24 T. denitri¢cans [381], A. pyrophilus [82], Thioploca chileae, Galena ‡ 2O aq†!Pb2‡ ‡ SO23 F11† Thioploca araucae [411] 2 4 C25 F. placidus [84], T. thioparus [277,278] even though the energy is obtained through oxidation of C26 T. chileae, T. araucae [411], T. thioparus [277,278] sul¢de to sulfate. C27 T. chileae, T. araucae [411], T. thioparus [277,278]

FEMSRE 711 7-3-01 204 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

Table 7.1 0 31 Values of vG (kJ mol )atPSAT as a function of temperature for inorganic compounds in the system H^O^N^S^Cinorganic Compounds T (³C) 2 18 25 37 45 55 70 85 100 115 150 200

CO2(g) 3389.48 3392.87 3394.36 3396.93 3398.66 3400.83 3404.10 3407.40 3410.73 3414.08 3421.99 3433.51 CO2(aq) 3383.51 3385.17 3385.98 3387.44 3388.48 3389.84 3391.99 3394.26 3396.66 3399.17 3405.42 3415.22 32 CO3 3528.83 3528.31 3527.98 3527.32 3526.81 3526.10 3524.91 3523.56 3522.07 3520.43 3515.98 3507.92 3 HCO3 3584.63 3586.25 3586.94 3588.12 3588.89 3589.86 3591.29 3592.71 3594.11 3595.49 3598.61 3602.71 COS(g) 3160.36 3164.03 3165.64 3168.43 3170.30 3172.65 3176.20 3179.77 3183.38 3187.01 3195.59 3208.07 CO(g) 3132.65 3135.79 3137.17 3139.55 3141.14 3143.14 3146.16 3149.19 3152.25 3155.32 3162.56 3173.04 CO(aq) 3117.91 3119.31 3120.01 3121.30 3122.23 3123.45 3125.42 3127.52 3129.76 3132.13 3138.11 3147.70 CN3 174.63 173.04 172.38 171.26 170.54 169.65 168.34 167.06 165.82 164.62 161.95 158.65 HCN(aq) 122.36 120.52 119.66 118.12 117.06 115.68 113.54 111.30 108.97 106.57 100.65 91.55 OCN3 394.88 396.65 397.41 398.67 399.50 3100.52 3102.04 3103.52 3104.96 3106.38 3109.55 3113.62 SCN3 96.08 93.73 92.71 90.99 89.85 88.43 86.32 84.22 82.14 80.08 75.36 68.97

CH4(g) 346.47 349.42 350.72 352.97 354.47 356.36 359.22 362.10 365.02 367.95 374.89 385.01 CH4(aq) 332.71 333.87 334.46 335.57 336.38 337.47 339.23 341.12 343.17 345.34 350.87 359.83 as well as in the partial TCA cycle in methanogens, acetyl^ base, nucleoside, nucleotide, or nucleic acid. Because or- and succinyl^CoA, both of which contain several phos- gano-phosphates are ubiquitous in assimilatory and dis- phate groups, serve as intermediates. Nicotinamide ad- similatory metabolic processes, the dearth of vG0 values enine dinucleotide phosphate in its protonated (NADPH) as a function of temperature for this class of compounds and deprotonated (NADP‡) forms serve as electron donor currently prohibits the quantitative evaluation of the en- and acceptor, respectively, in a number of microbes that ergetics for many stepwise reactions in metabolic pathways use the Entner^Doudoro¡ and Embden^Meyerhof path- of thermophiles and hyperthermophiles. Consequently, we ways, the TCA cycle, glycine, sarcosine, or betaine reduc- are limited in this review to tabulating values of vG0 as a tion reactions, and the of peptides [8,123^ function of temperature for Pi, phosphite, and hypophos- 125]. Cleavage of the terminal phosphate group from ad- phite (Table 9.8). Because redox reactions among these enosine triphosphate (ATP) to yield adenosine diphos- compounds cannot currently be linked to speci¢c micro- phate (ADP) and inorganic phosphate (Pi) supplies the organisms, these reactions and corresponding values of 0 requisite energy in otherwise endergonic intracellular reac- vGr as a function of temperature are listed in Tables tions. A.10 and A.11 in the Appendix. The thermodynamic properties of many organo-phos- phate compounds are not only limited at elevated temper- atures but even at 25³C. This is particularly true for sol- 6. Concluding remarks utes with complex structures including acetyl^ and succinyl^CoA, NADP‡, NADPH, and compounds in the Even organisms that branch deeply in the global phylo- AMP, ADP, and ATP series. For example, although val- genetic tree are intensely complex living systems. One of 0 ues of vGr at 25³C and 1 bar are known for the hydrolysis these organisms embedded very near the root of the tree is reactions of ATP, ADP, and AMP, represented by: the autotrophic, hyperthermophilic, methanogenic Ar- ATP ‡ H O ˆ ADP ‡ P 22† chaeon M. jannaschii. This organism was originally iso- 2 i lated from a sediment sample collected at a depth of V2600 m at 21³N on the East Paci¢c Rise [126]. Its com- ADP ‡ H2O ˆ AMP ‡ Pi 23† plete 1.66-Mb pair has been sequenced, and 1738 AMP ‡ H2O ˆ adenosine ‡ Pi; 24† predicted -coding genes have been identi¢ed; how- ever, of these, only about 38% could be con¢dently linked 0 values of vGf for the individual nucleosides and nucleo- 0 Table 7.2 tides are not. In fact, to permit calculating values of vGr for reactions among the di¡erent protonated and depro- Inorganic carbon metabolic reactions tonated forms and metal complexes of ATP, ADP, and D1 CO2(aq)+4H2(aq)HCH4(aq)+2H2O(l) 23 ‡ AMP, an arbitrary convention is usually adopted in which D2 COS(g)+2O2(aq)+H2O(l)HSO4 +CO2(aq)+2H vG0 and vH0 of aqueous adenosine are set equal to zero D3 COS(g)+H2O(l)HCO2(aq)+H2S(aq) f f D4 CO(aq)+0.5O (aq)HCO (aq) [79]. As a result of adopting this convention, values of 2 2 D5 4CO(aq)+2H2O(l)HCH4(aq)+3CO2(aq) 0 0 0 ‡ vG , vH , and S for both adenosine(aq) and H are D6 CO(aq)+3H (aq)HCH (aq)+H O(l) f f T rPr 2 4 2 0 D7 SCN3+2O (aq)+2H O(l)HSO23+CO (aq)+NH‡ all assigned zero. As a consequence, vGr at 25³C or at 2 2 4 2 4 3 3 elevated temperature can not be calculated for the synthe- D8 SCN +H2O(l)HH2S(aq)+OCN sis from environmental carbon sources of any nucleic acid D9 CH4(aq)+2O2(aq)HCO2(aq)+2H2O(l)

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 205

Table 7.3 0 31 Values of vGr (kJ mol )atPSAT as a function of temperature for reactions given in Table 7.2 Reaction T (³C) 2 18 25 37 45 55 70 85 100 115 150 200 D1 3196.02 3194.53 3193.73 3192.17 3191.01 3189.45 3186.87 3184.04 3180.98 3177.69 3169.22 3155.32 D2 3768.89 3763.32 3760.69 3755.96 3752.66 3748.38 3741.67 3734.62 3727.25 3719.57 3700.41 3669.86 D3 312.72 311.51 311.07 310.44 310.10 39.73 39.33 39.08 38.96 38.98 39.47 311.15 D4 3275.01 3274.50 3274.24 3273.73 3273.36 3272.86 3272.04 3271.14 3270.17 3269.13 3266.44 3261.93 D5 3240.31 3238.73 3237.99 3236.62 3235.65 3234.38 3232.36 3230.21 3227.92 3225.51 3219.35 3209.28 D6 3207.10 3205.59 3204.79 3203.28 3202.17 3200.68 3198.25 3195.59 3192.72 3189.64 3181.75 3168.81 D7 3866.64 3863.06 3861.32 3858.14 3855.90 3852.95 3848.28 3843.31 3838.06 3832.52 3818.55 3795.92 D8 19.47 19.26 19.14 18.91 18.73 18.50 18.11 17.68 17.22 16.72 15.45 13.40 D9 3859.72 3859.28 3858.97 3858.31 3857.79 3857.05 3855.80 3854.36 3852.77 3851.03 3846.39 3838.43 to a speci¢c cellular function [127]. Since a majority of the NAG5-7696, and Carnegie/Astrobiology Grant 8210- intracellular catabolic and anabolic processes remain ob- 14568-15. scure, even in relatively simple organisms such as M. jan- naschii, it follows that evaluation of the energetics of most metabolic reactions is similarly problematic. This situation Appendix is compounded in the case of thermophiles by the paucity of thermodynamic data at elevated temperatures for aque- Many topics mentioned in passing in the text are as- ous organic and inorganic species. However, all is not lost! sembled in this appendix where proper attention can be 0 Although calculating values of vGr as a function of tem- given to the details that might have derailed other discus- 0 perature for most stepwise redox reactions in metabolic sions. These topics include the interconversion of vGr and 00 0 pathways, including those in electron transport chains, vGr , the relation between vGr and standard potentials, may remain a formidable challenge for some time to methods for calculating activities from concentration 0 come, values of vGr at elevated temperatures can be read- data, and a review of the revised HKF equations of state. ily computed for a staggering array of known, putative, We have also included in this appendix tables of auxiliary 0 and hypothesized overall metabolic processes in thermo- reactions and corresponding vGr values. Some of these 0 philic microorganisms. In this review, values of vGr as a reactions are generally so rapid in their abiotic form (gas function of temperature are given for 188 established met- solubility, acid dissociation, cation hydrolysis, etc.) that abolic redox reactions plus an additional 182 reactions microbial mediation is not directly involved. Nevertheless, that chemically link metabolic processes to the composi- these reactions will have indirect e¡ects on microbial me- tion of arti¢cial and natural systems. In addition, thou- 0 Table 7.4 sands of vGr values can be calculated with the tabulated values of vG0. We hope that these data prove useful in Microorganisms that use the carbon reactions speci¢ed in Table 7.2 designing culture media, quantifying microbial energetics, Reaction and placing thermophiles and hyperthermophiles in their D1 As written: Methanococcus vannielii, M. barkeri [387] geochemical and ecological contexts. Methanobacterium wolfei, Methanobacterium alcaliphilum [391], M. thermolithotrophicus [302], M. jannaschii [126] M. kandleri [94], Methanococcus CS-1 [165], Methanococcus fervens (AG86)[303,339], Methanobacterium thermoautotrophicus [306], Acknowledgements [343], Methanothermus sociabilis [344], Methanococcus igneus [340], Methanobacterium This paper is dedicated to Harold Helgeson who stood thermoalcaliphilum [300], Methanobacterium thermoaggregans there and pointed the way even though none of us knew [299], Methanocalculus halotolerans [412], Methanobacterium where we were going. We wish to thank several colleagues thermo£exum, Methanobacterium de£uvii [298], Methanobacterium subterraneum [43], Methanococcus infernus for helpful discussions during the course of this study in- [341], Methanococcus vulcanius [303], Methanoplanus cluding Tom McCollom, Mitch Schulte, D'Arcy Meyer, petrolearius [413] Karyn Rogers, Panjai Prapaipong, Giles Farrant, Andrey D2 As written: T. thioparus, Paracoccus [87] Plyasunov, Mikhail Zolotov, Anna-Louise Reysenbach, D3 As written: T. thioparus, Paracoccus [87] Mel Summit, Jill Ban¢eld, and Mike Adams. Technical D4 As written: B. schlegelii, Pseudomonas carboxydovorans, Alcaligenes carboxydus [387] assistance was provided by Barb Winston and Gavin D5 As written: Methanobacterium thermoautotrophicum [387] Chan. A special thanks goes to Brian Kristall without D6 As written: Methanobacterium formicicum [381] whose e¡orts this work could not have been completed. D7 As written: T. thioparus, Paracoccus [87] Financial support was provided by NSF-LExEn Grants D8 As written: T. thioparus, Paracoccus [87] OCE-9714288, OCE-9817730, NASA Exobiology Grant D9 As written: Methylococcus thermophilus [233]

FEMSRE 711 7-3-01 206 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

Fig. 13. Plots of vG (represented as solid contours) at P and 25, 55, 100, and 150³C for Reaction (D1) as a function of log a and log a . The r SAT CH4 CO2 33 activity of H2(aq) is set at 10 , and the activity of H2O(l) is taken to be unity. tabolism. In addition, we include here redox and dispro- vG0 0 ˆ 32:303 RT log a 1A CO2 aq† portionation reactions that have not, to our knowledge, been shown to be microbially mediated, but may be. Many ‡log a 3log a 3 † 3A† CH4 aq† CH3COO of these auxiliary reactions are also required to connect known microbial processes with the larger realm of geo- 0 chemical processes that support life at high temperatures where vG1AP designates the standard Gibbs free energy of and pressures. the reaction in the biological standard state, i.e., neutral pH (sometimes called the revised standard Gibbs free en-

ergy). Hence, because eH‡ in Reaction 1A equals 31, Eq. 0 00 A.1. Interconversion of vGr and vGr 4 can be written as: vG0 0 ˆ vG0 3G ˆ vG0 ‡ 2:303 RT pH† 4A† As stated in the text, di¡erences in the conventional and 1A 1A n 1A biologic standard states can be accounted for explicitly and at 55³C and 1 bar where M. thermophila grows opti- (see Eq. 4). If we consider, for example, acetate fermenta- mally in the laboratory [128] and where neutral pH is tion represented by 6.58: CH COO3 ‡ H‡ ! CO aq†‡CH aq† 1A† 0 0 0 31 3 2 4 vG1A ˆ vG1A ‡ 41:30 kJ mol 5A† carried out, among others, by the thermophilic Archaeon For comparison, at neutral pH, PSAT, and 25 or 100³C, Methanosarcina thermophila [6], we can write in the con- the conversions can be calculated with: ventional form: vG0 0 ˆ vG0 ‡ 39:95 kJ mol31 6A† 1A 1A vG0 ˆ 32:303 RT log a 1A CO2 aq† and:

‡log a 3log a 3 3log a ‡ † 2A† 0 0 0 31 CH4 aq† CH3COO H vG1A ˆ vG1A ‡ 43:79 kJ mol 7A† However, this equation can also be written as: respectively. Other values of neutral pH and interconver-

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 207

35 Fig. 14. Same as for Fig. 13, except that the activity of H2(aq) is set at 10 .

0 0 sion of vG1A and vG1AP for water dissociation are given in (Reactions 9 and 10) that explicitly include the transfer of 0 Table 3. two electrons. E11 can be calculated from Eq. 8A by re- writing it as: vG0 A.2. Relationship between Gibbs free energies and electrode E0 ˆ r 10A† r nF potentials 0 31 At 25³C and 1 bar, vG11 equals 3176.21 kJ mol , and 0 In this review, the energetics of all reactions are ex- E11, for n equals 2, is 30.91 V. Corresponding values of 0 0 31 pressed in terms of their standard and overall Gibbs free vG11 and E11 at 100³C and PSAT are 3174.44 kJ mol 0 energies, vGr and vGr, respectively. It is not uncommon, and 30.90 V, respectively. As in the case of vGr, the however, when describing redox reactions to express the composition of the system can have a large e¡ect on values 0 energetics in terms of standard and overall electrode po- of Er relative to Er . As an example, at 25³C, 1 bar, and 0 3 3 tentials represented as Er and Er, respectively. The rela- equal activities of NO3 and NO2 , E11 varies between 0 0 tionship between vGr and Er is given by: 30.62 and 30.82 V as the fugacity of H2 changes from 310 33 0 0 10 to 10 . vGr ˆ nFEr 8A† and that between vGr and Er is given by: A.3. Calculating activities from concentrations vGr ˆ nFEr 9A† where n denotes the number of electrons transferred in the Chemical information commonly required when evalu- reaction, and F stands for the Faraday constant (96.48 kJ ating metabolic reactions includes the concentration of 31 31 0 mol V ). The relation between Er and Er is analogous individual compounds. However, to calculate values of 0 to that between vGr and vGr . Here we consider, as an vGr, the activities of individual compounds, rather than 3 example, the reduction at 25³C and 1 bar of NO3 to their concentrations, need to be known. Here, we brie£y 3 NO2 (Reaction 11) which is the sum of two half reactions review activity^concentration relations, focusing predom-

FEMSRE 711 7-3-01 208 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

37 Fig. 15. Same as for Fig. 13, except that the activity of H2(aq) is set at 10 . inantly on aqueous solutes. For more detailed discussions, In Fig. A1 curves are shown of QÆ versus ionic strength textbooks in solution chemistry, thermodynamics, physical for several common electrolytes. The e¡ect of valence of chemistry, or geochemistry [129^131] should be consulted. an electrolyte on the value of QÆ can clearly be seen in this The relationship between the concentration (commonly ¢gure. As an example, NaCl, an electrolyte consisting of expressed in units of molality) and the activity of an in- two univalent ions, has the largest value of QÆ over the dividual aqueous electrolyte, nonelectrolyte, or ionic spe- entire range of ionic strength; CuSO4, composed of two cies can be given by: divalent ions, exhibits the smallest value of QÆ. Fig. A1 a ˆ Q m 11A† further illustrates that values of QÆ di¡er considerably from unity with increasing ionic strength, in some cases where a, Q, and m represent the activity, activity coe¤cient, even at very modest values of I. For example, QÆ for and molality, respectively. Thus, to convert a concentra- CuSO4 equals V0.65 at I = 0.01. A thorough analysis of tion, which can be measured, into an activity, which is activity coe¤cient relations in aqueous electrolyte solu- required for thermodynamic analysis of reaction ener- tions is given by Helgeson et al. (1981) [71]. getics, the activity coe¤cient needs to be calculated. As Activity coe¤cients of individual ions are most com- an example, we discuss here the activity coe¤cients of monly calculated with a form of the Debye^Hu«ckel equa- electrolytes such as NaCl, K2SO4, and others. In an elec- tion which takes account of long-range electrostatic forces trolyte solution, the solute is partially or completely dis- of one ion upon another. Di¡erent Debye^Hu«ckel expres- sociated into its ions. It has been shown that the activity sions are appropriate for di¡erent ionic strengths, but each coe¤cient of an electrolyte, commonly speci¢ed as QÆ,isa expression explicitly accounts for the charge of the ion and function of the ionic strength (I) of the aqueous solution the value of I. At very low concentrations, below V0.01 I, which is de¢ned as: the Debye^Hu«ckel limiting law is used, which is given by: X p 1 2 2 I ˆ 2 mizi 12A† log Q i ˆ 3Azi I 13A†

where Qi and zi denote the activity coe¤cient and charge of where mi and zi stand for the molality and charge of the the ith ion and A stands for a constant characteristic of ith ion in the solution, respectively. the solvent. At higher concentrations, between approxi-

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 209

Table 8.1 0 31 Values of vG (kJ mol )atPSAT as a function of temperature for aqueous and liquid organic compounds Compound T (³C) 2 18 25 37 45 55 70 85 100 115 150 200 Carboxylic acids Formate3 3348.69 3350.24 3350.88 3351.95 3352.65 3353.51 3354.78 3356.03 3357.26 3358.48 3361.21 3364.79 Formic acid(aq) 3368.64 3371.17 3372.30 3374.28 3375.62 3377.33 3379.96 3382.66 3385.44 3388.29 3395.22 3405.78 Acetate3 3367.36 3368.72 3369.33 3370.37 3371.07 3371.96 3373.31 3374.69 3376.08 3377.49 3380.79 3385.40 Acetic acid(aq) 3392.52 3395.25 3396.48 3398.66 3400.17 3402.09 3405.08 3408.18 3411.40 3414.72 3422.88 3435.44 Glycolate3 3504.47 3506.21 3506.98 3508.30 3509.19 3510.32 3512.03 3513.75 3515.51 3517.27 3521.43 3527.28 Glycolic acid(aq) 3524.89 3527.61 3528.86 3531.07 3532.59 3534.55 3537.60 3540.77 3544.07 3547.48 3555.90 3568.93 Propanoate3 3360.66 3362.33 3363.09 3364.46 3365.40 3366.63 3368.55 3370.56 3372.66 3374.85 3380.23 3388.35 Propanoic acid(aq) 3386.48 3389.58 3391.00 3393.54 3395.30 3397.58 3401.15 3404.89 3408.80 3412.87 3422.96 3438.69 Lactate3 3509.69 3511.75 3512.67 3514.30 3515.41 3516.85 3519.06 3521.35 3523.72 3526.15 3532.04 3540.80 Lactic acid(aq) 3530.19 3533.29 3534.72 3537.29 3539.07 3541.38 3544.99 3548.78 3552.74 3556.87 3567.09 3583.05 Butanoic acid(aq) 3376.55 3380.02 3381.63 3384.53 3386.54 3389.16 3393.26 3397.57 3402.09 3406.79 3418.48 3436.74 Butanoate3 3351.28 3353.27 3354.18 3355.82 3356.97 3358.45 3360.79 3363.26 3365.84 3368.54 3375.20 3385.41 Pentanoic acid(aq) 3367.75 3371.59 3373.39 3376.64 3378.92 3381.89 3386.57 3391.52 3396.71 3402.15 3415.71 3437.02 Pentanoate3 3342.31 3344.64 3345.73 3347.72 3349.13 3350.97 3353.91 3357.05 3360.37 3363.86 3372.63 3386.39 Benzoate3 3207.58 3209.84 3210.88 3212.75 3214.05 3215.75 3218.41 3221.22 3224.17 3227.25 3234.86 3246.58 Benzoic acid(aq) 3229.90 3233.27 3234.86 3237.71 3239.71 3242.31 3246.40 3250.73 3255.29 3260.04 3271.92 3290.58 Dicarboxylic acids Oxalate32 3672.66 3673.70 3674.05 3674.52 3674.76 3674.99 3675.18 3675.22 3675.09 3674.80 3673.49 3669.86 H^oxalate3 3694.80 3697.28 3698.34 3700.13 3701.31 3702.78 3704.94 3707.08 3709.18 3711.26 3715.97 3722.25 Oxalic acid(aq) 3701.44 3704.31 3705.59 3707.83 3709.34 3711.26 3714.21 3717.23 3720.32 3723.48 3731.11 3742.65 Malonate32 3683.68 3684.78 3685.18 3685.75 3686.07 3686.39 3686.72 3686.87 3686.83 3686.62 3685.36 3681.53 H^malonate3 3713.55 3716.43 3717.69 3719.83 3721.25 3723.02 3725.68 3728.32 3730.96 3733.59 3739.65 3748.04 Malonic acid(aq) 3728.75 3732.35 3733.97 3736.80 3738.73 3741.19 3744.98 3748.88 3752.88 3756.99 3766.94 3782.03 Succinate32 3685.69 3687.18 3687.77 3688.70 3689.27 3689.92 3690.78 3691.49 3692.07 3692.50 3692.89 3691.75 H^succinate3 3715.58 3718.59 3719.91 3722.18 3723.71 3725.64 3728.56 3731.52 3734.51 3737.51 3744.61 3754.76 Succinic acid(aq) 3738.13 3742.12 3743.92 3747.10 3749.28 3752.07 3756.37 3760.82 3765.41 3770.13 3781.64 3799.16 Glutaric acid(aq) 3732.86 3737.53 3739.66 3743.40 3745.96 3749.23 3754.30 3759.53 3764.92 3770.47 3783.99 3804.54 H^glutarate3 3709.86 3713.34 3714.89 3717.56 3719.37 3721.66 3725.14 3728.69 3732.30 3735.95 3744.66 3757.38 Glutarate32 3681.28 3683.18 3683.97 3685.24 3686.05 3687.02 3688.38 3689.63 3690.76 3691.77 3693.64 3694.82 Alcohols Methanol(aq) 3172.98 3175.01 3175.94 3177.59 3178.74 3180.22 3182.53 3184.95 3187.47 3190.10 3196.61 3206.76 Ethanol(aq) 3178.08 3180.27 3181.30 3183.16 3184.47 3186.18 3188.90 3191.78 3194.83 3198.04 3206.10 3218.94 Propanol(aq) 3171.70 3174.18 3175.36 3177.52 3179.05 3181.07 3184.28 3187.72 3191.38 3195.25 3205.05 3220.76 2-Propanol(aq) 3182.37 3184.52 3185.56 3187.48 3188.86 3190.68 3193.62 3196.80 3200.21 3203.85 3213.17 3228.39 Butanol(aq) 3158.41 3161.18 3162.51 3164.97 3166.72 3169.03 3172.74 3176.72 3180.96 3185.46 3196.90 3215.35 Pentanol(aq) 3156.32 3159.45 3160.97 3163.77 3165.78 3168.42 3172.68 3177.27 3182.18 3187.38 3200.64 3222.10 Alkanes Ethane(aq) 314.01 315.51 316.26 317.68 318.70 320.08 322.32 324.77 327.42 330.26 337.58 349.58 Propane(aq) 35.38 37.28 38.22 39.99 311.27 312.97 315.75 318.78 322.04 325.52 334.46 349.04 Butane(aq) 3.43 1.27 0.14 32.00 33.55 35.64 39.02 312.69 316.61 320.80 331.45 348.67 Pentane(aq) 12.83 10.24 8.90 6.37 4.53 2.08 31.90 36.19 310.79 315.67 328.08 348.10 Octane(l)a 15.23 9.64 7.13 2.75 30.24 34.04 39.89 315.90 322.09 328.44 343.88 367.39 Nonane(l)a 21.22 15.16 12.43 7.64 4.38 0.21 36.20 312.82 319.63 326.63 343.69 369.72 Decane(l)a 27.22 20.66 17.71 12.53 8.99 4.48 32.48 39.66 317.05 324.65 343.17 371.45 Undecane(l)a 33.23 26.18 23.00 17.42 13.61 8.75 1.26 36.48 314.45 322.65 342.64 373.17 Hexadecane(l)a 63.24 53.74 49.44 41.88 36.71 30.10 19.89 9.34 31.54 312.76 340.15 382.09 Amino acids Alanine(aq) 3367.97 3370.46 3371.59 3373.57 3374.93 3376.67 3379.38 3382.18 3385.08 3388.08 3395.45 3406.80 Arginine(aq) 3232.53 3237.68 3240.01 3244.09 3246.90 3250.49 3256.06 3261.84 3267.84 3274.04 3289.30 3312.88 Arginine‡ 3284.86 3290.20 3292.60 3296.81 3299.69 3303.37 3309.06 3314.96 3321.07 3327.37 3342.81 3366.50 Asparagine(aq) 3519.57 3523.37 3525.06 3528.00 3530.00 3532.54 3536.47 3540.52 3544.71 3549.03 3559.59 3575.81 Aspartic acid(aq) 3716.56 3720.18 3721.79 3724.59 3726.51 3728.94 3732.70 3736.60 3740.62 3744.78 3754.97 3770.65 Aspartate3 3695.24 3698.18 3699.44 3701.62 3703.09 3704.93 3707.74 3710.60 3713.51 3716.48 3723.57 3733.94 Cysteine(aq) 3331.80 3334.77 3336.11 3338.48 3340.11 3342.22 3345.50 3348.93 3352.51 3356.23 3365.44 3379.79 Glutamic acid(aq) 3718.30 3722.27 3724.05 3727.17 3729.30 3732.02 3736.23 3740.61 3745.13 3749.81 3761.29 3779.01 Glutamate3 3695.38 3698.33 3699.62 3701.82 3703.31 3705.20 3708.08 3711.02 3714.03 3717.10 3724.48 3735.34 Glutamine(aq) 3522.50 3526.55 3528.36 3531.54 3533.72 3536.50 3540.81 3545.28 3549.92 3554.71 3566.48 3584.67 Glycine(aq) 3376.78 3379.39 3380.54 3382.52 3383.86 3385.54 3388.10 3390.71 3393.36 3396.05 3402.51 3412.17 Histidine(aq) 3196.45 3200.69 3202.60 3205.97 3208.29 3211.26 3215.87 3220.68 3225.68 3230.85 3243.61 3263.38 Histidine‡ 3230.15 3234.67 3236.70 3240.26 3242.70 3245.81 3250.64 3255.65 3260.84 3266.21 3279.38 3299.64 Isoleucine(aq) 3338.63 3341.63 3343.05 3345.64 3347.46 3349.85 3353.62 3357.64 3361.89 3366.35 3377.57 3395.40

FEMSRE 711 7-3-01 210 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

Table 8.1 (continued) Compound T (³C) 2 18 25 37 45 55 70 85 100 115 150 200 Leucine(aq) 3347.82 3350.86 3352.30 3354.93 3356.78 3359.20 3363.05 3367.15 3371.48 3376.05 3387.53 3405.81 Lysine(aq) 3332.23 3335.90 3337.58 3340.55 3342.60 3345.25 3349.39 3353.74 3358.27 3362.99 3374.70 3392.98 Lysine‡ 3382.91 3386.87 3388.66 3391.83 3394.00 3396.80 3401.16 3405.71 3410.44 3415.35 3427.48 3446.28 Methionine(aq) 3496.85 3500.79 3502.59 3505.79 3508.00 3510.85 3515.29 3519.92 3524.75 3529.76 3542.10 3561.25 Phenylalanine(aq) 3201.72 3205.20 3206.83 3209.76 3211.82 3214.51 3218.76 3223.30 3228.09 3233.13 3245.85 3266.17 Proline(aq) 3303.13 3306.34 3307.78 3310.33 3312.07 3314.30 3317.75 3321.34 3325.04 3328.87 3338.26 3352.74 Serine(aq) 3514.03 3517.11 3518.49 3520.89 3522.53 3524.62 3527.84 3531.18 3534.63 3538.19 3546.91 3560.30 Threonine(aq) 3497.29 3500.10 3501.38 3503.65 3505.22 3507.26 3510.44 3513.79 3517.31 3520.97 3530.10 3544.42 Tryptophan(aq) 3106.79 3110.51 3112.23 3115.34 3117.54 3120.43 3125.05 3130.02 3135.34 3141.00 3155.48 3179.02 Tyrosine(aq) 3378.64 3382.39 3384.10 3387.16 3389.28 3392.01 3396.30 3400.81 3405.54 3410.46 3422.72 3441.93 Valine(aq) 3352.91 3355.72 3357.03 3359.39 3361.05 3363.20 3366.59 3370.18 3373.96 3377.91 3387.78 3403.37 Miscellaneous Methanamine(aq) 23.88 21.96 21.08 19.51 18.43 17.02 14.83 12.52 10.12 7.61 1.38 38.34 (aq) 130.42 127.85 126.60 124.29 122.65 120.47 116.96 113.19 109.15 104.86 93.94 76.28 Toluene(l) 122.76 119.56 118.11 115.58 113.85 111.63 108.23 104.70 101.08 97.34 88.23 74.29 Ethylbenzene(aq) 140.05 137.13 135.72 133.10 131.23 128.76 124.80 120.53 115.98 111.16 98.92 79.24 Ethylbenzene(l) 125.55 121.61 119.83 116.72 114.60 111.89 107.72 103.42 98.99 94.43 83.33 66.39 aThermodynamic data for liquid n-alkanes are taken from Helgeson et al. (1998) [74]. mately 0.01 and 0.1 I, the most common Debye^Hu«ckel A.4. Review of the revised HKF equations of state equation is: p 2 The revised HKF equations of state can be used to 3Azi I log Q i ˆ p 14A† calculate the standard state thermodynamic properties of 1 ‡ Ba I organic and inorganic charged and neutral aqueous species where B denotes another constant of the solvent and a® at elevated temperatures and pressures. In order to calcu- stands for the distance of closest approach between oppo- late values of vG0 for aqueous species in accord with Eq. 8 0 sitely charged ions. At concentrations s V0.1 I, a further in the text, the standard partial molal heat capacity (Cp) extension of the Debye^Hu«ckel limiting law is often used; and volume (V0) as functions of temperature and pressure a common one [71] is represented by: need to be integrated. The revised HKF equations of state p 2 for these properties are given, respectively, by: 3Azi I log Q i ˆ p ‡ bQ I 15A† 1 ‡ Ba I c C0 ˆ c ‡ 2 3 p 1 T33 †2 where bQ stands for an extended term parameter for com- puting the mean ionic activity coe¤cient. Regardless  2T 8 ‡ P which of the numerous Debye^Hu«ckel expressions is a P3P †‡a ln T33 †3 3 r 4 8 ‡ P used, each accounts explicitly for the fact that values of r Q for ions may di¡er considerably from unity, even at   i Dg 1 D2g ionic strengths well below 0.1. This is particularly true ‡g TX ‡ 2TY 3T 31 16A† 2 23 33 DT P O DT P for multivalent ions such as, for example, SO4 ,PO4 , 2‡ 3‡ Fe , and Fe . The general trend is that values of Qi for ions decrease from unity with increasing values of I, before increasing at high ionic strength [129,132]. Table 8.2 Metabolic reactions involving organic and inorganic carbon Activity coe¤cients of neutral molecules in electrolyte solutions can also di¡er considerably from unity and thus E1 4H2(aq)+2CO2(aq)Hacetic acid(aq)+2H2O(l) E2 4formic acid(aq)HCH (aq)+3CO (aq)+2H O(l) need to be calculated explicitly. For example, gases dis- 4 2 2 E3 acetic acid(aq)+2O2(aq)H2CO2(aq)+2H2O(l) solved in electrolyte solutions generally have activity co- E4 acetic acid(aq)HCH4(aq)+CO2(aq) e¤cients greater than unity, as opposed to activity coe¤- E5 propanoic acid(aq)+3.5O2(aq)H3CO2(aq)+3H2O(l) cients of ions and electrolytes discussed above. This is E6 2lactic acid(aq)H3acetic acid(aq) E7 2succinic acid(aq)+7O2(aq)H8CO2(aq)+6H2O(l) shown in Fig. A2 where activity coe¤cients, Qm, for gas- E8 methanol(aq)+H2(aq)HCH4(aq)+H2O(l) eous N2,H2,O2,H2S, and NH3 dissolved in NaCl solu- E9 4methanol(aq)H3CH4(aq)+CO2(aq)+2H2O(l) tions at 25³C are plotted against ionic strength. It can be E10 2ethanol(aq)+2CO2(aq)H3acetic acid(aq) seen in this ¢gure that values of the activity coe¤cients E11 2ethanol(aq)+CO2(aq)H2acetic acid(aq)+CH4(aq) increase rapidly above 1.0 with increasing values of I. For E12 4(2-)propanol(aq)+3CO2(aq)+2H2O(l)H example, Q s 1.5 at I = 1.0. 3CH4(aq)+4lactic acid(aq) N2 g†

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 211

Table 8.3 0 31 Values of vGr (kJ mol )atPSAT as a function of temperature for reactions given in Table 8.2 Reaction T (³C) 218253745557085100115150200 E1 3172.32 3170.74 3169.78 3167.82 3166.31 3164.23 3160.74 3156.84 3152.55 3147.91 3135.81 3115.71 E2 3179.98 3178.10 3177.54 3176.86 3176.59 3176.42 3176.47 3176.86 3177.54 3178.48 3181.56 3187.72 E3 3883.42 3883.07 3882.92 3882.66 3882.49 3882.27 3881.92 3881.57 3881.20 3880.81 3879.80 3878.03 E4 323.70 323.79 323.95 324.35 324.70 325.21 326.13 327.21 328.43 329.78 333.41 339.61 E5 31536.84 31536.54 31536.37 31536.03 31535.78 31535.43 31534.83 31534.14 31533.37 31532.52 31530.19 31525.93 E6 3117.19 3119.16 3120.00 3121.42 3122.36 3123.52 3125.26 3126.99 3128.71 3130.44 3134.46 3140.21 E7 33137.41 33138.35 33138.85 33139.84 33140.57 33141.56 33143.18 33144.95 33146.84 33148.85 33153.85 33161.34 E8 3114.26 3113.66 3113.42 3113.01 3112.74 3112.40 3111.89 3111.38 3110.86 3110.32 3109.04 3107.09 E9 3261.00 3260.12 3259.94 3259.86 3259.94 3260.15 3260.69 3261.47 3262.45 3263.60 3266.93 3273.03 E10 354.38 354.85 354.89 354.78 354.59 354.23 353.47 352.45 351.21 349.75 345.59 338.01 E11 378.08 378.64 378.84 379.13 379.29 379.45 379.60 379.66 379.64 379.53 379.00 377.62 E12 132.52 132.26 132.29 132.49 132.74 133.15 133.98 135.04 136.31 137.79 141.97 149.53

 1 Dln O and Yr 20A†  O DT a a 1 P V 0 ˆ a ‡ 2 ‡ a ‡ 4 3gQ 1 8 ‡ P 3 8 ‡ P T33 and g stands for the conventional Born coe¤cient of the  1 Dg species, which can be expressed as: ‡ 31 17A† O DP 694657Z2 T g e 3225392Z 21A† re where a1, a2, a3, a4, c1, and c2 stand for temperature/pres- sure independent parameters unique to each aqueous spe- where Ze and Z stand for the e¡ective and formal charge cies; T, P, and Pr designate the temperature and pressure (which are equivalent for charged species), respectively, of interest and the reference pressure of 1 bar, respec- and re denotes the e¡ective electrostatic radius of the spe- tively; O corresponds to the dielectric constant for H2O; cies, which for monoatomic ions is given by: 8 and 3 refer to solvent parameters equal to 2600 bars r ˆ r ‡ MZM k ‡ g† 22A† and 228 K, respectively; Q, X, and Y represent Born func- e x Z tions given by: where rx designates the crystal radius of the ion; kZ = 0.0  for anions and 0.94 for cations; and g stands for a solvent 1 Dln O Qr 18A† function of density and temperature [51,72]. If the species O DP T ! 1 D2ln O Dln O 2 Xr 3 19A† Table 8.5 2 O DT P DT P Coupled metabolic reactions involving organic carbon and inorganic ni- trogen

3 3 E13 formic acid(aq)+NO3 HNO2 +H2O(l)+CO2(aq) 3 ‡ Table 8.4 E14 4formic acid(aq)+NO3 +H HNH3(aq)+4CO2(aq)+3H2O 3 3 Microorganisms that use the reactions speci¢ed in Table 8.2 E15 acetic acid(aq)+4NO3 H2CO2(aq)+4NO2 +2H2O(l) 3 ‡ E16 5acetic acid(aq)+8NO3 +8H H4N2(aq)+10CO2(aq)+14H2O(l) Reaction 3 ‡ E17 acetic acid(aq)+NO3 +H H2CO2(aq)+NH3(aq)+H2O(l) E1 Acetogenium kivui [254], Desulfotomaculum thermobenzoicum 3 ‡ E18 2.5propanoic acid(aq)+7NO3 +7H H [211], D. thermoacetoxidans [210] 3.5N2(aq)+7.5CO2(aq)+11H2O(l) E2 M. halotolerans [412], Methanococcus CS-1[165], M. 3 3 E19 lactic acid(aq)+6NO3 H6NO2 +3H2O(l)+3CO2(aq) thermolithotrophicus [302], M. thermo£exum, M. de£uvii [298], 3 3 E20 lactic acid(aq)+2NO3 Hacetic acid(aq)+2NO2 +CO2(aq)+H2O(l) M. subterraneum [43], M. petrolearius [413] 3 ‡ E21 4lactic acid(aq)+2NO3 +2H H E3 P. aerophilum [345], S. arcachonense [380] 4acetic acid(aq)+2NH3(aq)+4CO2(aq)+2H2O(l) E4 Methanothrix thermoacetophila [414] 3 ‡ E22 3lactic acid(aq)+2NO2 +2H H E5 P. aerophilum [345], S. arcachonense [380] 3acetic acid(aq)+2NH3(aq)+3CO2(aq)+H2O(l) E6 Natroniella acetigena [415] 3 ‡ E23 2.5succinic acid(aq)+7NO3 +7H H E7 Bacillus stearothermophilus [416], S. arcachonense [380] 3.5N2(aq)+10CO2(aq)+11H2O(l) E8 Methanolobus siciliae [417], Methanohalophilus zhilinae [418] 3 ‡ E24 benzoic acid(aq)+3.75NO3 +3.75H +0.75H2O(l)H E9 M. barkeri, Methanolobus tindarius [419] 3.75NH3(aq)+7CO2(aq) E10 N. acetigena [415] E25 4methanamine(aq)+2H2O(l)H3CH4(aq)+CO2(aq)+4NH3(aq) E11 strain CV [420,421] 3 ‡ E26 ethylbenzene(aq)+8.4NO3 +8.4H H E12 M. petrolearius [413] 8CO2(aq)+4.2N2(aq)+9.2H2O(l)

FEMSRE 711 7-3-01 212 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

Table 8.6 0 31 Values of vGr (kJ mol )atPSAT as a function of temperature for reactions given in Table 8.5 Reaction T (³C) 218253745557085100115150200 E13 3172.35 3172.18 3172.17 3172.22 3172.30 3172.44 3172.74 3173.12 3173.58 3174.11 3175.57 3178.11 E14 3683.27 3682.20 3682.04 3682.14 3682.42 3683.00 3684.28 3686.00 3688.12 3690.61 3697.73 3710.66 E15 3533.12 3534.41 3535.08 3536.37 3537.31 3538.57 3540.61 3542.83 3545.21 3547.73 3554.12 3564.32 E16 34231.31 34234.99 34237.93 34244.50 34249.85 34257.54 34270.98 34286.53 34304.07 34323.50 34375.81 34466.95 E17 3527.00 3527.89 3528.46 3529.63 3530.54 3531.79 3533.93 3536.35 3539.01 3541.92 3549.57 3562.55 E18 33679.53 33683.53 33686.34 33692.38 33697.19 33704.00 33715.75 33729.20 33744.26 33760.83 33805.19 33882.00 E19 3858.28 3861.19 3862.63 3865.26 3867.14 3869.62 3873.55 3877.74 3882.17 3886.82 3898.41 3916.58 E20 3325.16 3326.78 3327.54 3328.90 3329.83 3331.05 3332.94 3334.91 3336.96 3339.08 3344.29 3352.26 E21 31288.37 31294.10 31296.91 31302.09 31305.78 31310.63 31318.39 31326.67 31335.44 31344.70 31368.06 31405.51 E22 3963.22 3967.32 3969.37 3973.20 3975.95 3979.59 3985.45 3991.75 3998.49 31005.62 31023.77 31053.25 E23 33759.19 33765.11 33768.98 33777.09 33783.45 33792.38 33807.66 33825.03 33844.38 33865.59 33922.03 34018.86 E24 3371.58 3371.71 3371.71 3372.36 3372.45 3373.02 3373.81 3375.54 3375.72 3378.17 3385.84 3401.48 E25 3203.07 3205.06 3206.14 3208.23 3209.75 3211.79 3215.10 3218.66 3222.45 3226.47 3236.57 3252.65 E26 34388.83 34394.12 34397.62 34404.99 34410.78 34418.92 34432.87 34448.76 34466.49 34485.96 34537.93 34627.75

under consideration has no formal charge, (Dg/DP), (Dg/DT), not represent the results of ¢tting curves to the data shown 2 2 and (D /DT )P in Eqs. 16A and 17A are taken to be zero. In (which in the case of Fig. A4 should be obvious as the the absence of crystal radii and experimental data at high data post-date the prediction). Instead, they are con- 0 0 temperatures and pressures, values of a1, a2, a3, a4, c1, c2, strained by Cp and V data for each species, values of and g can be estimated for both charged and neutral log K at 25³C and 1 bar, and correlations among thermo- species using correlation algorithms [49,50,57,61] or pre- dynamic data and parameters in the revised HKF equa- dicted using group additivity relations among organic tions of state. It can be seen in these ¢gures that predicted compounds [63]. values of log K for these dissociation reactions are in very The revised HKF equations of state have been shown to close agreement with the available experimental data over be highly reliable in predicting the temperature and pres- the entire temperature range investigated. sure dependencies of aqueous reactions. As examples, we In addition to equations of state for aqueous species, include here plots of log K for the dissociation of acetic equations of state have also been generated for organic 3 23 acid to acetate (Fig. A3) and HSO4 to SO4 (Fig. A4) solids, liquids, and gases; inorganic gases; and rock-form- from 0 to 350³C at PSAT. The symbols represent experi- ing minerals. These equations are not documented explic- mental data taken from the literature, but the curves were itly here, because most of the compounds considered in generated independently with the revised HKF equations. this review are in the aqueous phase. For discussions of In other words, the curves shown in Figs. A3 and A4 do the equations for non-aqueous species see Helgeson et al. [74,76], Richard and Helgeson [75], and Sassani and Shock [56]. An example (Fig. A5 [50]) is included here to show Table 8.7 how well the temperature dependencies of gas solubility Microorganisms that use the coupled carbon and nitrogen reactions reactions can be predicted. It can be seen in this ¢gure speci¢ed in Table 8.5 that the calculated equilibrium constant for the solubility

Reaction in water of CO2(g) matches closely the experimental values E13 B. infernus [116] as a function of temperature taken from the literature. E14 A. degensii [187], T. thioparus [277,278], P. aerophilum [345] The revised HKF equations of state were used in this E15 P. aerophilum [345], T. thioparus [277,278] 0 0 review to calculate values of vG and vGr as functions of E16 P. aerophilum [345] temperature and pressure for individual aqueous solutes E17 metallireducens [422,423] E18 P. aerophilum [345] and reactions in microbial metabolism. In Table A.1, we E19 B. infernus [116] list sources of thermodynamic data for organic solutes E20 Sulfurospirillum barnesii strain SES-3 [380,424], Bacillus that may serve as substrates in microbial metabolism, arsenicoselenatis, Bacillus selenitireducens [425] but for which we have not recovered direct, unequivocal E21 S. barnesii strain SES-3 [380,424], B. selenitireducens [425] evidence of microbial involvement. In each case, the sour- E22 B. selenitireducens [425], S. barnesii strain SES-3 [380,424,426], B. stearothermophilus [381,416] ces of thermodynamic properties of aqueous solutes listed E23 B. stearothermophilus [416] are consistent with the revised HKF equations of state. In E24 D. thermobenzoicum [211] the course of this study, we found it necessary to include E25 M. barkeri [427] thermodynamic data for a few additional compounds, E26 strain EbN1, strain PbN1 [428] which are listed in Table A.2.

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 213

Table 8.8 Table 8.8 (continued) Coupled metabolic reactions involving organic carbon and inorganic E70 1.5ethanol(aq)+SO23+2H‡H sulfur 3 H2S(aq)+1.5acetic acid(aq)+1.5H2O 23 ‡ 23 ‡ E27 CH4(aq)+SO4 +2H HH2S(aq)+CO2(aq)+2H2O(l) E71 2ethanol(aq)+3S2O3 +6H H6H2S(aq)+4CO2(aq)+3H2O(l) 23 ‡ 23 ‡ E28 4formic acid(aq)+SO4 +2H HH2S(aq)+4CO2(aq)+4H2O(l) E72 2ethanol(aq)+S2O3 +2H H2H2S(aq)+2acetic acid(aq)+H2O 23 ‡ E29 3formic acid(aq)+SO3 +2H H3CO2(aq)+H2S(aq)+3H2O(l) E73 ethanol(aq)+6S(s)+3H2O(l)H2CO2(aq)+6H2S(aq) 23 ‡ 23 ‡ E30 4formic acid(aq)+S2O3 +2H H2H2S(aq)+4CO2(aq)+3H2O(l) E74 2propanol(aq)+4.5SO4 +9H H6CO2(aq)+4.5H2S(aq)+8H2O(l) 23 ‡ E31 formic acid(aq)+S(s)HCO2(aq)+H2S(aq) E75 4propanol(aq)+5SO4 +10H H ‡ 23 E32 acetic acid(aq)+2H +SO4 H2CO2(aq)+H2S(aq)+2H2O(l) 4acetic acid(aq)+4CO2(aq)+5H2S(aq)+8H2O(l) 23 ‡ 23 ‡ E33 3acetic acid(aq)+4SO3 +8H H6CO2(aq)+4H2S(aq)+6H2O(l) E76 2propanol(aq)+SO4 +2H H 23 ‡ E34 acetic acid(aq)+S2O3 +2H H2H2S(aq)+2CO2(aq)+H2O(l) 2propanoic acid(aq)+H2S(aq)+2H2O(l) 23 ‡ E35 acetic acid(aq)+4S(s)+2H2O(l)H2CO2(aq)+4H2S(aq) E77 propanol(aq)+3SO3 +6H H3H2S(aq)+3CO2(aq)+4H2O(l) 23 ‡ 23 ‡ E36 4propanoic acid(aq)+7SO4 +14H H E78 3propanol(aq)+5SO3 +10H H 7H2S(aq)+12CO2(aq)+12H2O(l) 3acetic acid(aq)+5H2S(aq)+3CO2(aq)+6H2O(l) 23 ‡ 23 ‡ E37 4propanoic acid(aq)+3SO4 +6H H E79 2propanol(aq)+4.5S2O3 +9H H9H2S(aq)+6CO2(aq)+3.5H2O(l) 23 ‡ 4acetic acid(aq)+4CO2(aq)+3H2S(aq)+4H2O(l) E80 4propanol(aq)+5S2O3 +10H H 23 ‡ E38 3propanoic acid(aq)+7SO3 +14H H 4acetic acid(aq)+10H2S(aq)+4CO2(aq)+3H2O(l) 7H2S(aq)+9CO2(aq)+9H2O(l) E81 propanol(aq)+9S(s)+5H2O(l)H3CO2(aq)+9H2S(aq) 23 ‡ 23 ‡ E39 propanoic acid(aq)+SO3 +2H H E82 butanol(aq)+3SO4 +6H H4CO2(aq)+3H2S(aq)+5H2O(l) 23 ‡ acetic acid(aq)+H2S(aq)+CO2(aq)+H2O(l) E83 butanol(aq)+SO4 +2H HH2S(aq)+2acetic acid(aq)+H2O 23 ‡ 23 ‡ E40 4propanoic acid(aq)+7S2O3 +14H H E84 butanol(aq)+4SO3 +8H H4CO2(aq)+4H2S(aq)+5H2O(l) 23 ‡ 14H2S(aq)+12CO2(aq)+5H2O(l) E85 3butanol(aq)+4SO3 +8H H4H2S(aq)+6acetic acid(aq)+3H2O 23 ‡ 23 ‡ E41 4propanoic acid(aq)+3S2O3 +6H H E86 butanol(aq)+3S2O3 +6H H4CO2(aq)+6H2S(aq)+2H2O(l) 23 ‡ 4acetic acid(aq)+6H2S(aq)+4CO2(aq)+H2O(l) E87 butanol(aq)+ S2O3 +2H H2H2S(aq)+2acetic acid(aq) 23 ‡ E42 propanoic acid(aq)+7S(s)+4H2O(l)H3CO2(aq)+7H2S(aq) E88 4pentanol(aq)+15SO4 +30H H15H2S(aq)+20CO2(aq)+24H2O 23 ‡ 23 ‡ E43 2lactic acid(aq)+3SO4 +6H H6CO2(aq)+3H2S(aq)+6H2O(l) E89 pentanol(aq)+5SO3 +10H H5H2S(aq)+5CO2(aq)+6H2O 23 ‡ 23 ‡ E44 lactic acid(aq)+0.5SO4 +H H E90 4pentanol(aq)+15S2O3 +30H H30H2S(aq)+20CO2(aq)+9H2O 23 ‡ acetic acid(aq)+0.5H2S(aq)+CO2(aq)+H2O(l) E91 octane(l)+6.25SO4 +12.5H H8CO2(aq)+6.25H2S(aq)+9H2O(l) 23 ‡ 23 ‡ E45 lactic acid(aq)+2SO3 +4H H3CO2(aq)+2H2S(aq)+3H2O(l) E92 nonane(l)+7SO4 +14H H9CO2(aq)+7H2S(aq) 10H2O(l) 23 ‡ 23 ‡ E46 1.5lactic acid(aq)+SO3 +2H H E93 decane(l)+7.75SO4 +15.5H H 1.5acetic acid(aq)+1.5CO2(aq)+H2S(aq)+1.5H2O(l) 10CO2(aq)+7.75H2S(aq)+11H2O(l) 23 ‡ 23 ‡ E47 2lactic acid(aq)+3S2O3 +6H H6H2S(aq)+6CO2(aq)+3H2O(l) E94 undecane(l)+8.5SO4 +17H H11CO2(aq)+8.5H2S(aq)+12H2O(l) 23 ‡ 23 ‡ E48 2lactic acid(aq)+S2O3 +2H H E95 hexadecane(l)+12.25SO4 +24.5H H 2H2S(aq)+2acetic acid(aq)+2CO2(aq)+H2O(l) 16CO2(aq)+12.25H2S(aq)+17H2O(l) 23 ‡ E49 lactic acid(aq)+6S(s)+3H2O(l)H3CO2(aq)+6H2S(aq) E96 toluene(aq)+4.5SO4 +9H H7CO2(aq)+4.5H2S(aq)+4H2O(l) E50 lactic acid(aq)+2S(s)+H2O(l)H 2H2S(aq)+acetic acid(aq)+CO2(aq) 23 ‡ E51 2butanoic acid(aq)+5SO4 +10H H5H2S(aq)+8CO2(aq)+8H2O 23 ‡ E52 butanoic acid(aq)+1.5SO4 +3H H A.5. Gas solubility reactions acetic acid(aq)+2CO2(aq)+1.5H2S(aq)+2H2O(l) E53 1.5butanoic acid(aq)+5SO23+10H‡H 3 Reports in the literature may represent microbial meta- 5H2S(aq)+6CO2(aq)+6H2O 23 ‡ bolic processes that occur in the gas phase, the aqueous E54 butanoic acid(aq)+2SO3 +4H H acetic acid(aq)+2CO2(aq)+2H2S(aq)+2H2O(l) phase, or both. Furthermore, chemical analyses of reac- 23 ‡ E55 2butanoic acid(aq)+5S2O3 +10H H tants and products in natural and laboratory systems may 10H2S(aq)+8CO2(aq)+3H2O be given either as concentrations for aqueous species or E56 butanoic acid(aq)+1.5S O23+3H‡H 2 3 partial pressures for gases. Therefore, converting proper- acetic acid(aq)+2CO2(aq)+3H2S(aq)+0.5H2O(l) 23 ‡ ties of gases to those of the corresponding aqueous solutes E57 4succinic acid(aq)+7SO4 +14H H 16CO2(aq)+7H2S(aq)+12H2O(l) and vice versa in representations of chemical reactions 23 ‡ E58 3succinic acid(aq)+7SO3 +14H H may prove useful. To permit this conversion, we list 11 7H2S(aq)+12CO2(aq)+9H2O(l) gas solubility reactions in Table A.3 with their correspond- 23 ‡ E59 4succinic acid(aq)+7S2O3 +14H H 0 ing values of vGr as a function of temperature in Table 14H2S(aq)+16CO2(aq)+5H2O(l) 23 ‡ A.4. These can be combined as necessary with the appro- E60 benzoic acid(aq)+3.75SO4 +7.5H H 3.75H2S(aq)+7CO2(aq)+3H2O(l) priate reactions as described in the text (see Section 5.1). 23 ‡ E61 benzoic acid(aq)+5SO3 +10H H5H2S(aq)+7CO2(aq)+3H2O(l) 23 ‡ E62 benzoic acid(aq)+3.75S2O3 +7.5H +0.75H2O(l)H 7.5H2S(aq)+7CO2(aq) 23 ‡ A.6. Dissociation reactions E63 4methanol(aq)+3SO4 +6H H3H2S(aq)+4CO2(aq)+8H2O(l) 23 ‡ E64 methanol(aq)+SO3 +2H HH2S(aq)+CO2(aq)+2H2O(l) 23 ‡ E65 4methanol(aq)+3S2O3 +6H H6H2S(aq)+4CO2(aq)+5H2O(l) The metabolic reactions discussed in this review are cat- E66 methanol(aq)+3S(s)+H2O(l)HCO2(aq)+H2S(aq) alyzed by a large number of microorganisms over a wide E67 2ethanol(aq)+3SO23+6H‡H4CO (aq)+3H S(aq)+6H O(l) 4 2 2 2 range of pH. It is evident from the illustrations in Figs. 3, E68 2ethanol(aq)+SO23+2H‡HH S(aq)+2acetic acid(aq)+2H O 4 2 2 4, A3, and A4 that aqueous inorganic and organic species E69 ethanol(aq)+2SO23+4H‡H2CO (aq)+2H S(aq)+3H O(l) 3 2 2 2 may occur in various protonated and deprotonated forms

FEMSRE 711 7-3-01 214 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

Table 8.9 0 31 Values of vGr (kJ mol )atPSAT as a function of temperature for reactions given in Table 8.8 Reaction T (³C) 218253745557085100115150200 E27 3103.56 3107.47 3109.35 3112.80 3115.23 3118.41 3123.46 3128.82 3134.48 3140.44 3155.45 3179.71 E28 3283.54 3285.56 3286.89 3289.66 3291.82 3294.83 3299.93 3305.68 3312.02 3318.91 3337.02 3367.43 E29 3289.79 3292.39 3293.89 3296.90 3299.16 3302.26 3307.42 3313.13 3319.36 3326.07 3343.53 3372.59 E30 3296.06 3298.14 3299.50 3302.38 3304.63 3307.78 3313.12 3319.15 3325.81 3333.07 3352.17 3384.30 E31 340.79 341.28 341.59 342.25 342.75 343.45 344.63 345.95 347.39 348.93 352.79 359.05 E32 3127.26 3131.26 3133.30 3137.15 3139.93 3143.62 3149.59 3156.03 3162.91 3170.21 3188.86 3219.32 E33 3690.31 3706.64 3714.82 3730.06 3740.99 3755.45 3778.65 3803.57 3830.11 3858.20 3929.64 31045.98 E34 3139.78 3143.83 3145.92 3149.87 3152.74 3156.57 3162.77 3169.50 3176.70 3184.38 3204.01 3236.18 E35 36.90 310.82 312.79 316.47 319.11 322.59 328.18 334.14 340.44 347.02 363.02 388.09 E36 3854.25 3883.47 3898.16 3925.55 3945.21 3971.20 31012.95 31057.76 31105.46 31155.94 31284.20 31492.70 E37 3345.20 3358.43 3364.95 3376.96 3385.50 3396.71 3414.60 3433.65 3453.83 3475.08 3528.76 3615.42 E38 31180.61 31210.10 31224.71 31251.74 31271.02 31296.42 31337.02 31380.43 31426.52 31475.18 31598.50 31798.57 E39 3163.43 3167.82 3169.96 3173.90 3176.68 3180.32 3186.12 3192.29 3198.80 3205.66 3222.95 3250.86 E40 3941.86 3971.46 3986.47 31014.62 31034.91 31061.84 31105.26 31152.06 31202.04 31255.07 31390.26 31610.75 E41 3382.75 3396.15 3402.80 3415.13 3423.94 3435.56 3454.16 3474.07 3495.22 3517.56 3574.21 3666.02 E42 32.92 310.10 313.65 320.21 324.87 331.00 340.76 351.14 362.04 373.39 3100.83 3143.53 E43 3498.98 3512.94 3519.91 3532.86 3542.14 3554.39 3574.02 3595.07 3617.44 3641.08 3701.04 3798.16 E44 3122.23 3125.21 3126.65 3129.29 3131.14 3133.57 3137.42 3141.51 3145.81 3150.33 3161.66 3179.76 E45 3403.75 3412.90 3417.41 3425.74 3431.68 3439.48 3451.96 3465.28 3479.41 3494.32 3532.05 3593.09 E46 3260.47 3266.03 3268.70 3273.58 3277.01 3281.50 3288.61 3296.14 3304.06 3312.38 3333.26 3366.65 E47 3536.53 3550.65 3557.76 3571.04 3580.58 3593.23 3613.58 3635.48 3658.83 3683.57 3746.49 3848.75 E48 3256.97 3262.99 3265.92 3271.29 3275.10 3280.09 3288.03 3296.48 3305.42 3314.81 3338.47 3376.39 E49 368.94 375.81 379.19 385.42 389.84 395.65 3104.89 3114.70 3125.01 3135.75 3161.77 3202.24 E50 362.04 364.99 366.40 368.95 370.73 373.06 376.72 380.56 384.58 388.73 398.74 3114.15 E51 3607.51 3628.74 3639.34 3659.04 3673.16 3691.80 3721.69 3753.76 3787.87 3823.95 3915.58 31064.48 E52 3176.49 3183.11 3186.36 3192.37 3196.65 3202.28 3211.26 3220.85 3231.02 3241.76 3268.93 3312.93 E53 3841.29 3862.62 3873.14 3892.55 3906.38 3924.58 3953.63 3984.69 31017.63 31052.41 31140.50 31283.40 E54 3330.76 3339.54 3343.82 3351.68 3357.26 3364.57 3376.20 3388.60 3401.72 3415.53 3450.46 3506.94 E55 3670.09 3691.59 3702.41 3722.66 3737.23 3756.54 3787.63 3821.11 3856.85 3894.76 3991.33 31148.81 E56 3195.27 3201.97 3205.29 3211.46 3215.87 3221.70 3231.04 3241.06 3251.72 3263.00 3291.65 3338.22 E57 3981.70 31014.00 31030.38 31061.08 31083.23 31112.61 31160.00 31211.08 31265.65 31323.56 31471.14 31711.67 E58 31276.20 31308.01 31323.88 31353.39 31374.54 31402.47 31447.31 31495.43 31546.66 31600.89 31738.71 31962.79 E59 31069.32 31102.00 31118.69 31150.15 31172.93 31203.24 31252.31 31305.38 31362.23 31422.69 31577.20 31829.72 E60 3467.13 3483.38 3491.52 3506.69 3517.56 3531.94 3555.02 3579.79 3606.15 3634.05 3704.91 3820.03 E61 3852.79 3874.45 3885.15 3904.96 3919.07 3937.67 3967.38 3999.16 31032.88 31068.49 31158.73 31305.06 E62 3514.07 3530.51 3538.83 3554.40 3565.61 3580.49 3604.47 3630.31 3657.89 3687.16 3761.73 3883.27 E63 3571.68 3582.52 3588.00 3598.25 3605.62 3615.38 3631.06 3647.92 3665.88 3684.90 3733.29 3812.16 E64 3220.05 3223.84 3225.73 3229.22 3231.71 3234.99 3240.24 3245.86 3251.82 3258.12 3274.09 3300.05 E65 3609.23 3620.23 3625.85 3636.42 3644.06 3654.22 3670.63 3688.33 3707.27 3727.39 3778.74 3862.75 E66 352.65 355.30 356.62 359.06 360.79 363.07 366.71 370.57 374.62 378.83 388.94 3104.62 E67 3436.16 3448.63 3454.80 3466.23 3474.37 3485.10 3502.23 3520.53 3539.93 3560.40 3612.18 3695.96 E68 3181.64 3186.10 3188.20 3191.93 3194.52 3197.86 3203.06 3208.48 3214.12 3219.97 3234.45 3257.33 E69 3372.34 3380.74 3384.85 3392.42 3397.79 3404.84 3416.06 3428.01 3440.66 3453.98 3487.62 3542.00 E70 3213.36 3217.79 3219.87 3223.60 3226.19 3229.54 3234.76 3240.23 3245.94 3251.86 3266.60 3290.00 E71 3473.71 3486.34 3492.65 3504.40 3512.82 3523.94 3541.79 3560.94 3581.32 3602.89 3657.63 3746.56 E72 3194.15 3198.68 3200.81 3204.66 3207.33 3210.80 3216.24 3221.95 3227.92 3234.13 3249.60 3274.19 E73 337.53 343.66 346.64 352.10 355.96 361.01 368.99 377.43 386.26 395.40 3117.33 3151.14 E74 3609.44 3628.69 3638.19 3655.75 3668.24 3684.68 3710.90 3738.89 3768.55 3799.81 3878.82 31006.54 E75 3709.83 3732.35 3743.18 3762.90 3776.78 3794.87 3823.46 3853.68 3885.46 3918.75 31002.21 31135.80 E76 3182.32 3186.95 3189.12 3192.97 3195.64 3199.08 3204.43 3210.02 3215.81 3221.84 3236.73 3260.19 E77 3536.12 3548.99 3555.28 3566.84 3575.03 3585.78 3602.87 3621.07 3640.31 3660.57 3711.70 3794.29 E78 3918.04 3940.33 3951.02 3970.45 3984.09 31001.88 31029.96 31059.63 31090.83 31123.50 31205.47 31336.88 E79 3665.77 3685.26 3694.97 3713.00 3725.91 3742.94 3770.25 3799.51 3830.63 3863.53 3947.00 31082.43 E80 3772.42 3795.19 3806.26 3826.52 3840.85 3859.61 3889.40 3921.04 3954.45 3989.56 31077.96 31220.12 E81 333.90 343.36 347.95 356.35 362.28 370.03 382.27 395.20 3108.71 3122.71 3156.28 3208.01 E82 3398.27 3411.28 3417.70 3429.54 3437.96 3449.04 3466.72 3485.57 3505.55 3526.61 3579.82 3665.79 E83 3143.75 3148.77 3151.09 3155.24 3158.11 3161.80 3167.54 3173.52 3179.74 3186.18 3202.10 3227.15 E84 3706.80 3724.14 3732.61 3748.15 3759.17 3773.63 3796.61 3821.07 3846.93 3874.16 3942.88 31053.82 E85 3739.77 3759.15 3768.19 3784.35 3795.54 3809.98 3832.52 3856.07 3880.59 3906.08 3969.35 31069.49 E86 3435.82 3448.99 3455.55 3467.71 3476.41 3487.89 3506.28 3525.99 3546.94 3569.09 3625.27 3716.38 E87 3156.26 3161.34 3163.71 3167.97 3170.92 3174.75 3180.73 3187.00 3193.54 3200.34 3217.25 3244.02 E88 31922.48 31987.81 32020.01 32079.43 32121.71 32177.29 32265.96 32360.57 32460.78 32566.41 32833.37 33264.64

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 215

Table 8.9 (continued) Reaction T (³C) 218253745557085100115150200 E89 3866.28 3888.02 3898.64 3918.13 3931.94 3950.05 3978.86 31009.51 31041.92 31076.05 31162.16 31301.19 E90 32110.23 32176.37 32209.25 32270.28 32313.92 32371.51 32463.77 32562.64 32667.74 32778.83 33060.63 33517.61 E91 3713.31 3738.55 3751.25 3774.94 3791.98 3814.53 3850.83 3889.89 3931.56 3975.74 31088.29 31271.94 E92 3793.56 3822.49 3837.00 3864.06 3883.49 3909.20 3950.55 3995.01 31042.42 31092.66 31220.56 31429.06 E93 3885.81 3917.45 3933.33 3962.96 3984.23 31012.39 31057.68 31106.38 31158.32 31213.36 31353.53 31582.11 E94 3972.08 31006.91 31024.38 31056.97 31080.37 31111.34 31161.14 31214.68 31271.77 31332.27 31486.32 31737.50 E95 31403.39 31454.17 31479.61 31527.02 31561.04 31606.05 31678.38 31756.12 31838.97 31926.74 32150.12 32514.15 E96 3524.20 3543.26 3552.75 3570.36 3582.95 3599.55 3626.12 3654.57 3684.79 3716.71 3797.61 3928.79 as a function of temperature and pH. In order to ensure pyrophosphate hydrolysis (Table A.8) and/or phosphate that the appropriate aqueous species are used in represent- or pyrophosphate dissociation (Table A.5) reactions to ing metabolic processes, reactions from tables in the text write the most appropriate and representative redox pro- 0 can be combined with dissociation reactions listed in Table cess in a system. Values of vGr for reactions in Table A.10 A.5. For example, at 100³C and pH = 8, the reduction of are listed in Table A.11. elemental sulfur to hydrogen sul¢de (Reaction C19) should be combined with the dissociation reaction for

H2S (H8) in Table A.5 to yield: A.8. Microbially mediated Cl redox reactions S s†‡H aq†!HS3 ‡ H‡ 23A† 2 It has long been known that microbes can reduce chlo- 3 3 3 3 because HS is the dominant form of aqueous sul¢de at rate (ClO3 ) or perchlorate (ClO4 ) to chloride (Cl ) and in 0 3 this temperature and pH (see Fig. 3b). Values of vGr and some cases to chlorite (ClO2 ) [133^138]. Many of these pKa as functions of temperature for reactions given in organisms were isolated from industrial or domestic sew- Table A.5 are listed in Tables A.6 and A.7, respectively. age, including waste from paper mills, swine farm lagoons, and match and sugar factories, and others were cultured from natural systems, such as , sediments, and river A.7. Auxiliary redox, disproportionation, and hydrolysis water [139^143]. They include species of Aerobacter, Mi- reactions crococcus, Staphylococcus, Proteus, Acinetobacter, Ankis- trodesmus, Ideonella, , Chlorella, Aspergillus, In the tables in the text, we only list metabolic reactions Rhodobacter, Sarcina, Bacillus, Escherichia, and members known to be mediated by microorganisms. Our main cri- of the L subclass of the [138^141,144^150]. terion for including a reaction is a direct or inferred refer- In the laboratory, (per)chlorate reducers grow anaero- ence in the literature to that speci¢c metabolic process. In bically on organic acids and other organic compounds as this section, however, we include auxiliary aqueous redox their carbon source. Among the organic acids metabo- and disproportionation reactions (Table A.8) which, to lized, acetic acid is the most common, but propanoic, bu- our knowledge, have not yet been documented as en- tanoic, lactic, succinic, fumaric, and maleic acids can also ergy-yielding processes in microorganisms. Many of these be oxidized. To date, there are no known thermophiles or proposed metabolic reactions involve the oxidation or re- hyperthermophiles that can mediate this mode of respira- duction of trace aqueous species such as V, Cr, Mn, Co, tion (J.D. Coates, 1999, personal communication), As, Se, and Au. In addition, we list in Table A.8 one although one species, Acinetobacter thermotoleranticus,is 23 reaction denoting the hydrolysis of Cr2O7 and several thermotolerant to 47³C [139]. Based on a thermodynamic 0 hydrolysis reactions in the H^O^P system. Values of vGr analysis, neither thermophilic nor hyperthermophilic mi- for reactions in Table A.8 as a function of temperature are crobial chlorate and perchlorate reduction can be dis- listed in Table A.9. Reactions of the type given in Table missed a priori as an energy-yielding process. There- A.8 may be essential in linking microbial metabolism to fore, we calculated values of vG0 as a function of abiotic processes in both natural and arti¢cial aqueous temperature for Cl-species in di¡erent oxidation states systems. As noted in Section 5.8 above, most of the P in (Table A.12). A subset of reactions known to be carried metabolic processes does not undergo oxidation or reduc- out by (per)chlorate reducers is listed in Table A.13, and 0 tion, remaining predominantly in the +5 oxidation state of values of vGr as a function of temperature for these re- phosphate. However, in Table A.10, we list several redox actions is given in Table A.14. We did not include every processes in the H^O^P system which involve species with microbial Cl-redox reaction discussed in the literature as P in the +3 and +1 oxidation state of phosphite and hy- this would yield a table of unjusti¢ed length in a review on pophosphite as well as the +5 oxidation state of phos- thermophilic and hyperthermophilic metabolism. How- phate. These redox reactions can now be combined with ever, the reader can readily combine reactions and solutes

FEMSRE 711 7-3-01 216 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

Table 8.10 Table 8.10 (continued) Microorganisms that use the coupled carbon and sulfur reactions speci- Reaction ¢ed in Table 8.8 E55 D. thermocisternum [180]a Reaction E56 D. thermobenzoicum [211], D. kuznetsovii [207], E27 Cluster ANME-1 (suggested) [429] D. thermosapovorans [212]b E28 D. putei [175], D. luciae [175,208], D. kuznetsovii [207], E57 D. toluolica [434], D. kuznetsovii [207] D. thermobenzoicum [211], D. geothermicum [35], E58 D. kuznetsovii [207] D. hydrogenovorans [395], D. thermosapovorans [212], E59 D. kuznetsovii [207] A. degensii [187], D. australicum [178], A. fulgidus [328,329] E60 D. thermobenzoicum [211], D. toluolica [434], D. australicum E29 A. vene¢cus [295], D. putei [175], D. kuznetsovii [207], [170] D. thermobenzoicum [211], D. geothermicum [35], E61 D. thermobenzoicum [211] D. hydrogenovorans [395], D. thermosapovorans [212], E62 D. thermobenzoicum [211] D. australicum [178], A. fulgidus [328,329] E63 D. putei [175], D. kuznetsovii [207], D. thermosapovorans [212] E30 D. putei [175], D. luciae [175,208], D. kuznetsovii [207], E64 D. kuznetsovii [207], D. thermosapovorans [212] D. thermobenzoicum [211], D. thermosapovorans [212], E65 D. kuznetsovii [207], D. thermosapovorans [212] D. australicum [178], A. fulgidus [328,329] E66 T. tenax [377] E31 T. tenax [377], S. arcachonense [380] E67 D. nigri¢cans ssp. salinus [209], D. putei [175], D. luciae E32 D. thermoacetoxidans [210], Thermodesulforhabdus norvegicus [175,208], D. toluolica [434], D. kuznetsovii [207], [266], D. kuznetsovii [207], D. australicum [170] D. thermobenzoicum [211], D. geothermicum [35], E33 A. vene¢cus [295], D. kuznetsovii [207] D. thermocisternum [180], D. australicum [170] E34 D. kuznetsovii [207], D. propionica [214] E68 D. thermosapovorans [212], D. australicum [178], E35 Desulfuromonas palmitatis [430], Desulfuromonas acetoxidans D. rhabdoformis [396] [431], Geobacter sulfurreducens [432], D. kamchatkensis, E69 A. vene¢cus [295], D. putei [175], D. kuznetsovii [207], D. propionica [214], Desulfurella acetivorans [213] D. thermobenzoicum [211], D. geothermicum [35], E36 D. kuznetsovii [207], D. thermobenzoicum [211], D. thermocisternum [180] D. thermocisternum [180] E70 D. thermosapovorans [212], D. australicum [178], E37 Desulforhopalus vacuolatus [433], D. geothermicum [35], D. rhabdoformis [396] D. rhabdoformis [237] E71 D. kuznetsovii [207], D. thermobenzoicum [211], E38 D. kuznetsovii [207], D. thermobenzoicum [211], D. thermocisternum [180] D. thermocisternum [180] E72 D. thermosapovorans [212], D. australicum [178], E39 D. rhabdoformis [237], D. vacuolatus [433], D. geothermicum D. rhabdoformis [396] [35] E73 D. acetoxidans [431], T. tenax [377] E40 D. kuznetsovii [207], D. thermobenzoicum [211], D. propionica E74 D. toluolica [434], D. kuznetsovii [207], D. thermobenzoicum [214], D. thermocisternum [180] [211], D. thermocisternum [180] E41 D. rhabdoformis [237], D. vacuolatus [433] E75 D. rhabdoformis [396] E42 D. propionica [214] E76 D. thermosapovorans [212] E43 A. fulgidus [328^330], D. thermoacetoxidans [210], E77 D. kuznetsovii [207], D. thermobenzoicum [211], Desulfotomaculum nigri¢cans ssp. salinus [209], T. mobile D. thermocisternum [180] [264,265], D. kuznetsovii [207], D. thermobenzoicum [211], E78 D. rhabdoformis [396] D. thermosapovorans [212], D. australicum [170] E79 D. kuznetsovii [207], D. thermobenzoicum [211], E44 D. auripigmentum [393], D. vacuolatus [433], T. commune [263], D. thermocisternum [180] D. putei [175], D. luciae [175,208], T. yellowstonii [267], E80 D. rhabdoformis [396] D. geothermicum [35], D. thermocisternum [180], D. australicum E81 D. acetoxidans [431] [178], D. rhabdoformis [396] E82 D. thermobenzoicum [211], D. toluolica [434], D. kuznetsovii E45 D. nigri¢cans ssp. salinus [209], T. mobile [264,265], [207], D. thermocisternum [180] D. kuznetsovii [207], D. thermobenzoicum [211], E83 D. thermosapovorans [212], D. australicum [178] D. thermosapovorans [212], A. fulgidus [328^330] E84 D. thermobenzoicum [211], D. kuznetsovii [207], E46 D. australicum [178], D. rhabdoformis [396], D. vacuolatus D. thermocisternum [180] [433], D. geothermicum [35], D. putei [175], D. thermocisternum E85 D. thermosapovorans [212], D. australicum [178] [180] E86 D. thermobenzoicum [211], D. kuznetsovii [207], E47 D. nigri¢cans ssp. salinus [209], T. mobile [264,265], D. thermocisternum [180] D. kuznetsovii [207], D. thermobenzoicum [211], D. propionica E87 D. thermosapovorans [212], D. australicum [178] [214], D. thermosapovorans [212], A. fulgidus [328^330] E88 D. thermosapovorans [212] E48 S. barnesii strain SES-3 ([380,426], T. commune [263], D. putei E89 D. thermosapovorans [212] [175], D. luciae [175,208], D. australicum [178], D. rhabdoformis E90 D. thermosapovorans [212] [396], D. thermocisternum [180], Thermoanaerobacter E91 strain TD3[436] sulfurophilus [256] E92 strain TD3[436] E49 D. kamchatkensis, D. propionica [214] E93 strain TD3[436] E50 S. barnesii strain SES-3 [380,426], S. arcachonense [380], E94 strain TD3[436] T. sulfurophilus [256] E95 strain Hxd3[437] E51 D. thermocisternum [180]a E96 D. toluolica [434] E52 D. thermobenzoicum [211], Desulfobacula toluolica [434], aD. thermocisternum can also utilize long chain fatty acids C ^C and D. auripigmentum [435], D. kuznetsovii [207], D. geothermicum 5 10 C ^C with sulfate, sul¢te and thiosulfate for growth [180]. [35], D. thermosapovorans [212]b 14 17 bD. thermosapovorans can also utilize long chain fatty acids C ^C , E53 D. thermocisternum [180]a 5 10 C ,C ,C ,C , and C with sulfate, sul¢te and thiosulfate for E54 D. thermobenzoicum [211], D. kuznetsovii [207], 12 16 18 20 22 growth [212]. D. geothermicum [35], D. thermosapovorans [212]b

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 217

Table 8.11 Microbial redox reactions involving other halogens, Metabolic reactions involving amino acids such as Br and I, for example, have not received compa- a E97 3acetic acid(aq)+NH3(aq)+1.5O2(aq)H rable attention. Tsunogai and Sase (1969) [151] indicate glutamic acid(aq)+CO2(aq)+3H2O(l) that in near-surface seawater, use b E98 3ethanol(aq)+NH3(aq)+4.5O2(aq)H the enzyme to catalyze the reduction of glutamic acid(aq)+CO (aq)+6H O(l) 2 2 3 3 b iodate (IO ) to iodide (I ). The ability of chlorate reduc- E99 2lactic acid(aq)+NH3(aq)+1.5O2(aq)H 3 3 glutamic acid(aq)+CO2(aq)+3H2O(l) ers to make use of bromate (BrO3 ) or iodate as an elec- E100 serine(aq)+H2O(l)Hacetic acid(aq)+formic acid(aq)+NH3(aq) tron acceptor is only now starting to be investigated in E101 threonine(aq)+H2O(l)H detail (J.D. Coates, 1999, personal communication). In propanoic acid(aq)+formic acid(aq)+NH3(aq) anticipation of the discovery of a wide variety of halate E102c serine(aq)+0.5H O(l)H1.25acetic acid(aq)+0.5CO (aq)+NH (aq) 2 2 3 0 c 23 ‡ reducers, we included in Table A.12 values of vG as a E103 alanine(aq)+0.5H2O(l)+0.5S2O3 +H H acetic acid(aq)+CO2(aq)+H2S(aq)+NH3(aq) function of temperature for Br and I compounds in vari- c 23 ‡ E104 asparagine(aq)+1.5H2O(l)+0.5S2O3 +H H ous oxidation states ranging from +7 for perbromate acetic acid(aq)+2CO2(aq)+H2S(aq)+2NH3(aq) (BrO3) and periodate (IO3)to31 for bromide (Br3) E105c methionine(aq)+H O(l)+S O23+2H‡H 4 4 2 2 3 and iodide. To ensure that the appropriate protonated propanoic acid(aq)+2CO2(aq)+3H2S(aq)+NH3(aq) d or deprotonated forms of Cl-, Br-, and I-species are used E106 methionine(aq)+threonine(aq)+5H2O(l)H2propanoic acid(aq)+3formic acid(aq)+2NH3(aq)+H2S(aq)+2H2(aq) in writing reactions, we included several dissociation reac- e E107 glutamic acid(aq)+H2(aq)Halanine(aq)+acetic acid(aq) tions for the halogen-containing compounds in Table A.5 e E108 glutamic acid(aq)+2H2O(l)H 0 and their values of vGr as function of temperature in 2acetic acid(aq)+formic acid(aq)+NH3(aq) e Table A.6. E109 glutamic acid(aq)+2H2O(l)H 2acetic acid(aq)+CO2(aq)+NH3(aq)+H2(aq) E110 alanine(aq)+2glycine(aq)+2H2O(l)H 3acetic acid(aq)+CO2(aq)+3NH3(aq) A.9. Mineral redox and hydrolysis and cation hydrolysis aReaction taken from Yamada et al. (1972) [438]. reactions bReaction inferred from Yamada et al. (1972) [438]. cReaction inferred from Magot et al. (1997) [439]. As noted in the text (see Section 5.7), numerous mineral d Reaction inferred from Tarlera et al. (1997) [200]. oxidation or reduction reactions are known to be micro- eReaction inferred from Tarlera et al. (1997) [200] who state that `the fermentation products from glutamate (10 mM) included acetate (15.9 bially mediated, energy-yielding processes. Perhaps the mM), formate (2.7), alanine (1.9 mM), bicarbonate (5.2 mM) (which most well-known of these redox processes involve iron was not measured but calculated by subtracting the amount of formate sul¢de minerals such as pyrite (FeS2) or pyrrhotite from half of the amount of acetate), and hydrogen (2.2 mmol per liter)'. (FeS). Here, we include mineral redox reactions (Table Mass balance determined for the overall reaction matches the sum of A.15) which, to our knowledge, have not been docu- these reactions using stoichiometry imposed from the concentrations of the measured products alanine, formate, and acetate. mented in the literature as being microbially mediated, 0 but may well be. Values of vGr as a function of temper- in Tables A.12 and A.13 with reactions and chemical spe- ature for these reactions are listed in Table A.16. Regard- cies given in tables throughout the text and appendix to less of whether these reactions are biotically or abiotically generate a wide array of known and hypothesized Cl-re- catalyzed, they can be coupled to known microbial meta- dox reactions. bolic processes in order to describe accurately many net

Table 8.12 0 31 Values of vGr (kJ mol )atPSAT as a function of temperature for reactions given in Table 8.11 Reaction T (³C) 218253745557085100115150200 E97 3635.10 3631.78 3630.24 3627.48 3625.58 3623.12 3619.30 3615.32 3611.18 3606.90 3596.37 3580.06 E98 32219.88 32218.93 32218.25 32216.81 32215.67 32214.06 32211.29 32208.14 32204.62 32200.78 32190.56 32173.06 E99 3752.29 3750.94 3750.23 3748.90 3747.94 3746.64 3744.56 3742.30 3739.89 3737.33 3730.83 3720.27 E100 335.79 338.56 339.82 342.04 343.55 345.48 348.45 351.50 354.63 357.84 365.61 377.40 E101 346.48 349.91 351.45 354.16 355.99 358.33 361.92 365.59 369.35 373.20 382.50 396.54 E102 374.86 377.14 378.22 380.17 381.52 383.28 386.03 388.91 391.91 395.01 3102.65 3114.43 E103 379.35 383.58 385.62 389.35 391.97 395.42 3100.88 3106.67 3112.78 3119.20 3135.29 3160.93 E104 399.92 3105.11 3107.65 3112.34 3115.68 3120.05 3127.01 3134.42 3142.23 3150.43 3170.99 3203.60 E105 30.15 37.48 311.08 317.70 322.41 328.61 338.50 349.06 360.25 372.04 3101.79 3149.54 E106 257.45 248.96 245.07 238.18 233.43 227.35 217.90 208.09 197.93 187.44 161.71 122.02 E107 361.09 361.55 361.74 362.06 362.26 362.50 362.84 363.15 363.43 363.68 364.14 364.55 E108 11.60 8.05 6.44 3.61 1.69 30.77 34.56 38.45 312.44 316.54 326.44 341.43 E109 15.61 12.16 10.49 7.44 5.29 2.49 31.96 36.65 311.58 316.73 329.53 349.53 E110 341.14 346.15 348.51 352.81 355.82 359.75 365.95 372.50 379.39 386.58 3104.50 3132.52

FEMSRE 711 7-3-01 218 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

Table 8.13 [2] Olsen, G.J. and Woese, C.R. (1997) Archaeal genomics: an overview. Microorganisms that use the reactions speci¢ed in Table Cell 89, 991^994. 8.11 [3] Pennisi, E. (1998) Genome data shake the tree of life. Science 280, 672^674. Reaction [4] Woese, C. (1998) The universal ancestor. Proc. Natl. Acad. Sci. USA E97 £avum, acetoacidophilum, 95, 6854^6859. Corynebacterium acetoglutamicum, Corynebacterium [5] Pace, N.R. (1997) A molecular view of microbial diversity and the acetophilum [438] biosphere. Science 276, 734^740. E98 Brevibacterium [438] [6] Thauer, R.K., Jungermann, K. and Decker, K. (1977) Energy con- E99 Brevibacterium glutaricum [438] servation in chemotrophic anaerobic bacteria. Bacteriol. Rev. 41, E100 E. coli [440] 100^180. E101 E. coli [440] [7] Madigan, M.T., Martinko, J.M. and Parker, J. (2000) Brock Biology E102 Dethiosulfovibrio peptidovorans [439] of Microorganisms, edn. 9, Prentice Hall, Upper Saddle River, NJ. E103 D. peptidovorans [439] [8] Kelly, R.M. and Adams, M.W.W. (1994) Metabolism in hyperther- E104 D. peptidovorans [439] mophilic microorganisms. 66, 247^270. E105 D. peptidovorans [439] [9] Blo«chl, E., Rachel, R., Burggraf, S., Hafenbradl, D., Jannasch, H.W. E106 Caloramator proteoclasticus [200] and Stetter, K.O. (1997) Pyrolobus fumarii, gen. and sp. nov., repre- E107 C. proteoclasticus [200] sents a novel group of archaea, extending the upper temperature limit E108 C. proteoclasticus [200] for life to 113³C. 1, 14^21. E109 C. proteoclasticus [200] [10] Daniel, R.M. (1992) Modern life at high temperatures. Orig. Life E110 Clostridium sporogenes [441] Evol. Biosph. 22, 33^42. [11] Segerer, A.H., Burggraf, S., Fiala, G., Huber, G., Huber, R., Pley, U. and Stetter, K.O. (1993) Life in hot springs and hydrothermal vents. biogeochemical processes including mineral dissolution Orig. Life Evol. Biosph. 23, 77^90. and precipitation. In this vein, mineral and cation hydro- [12] Baross, J.A. and Deming, J.W. (1983) Growth of `black smoker' lysis reactions (Tables A.15 and A17, respectively) may bacteria at temperatures of at least 250³C. Nature 303, 423^426. [13] Straube, W.L., Deming, J.W., Somerville, C.C., Colwell, R.R. and also prove helpful to best characterize the chemical pro- Baross, J.A. (1990) Particulate DNA in smoker £uids: evidence for 0 cesses in biogeochemical systems. Values of vGr as a func- existence of microbial populations in hot hydrothermal systems. tion of temperature for reactions given in Tables A.15 and Appl. Environ. Microbiol. 56, 1440^1447. A17 are in Tables A.16 and A18, respectively. Chemical [14] Deming, J.W. and Baross, J.A. (1993) Deep-sea smokers: Windows formulas for minerals mentioned in Tables 9.1, 9.2, 9.5 to a subsurface biosphere. Geochim. Cosmochim. Acta 57, 3219^ 3230. and A15 are listed in Table A.19. [15] Cragg, B.A. and Parkes, R.J. (1994) Bacterial pro¢les in hydrother- mally active deep sediment layers from Middle Valley (N.E. Paci¢c), sites 857 and 858. Proc. Ocean Drill. Prog. Sci. Res. 139. References [16] Bargar, K.E., Fournier, R.O. and Theodore, T.G. (1985) Particles in £uid inclusions from Yellowstone National Park ^ Bacteria? Geology [1] Woese, C.R., Kandler, O. and Wheelis, M.L. (1990) Towards a nat- 13, 483^486. ural system of organisms: Proposal for the domains Archaea, Bac- [17] White, R.H. (1984) Hydrolytic stability of biomolecules at high tem- teria, and Eucarya. Proc. Natl. Acad. Sci. USA 87, 4576^4579. peratures and its implication for life at 250³C. Nature 310, 430^432.

Table 8.14

Standard and overall Gibbs free energies of heterotrophic reactions in which organic compounds are oxidized to CO2 coupled to the reduction of sul- fate to sul¢de

0 31 23 Reaction vGr (kJ mol ) vGr (per mol of organic C species) vGr (per mol of SO4 ) E27 3134.48 363.05 363.05 E28 3312.02 360.15 3240.59 E32 3162.91 3120.06 3120.06 E36 31105.46 3208.50 3119.14 E43 3617.44 3258.72 3172.48 E51 3787.87 3301.07 3120.43 E57 31265.65 3277.12 3158.36 E60 3606.15 3509.71 3135.92 E63 3665.88 3112.89 3150.53 E67 3539.93 3191.39 3127.59 E74 3768.55 3280.69 3124.75 E82 3505.55 3376.97 3125.66 E88 32460.78 3461.61 3123.10 E91 3931.56 3685.11 3109.62 E92 31042.42 3770.97 3110.14 E93 31158.32 3861.87 3111.21 E94 31271.77 3950.31 3111.80 E95 31838.97 31392.50 3113.67 E96 3684.79 3534.78 3118.84

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 219

Table 9.1 0 31 a Values of vG (in kJ mol )atPSAT as a function of temperature for minerals and aqueous compounds containing metals Compound T (³C) 2 18 25 37 45 55 70 85 100 115 150 200 Mg2‡ 3457.12 3454.95 3453.98 3452.32 3451.21 3449.82 3447.73 3445.65 3443.55 3441.45 3436.47 3429.13 MgOH‡ 3626.45 3625.05 3624.48 3623.55 3622.97 3622.27 3621.27 3620.35 3619.49 3618.68 3616.98 3614.86 ‡ MgHCO3 31046.70 31046.70 31046.80 31046.80 31047.00 31047.00 31047.40 31047.40 31047.80 31048.40 31050.10 31053.30 MgCO3(aq) 31001.20 3999.66 3998.97 3997.74 3996.89 3995.81 3994.15 3992.44 3990.69 3988.91 3984.63 3978.30 Magnesite 31026.40 31027.40 31027.80 31028.60 31029.20 31029.90 31031.10 31032.20 31033.50 31034.80 31037.90 31043.00 Ca2‡ 3554.05 3553.18 3552.79 3552.10 3551.64 3551.05 3550.16 3549.24 3548.31 3547.35 3545.00 3541.28 CaOH‡ 3716.07 3716.52 3716.72 3717.06 3717.29 3717.58 3718.02 3718.47 3718.94 3719.41 3720.54 3722.15 ‡ CaHCO3 31144.40 31145.30 31145.70 31146.60 31147.20 31148.00 31149.40 31150.90 31152.50 31154.20 31158.60 31165.60 CaCO3(aq) 31099.40 31099.70 31099.80 31099.90 31099.90 31099.90 31099.90 31099.80 31099.70 31099.60 31099.10 31098.20 Calcite 31127.10 31128.50 31129.20 31130.30 31131.10 31132.10 31133.60 31135.20 31136.90 31138.60 31142.80 31149.30 Dolomite 32162.90 32165.20 32166.30 32168.20 32169.50 32171.20 32173.80 32176.60 32179.40 32182.40 32189.60 32201.00 33 VO4 3902.69 3900.18 3899.14 3897.41 3896.29 3894.94 3892.96 3891.04 3889.15 3887.28 3882.82 3875.66 23 HVO4 3974.86 3974.79 3974.87 3975.16 3975.43 3975.86 3976.68 3977.65 3978.77 3980.02 3983.28 3988.36 3 H2VO4 31018.21 31020.02 31020.86 31022.35 31023.38 31024.70 31026.76 31028.90 31031.10 31033.35 31038.80 31046.82 H3VO4(aq) 31039.16 31041.58 31042.66 31044.54 31045.81 31047.43 31049.90 31052.41 31054.97 31057.59 31063.85 31073.21 ‡ VO2 3587.92 3587.31 3587.02 3586.50 3586.14 3585.68 3584.97 3584.24 3583.49 3582.72 3580.83 3577.89 VOOH‡ 3653.27 3651.98 3651.44 3650.59 3650.04 3649.39 3648.48 3647.63 3646.85 3646.11 3644.57 3642.69 VO2‡ 3449.64 3447.38 3446.43 3444.86 3443.83 3442.60 3440.80 3439.06 3437.38 3435.76 3432.09 3427.03 VO‡ 3443.16 3443.75 3443.92 3444.10 3444.16 3444.17 3444.07 3443.84 3443.50 3443.05 3441.60 3438.68 VOH2‡ 3467.42 3466.82 3466.52 3465.96 3465.57 3465.05 3464.24 3463.37 3462.47 3461.51 3459.09 3455.14 V3‡ 3247.50 3243.86 3242.25 3239.48 3237.63 3235.30 3231.81 3228.28 3224.74 3221.16 3212.65 3199.93 VOH‡ 3419.25 3418.05 3417.56 3416.76 3416.26 3415.66 3414.82 3414.04 3413.32 3412.65 3411.25 3409.56 V2‡ 3220.50 3218.47 3217.56 3216.00 3214.94 3213.62 3211.61 3209.59 3207.54 3205.46 3200.51 3193.05 23 Cr2O7 31302.41 31307.35 31309.47 31313.06 31315.42 31318.35 31322.69 31326.97 31331.18 31335.33 31344.71 31357.19 23 CrO4 3729.76 3730.94 3731.36 3732.00 3732.36 3732.75 3733.22 3733.56 3733.76 3733.82 3733.43 3731.32 3 HCrO4 3764.12 3767.24 3768.60 3770.95 3772.51 3774.47 3777.41 3780.37 3783.32 3786.28 3793.17 3802.86 3 CrO2 3524.80 3524.44 3524.26 3523.90 3523.64 3523.31 3522.76 3522.17 3521.54 3520.87 3519.10 3515.95 HCrO2(aq) 3577.07 3577.62 3577.81 3578.08 3578.22 3578.36 3578.51 3578.60 3578.63 3578.61 3578.36 3577.64 CrO‡ 3390.66 3389.03 3388.27 3386.92 3385.99 3384.81 3382.97 3381.08 3379.13 3377.13 3372.27 3364.82 CrOH2‡ 3424.99 3421.84 3420.49 3418.19 3416.67 3414.79 3412.01 3409.25 3406.52 3403.81 3397.51 3388.43 Cr3‡ 3213.57 3208.51 3206.27 3202.38 3199.77 3196.48 3191.51 3186.48 3181.40 3176.26 3163.98 3145.64 3 MnO4 3445.71 3448.84 3450.20 3452.54 3454.09 3456.04 3458.95 3461.87 3464.79 3467.70 3474.47 3483.93 23 MnO4 3501.98 3503.28 3503.75 3504.47 3504.88 3505.34 3505.89 3506.29 3506.57 3506.69 3506.42 3504.44 Mn3‡ 391.94 387.09 384.93 381.19 378.68 375.50 370.70 365.84 360.92 355.94 344.02 326.15 Mn2‡ 3232.07 3231.01 3230.54 3229.72 3229.17 3228.49 3227.45 3226.41 3225.37 3224.31 3221.76 3217.86 MnOH‡ 3407.10 3407.09 3407.10 3407.12 3407.15 3407.20 3407.28 3407.40 3407.53 3407.69 3408.12 3408.83 MnO(aq) 3338.09 3339.03 3339.65 3339.91 3340.16 3340.40 3340.62 3340.76 3340.86 3341.00 3341.06 3341.18 23 MnO2 3430.43 3429.70 3429.28 3428.45 3427.82 3426.97 3425.57 3424.00 3422.28 3420.41 3415.42 3406.54 3 HMnO2 3507.12 3506.53 3506.26 3505.80 3505.49 3505.11 3504.52 3503.93 3503.33 3502.72 3501.18 3498.59 Alabandite 3216.51 3217.76 3218.31 3219.29 3219.95 3220.80 3222.09 3223.42 3224.78 3226.16 3229.51 3234.53 Rhodochrosite 3813.84 3815.38 3816.07 3817.29 3818.13 3819.19 3820.84 3822.55 3824.31 3826.13 3830.58 3837.41 Fe3‡ 323.53 319.17 317.23 313.89 311.64 38.82 34.54 30.22 4.14 8.56 19.09 34.87 FeOH2‡ 3244.24 3242.57 3241.83 3240.55 3239.69 3238.61 3236.97 3235.32 3233.65 3231.96 3227.93 3221.84 FeO‡ 3223.02 3222.48 3222.17 3221.56 3221.12 3220.51 3219.52 3218.44 3217.28 3216.03 3212.84 3207.61

HFeO2(aq) 3420.54 3422.32 3423.00 3424.05 3424.67 3425.38 3426.32 3427.11 3427.77 3428.32 3429.19 3429.56 3 FeO2 3366.92 3367.86 3368.19 3368.67 3368.94 3369.22 3369.53 3369.73 3369.83 3369.82 3369.41 3367.77 Hematite 3743.48 3744.80 3745.40 3746.48 3747.22 3748.19 3749.69 3751.27 3752.92 3754.64 3758.91 3765.62 31011.72 31013.93 31014.93 31016.72 31017.95 31019.53 31021.99 31024.56 31027.23 31029.99 31036.82 31047.44 Fe2‡ 393.90 392.24 391.50 390.22 389.37 388.29 386.66 385.02 383.36 381.68 377.67 371.62 FeOH‡ 3276.53 3275.81 3275.52 3275.03 3274.72 3274.35 3273.83 3273.35 3272.90 3272.48 3271.60 3270.48 FeO(aq) 3213.17 3212.51 3212.21 3211.71 3211.38 3210.97 3210.35 3209.75 3209.16 3208.59 3207.30 3205.58 3 HFeO2 3400.68 3399.60 3399.15 3398.42 3397.96 3397.40 3396.61 3395.85 3395.14 3394.45 3392.91 3390.62 Pyrrhotite 399.43 3100.35 3100.77 3101.50 3102.01 3102.66 3103.66 3104.71 3105.79 3106.91 3109.73 3114.30 Siderite 3677.20 3678.82 3679.54 3680.82 3681.70 3682.82 3684.54 3686.32 3688.16 3690.05 3694.66 3701.71 Pyrite 3159.06 3159.85 3160.22 3160.87 3161.32 3161.90 3162.81 3163.76 3164.75 3165.78 3168.33 3172.32 Co3‡ 126.98 131.76 133.89 137.58 140.06 143.19 147.92 152.71 157.56 162.47 174.21 191.81 CoOH2‡ 398.88 397.04 396.23 394.83 393.89 392.72 390.94 389.17 387.37 385.57 381.27 374.83 Co2‡ 356.95 355.18 354.39 353.03 352.11 350.97 349.23 347.48 345.71 343.93 339.67 333.25 CoOH‡ 3235.47 3234.71 3234.41 3233.93 3233.63 3233.29 3232.83 3232.43 3232.07 3231.76 3231.18 3230.63 CoO(aq) 3185.82 3184.61 3184.09 3183.20 3182.62 3181.90 3180.82 3179.77 3178.74 3177.74 3175.47 3172.43 3 HCoO2 3351.54 3349.70 3348.95 3347.70 3346.90 3345.94 3344.56 3343.26 3342.00 3340.80 3338.10 3334.31 23 CoO2 3267.43 3265.37 3264.42 3262.76 3261.61 3260.15 3257.89 3255.56 3253.15 3250.66 3244.42 3234.25

FEMSRE 711 7-3-01 220 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

Table 9.1 (continued) Compound T (³C) 2 18 25 37 45 55 70 85 100 115 150 200 Ni2‡ 348.51 346.50 345.60 344.04 343.00 341.68 339.68 337.66 335.61 333.55 328.59 321.13 NiOH‡ 3222.98 3221.66 3221.12 3220.25 3219.70 3219.04 3218.12 3217.27 3216.48 3215.75 3214.22 3212.38 NiO(aq) 3162.23 3163.87 3164.59 3165.86 3166.72 3167.80 3169.45 3171.13 3172.84 3174.58 3178.76 3184.99 3 HNiO2 3346.67 3344.08 3343.00 3341.24 3340.11 3338.76 3336.81 3334.96 3333.18 3331.49 3327.71 3322.53 23 NiO2 3272.27 3269.74 3268.61 3266.64 3265.31 3263.63 3261.08 3258.48 3255.82 3253.10 3246.43 3235.80 Cu2‡ 63.37 64.91 65.59 66.75 67.53 68.50 69.96 71.41 72.87 74.34 77.80 82.98 CuOH‡ 3127.01 3126.54 3126.36 3126.06 3125.89 3125.69 3125.42 3125.19 3125.00 3124.83 3124.56 3124.35 CuO(aq) 388.21 387.39 387.03 386.40 385.99 385.47 384.69 383.92 383.15 382.39 380.58 377.89 3 HCuO2 3251.32 3251.44 3251.46 3251.45 3251.42 3251.37 3251.24 3251.07 3250.86 3250.62 3249.91 3248.52 23 CuO2 3174.37 3173.04 3172.38 3171.17 3170.31 3169.18 3167.39 3165.48 3163.45 3161.30 3155.75 3146.28 Chalcopyrite 3184.95 3186.96 3187.87 3189.45 3190.54 3191.92 3194.05 3196.24 3198.50 3200.82 3206.46 3215.01 Covellite 351.28 352.31 352.77 353.58 354.13 354.84 355.92 357.03 358.17 359.35 362.19 366.48 Cu‡ 50.88 50.28 50.00 49.50 49.15 48.70 47.99 47.24 46.46 45.65 43.66 40.61 Chalcocite 383.59 385.46 386.30 387.77 388.77 390.04 391.99 394.00 396.05 398.28 3103.77 3112.09 Cuprite 3145.98 3147.41 3148.05 3149.17 3149.94 3150.91 3152.41 3153.95 3155.53 3157.15 3161.08 3167.00 Bornite 3353.45 3359.89 3362.78 3367.82 3371.25 3375.60 3382.28 3389.11 3396.11 3403.26 3420.51 3446.42 Copper 0.74 0.23 0 30.41 30.68 31.03 31.57 32.13 32.70 33.29 34.72 36.87 Zn2‡ 3149.76 3148.04 3147.27 3145.95 3145.07 3143.96 3142.30 3140.63 3138.95 3137.26 3133.26 3127.29 ZnOH‡ 3338.29 3339.26 3339.70 3340.46 3340.98 3341.64 3342.67 3343.71 3344.79 3345.89 3348.54 3352.50 ZnO(aq) 3282.23 3282.14 3282.08 3281.97 3281.89 3281.78 3281.61 3281.43 3281.24 3281.05 3280.59 3279.93 23 ZnO2 3394.10 3391.49 3390.32 3388.30 3386.94 3385.22 3382.61 3379.97 3377.26 3374.50 3367.75 3357.05 3 HZnO2 3464.87 3463.73 3463.25 3462.47 3461.97 3461.36 3460.49 3459.66 3458.86 3458.09 3456.33 3453.70 Sphalerite 3199.30 3200.20 3200.61 3201.33 3201.82 3202.44 3203.40 3204.39 3205.41 3206.46 3209.02 3212.89 33 AsO4 3651.63 3649.49 3648.39 3646.33 3644.84 3642.86 3639.68 3636.23 3632.52 3628.57 3618.30 3600.79 23 HAsO4 3714.41 3714.58 3714.59 3714.52 3714.43 3714.28 3713.95 3713.51 3712.98 3712.33 3710.34 3706.11 3 H2AsO4 3750.46 3752.35 3753.17 3754.57 3755.51 3756.68 3758.45 3760.21 3761.97 3763.73 3767.79 3773.33 H3AsO4(aq) 3761.96 3764.81 3766.09 3768.33 3769.85 3771.77 3774.71 3777.72 3780.79 3783.91 3791.43 3802.69 3 AsO2 3348.93 3349.70 3349.99 3350.45 3350.74 3351.06 3351.50 3351.88 3352.21 3352.49 3352.90 3352.82 HAsO2(aq) 3399.78 3401.79 3402.67 3404.19 3405.20 3406.47 3408.40 3410.34 3412.30 3414.27 3418.95 3425.79 23 SeO4 3439.93 3441.01 3441.41 3442.01 3442.35 3442.73 3443.19 3443.52 3443.73 3443.83 3443.54 3441.67 3 HSeO4 3448.91 3451.25 3452.29 3454.10 3455.32 3456.85 3459.18 3461.53 3463.91 3466.31 3471.94 3479.93 23 SeO3 3369.30 3369.75 3369.87 3369.96 3369.97 3369.92 3369.72 3369.39 3368.93 3368.34 3366.40 3362.07 3 HSeO3 3408.37 3410.51 3411.46 3413.09 3414.18 3415.55 3417.63 3419.73 3421.84 3423.95 3428.89 3435.81 H2SeO3(aq) 3421.50 3424.70 3426.14 3428.68 3430.40 3432.59 3435.95 3439.39 3442.92 3446.52 3455.20 3468.28 Seleniumb 0.95 0.29 0 30.51 30.86 31.31 31.98 32.68 33.39 34.12 35.87 38.50 HSe3 45.85 44.49 43.93 42.99 42.39 41.65 40.57 39.53 38.53 37.58 35.51 33.08 23 MoO4 3837.40 3838.20 3838.48 3838.88 3839.11 3839.34 3839.61 3839.77 3839.82 3839.76 3839.17 3836.96 3 HMoO4 3860.57 3862.64 3863.58 3865.24 3866.38 3867.83 3870.06 3872.35 3874.70 3877.09 3882.81 3891.13 Molybdeniteb 3261.58 3262.53 3262.96 3263.73 3264.25 3264.93 3265.99 3267.08 3268.22 3269.40 3272.29 3276.76 Ag‡ 78.76 77.61 77.10 76.21 75.61 74.84 73.68 72.49 71.27 70.04 67.07 62.66 Silver 0.95 0.29 0 30.52 30.87 31.31 32.00 32.70 33.41 34.15 35.91 38.54 23 WO4 3913.08 3913.91 3914.21 3914.65 3914.91 3915.18 3915.51 3915.74 3915.86 3915.89 3915.50 3913.61 3 HWO4 3931.83 3933.81 3934.71 3936.30 3937.40 3938.80 3940.96 3943.19 3945.48 3947.81 3953.41 3961.57 Au3‡ 428.23 431.86 433.47 436.22 438.07 440.38 443.87 447.38 450.91 454.47 462.95 475.61 Au‡ 165.65 163.92 163.18 161.89 161.03 159.95 158.34 156.71 155.07 153.42 149.55 143.96 Gold 1.07 0.33 0 30.58 30.97 31.46 32.22 32.99 33.78 34.58 36.51 39.39 Hg2‡ 163.85 164.43 164.68 165.12 165.40 165.75 166.28 166.79 167.29 167.80 168.99 170.82 HgOH‡ 351.72 352.66 353.14 354.02 354.66 355.50 356.86 358.32 359.88 361.53 365.68 372.26 HgO(aq) 336.33 336.99 337.24 337.63 337.86 338.14 338.51 338.84 339.14 339.41 339.93 340.48 3 HHgO2 3188.77 3189.04 3189.12 3189.20 3189.24 3189.25 3189.22 3189.13 3188.97 3188.77 3188.04 3186.30 Quicksilver 1.72 0.53 0 30.92 31.54 32.32 33.51 34.72 35.95 37.18 310.14 314.49 Pb2‡ 323.42 323.76 323.89 324.09 324.21 324.35 324.55 324.72 324.87 325.00 325.19 325.16 PbOH‡ 3226.60 3226.01 3225.73 3225.21 3224.84 3224.37 3223.63 3222.85 3222.04 3221.20 3219.11 3215.81 PbO(aq) 3162.34 3163.98 3164.64 3165.71 3166.38 3167.18 3168.31 3169.36 3170.35 3171.28 3173.23 3175.58 Galena 394.66 396.08 396.72 397.82 398.57 399.52 3100.98 3102.47 3103.99 3105.54 3109.26 3114.80 Anglesite 3809.86 3812.15 3813.18 3814.98 3816.22 3817.79 3820.20 3822.68 3825.23 3827.84 3834.17 3843.72 3 HPbO2 3336.87 3338.35 3338.90 3339.74 3340.23 3340.78 3341.47 3342.03 3342.45 3342.74 3342.95 3342.05 2‡ UO2 3954.91 3953.30 3952.61 3951.44 3950.67 3949.71 3948.30 3946.90 3945.50 3944.11 3940.85 3936.02 ‡ UO2OH 31159.63 31159.90 31160.01 31160.23 31160.37 31160.56 31160.86 31161.17 31161.50 31161.84 31162.68 31163.90 UO3(aq) 31132.17 31131.32 31130.94 31130.29 31129.86 31129.32 31128.52 31127.73 31126.95 31126.18 31124.43 31122.02 3 HUO4 31319.16 31317.73 31317.12 31316.13 31315.49 31314.72 31313.60 31312.52 31311.48 31310.46 31308.14 31304.70 23 UO4 31240.88 31239.24 31238.46 31237.06 31236.08 31234.82 31232.84 31230.75 31228.56 31226.26 31220.41 31210.61 ‡ UO2 3961.50 3961.19 3961.02 3960.70 3960.47 3960.16 3959.65 3959.11 3958.53 3957.91 3956.35 3953.77

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 221

Table 9.1 (continued) Compound T (³C) 2 18 25 37 45 55 70 85 100 115 150 200

UO2OH(aq) 31095.97 31094.95 31094.53 31093.86 31093.44 31092.94 31092.24 31091.60 31091.02 31090.50 31089.47 31088.44 3 UO3 3991.83 3990.51 3989.93 3988.96 3988.32 3987.53 3986.36 3985.19 3984.04 3982.88 3980.14 3975.91 U4‡ 3539.48 3532.82 3529.90 3524.90 3521.56 3517.40 3511.15 3504.89 3498.61 3492.30 3477.37 3455.34 UOH3‡ 3768.66 3765.40 3764.00 3761.61 3760.04 3758.10 3755.22 3752.36 3749.53 3746.71 3740.14 3730.53 UO2‡ 3758.74 3756.60 3755.63 3753.93 3752.78 3751.32 3749.09 3746.81 3744.48 3742.12 3736.39 3727.66 ‡ HUO2 3976.81 3976.04 3975.71 3975.14 3974.76 3974.30 3973.61 3972.93 3972.25 3971.59 3970.04 3967.79 UO2(aq) 3980.80 3978.99 3978.22 3976.93 3976.09 3975.07 3973.57 3972.13 3970.73 3969.38 3966.39 3962.49 Uraninite 31030.10 31031.28 31031.82 31032.76 31033.40 31034.22 31035.49 31036.81 31038.16 31039.56 31042.97 31048.19 3 HUO3 31151.10 31148.07 31146.83 31144.83 31143.56 31142.05 31139.91 31137.91 31136.03 31134.26 31130.44 31125.46 aSee text for discussion of nonconventional hydroxide species and Table A.19 in the Appendix for chemical formulas of the minerals. bSee Table A.2 in the Appendix for the thermodynamic properties and equation of state parameters used to calculate these values of vG0.

[18] Yanagawa, H. and Kojima, K. (1985) Thermophilic microspheres of (1994) Deep bacterial biosphere in Paci¢c Ocean sediments. Nature peptide-like and silicates formed at 250³C. J. Biochem. 97, 371, 410^413. 1521^1524. [29] Stevens, T.O., McKinley, J.P., Boone, D.R., Gri¤n, W.T., Russell, [19] Hennet, R.J.-C., Holm, N.G. and Engel, M.H. (1992) Abiotic syn- B.F., Colwell, F.S., Phelps, T.J. and Balkwill, D.L. (1993) Detection thesis of amino acids under hydrothermal conditions and the origin of anaerobic bacteria in 2800-m-deep samples from the terrestrial of life: a perpetual phenomenon? Naturwissenschaften 79, 361^365. subsurface (Abstract). Am. Soc. Microbiol., 16^20. [20] Helgeson, H.C. and Amend, J.P. (1994) Relative stabilities of bio- [30] Stevens, T.O. and McKinley, J.P. (1995) Lithoautotrophic microbial molecules at high temperatures and pressures. Thermochim. Acta ecosystems in deep basalt aquifers. Science 270, 450^454. 245, 89^119. [31] Onstott, T.C., Tobin, K., Dong, H., DeFlaun, M.F., Frederickson, [21] Pace, N.R. (1991) Origin of life: Facing up to the physical setting. J.K., Bailey, T., Brockman, F., Kieft, T., Peacock, A., White, D.C., Cell 65, 531^533. Balkwill, D., Phelps, T.J. and Boone, D.R. (1997) The deep gold [22] Russell, M.J. and Hall, A.J. (1997) The of life from iron mines of South Africa: Windows into the subsurface biosphere. monosulphide bubbles at a submarine hydrothermal redox and pH Proc. SPIE-Int. Soc. Opt. Eng. 3111, 344^357. front. J. Geol. Soc. Lond. 154, 377^402. [32] Kieft, T.L., Fredrickson, J.K., Onstott, T.C., Gorby, Y.A., Kostan- [23] Galtier, N., Tourasse, N. and Gouy, M. (1999) A nonhyperthermo- darithes, H.M., Bailey, T.J., Kennedy, D.W., Li, S.W., Plymale, A.E., philic common ancestor to extant life forms. Science 283, 220^221. Spadoni, C.M. and Gray, M.S. (1999) Dissimilatory reduction of [24] Brock, T.D. (1971) Bimodal distribution of pH values of thermal Fe(III) and other electron acceptors by a Thermus isolate. Appl. springs of the world. Geol. Soc. Am. Bull. 82, 1393^1394. Environ. Microbiol. 65, 1214^1221. [25] Holden, J.F. and Baross, J.A. (1995) Enhanced thermotolerance by [33] Szewzyk, U., Szewzyk, R. and Stenstrom, T. (1994) Thermophilic, hydrostatic pressure in the deep-sea hyperthermophile Pyrococcus anaerobic bacteria isolated from a granite in Sweden. Proc. Natl. strain ES4. FEMS Microbiol. Ecol. 18, 27^34. Acad. Sci. USA 91, 1810^1813. [26] Miller, J.F., Shah, N.N., Nelson, C.M., Ludlow, J.M. and Clark, [34] Szewzyk, U., Szewzyk, R. and Stenstrom, T. (1997) Thermophilic D.S. (1988) Pressure and temperature e¡ects on growth and methane fermentative bacteria from a deep borehole in granitic rock in Swe- production of the extreme thermophile Methanococcus jannaschii. den. Proc. SPIE-Int. Soc. Opt. Eng. 3111, 330^334. Appl. Environ. Microbiol. 54, 3039^3042. [35] Daumas, S., Cord-Ruwisch, R. and Garcia, J.L. (1988) Desulfotoma- [27] Whitman, W.B., Coleman, D.C. and Wiebe, W.J. (1998) Prokary- culum geothermicum sp. nov., a thermophilic, fatty acid-degrading,

otes: the unseen majority. Proc. Natl. Acad. Sci. USA 95, 6578^ sulfate reducing bacterium isolated with H2 from geothermal ground 6583. water. Antonie Van Leeuwenhoek 54, 165^178. [28] Parkes, R.J., Cragg, B.A., Bale, S.J., Getli¡, J.M., Goodman, K., [36] Rosnes, J.T., Torsvik, T. and Lien, T. (1991) Spore-forming thermo- Rochelle, P.A., Fry, J.C., Weightman, A.J. and Harvey, S.M. philic sulfate-reducing bacteria isolated from North Sea oil ¢eld waters. Appl. Environ. Microbiol. 57, 2302^2307. Table 9.2 [37] Stetter, K.O., Huber, R., Blo«chl, E., Kurr, M., Eden, R.D., Fielder, Coupled metabolic reactions involving inorganic aqueous compounds M., Cash, H. and Vances, I. (1993) Hyperthermophilic archaea are and/or minerals thriving in deep North Sea and Alaskan oil reservoirs. Nature 365, 743^745. 23 3‡ 23 ‡ 2‡ F1 S4O6 +10H2O(l)+14Fe H4SO4 +20H +14Fe [38] L'Haridon, S., Reysenbach, A.-L., Glenat, P., Prieur, D. and Jean- 3‡ 3 2‡ ‡ F2 S(s)+6Fe +4H2O(l)HHSO4 +6Fe +7H thon, C. (1995) Hot subterranean biosphere in a continental oil res- 3‡ 2‡ ‡ F3 H2(aq)+2Fe H2Fe +2H ervoir. Nature 377, 223^224. 2‡ ‡ 3‡ F4 2Fe +0.5O2(aq)+2H H2Fe +H2O(l) [39] Zobell, C.E. and Morita, R.Y. (1957) Barophilic bacteria in some 3‡ 23 ‡ F5 2pyrite(s)+7.5O2(aq)+H2O(l)H2Fe +4SO4 +2H deep sea sediments. J. Bacteriol. 73, 563^568. 2‡ 23 ‡ F6 pyrite(s)+3.5O2(aq)+H2O(l)HFe +2SO4 +2H [40] Pedersen, K. and Ekendahl, S. (1990) Distribution and activity of 2‡ 23 F7 pyrrhotite(s)+2O2(aq)HFe +SO4 bacteria in deep granitic groundwaters of southeastern Sweden. Mi- ‡ F8 2chalcopyrite(s)+8.5O2(aq)+2H H crob. Ecol. 20, 37^52. 2‡ 3‡ 23 2Cu +2Fe +4SO4 +H2O(l) [41] Pedersen, K. (1997) Microbial life in deep granitic rock. FEMS Mi- 2‡ 23 F9 covellite(s)+2O2(aq)HCu +SO4 crobiol. Rev. 20, 399^414. 2‡ 23 F10 sphalerite(s)+2O2(aq)HZn +SO4 [42] Motamedi, M. and Pedersen, K. (1998) Desulfovibrio aespoeensis sp. 2‡ 23 F11 galena(s)+2O2(aq)HPb +SO4 nov., a mesophilic sulfate-reducing bacterium from deep groundwater 2‡ ‡ F12 H2(aq)+UO2 HUraninite(s)+2H at Aë spo« hard rock laboratory, Sweden. Int. J. Syst. Bacteriol. 48, ‡ 2‡ F13 uraninite(s)+0.5O2(aq)+2H HUO2 +H2O(l) 311^315.

FEMSRE 711 7-3-01 222 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

Table 9.3 0 31 Values of vGr (kJ mol )atPSAT as a function of temperature for reactions given in Table 9.2 Reaction T (³C) 218253745557085100115150200 F1 3569.15 3594.45 3605.19 3623.18 3634.91 3649.31 3670.38 3690.90 3710.90 3730.44 3774.47 3834.00 F2 3233.23 3246.73 3252.63 3262.74 3269.47 3277.86 3290.42 3302.94 3315.45 3327.96 3357.12 3399.30 F3 3159.62 3164.25 3166.26 3169.66 3171.91 3174.71 3178.86 3182.98 3187.08 3191.15 3200.64 3214.30 F4 3104.32 399.20 396.92 392.96 390.29 386.92 381.80 376.62 371.36 366.03 353.26 334.13 F5 32609.37 32588.78 32578.74 32560.34 32547.33 32530.29 32503.23 32474.47 32444.08 32412.10 32331.30 32200.16 F6 31252.53 31244.79 31240.91 31233.69 31228.52 31221.69 31210.71 31198.93 31186.36 31173.04 31139.01 31083.01 F7 3775.83 3770.76 3768.27 3763.70 3760.46 3756.21 3749.45 3742.25 3734.63 3726.59 3706.17 3672.72 F8 32920.94 32895.43 32883.18 32860.94 32845.31 32824.98 32792.92 32759.09 32723.56 32686.36 32593.04 32443.04 F9 3666.72 3661.65 3659.19 3654.65 3651.44 3647.24 3640.57 3633.49 3626.01 3618.14 3598.25 3565.95 F10 3731.83 3726.71 3724.20 3719.61 3716.36 3712.11 3705.35 3698.18 3690.59 3682.62 3662.49 3629.82 F11 3710.13 3706.55 3704.72 3701.25 3698.74 3695.41 3690.02 3684.18 3677.94 3671.28 3654.17 3625.76 F12 394.08 396.09 396.93 398.30 399.19 3100.27 3101.81 3103.30 3104.73 3106.12 3109.24 3113.51 F13 3169.86 3167.36 3166.25 3164.31 3163.01 3161.36 3158.85 3156.30 3153.70 3151.05 3144.67 3134.93

[43] Kotelnikova, S., Macario, A.J.L. and Pedersen, K. (1998) Methano- volatile fatty acids in the hot springs of Vulcano, Aeolian Islands, bacterium subterraneum sp. nov., a new alkaliphilic, eurythermic and Italy. Org. Geochem. 28, 699^705. halotolerant methanogen isolated from deep granitc groundwater. [47] Stetter, K.O. (1982) Ultrathin mycelia-forming organisms from sub- Int. J. Syst. Bacteriol. 48, 357^367. marine volcanic areas having an optimum growth temperature of [44] Stevens, T. (1997) Lithoautotrophy in the subsurface. FEMS Micro- 105³C. Nature 300, 258^260. biol. Rev. 20, 327^337. [48] Amend, J.P. (2001) Calculation of metabolic energy from sulfur re- [45] Anderson, R.T., Chapelle, F.H. and Lovley, D.R. (1998) Evidence duction by hyperthermophiles in Vulcano hot springs. Extremophiles, against hydrogen-based microbial ecosystems in basalt aquifers. Sci- in preparation. ence 281, 976^977. [49] Shock, E.L. and Helgeson, H.C. (1988) Calculation of the thermody- [46] Amend, J.P., Amend, A.C. and Valenza, M. (1998) Determination of namic and transport properties of aqueous species at high pressures and temperatures: Correlation algorithms for ionic species and equa- tion of state predictions to 5 kb and 1000³C. Geochim. Cosmochim. Table 9.4 Acta 52, 2009^2036. Microorganisms that use the metal reactions speci¢ed in Table 9.2 [50] Shock, E.L., Helgeson, H.C. and Sverjensky, D.A. (1989) Calculation Reaction of the thermodynamic and transport properties of aqueous species at high pressures and temperatures: Standard partial molal properties F1 As written: S. acidophilus, S. thermosul¢dooxidans [183] of inorganic neutral species. Geochim. Cosmochim. Acta 53, 2157^ F2 As written: S. acidocaldarius, T. thiooxidans, T. ferrooxidans 2183. [442] [51] Shock, E.L., Oelkers, E.H., Johnson, J.W., Sverjensky, D.A. and F3 As written: G. sulfurreducens [432], Thermoterrabacterium Helgeson, H.C. (1992) Calculation of the thermodynamic properties ferrireducens [275] of aqueous species at high pressures and temperatures: E¡ective elec- F4 As written: S. thermosul¢dooxidans [246,443], A. brierleyi trostatic radii, dissociation constants and standard partial molal [292,294], T. prosperus [406], S. acidophilus [245], properties to 1000³C and 5 kbar. J. Chem. Soc. Faraday Trans. 88, Acidimicrobium ferrooxidans [182], S. yellowstonii [322] 803^826. F5 As written: S. thermosul¢dooxidans [246,443], T. ferrooxidans [52] Shock, E.L., Sassani, D.C., Willis, M. and Sverjensky, D.A. (1997) [387], S. yellowstonii [322], T. prosperus [406] Inorganic species in geologic £uids: correlations among standard Inferred: A. brierleyi [292,297,444], molal thermodynamic properties of aqueous ions and hydroxide com- F6 As written: S. thermosul¢dooxidans [246,443], M. sedula [297], plexes. Geochim. Cosmochim. Acta 61, 907^950. S. metallicus [317], M. prunae [296], T. prosperus [406], [53] Shock, E.L., Sassani, D.C. and Betz, H. (1997) Uranium in geologic S. yellowstonii [322] £uids: estimates of standard partial molal properties, oxidation po- Inferred: A. brierleyi [292,297,444] tential, and hydrolysis constants at high temperatures and pressures. F7 As written: S. hakonensis [316] Geochim. Cosmochim. Acta 61, 4245^4266. F8 As written: S. thermosul¢dooxidans [246,443], M. sedula [297], [54] Haas, J.R., Shock, E.L. and Sassani, D.C. (1995) Rare earth elements S. metallicus [317], M. prunae [296], T. prosperus [406], in hydrothermal systems: Estimates of standard partial molal ther- S. yellowstonii [322] modynamic properties of aqueous complexes of the REE at high Inferred: A. brierleyi [297] pressures and temperatures. Geochim. Cosmochim. Acta 59, 4329^ F9 As written: S. thermosul¢dooxidans [246] 4350. F10 As written: S. yellowstonii [322], T. prosperus [406], [55] Sverjensky, D.A., Shock, E.L. and Helgeson, H.C. (1997) Prediction S. metallicus [317], S. thermosul¢dooxidans [246,443], of the thermodynamic and transport properties of aqueous metal M. sedula [297], M. prunae [296] complexes to 1000³C and 5 kb. Geochim. Cosmochim. Acta 61, Inferred: A. brierleyi [297] 1359^1412. F11 As written: S. thermosul¢dooxidans [246], T. prosperus [406] [56] Sassani, D.C. and Shock, E.L. (1998) Solubility and transport of F12 As written: [114,115], D. desulfuricans platinum-group elements in supercritical £uids: Summary and esti- [114] mates of thermodynamic properties for Ru, Rh, Pd, and Pt solids, F13 Inferred: T. prosperus [406], S. metallicus [317], M. sedula aqueous ions and aqueous complexes. Geochim. Cosmochim. Acta [297], M. prunae [296] 62, 2643^2671.

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 223

Table 9.5 [61] Shock, E.L. (1995) Organic acids in hydrothermal solution: Standard Coupled metabolic reactions involving organic compounds and inor- molal thermodynamic properties of carboxylic acids and estimates of ganic aqueous compounds or minerals dissociation constants at high temperatures and pressures. Am. J. Sci. 295, 496^580. F14 formic acid(aq)+2Fe3‡+H O(l)Hsiderite(s)+Fe2‡+4H‡ 2 [62] Schulte, M.D. and Shock, E.L. (1993) Aldehydes in hydrothermal F15 acetic acid(aq)+8Fe3‡+2H O(l)H8Fe2‡+2CO (aq)+8H‡ 2 2 solution: Standard partial molal thermodynamic properties and rel- F16 acetic acid(aq)+8Co3‡+2H O(l)H2CO (aq)+8Co2‡+8H‡ 2 2 ative stabilities at high temperatures and pressures. Geochim. Cos- F17 3acetic acid(aq)+4SeO23+8H‡H 4 mochim. Acta 57, 3835^3846. 4selenium(s)+6CO (aq)+10H O(l) 2 2 [63] Amend, J.P. and Helgeson, H.C. (1997) Group additivity equations F18 acetic acid(aq)+2H O(l)+4UO2‡H4uraninite(s)+2CO (aq)+8H‡ 2 2 2 of state for calculating the standard molal thermodynamic properties F19 lactic acid(aq)+12Fe3‡+3H O(l)H3CO (aq)+12Fe2‡+12H‡ 2 2 of aqueous organic species at elevated temperatures and pressures. F20 lactic acid(aq)+12Fe3‡+6H O(l)H3siderite(s)+9Fe2‡+18H‡ 2 Geochim. Cosmochim. Acta 61, 11^46. F21 lactic acid(aq)+4Fe3‡+H O(l)H 2 [64] Amend, J.P. and Helgeson, H.C. (1997) Calculation of the standard 4Fe2‡+acetic acid(aq)+CO (aq)+4H‡ 2 molal thermodynamic properties of aqueous biomolecules at elevated F22 lactic acid(aq)+2HAsO23+4H‡H 4 temperatures and pressures. Part 1. -K-Amino acids. J. Chem. Soc. acetic acid(aq)+2HAsO (aq)+CO (aq)+3H O(l) L 2 2 2 Faraday Trans. 93, 1927^1941. F23 lactic acid(aq)+2HAsO23+2H‡H 4 [65] Dale, J.D., Shock, E.L., MacLeod, G., Aplin, A.C. and Larter, S.R. acetic acid(aq)+2AsO3+CO (aq)+3H O(l) 2 2 2 (1997) Standard partial molal properties of aqueous alkylphenols at F24 lactic acid(aq)+2SeO23H 4 high pressures and temperatures. Geochim. Cosmochim. Acta 61, acetic acid(aq)+2SeO23+CO (aq)+H O(l) 3 2 2 4017^4024. F25 3lactic acid(aq)+2SeO23+4H‡H 4 [66] Haas, J.R. and Shock, E.L. (1999) Halocarbons in the environment: 3acetic acid(aq)+2selenium(s)+3CO (aq)+5H O(l) 2 2 Estimates of thermodynamic properties for aqueous chloroethylene F26 lactic acid(aq)+SeO23+2H‡H 3 species and their stabilities in natural settings. Geochim. Cosmochim. acetic acid(aq)++CO (aq)+2H O(l) 2 2 Acta 63, 3429^3441. F27 lactic acid(aq)+3H O(l)+6UO2‡H 2 2 [67] Plyasunov, A.V. and Shock, E.L. (2000) Thermodynamic functions of 6uraninite(s)+3CO (aq)+12H‡ 2 hydration of hydrocarbons at 298.15 K and 0.1 MPa. Geochim. F28 butanoic acid(aq)+6HAsO23+12H‡H 4 Cosmochim. Acta 64, 439^468. acetic acid(aq)+2CO (aq)+6HAsO (aq)+8H O(l) 2 2 2 [68] Shock, E.L. and Koretsky, C.M. (1993) Metal^organic complexes in F29 succinic acid(aq)+14Fe3‡+4H O(l)H4CO (aq)+14Fe2‡+14H‡ 2 2 geochemical processes: Calculation of standard partial molal thermo- dynamic properties of aqueous acetate complexes at high pressures and temperatures. Geochim. Cosmochim. Acta 57, 4899^4922. [57] Shock, E.L. and Helgeson, H.C. (1990) Calculation of the thermody- [69] Shock, E.L. and Koretsky, C.M. (1995) Metal^organic complexes in namic and transport properties of aqueous species at high pressures geochemical processes: Estimation of standard partial molal thermo- and temperatures: Standard partial molal properties of organic spe- dynamic properties of aqueous complexes between metal cations and cies. Geochim. Cosmochim. Acta 54, 915^945. monovalent ligands at high pressures and temperatures. [58] Helgeson, H.C. (1992) Calculation of the thermodynamic properties Geochim. Cosmochim. Acta 59, 1497^1532. and relative stabilities of aqueous acetic and chloroacetic acids, ace- [70] Prapaipong, P., Shock, E.L. and Koretsky, C.M. (1999) Metal^or- tate and chloroacetates, and acetyl and chloroacetyl chlorides at high ganic complexes in geochemical processes: Temperature dependence and low temperatures and pressures. Appl. Geochem. 7, 291^308. of the standard thermodynamic properties of aqueous complexes be- [59] Shock, E.L. (1992) Chemical environments of submarine hydrother- tween metal cations and dicarboxylate ligands. Geochim. Cosmo- mal systems. Orig. Life Evol. Biosph. 22, 67^107. chim. Acta 63, 2547^2577. [60] Shock, E.L. (1993) Hydrothermal dehydration of aqueous organic [71] Helgeson, H.C., Kirkham, D.H. and Flowers, G.C. (1981) Theoret- compounds. Geochim. Cosmochim. Acta 57, 3341^3349. ical prediction of the thermodynamic behavior of aqueous electro-

Table 9.6 0 31 Values of vGr (kJ mol )atPSAT as a function of temperature for reactions given in Table 9.5 Reaction T (³C) 218253745557085100115150200 F14 3119.75 3124.84 3127.09 3130.95 3133.53 3136.75 3141.59 3146.42 3151.27 3156.14 3167.63 3184.59 F15 3466.16 3486.27 3495.25 3510.83 3521.34 3534.60 3554.71 3575.10 3595.76 3616.70 3666.75 3741.49 F16 31374.63 31397.23 31407.36 31425.00 31436.93 31452.01 31474.95 31498.27 31521.96 31546.03 31603.69 31690.09 F17 31716.45 31727.08 31732.60 31743.09 31750.74 31760.97 31777.61 31795.72 31815.22 31836.07 31889.84 31979.19 F18 3204.00 3213.63 3217.93 3225.40 3230.45 3236.83 3246.52 3256.37 3266.39 3276.59 3301.12 3338.32 F19 3757.84 3788.98 3802.87 3826.96 3843.19 3863.66 3894.70 3926.15 3957.99 3990.26 31067.35 31182.34 F20 3650.28 3683.08 3697.51 3722.30 3738.85 3759.55 3790.66 3821.85 3853.16 3884.64 3959.06 31068.91 F21 3291.68 3302.71 3307.62 3316.13 3321.85 3329.06 3339.99 3351.05 3362.24 3373.57 3400.60 3440.85 F22 76.27 70.14 67.22 61.91 58.20 53.35 45.71 37.61 29.09 20.14 32.46 339.23 F23 3221.81 3227.47 3230.10 3234.81 3238.07 3242.29 3248.89 3255.81 3263.04 3270.57 3289.32 3319.08 F24 3340.23 3341.31 3341.82 3342.77 3343.44 3344.32 3345.72 3347.21 3348.79 3350.45 3354.59 3361.10 F25 31034.01 31042.28 31046.30 31053.67 31058.90 31065.77 31076.69 31088.34 31100.68 31113.69 31146.61 31199.90 F26 3346.89 3350.49 3352.24 3355.45 3357.73 3360.72 3365.48 3370.56 3375.94 3381.62 3396.01 3419.40 F27 3364.59 3380.02 3386.89 3398.81 3406.85 3417.00 3432.41 3448.06 3463.95 3480.10 3518.92 3577.58 F28 3780.34 3802.43 3812.78 3831.33 3844.23 3860.92 3887.06 3914.50 3943.20 3973.18 31048.19 31168.72 F29 3838.49 3874.77 3891.00 3919.22 3938.28 3962.36 3998.97 31036.16 31073.90 31112.24 31204.08 31341.73

FEMSRE 711 7-3-01 224 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

Table 9.7 talline, liquid, and gas organic molecules at high temperatures and Microorganisms that use the coupled metal and organic carbon reac- pressures. Geochim. Cosmochim. Acta 62, 985^1081. tions speci¢ed in Table 9.5 [75] Richard, L. and Helgeson, H.C. (1998) Calculation of the thermody- namic properties at elevated temperatures and pressures of saturated Reaction and aromatic high molecular weight solid and liquid hydrocarbons in F14 B. infernus [116] kerogen, bitumen, , and other organic matter of biogeo- F15 G. metallireducens [422,423], D. palmitatis [430], chemical interest. Geochim. Cosmochim. Acta 62, 3591^3636. G. sulfurreducens [432] [76] Helgeson, H.C., Delany, J.M., Nesbitt, W.H. and Bird, D.K. (1978) F16 G. sulfurreducens [432] Summary and critique of the thermodynamic properties of rock- F17 strain SES [445] forming minerals. Am. J. Sci. 278A, 1^229. F18 G. metallireducens [114,115] [77] Wagman, D.D., Evans, W.H., Parker, V.B., Schumm, R.H., Halow, F19 D. palmitatis [430] I., Bailey, S.M., Cherney, K.L. and Nuttall, R.L. (1982) The NBS F20 B. infernus [116] tables of chemical thermodynamic properties. Selected values for in-

F21 S. barnesii strain SES-3 [380,426], B. arsenicoselenatis, organic and C1 and C2 organic substances in SI units. J. Phys. Chem. B. selenitireducens [425] Ref. Data 11, 392. F22 D. auripigmentum [393], B. arsenicoselenatis, B. selenitireducens [78] Chan, G.W. and Shock, E.L. (2001) Geochemical bioenergetics in the [425] hydrothermal of the pink ¢lament of Octopus F23 S. barnesii strain SES-3 [380,426], B. arsenicoselenatis, Spring, Yellowstone National Park. Appl. Environ. Microbiol., in B. selenitireducens [425] preparation. F24 S. barnesii strain SES-3 [380,424], B. arsenicoselenatis, [79] Alberty, R.A. and Goldberg, R.N. (1992) Standard thermodynamic B. selenitireducens [425] formation properties for the adenosine 5P-triphosphate series. Bio- F25 S. barnesii strain SES-3 [380,424], B. arsenicoselenatis, chemistry 31, 10610^10615. B. selenitireducens [425] [80] Alberty, R.A. (1998) Calculation of standard transformed Gibbs en- F26 B. arsenicoselenatis, B. selenitireducens [425] ergies and standard transformed enthalpies of biochemical reactants. F27 S. putrefaciens [114,115], D. desulfuricans [114], Arch. Biochem. Biophys. 353, 116^130. G. metallireducens [114,115] [81] Gurrieri, S., Helgeson, H.C., Amend, J.P. and Danti, K. (2000) Bio- F28 D. auripigmentum [393] geochemistry of the geothermal system in the Aeolian Islands: Au- F29 D. palmitatis [430] thigenic phase relations in the hot springs of Vulcano. Chem. Geol., in preparation. [82] Huber, R., Wilharm, T., Huber, D., Trincone, A., Burggraf, S., Ko«- nig, H., Rachel, R., Rockinger, I., Fricke, H. and Stetter, K.O. (1992) lytes at high pressures and temperatures: IV. Calculation of activity Aquifex pyrophilus gen. nov. sp. nov., represents a novel group of coe¤cients, osmotic coe¤cients, and apparent molal and standard marine hyperthermophilic hydrogen oxidizing bacteria. Syst. Appl. and relative partial molal properties to 600³C and 5 kb. Am. J. Sci. Microbiol. 15, 340^351. 281, 1249^1516. [83] Deckert, G., Warren, P.V., Gaasterland, T., Young, W.G., Lenox, [72] Tanger, J.C. and Helgeson, H.C. (1988) Calculation of the thermo- A.L., Graham, D.E., Overbeek, R., Snead, M.A., Keller, M., Aujay, dynamic and transport properties of aqueous species at high pres- M., Huber, R., Feldman, R.A., Short, J.M., Olsen, G.J. and Swan- sures and temperatures: Revised equations of state for the standard son, R.V. (1998) The complete genome of the hyperthermophilic partial molal properties of ions and electrolytes. Am. J. Sci. 288, 19^ bacterium Aquifex aeolicus. Nature 392, 353^358. 98. [84] Hafenbradl, D., Keller, M., Dirmeier, R., Rachel, R., Rossnagel, P., [73] Johnson, J.W., Oelkers, E.H. and Helgeson, H.C. (1992) Burggraf, S., Huber, H. and Stetter, K.O. (1996) Ferroglobus placidus SUPCRT92: A software package for calculating the standard molal gen. nov., sp. nov., a novel hyperthermophilic archaeum that oxidizes properties of minerals, gases, aqueous species, and reactions from 1 Fe2‡ at neutral pH under anoxic conditions. Arch. Microbiol. 166, to 5000 bar and 0 to 1000³C. Comput. Geosci. 18, 899^947. 308^314. [74] Helgeson, H.C., Owens, C.E., Knox, A.M. and Richard, L. (1998) [85] Broda, E. (1977) Two kinds of missing in nature. Z. Allg. Calculation of the standard molal thermodynamic properties of crys- Mikrobiol. 17, 491^493.

Table 9.8 0 31 Values of vG (kJ mol )atPSAT as a function of temperature for inorganic aqueous compounds in the system H^O^P Compound T (³C) 2 18 25 37 45 55 70 85 100 115 150 200

H3PO4(aq) 31139.09 31141.55 31142.65 31144.59 31145.90 31147.56 31150.11 31152.73 31155.39 31158.11 31164.66 31174.47 3 H2PO4 31128.15 31129.63 31130.27 31131.35 31132.06 31132.95 31134.27 31135.58 31136.87 31138.15 31141.04 31144.80 23 HPO4 31089.65 31089.35 31089.14 31088.68 31088.32 31087.81 31086.94 31085.94 31084.81 31083.55 31080.07 31073.54 33 PO4 31023.36 31020.31 31018.80 31016.02 31014.05 31011.46 31007.33 31002.92 3998.24 3993.29 3980.65 3959.59 H4P2O7(aq) 32026.26 32030.32 32032.17 32035.44 32037.68 32040.55 32044.95 32049.49 32054.16 32058.95 32070.57 32088.19 3 H3P2O7 32018.63 32021.91 32023.39 32025.98 32027.75 32030.01 32033.45 32036.98 32040.59 32044.26 32053.02 32065.87 23 H2P2O7 32006.32 32008.86 32010.00 32011.97 32013.31 32015.00 32017.56 32020.15 32022.76 32025.38 32031.46 32039.74 33 HP2O7 31971.15 31972.01 31972.34 31972.86 31973.19 31973.56 31974.07 31974.49 31974.83 31975.07 31975.18 31973.79 43 P2O7 31921.30 31919.97 31919.20 31917.67 31916.50 31914.91 31912.25 31909.28 31905.99 31902.39 31892.71 31875.29 H3PO2(aq) 3519.92 3522.35 3523.42 3525.29 3526.55 3528.14 3530.56 3533.02 3535.53 3538.06 3544.13 3553.14 3 H2PO2 3509.77 3511.41 3512.13 3513.33 3514.13 3515.12 3516.59 3518.06 3519.51 3520.95 3524.21 3528.53 H3PO3(aq) 3852.79 3855.62 3856.88 3859.10 3860.60 3862.51 3865.42 3868.40 3871.43 3874.53 3881.97 3893.13 3 H2PO3 3843.60 3845.71 3846.63 3848.23 3849.30 3850.65 3852.69 3854.73 3856.80 3858.86 3863.68 3870.42 23 HPO3 3811.13 3811.57 3811.70 3811.86 3811.93 3811.98 3811.98 3811.88 3811.70 3811.41 3810.33 3807.51

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 225

Fig. A1. Activity coe¤cients of electrolytes (QÆ) plotted against ionic strength (redrawn from data given by Garrels and Christ (1965) [129]).

Fig. A3. Log K (=-pKa) plotted against temperature at PSAT for the dissociation of acetic acid. Symbols represent experimental data from [86] Strous, M., Fuerst, J.A., Kramer, E.H.M., Logemann, S., Muyzer, the literature [152^158], but the curve is an independent prediction with G., Van De-Pas-Schoonen, K.T., Webb, R., Kuenen, J.G. and Jetten, the revised HKF equation of state [61]. M.S.M. (1999) Missing identi¢ed as new planctomycete. Nature 400, 446^449. [87] Kelly, D.P. (1999) Thermodynamic aspects of energy conservation by philic methanoges, growing at 110³C. Arch. Microbiol. 156, 239^ chemolithotrophic sulfur bacteria in relation to sulfur oxidation path- 247. ways. Arch. Microbiol. 171, 219^229. [95] Casagrande, D.J. (1984) in: The Okefenokee Swamp (Cohen, A.D., [88] Balch, W.E., Fox, G.E., Magrum, L.J., Woese, C.R. and Wolfe, R.S. Casagrande, D.J., Andrejko, M.J., Best, G.R., Eds.), Los Alamos, (1979) Methanogens: Reevaluation of a unique biological group. NM: Wetland surveys, pp. 391^408. Microbiol. Rev. 43, 260^296. [96] Fisher, J.B. (1987) Distribution and occurrence of aliphatic acid [89] Daniels, L., Sparling, R. and Sprott, G.D. (1984) The bioenergetics anions in deep subsurface waters. Geochim. Cosmochim. Acta 51, of methanogens. Biochim. Biophys. Acta 768, 113^163. 2459^2468. [90] Thauer, R.K., Mo«ller-Zinkhan, D. and Spormann, A.M. (1989) Bio- [97] Cody, J.D., Hutcheon, I.E. and Krouse, H.R. (1999) Fluid £ow,

chemistry of acetate catabolism in anaerobic chemotrophic bacteria. mixing and the origin of CO2 and H2S by bacterial sulphate reduc- Annu. Rev. Microbiol. 43, 43^67. tion in the Mannville Group, southern Alberta, Canada. Mar. Pet. [91] Sprott, G.D., Ekiel, I. and Patel, G.B. (1993) Metabolic pathways in Geol. 16, 495^510. Methanococcus jannaschii and other methanogenic bacteria. Appl. [98] Nordstrom, D.K. and Southam, G. (1997) in: : Environ. Microbiol. 59, 1092^1098. Interactions between Microbes and Minerals, vol. 35 (Ban¢eld, [92] Blaut, M. (1994) Metabolism of methanogens. Antonie Van Leeu- J.F., Nealson, K.H., Eds.), pp. 361^390. Mineralogical Society of wenhoek 66, 187^208. America, Washington DC. [93] Stams, A.J.M. (1994) Metabolic interactions between anaerobic bac- [99] Edwards, K.J., Schrenk, M.O., Hamers, R. and Ban¢eld, J.F. (1998) teria in methanogenic environments. Antonie Van Leeuwenhoek 66, Microbial oxidation of pyrite: experiments using microorganisms 271^294. from an extreme acidic environment. Am. Mineral. 83, 1444^1453. [94] Kurr, M., Huber, R., Ko«nig, H., Jannasch, H.W., Fricke, H., Trin- [100] Edwards, K.J., Goebel, B.M., Rodgers, T.M., Schrenk, M.O., Gihr- cone, A., Kristjansson, J.K. and Stetter, K.O. (1991) Methanopyrus ing, T.M., Cardona, M.M., Hu, B., McGuire, M.M., Hamers, R.J., kandleri, gen. and sp. nov. represents a novel group of hyperthermo- Pace, N.R. and Ban¢eld, J.F. (1999) Geomicrobiology of pyrite

Fig. A4. Log K against temperature at PSAT for the dissociation of 3 HSO4 . The curve depicts values calculated with data and parameters Fig. A2. Activity coe¤cients of gases (Qm) dissolved in NaCl solutions from Shock and Helgeson (1988) [49], and the symbols represent subse- at 25³C plotted against ionic strength (redrawn from data given by Gar- quent experimental data [159] con¢rming the accuracy of the predicted rels and Christ (1965) [129]). values.

FEMSRE 711 7-3-01 226 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

An archaeal iron-oxidizing extreme important in . Science 287, 1796^1799. [103] White, R.H. (1999) Morenci: making the most of world class re- sources, in: Copper Leaching, Solvent Extraction, Electrowinning Technology (Jergensen, G.V., II., Ed.), Society for Mining, Metal- lurgy, and Exploration, Littleton, CO. [104] Krebs, W., Brombacher, C., Bosshard, P.P., Bachofen, R. and Brandl, H. (1997) Microbial recovery of metals from solids. FEMS Microbiol. Rev. 20, 605^617. [105] Stolz, J.F. and Oremland, R.S. (1999) Bacterial respiration of ar- senic and selenium. FEMS Microbiol. Rev. 23, 615^627. [106] Newman, D.K., Ahmann, D. and Morel, F.M.M. (1998) A brief review of microbial arsenate respiration. Geomicrobiol. J. 15, 255^ 268. [107] Lloyd, J.R., Yong, P. and Macaskie, L.E. (1998) Enzymatic recov- ery of elemental palladium by using sulfate-reducing bacteria. Appl. Environ. Microbiol. 64, 4607^4609. Fig. A5. Log K plotted against temperature at PSAT for the solubility in [108] Lloyd, J.R., Nolting, H.-F., Sole, V.A., Bosecker, K. and Macaskie, water of gaseous CO2. Symbols represent experimental data from the L.E. (1998) Technetium reduction and precipitation by sulfate-re- literature [154,160^162], but the curve is an independent prediction gen- ducing bacteria. Geomicrobiol. J. 15, 45^58. erated with the revised HKF equation of state [50]. [109] Smith, T., Pitts, K., McGarvey, J.A. and Summers, A.O. (1998) Bacterial oxidation of mercury metal vapor, Hg(0). Appl. Environ.

(FeS2) dissolution: case study at Iron Mountain, California. Geo- Microbiol. 64, 1328^1332. microbiol. J. 16, 155^179. [110] Southam, G. and Beveridge, T.J. (1994) The in vitro formation of [101] Schrenk, M.O., Edwards, K.J., Goodman, R.M., Hamers, R.J. and placer gold by bacteria. Geochim. Cosmochim. Acta 58, 4527^4530. Ban¢eld, J.F. (1998) Distribution of Thiobacillus ferrooxidans and [111] Watterson, J.R. (1991) Preliminary evidence for the involvement of Leptospirillum ferrooxidans: implications for generation of acid mine budding bacteria in the origin of Alaskan placer gold. Geology 20, drainage. Science 279, 1519^1522. 315^318. [102] Edwards, K.J., Bond, P.L., Gihring, T.M. and Ban¢eld, J.F. (2000) [112] Sillitoe, R.H., Folk, R.L. and Saric, N. (1996) Bacteria as mediators

Table A.1 References for thermodynamic properties and equation of state parameters of additional organic compounds Species References

a C5^C12 aqueous monocarboxylic acids Shock (1995) [61] C5^C20 aqueous monocarboxylic acids Amend and Helgeson (1997) [63] a C5^C12 monocarboxylate anions Shock (1995) [61] a C5^C10 aqueous dicarboxylic acids Shock (1995) [61] a C5^C10 dicarboxylate monovalent anions Shock (1995) [61] a C5^C10 dicarboxylate divalent anions Shock (1995) [61] C6^C8 aqueous alkanes Shock and Helgeson (1990) [57] C6^C20 aqueous alkanes Amend and Helgeson (1997) [63] C6^C8 aqueous alcohols Shock and Helgeson (1990) [57] C6^C20 aqueous alcohols Amend and Helgeson (1997) [63] C1^C50,C60,C70,C80,C90, and C100 liquid, solid, and gas alkanes Helgeson et al. (1998) [74] C1^C20 liquid and gas alcohols Helgeson et al. (1998) [74] C2^C20 liquid monocarboxylic acids Helgeson et al. (1998) [74] C2^C20 aqueous amides Amend and Helgeson (1997) [63] C1^C20 aqueous amines Amend and Helgeson (1997) [63] C3^C8 aqueous alkenes Shock and Helgeson (1990) [57] C3^C8 aqueous alkynes Shock and Helgeson (1990) [57] C3^C8 aqueous ketones Shock and Helgeson, 1990) [57] C1^C10 aqueous aldehydes Schulte and Shock (1993) [62] Metal^acetate complexes Shock and Koretsky (1993) [68] Metal^monocarboxylate complexes Shock and Koretsky (1995) [68] Metal^dicarboxylate complexes Prapaipong et al. (1999) [70] Chlorinated ethenes Haas and Shock (1999) [66] Aromatic compounds

C6^C14 aqueous alkylbenzenes Shock and Helgeson (1990) [57] Benzene(l) Helgeson et al. (1998) [74]

C6^C20 aqueous alkylbenzenes Amend and Helgeson (1997) [63] Phenol(aq) Dale et al. (1997) [65] m-o-p-Cresol(aq) Dale et al. (1997) [65] Aqueous m-o-p-toluic acid Shock (1995)a [61] Aqueous dimethylphenols Dale et al. (1997) [65] aSee also Shock (2001) [446] for minor corrections to enthalpies of formation.

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 227

Table A.2 Summary of thermodynamic properties and equation of state parameters for updated and new species

0 0 0 0 0 Species vGf vHf S V Cp Maier^Kelley coe¤cients T (K) (J mol31) (J mol31) (J mol31 K31) (cm3 mol31) (J mol31 K31) limit a b c (J mol31 K31) (U103 J mol31 K32) (U1035 J K mol31) NO(g) 86567a 90249a 210.761a ^ 29.79j 26.3400i 7.6827i 1.04090i 1000k a a a j i i i k N2O(g) 104198 82048 219.848 ^ 38.49 41.1429 14.6955 36.2409 1000 Seleniumb 0.0 0.0 42.271 16.42 25.058 25.4446 5.1940 31.73326 494 6160g 12.460h 18.8799 13.380 25.7634 957 Molybdenite 3262956f 3271800d 62.59c 32.02e 63.55c 71.6958c 7.448c 39.2107c 1200e aTaken from Wagman et al. (1982) [77]. bAll Selenium data taken or calculated from Robie and Hemingway (1995) [447]. cFredrickson and Chasanov (1971) [448]. dO'Hare et al. (1988) [449]. eRobie and Hemingway (1995) [447]. f 0 0 0 0 0 vGf calculated using vHf from O'Hare et al. (1988) [449] and Sf calculated using S for Mo from Wagman et al. (1982) [77], S for S from McCol- 0 lom and Shock (1997) [450], and S for MoS2 from Fredrickson and Chasanov (1971) [448]. gvH0 of fusion. hvS0 of fusion. i 0 Maier^Kelley Coe¤cients calculated from ¢tting a curve of the Maier^Kelley equation to the Cp data from Stull et al. (1969) [451]. jCalculated from the Maier^Kelley equation at 298.15 K. kStull et al. (1969) [451].

of copper sul¢de enrichment during weathering. Science 272, 1153^ [121] Stakes, D.S., Orange, D., Paduan, J.F., Salamy, K.A. and Maher, 1155. N. (1999) Cold-seeps and authigenic carbonate formation in Mon- [113] Gorby, Y.A. and Lovely, D.R. (1992) Enzymic uranium precipita- terey Bay, California. Mar. Geol. 159, 93^109. tion. Environ. Sci. Technol. 26, 205^207. [122] Criss, R.E., Cooke, G.A. and Day, S.D. (1988) An organic origin [114] Lovley, D.R. and Phillips, E.J.P. (1992) Reduction of uranium by for the carbonate concretions of the Ohio Shale. US Geol. Surv. Desulfovibrio desulfuricans. Appl. Environ. Microbiol. 58, 850^856. Bull. 1836, 1^21. [115] Lovley, D.R., Phillips, E.J.P., Gorby, Y.A. and Landa, E.R. (1991) [123] Danson, M.J. (1993) in: The of the Archaea (Arch- Microbial reduction of uranium. Nature 350, 413^416. aebacteria) (Kates, M. Ed.), p. 582. Elsevier Science, Amsterdam. [116] Boone, D.R., Liu, Y., Zhao, Z.-J., Balkwill, D., Drake, G.R., Ste- [124] Schro«der, C., Selig, M. and Scho«nheit, P. (1994) Glucose fermenta-

vens, T.O. and Aldrich, H. (1995) Bacillus infernus sp. nov., an tion to acetate, CO2 and H2 in the anaerobic hyperthermophilic Fe(III)- and Mn(IV)-reducing anaerobe from the deep terrestrial eubacterium Thermotoga maritima: involvement of the Embden^ subsurface. Int. J. Syst. Bacteriol. 45, 441^448. Meyerhof pathway. Arch. Microbiol. 161, 460^470. [117] Wilke, J.A. and Hering, J.G. (1998) Rapid oxidation of geothermal [125] Andreesen, J.R. (1994) Glycine metabolism in anaerobes. Antonie arsenic(III) in streamwaters of the eastern Sierra Nevada. Environ. Van Leeuwenhoek 66, 223^237. Sci. Technol. 32, 657^662. [126] Jones, W.J., Leigh, J.A., Mayer, F., Woese, C.R. and Wolfe, R.S. [118] Kirkland, D.W., Denison, R.E. and Rooney, M.A. (1995) Diage- (1983) Methanococcus jannaschii sp. nov., an extremely thermophilic netic alteration of Permian strata at oil ¢elds of south central Okla- methanogen from a submarine . Arch. Microbiol. homa, USA. Mar. Pet. Geol. 12, 629^644. 136, 254^261. [119] Kontak, D.J. and Kerrick, R. (1997) An isotopic (C, O, Sr) study of [127] Bult, C.J., White, O., Olsen, G.J., Zhou, L., Fleischmann, R.D., vein gold deposits in the Meguma terrane, Nova Scotia: Implication Sutton, G.G., Blake, J.A., FitzGerald, L.M., Clayton, R.A., Go- for source reservoirs. Econ. Geol. 92, 161^180. cayne, J.D., Kerlavage, A.R., Dougherty, B.A., Tomb, J.-F., [120] MaCaulay, C.I., Fallick, A.E., McLaughlin, O.M., Haszeldine, R.S. Adams, M.D., Reich, C.I., Overbeek, R., Kirkness, E.F., Wein- and Pearson, M.J. (1998) The signi¢cance of N13C of carbonate stock, K.G., Merrick, J.M., Glodek, A., Scott, J.L., Geoghagen, cements in reservoir sandstones: a regional perspective from the N.S.M., Weidman, J.F., Fuhrmann, J.L., Nguyen, D., Utterback, Jurassic of the northern North Sea. Int. Assoc. Sediment, Spec. T.R., Kelley, J.M., Peterson, J.D., Sadow, P.W., Hanna, M.C., Publ. 26, 395^408. Cotton, M.D., Roberts, K.M., Hurst, M.A., Kaine, B.P., Borodov- sky, M., Klenk, H.-P., Fraser, C.M., Smith, H.O., Woese, C.R. and Table A.3 Venter, J.C. (1996) Complete genome sequence of the methanogenic Gas solubility reactions Archaeon, Methanococcus jannaschii. Science 273, 1058^1073. [128] Zinder, S.H., Sowers, K.R. and Ferry, J.G. (1985) Methanosarcina G1 H2(g)HH2(aq) thermophila sp. nov., a thermophilic, acetotrophic, methane-produc- G2 O2(g)HO2(aq) ing bacterium. Int. J. Syst. Bacteriol. 35, 522^523. G3 NO(g)HNO(aq) [129] Garrels, R.M. and Christ, C.L. (1965) Solutions, Minerals, and G4 N2O(g)HN2O(aq) Equilibria, Freeman, Cooper and Company, San Francisco, CA. G5 N2(g)HN2(aq) [130] Stumm, W. and Morgan, J.J. (1996) Aquatic Chemistry: Chemical G6 NH3(g)HNH3(aq) Equilibria and Rates in Natural Waters, edn. 3, John Wiley and G7 SO2(g)HSO2(aq) Sons, New York. G8 H2S(g)HH2S(aq) [131] Anderson, G.M. (1996) Thermodynamics of Natural Systems, John G9 CO2(g)HCO2(aq) Wiley and Sons, New York. G10 CH4(g)HCH4(aq) [132] Langmuir, D. (1997) Aqueous Environmental Geochemistry, Pren- G11 CO(g)HCO(aq) tice Hall, Upper Saddle River, NJ.

FEMSRE 711 7-3-01 228 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

Table A.4 0 31 Values of vGr (kJ mol )atPSAT as a function of temperature for the reactions given in Table A.3 Reaction T (³C) 2 18 25 37 45 55 70 85 100 115 150 200 G1 15.91 17.20 17.72 18.56 19.09 19.72 20.59 21.40 22.13 22.79 24.11 25.46 G2 14.12 15.85 16.54 17.65 18.34 19.15 20.27 21.28 22.20 23.02 24.59 26.04 G3a 13.18 14.83 15.49 16.54 17.20 17.96 18.99 19.92 20.75 21.49 22.93 24.39 G4a 6.62 8.45 9.18 10.35 11.08 11.93 13.09 14.13 15.05 15.87 17.42 18.90 G5 15.77 17.50 18.18 19.29 19.97 20.78 21.89 22.90 23.82 24.63 26.19 27.63 G6 312.24 310.85 310.26 39.25 38.59 37.78 36.59 35.43 34.30 33.19 30.72 2.59 G7 33.12 31.59 30.97 0.03 0.66 1.41 2.46 3.44 4.34 5.18 6.88 8.76 G8 3.65 5.06 5.64 6.56 7.15 7.85 8.82 9.71 10.54 11.29 12.80 14.42 G9 5.96 7.69 8.38 9.49 10.18 10.99 12.12 13.14 14.07 14.91 16.57 18.29 G10 13.76 15.56 16.27 17.39 18.08 18.89 20.00 20.98 21.85 22.61 24.02 25.18 G11 14.73 16.47 17.16 18.25 18.91 19.69 20.74 21.67 22.48 23.19 24.45 25.34 aValues from Plyasunov et al. (2001) [452]

[133] Quastel, J.H., Stephenson, M. and Whetham, M.D. (1925) Some [138] Wallace, W., Ward, T., Breen, A. and Attaway, H. (1996) Iden- reactions of resting bacteria in relation to anaerobic growth. Bio- ti¢cation of an anaerobic bacterium which reduces perchlorate chem. J. 19, 304^317. and chlorate as Wolinella succinogenes. J. Ind. Microbiol. 16, 68^ [134] Aslander, A. (1928) Experiments on the eradication of Canada This- 72. tle, Cirsium arvense, with chlorates and other herbicides. J. Agric. [139] Stepanyuk, V.V., Smirnova, G.F., Klyushnikova, T.M., Kanyuk, Res. 36, 915^934. N.I., Panchenko, L.P., Nogina, T.M. and Prima, V.I. (1992) New [135] Bryan, E.H. and Rohlich, G.A. (1954) Biological reduction of so- species of the Acinetobacter genus ^ Acinetobacter thermotoleranticus dium chlorate as applied to measurement of sewage B.O.D. Sewage sp. nov. Mikrobiologiya (in Russian) 61, 490^500. and Industrial Wastes, 1315^1324. [140] van Ginkel, C.G., Plugge, C.M. and Stroo, C.A. (1995) Reduction [136] Hackenthal, E. (1965) Die Reduktion von Perchlorat durch Bakte- of chlorate with various energy subsrates and inocula under anaer- rien-II. Biochem. Pharmacol. 14, 1313^1324. obic conditions. Chemosphere 31, 4057^4066. [137] Malmqvist, A., Welander, T. and Gunnarsson, L. (1991) Anaerobic [141] Bruce, R.A., Achenbach, L.A. and Coates, J.D. (1999) Reduction of growth of microorganisms with chlorate as an electron acceptor. (per)chlorate by a novel organism isolated from paper mill waste. Appl. Environ. Microbiol. 57, 2229^2232. Environ. Microbiol. 1, 319^329.

Table A.5 Dissociation reactions

‡ 3 3 ‡ H1 H2O2(aq)HH +HO2 H29 glutamic acid(aq)Hglutamate +H ‡ ‡ ‡ ‡ H2 NH4 HNH3(aq)+H H30 histidine Hhistidine(aq)+H ‡ 3 ‡ ‡ H3 HNO3(aq)HH +NO3 H31 lysine Hlysine(aq)+H ‡ 3 ‡ ‡ H4 HNO2(aq)HH +NO2 H32 VO2 +2H2O(l)HH3VO4(aq)+H 3 ‡ 3 ‡ H5 SO2(aq)+H2OHHSO3 +H H33 H3VO4(aq)HH2VO4 +H 3 23 ‡ 3 23 ‡ H6 HSO3 HSO3 +H H34 H2VO4 HHVO4 +H 3 23 ‡ 23 33 ‡ H7 HSO4 HSO4 +H H35 HVO4 HVO4 +H 3 ‡ 3 ‡ H8 H2S(aq)HHS +H H36 H3AsO4(aq)HH2AsO4 +H 3 ‡ 3 23 ‡ H9 CO2(aq)+H2OHHCO3 +H H37 H2AsO4 HHAsO4 +H 3 32 ‡ 23 33 ‡ H10 HCO3 HCO3 +H H38 HAsO4 HAsO4 +H 3 ‡ 3 ‡ H11 formic acid(aq)Hformate +H H39 HAsO2(aq)HAsO2 +H 3 ‡ 3 23 ‡ H12 acetic acid(aq)Hacetate +H H40 HSeO4 HSeO4 +H 3 ‡ 3 ‡ H13 glycolic acid(aq)Hglycolate +H H41 H2SeO3(aq)HHSeO3 +H 3 ‡ 3 23 ‡ H14 propanoic acid(aq)Hpropanoate +H H42 HSeO3 HSeO3 +H 3 ‡ 3 23 ‡ H15 lactic acid(aq)Hlactate +H H43 HMoO4 HMoO4 +H 3 ‡ 3 23 ‡ H16 butanoic acid(aq)Hbutanoate +H H44 HWO4 HWO4 +H 3 ‡ 3 ‡ H17 pentanoic acid(aq)Hpentanoate +H H45 H3PO4(aq)HH2PO4 +H 3 3 23 ‡ H18 benzoic acid(aq)Hbenzoate +H+ H46 H2PO4 HHPO4 +H 3 ‡ 23 33 ‡ H19 oxalic acid(aq)HH^ +H H47 HPO4 HPO4 +H 3 32 ‡ 3 ‡ H20 H^oxalate Hoxalate +H H48 H4P2O7(aq)HH3P2O7 +H 3 ‡ 3 23 ‡ H21 malonic acid(aq)HH^malonate +H H49 H3P2O7 HH2P2O7 +H 3 32 ‡ 23 33 ‡ H22 H^malonate Hmalonate +H H50 H2P2O7 HHP2O7 +H 3 ‡ 33 43 ‡ H23 succinic acid(aq)HH^succinate +H H51 HP2O7 HP2O7 +H H24 H^succinate3Hsuccinate32+H‡ H52 HCl(aq)HH‡+Cl3 H25 glutaric acid(aq)HH^glutarate3+H‡ H53 HClO(aq)HH‡+ClO3 H26 H^glutarate3Hglutarate32+H‡ H54 HBrO(aq)HH‡+BrO3 ‡ ‡ ‡ 3 H27 arginine Harginine(aq)+H H55 HIO3(aq)HH +IO3 H28 aspartic acid(aq)Haspartate3+H‡ H56 HIO(aq)HH‡+IO3

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 229

Table A.6 0 31 Values of vGr (kJ mol )atPSAT as a function of temperature for the reactions given in Table A.5 Reaction T (³C) 218253745557085100115150200 H1 64.14 65.87 66.70 68.18 69.22 70.56 72.68 74.89 77.21 79.63 85.70 95.43 H2 52.66 52.72 52.75 52.79 52.81 52.83 52.86 52.87 52.87 52.86 52.78 52.53 H3 38.02 37.64 37.43 37.02 36.71 36.29 35.59 34.82 33.97 33.05 30.60 3.73 H4 18.25 18.33 18.41 18.59 18.74 18.95 19.34 19.79 20.32 20.91 22.56 25.69 H5 8.77 10.00 10.62 11.79 12.64 13.76 15.59 17.57 19.70 21.98 27.84 37.62 H6 37.53 39.97 41.13 43.22 44.69 46.57 49.54 52.66 55.91 59.30 67.78 81.32 H7 9.15 10.58 11.30 12.64 13.61 14.88 16.92 19.11 21.43 23.89 30.16 40.48 H8 38.84 39.51 39.89 40.64 41.20 41.98 43.28 44.72 46.31 48.04 52.63 60.54 H9 34.52 35.63 36.22 37.37 38.22 39.37 41.27 43.36 45.63 48.09 54.47 65.19 H10 55.81 57.94 58.96 60.80 62.09 63.76 66.38 69.14 72.04 75.06 82.63 94.79 H11 19.95 20.93 21.42 22.33 22.97 23.82 25.18 26.64 28.18 29.82 34.01 40.99 H12 25.16 26.52 27.15 28.30 29.10 30.13 31.77 33.50 35.32 37.23 42.09 50.04 H13 20.41 21.40 21.88 22.77 23.40 24.23 25.57 27.02 28.56 30.21 34.47 41.66 H14 25.82 27.25 27.91 29.09 29.90 30.96 32.60 34.33 36.13 38.02 42.73 50.34 H15 20.49 21.54 22.05 22.99 23.66 24.53 25.93 27.43 29.02 30.71 35.05 42.25 H16 25.26 26.75 27.45 28.70 29.58 30.70 32.47 34.32 36.25 38.26 43.28 51.33 H17 25.44 26.95 27.66 28.92 29.79 30.91 32.66 34.47 36.35 38.29 43.08 50.63 H18 22.32 23.43 23.97 24.96 25.65 26.56 27.99 29.51 31.11 32.80 37.05 44.00 H19 6.64 7.03 7.25 7.69 8.02 8.49 9.26 10.15 11.13 12.21 15.15 20.39 H20 22.14 23.59 24.30 25.61 26.56 27.79 29.76 31.86 34.10 36.46 42.48 52.40 H21 15.20 15.91 16.28 16.97 17.48 18.17 19.30 20.55 21.92 23.40 27.29 34.00 H22 29.86 31.66 32.51 34.07 35.18 36.63 38.96 41.46 44.13 46.97 54.30 66.50 H23 22.55 23.53 24.02 24.92 25.56 26.42 27.81 29.30 30.90 32.62 37.03 44.40 H24 29.89 31.40 32.13 33.48 34.45 35.73 37.79 40.02 42.43 45.01 51.71 63.02 H25 23.00 24.19 24.77 25.83 26.59 27.58 29.15 30.84 32.63 34.52 39.33 47.17 H26 28.58 30.16 30.92 32.32 33.32 34.64 36.76 39.06 41.53 44.18 51.02 62.55 H27 52.32 52.52 52.59 52.71 52.79 52.88 53.00 53.12 53.23 53.33 53.51 53.61 H28 21.32 22.01 22.34 22.97 23.42 24.01 24.97 26.00 27.11 28.30 31.40 36.71 H29 22.92 23.94 24.43 25.34 25.98 26.82 28.16 29.59 31.10 32.71 36.82 43.66 H30 33.70 33.98 34.10 34.29 34.41 34.56 34.77 34.97 35.17 35.36 35.77 36.25 H31 50.68 50.97 51.09 51.28 51.40 51.55 51.76 51.97 52.17 52.36 52.79 53.30 H32 20.05 19.13 18.73 18.04 17.59 17.03 16.22 15.44 14.68 13.95 12.31 10.06 H33 20.95 21.56 21.80 22.19 22.43 22.72 23.13 23.51 23.88 24.23 25.05 26.39 H34 43.36 45.23 45.98 47.19 47.94 48.84 50.09 51.25 52.32 53.33 55.52 58.45 H35 72.17 74.60 75.73 77.75 79.14 80.93 83.71 86.61 89.62 92.74 100.47 112.70 H36 11.50 12.47 12.93 13.76 14.34 15.09 16.27 17.51 18.81 20.18 23.64 29.36 H37 36.05 37.76 38.58 40.05 41.07 42.41 44.50 46.69 49.00 51.40 57.45 67.22 H38 62.78 65.09 66.20 68.19 69.59 71.41 74.27 77.29 80.45 83.76 92.04 105.32 H39 50.85 52.09 52.68 53.73 54.47 55.41 56.90 58.45 60.08 61.78 66.05 72.97 H40 8.97 10.24 10.88 12.09 12.96 14.12 15.99 18.01 20.18 22.48 28.40 38.26 H41 13.13 14.19 14.69 15.59 16.22 17.03 18.31 19.66 21.08 22.56 26.31 32.48 H42 39.07 40.76 41.59 43.12 44.21 45.64 47.91 50.34 52.90 55.61 62.49 73.73 H43 23.17 24.44 25.10 26.36 27.27 28.48 30.45 32.58 34.88 37.33 43.64 54.17 H44 18.75 19.90 20.50 21.65 22.49 23.62 25.46 27.46 29.62 31.93 37.91 47.95 H45 10.94 11.92 12.38 13.24 13.84 14.62 15.85 17.15 18.52 19.97 23.63 29.67 H46 38.50 40.28 41.13 42.67 43.74 45.13 47.33 49.64 52.06 54.60 60.97 71.26 H47 66.29 69.04 70.34 72.66 74.27 76.36 79.61 83.02 86.57 90.26 99.42 113.95 H48 7.63 8.41 8.79 9.46 9.93 10.54 11.50 12.51 13.57 14.69 17.54 22.32 H49 12.32 13.05 13.39 14.01 14.44 15.01 15.90 16.83 17.82 18.87 21.56 26.14 H50 35.16 36.85 37.66 39.11 40.12 41.43 43.49 45.66 47.93 50.31 56.28 65.94 H51 49.86 52.04 53.14 55.20 56.68 58.65 61.81 65.21 68.84 72.68 82.48 98.51 H52 32.82 33.73 34.05 34.52 34.77 35.02 35.27 35.38 35.34 35.17 34.19 31.29 H53 40.96 42.41 43.10 44.33 45.19 46.30 48.05 49.87 51.79 53.78 58.77 66.81 H54 46.79 48.26 48.96 50.20 51.07 52.19 53.94 55.79 57.71 59.71 64.74 72.84 H55 3.64 4.28 4.60 5.22 5.67 6.26 7.22 8.26 9.37 10.57 13.68 18.99 H56 58.45 59.97 60.67 61.91 62.76 63.85 65.54 67.29 69.10 70.97 75.62 83.01

[142] Coates, J.D., Michaelidou, U., Bruce, R.A., O'Connor, S.M. and [143] Michaelidou, U., Coates, J.D. and Achenbach, L.A. (1999) Isolation Crespi, J.N. (1999) Ubiquity and diversity of dissimilatory (per)- and characterization of two novel (per)chlorate-reducing bacteria chlorate-reducing bacteria. Appl. Environ. Microbiol. 65, 5234^ from swine waste lagoons. Book of Abstracts, 218th ACS National 5241. Meeting.

FEMSRE 711 7-3-01 230 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

Table A.7

Values of pKa at PSAT as a function of temperature for the reactions given in Table A.5 Reaction T (³C) 218253745557085100115150200 H1 12.18 11.82 11.69 11.48 11.36 11.23 11.06 10.92 10.81 10.72 10.58 10.54 H2 10.00 9.46 9.24 8.89 8.67 8.41 8.05 7.71 7.40 7.11 6.52 5.80 H3 31.52 31.37 31.30 31.18 31.10 31.00 30.85 30.70 30.56 30.41 30.07 0.41 H4 3.46 3.29 3.23 3.13 3.08 3.02 2.94 2.89 2.84 2.81 2.79 2.84 H5 1.67 1.79 1.86 1.99 2.07 2.19 2.37 2.56 2.76 2.96 3.44 4.15 H6 7.12 7.17 7.21 7.28 7.34 7.41 7.54 7.68 7.83 7.98 8.37 8.98 H7 1.74 1.90 1.98 2.13 2.23 2.37 2.58 2.79 3.00 3.22 3.72 4.47 H8 7.37 7.09 6.99 6.84 6.77 6.68 6.59 6.52 6.48 6.47 6.50 6.68 H9 6.55 6.39 6.35 6.29 6.28 6.27 6.28 6.32 6.39 6.47 6.72 7.20 H10 10.59 10.40 10.33 10.24 10.19 10.15 10.10 10.08 10.08 10.10 10.20 10.47 H11 3.79 3.76 3.75 3.76 3.77 3.79 3.83 3.88 3.95 4.01 4.20 4.53 H12 4.78 4.76 4.76 4.77 4.78 4.80 4.84 4.89 4.94 5.01 5.20 5.52 H13 3.88 3.84 3.83 3.84 3.84 3.86 3.89 3.94 4.00 4.07 4.26 4.60 H14 4.90 4.89 4.89 4.90 4.91 4.93 4.96 5.01 5.06 5.12 5.28 5.56 H15 3.89 3.87 3.86 3.87 3.88 3.91 3.95 4.00 4.06 4.13 4.33 4.66 H16 4.80 4.80 4.81 4.83 4.86 4.89 4.94 5.01 5.07 5.15 5.34 5.67 H17 4.83 4.84 4.85 4.87 4.89 4.92 4.97 5.03 5.09 5.15 5.32 5.59 H18 4.24 4.20 4.20 4.20 4.21 4.23 4.26 4.30 4.36 4.41 4.57 4.86 H19 1.26 1.26 1.27 1.30 1.32 1.35 1.41 1.48 1.56 1.64 1.87 2.25 H20 4.20 4.23 4.26 4.31 4.36 4.42 4.53 4.65 4.77 4.91 5.24 5.78 H21 2.89 2.86 2.85 2.86 2.87 2.89 2.94 3.00 3.07 3.15 3.37 3.75 H22 5.67 5.68 5.70 5.74 5.78 5.83 5.93 6.05 6.18 6.32 6.70 7.34 H23 4.28 4.22 4.21 4.20 4.20 4.21 4.23 4.27 4.33 4.39 4.57 4.90 H24 5.67 5.63 5.63 5.64 5.66 5.69 5.75 5.84 5.94 6.06 6.38 6.96 H25 4.37 4.34 4.34 4.35 4.37 4.39 4.44 4.50 4.57 4.65 4.85 5.21 H26 5.43 5.41 5.42 5.44 5.47 5.51 5.60 5.70 5.81 5.95 6.30 6.91 H27 9.93 9.42 9.21 8.88 8.67 8.42 8.07 7.75 7.45 7.18 6.61 5.92 H28 4.05 3.95 3.91 3.87 3.85 3.82 3.80 3.79 3.80 3.81 3.88 4.05 H29 4.35 4.30 4.28 4.27 4.27 4.27 4.29 4.32 4.35 4.40 4.55 4.82 H30 6.40 6.10 5.97 5.78 5.65 5.50 5.29 5.10 4.92 4.76 4.42 4.00 H31 9.62 9.14 8.95 8.64 8.44 8.21 7.88 7.58 7.30 7.05 6.52 5.88 H32 3.81 3.43 3.28 3.04 2.89 2.71 2.47 2.25 2.06 1.88 1.52 1.11 H33 3.98 3.87 3.82 3.74 3.68 3.62 3.52 3.43 3.34 3.26 3.09 2.91 H34 8.23 8.12 8.06 7.95 7.87 7.77 7.62 7.47 7.32 7.18 6.85 6.45 H35 13.70 13.38 13.27 13.09 12.99 12.88 12.74 12.63 12.55 12.48 12.40 12.44 H36 2.18 2.24 2.27 2.32 2.35 2.40 2.48 2.55 2.63 2.72 2.92 3.24 H37 6.84 6.78 6.76 6.75 6.74 6.75 6.77 6.81 6.86 6.92 7.09 7.42 H38 11.92 11.68 11.60 11.49 11.43 11.37 11.31 11.27 11.26 11.27 11.36 11.63 H39 9.65 9.35 9.23 9.05 8.94 8.82 8.66 8.53 8.41 8.31 8.15 8.06 H40 1.70 1.84 1.91 2.04 2.13 2.25 2.43 2.63 2.82 3.03 3.51 4.22 H41 2.49 2.55 2.57 2.63 2.66 2.71 2.79 2.87 2.95 3.04 3.25 3.59 H42 7.42 7.31 7.29 7.26 7.26 7.26 7.29 7.34 7.41 7.48 7.71 8.14 H43 4.40 4.39 4.40 4.44 4.48 4.53 4.64 4.75 4.88 5.02 5.39 5.98 H44 3.56 3.57 3.59 3.65 3.69 3.76 3.88 4.01 4.15 4.30 4.68 5.29 H45 2.08 2.14 2.17 2.23 2.27 2.33 2.41 2.50 2.59 2.69 2.92 3.28 H46 7.31 7.23 7.21 7.19 7.18 7.18 7.20 7.24 7.29 7.35 7.53 7.87 H47 12.58 12.39 12.32 12.24 12.19 12.15 12.12 12.11 12.12 12.15 12.27 12.58 H48 1.45 1.51 1.54 1.59 1.63 1.68 1.75 1.83 1.90 1.98 2.17 2.46 H49 2.34 2.34 2.35 2.36 2.37 2.39 2.42 2.46 2.50 2.54 2.66 2.89 H50 6.68 6.61 6.60 6.59 6.59 6.60 6.62 6.66 6.71 6.77 6.95 7.28 H51 9.47 9.34 9.31 9.30 9.31 9.34 9.41 9.51 9.64 9.78 10.18 10.88 H52 30.54 30.67 30.71 30.76 30.78 30.80 30.80 30.78 30.75 30.70 30.52 30.14 H53 7.78 7.61 7.55 7.47 7.42 7.37 7.31 7.27 7.25 7.24 7.25 7.38 H54 8.88 8.66 8.58 8.46 8.38 8.31 8.21 8.14 8.08 8.04 7.99 8.04 H55 0.69 0.77 0.81 0.88 0.93 1.00 1.10 1.20 1.31 1.42 1.69 2.10 H56 11.10 10.76 10.63 10.43 10.30 10.16 9.98 9.81 9.67 9.55 9.33 9.16

[144] Hackenthal, E., Mannheim, W., Hackenthal, R. and Becher, R. tase formation in Proteus mirabilis 1. Formation of reductases and (1964) Die Reduktion von Perchlorat durch Bakterien. I. Unter- enzymes of the formic hydrogen^lyase complex in the wild type and suchungen an intakten Zellen. Biochem. Pharm. 13, 195^206. in chlorate-resistant mutants. Arch. Microbiol. 66, 220^233. [145] Stouthamer, A.H. (1967) Nitrate reduction in Aerobacter aerogenes. [147] Romanenko, V.I., Koren'kov, V.N. and Kuznetsov, S.I. (1976) Bac- Arch. Mikrobiol. 56, 68^75. terial of ammonium perchlorate. Mikrobiologiya (in [146] De Groot, G.N. and Stouthamer, A.H. (1969) Regulation of reduc- Russian) 45, 204^209.

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 231

Table A.8 [154] Ellis, A.J. (1963) The ionization of acetic, propionic, n-butyric and Auxiliary redox, disproportionation, and hydrolysis reactions benzoic acid in water, from conductance measurements up to 225³. J. Chem. Soc. 1963, 2299^2310. J1 2H O (aq)H2H O(l)+O (aq) 2 2 2 2 [155] Lown, D.A., Thirsk, H.R. and Wynne-Jones, L. (1970) Temperature J2 VO‡+H‡+0.5H (aq)HVO2‡+H O(l) 2 2 2 and pressure dependence of the volume of ionization of acetic acid J3 VO2‡+H‡+0.5H (aq)HV3‡+H O(l) 2 2 in water from 25 to 225³C and 1^3000 bar. Trans. Faraday Soc. 66, J4 V3‡+0.5H (aq)HV2‡+H‡ 2 51^73. J5 Cr O23+H O(l)H2CrO23+2H‡ 2 7 2 4 [156] Fisher, J.R. and Barnes, H.L. (1972) The ion-product constant of J6 CrO23+5H‡+1.5H (aq)HCr3‡+4H O(l) 4 2 2 water to 350³C. J. Phys. Chem. 76, 90^99. J7 MnO3+0.5H (aq)HMnO23+H‡ 4 2 4 [157] Oscarson, J.L., Gillespie, S.E., Christensen, J.J., Izatt, R.M. and J8 MnO23+5H‡+1.5H (aq)HMn3‡+4H O(l) 4 2 2 Brown, P.R. (1988) Thermodynamic quantities for the interaction J9 Mn3‡+0.5H (aq)HMn2‡+H‡ 2 of H‡ and Na‡ with C H O3 and Cl3 in aqueous solution from J10 Co3‡+0.5H (aq)HCo2‡+H‡ 2 3 2 2 275 to 320³C. J. Sol. Chem. 17, 865^885. J11 Cu2‡+0.5H (aq)HCu2‡+H‡ 2 [158] Mesmer, R.E., Patterson, C.S., Busey, R.H. and Holmes, H.F. J12 HAsO (aq)+2H O(l)HHAsO23+2H‡+H (aq) 2 2 4 2 (1989) Ionization of acetic acid in NaCl(aq) media: A potentiomet- J13 SeO23+H O(l)HSeO23+H (aq) 3 2 4 2 ric study to 573 K and 130 bar. J. Phys. Chem. 93, 7483^7490. J14 HSe3+3H O(l)HSeO23+3H (aq)+H‡ 2 3 2 [159] Dickson, A.G., Wesolowski, D.J., Palmer, D.A. and Mesmer, R.E. J15 Au3‡+H (aq)HAu‡+2H‡ 2 (1990) Dissociation constant of bisulfate ion in aqueous sodium J16 P O43+H O(l)H2HPO23 2 7 2 4 chloride solutions to 250³C. J. Phys. Chem. 94, 7978^7985. J17 H P O23+H O(l)H2H PO3 2 2 7 2 2 4 [160] Harned, H.S. and Davis Jr., R. (1943) The ionization constant of J18 HP O33+H O(l)H2HPO23+H‡ 2 7 2 4 carbonic acid in water and the solubility of carbon dioxide in water and aqueous salt solutions from 0 to 50³. J. Am. Chem. Soc. 65, 2030^2037. [148] Malmqvist, A., Welander, T., Moore, E., Ternstrom, A., Molin, G. [161] Drummond, S.E. (1981) Ph.D. thesis, Pennsylvania State University, and Stenstrom, I.-M. (1994) Ideonella dechloratans gen. nov., sp. PA. nov., a new bacterium capable of growing anaerobically with chlo- [162] Zawisza, A. and Malesinska, B. (1981) Solubility of carbon dioxide rate as an electron acceptor. Syst. Appl. Microbiol. 17, 58^64. in liquid water and water in gaseous carbon dioxide in the range [149] Roldan, M.D., Reyes, F., Moreno-Vivian, C. and Castillo, F. (1994) 0.2^5 MPa and at temperatures up to 473 K. J. Chem. Eng. Data Chlorate and nitrate reduction in the phototrophic bacteria Rhodo- 26, 388^391. bacter capsulatus and . Curr. Microbiol. 29, [163] Krumholz, L.R., McKinley, J.P., Ulrich, G.A. and Su£ita, J.M. 241^245. (1997) Con¢ned subsurface microbial communities in Cretaceous [150] Rikken, G.B., Kroon, A.G.M. and van Ginkel, C.G. (1996) Trans- rock. Nature 386, 64^66. formation of (per)chlorate into chloride by a newly isolated bacte- [164] Phelps, T.J., Raione, E.G., White, D.C. and Fliermans, C.B. (1989) rium: reduction and dismutation. Appl. Microbiol. Biotechnol. 45, Microbial activities in deep subsurface environments. Geomicrobiol. 420^426. J. 7, 79^92. [151] Tsunogai, S. and Sase, T. (1969) Formation of iodide^iodine in the [165] Jones, W.J., Stugard, C.E. and Jannasch, H.W. (1989) Comparison ocean. Deep-Sea Res. 16, 489^496. of thermophilic methanogens from submarine hydrothermal vents. [152] Noyes, A.A., Kato, Y. and Sosman, R.B. (1910) The hydrolysis of Arch. Microbiol. 151, 314^318. ammonium acetate and the ionization of water at high temperatures. [166] Haldeman, D.L., Amy, P.S., Ringelberg, D. and White, D.C. (1993) J. Am. Chem. Soc. 32, 159^178. Characterization of the microbiology within a 21 m3 section of rock [153] Harned, H.S. and Ehlers, R.W. (1933) The dissociation constant of from the deep subsurface. Microb. Ecol. 26, 145^159. acetic acid from 0 to 60³ centigrade. J. Am. Chem. Soc. 55, 652^656. [167] Russell, C.E., Jacobson, R., Haldeman, D.L. and Amy, P.S. (1994)

Table A.9 0 31 Values of vGr (kJ mol )atPSAT as a function of temperature for the reactions given in Table A.8 Reaction T (³C) 2 18 25 37 45 55 70 85 100 115 150 200 J1 3190.99 3190.09 3189.79 3189.39 3189.20 3189.03 3188.93 3188.99 3189.19 3189.54 3190.88 3193.93 J2 3106.80 3105.83 3105.46 3104.89 3104.56 3104.19 3103.71 3103.32 3103.02 3102.78 3102.48 3102.50 J3 342.95 342.23 341.87 341.16 340.66 339.98 338.89 337.72 336.48 335.15 331.78 326.26 J4 17.56 16.33 15.82 14.99 14.45 13.81 12.88 12.00 11.16 10.36 8.59 6.22 J5 78.53 82.18 83.93 87.10 89.34 92.24 96.82 101.66 106.75 112.09 125.51 147.24 J6 3454.71 3451.54 3450.22 3448.03 3446.62 3444.93 3442.51 3440.23 3438.09 3436.08 3431.88 3427.07 J7 365.70 363.49 362.41 360.43 359.02 357.18 354.25 351.12 347.81 344.33 335.51 321.18 J8 3560.87 3557.78 3556.49 3554.37 3553.01 3551.37 3549.04 3546.85 3544.80 3542.89 3538.92 3534.46 J9 3149.58 3152.98 3154.46 3157.02 3158.73 3160.86 3164.06 3167.27 3170.49 3173.71 3181.30 3192.37 J10 3193.37 3196.00 3197.14 3199.10 3200.41 3202.03 3204.46 3206.89 3209.31 3211.74 3217.44 3225.73 J11 321.93 323.69 324.45 325.75 326.61 327.68 329.28 330.87 332.45 334.02 337.70 343.03 J12 175.54 178.72 180.17 182.73 184.49 186.74 190.22 193.82 197.56 201.43 211.05 226.39 J13 183.90 183.55 183.36 182.98 182.71 182.34 181.73 181.07 180.36 179.59 177.63 174.42 J14 348.44 350.18 350.92 352.13 352.92 353.88 355.29 356.67 358.01 359.34 362.42 366.91 J15 3281.47 3286.05 3288.01 3291.32 3293.50 3296.19 3300.16 3304.06 3307.92 3311.72 3320.51 3332.98 J16 322.36 322.03 321.89 321.66 321.51 321.32 321.05 320.79 320.54 320.30 319.77 319.10 J17 314.35 313.71 313.36 312.68 312.18 311.51 310.40 39.20 37.90 36.50 32.95 2.83 J18 27.49 30.01 31.25 33.54 35.18 37.33 40.76 44.42 48.30 52.38 62.71 79.41

FEMSRE 711 7-3-01 232 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

Table A.10 D.C. and Boone, D.R. (1998) Observations pertaining to the origin Redox reactions in the system H^O^P and of microorganisms recoverd from the deep subsurface of Taylorsville Basin, Virginia. Geomicrobiol. J. 15, 353^385. K1 H PO (aq)HH PO (aq)+0.5O (aq) 3 4 3 3 2 [180] Nilsen, R.K., Torsvik, T. and Lien, T. (1996) Desulfotomaculum K2 H P O (aq)+H O(l)H2H PO (aq)+O (aq) 4 2 7 2 3 3 2 thermocisternum sp. nov., a sulfate reducer isolated from a hot K3 H PO (aq)HH PO (aq)+O (aq) 3 4 3 2 2 North Sea oil reservoir. Int. J. Syst. Bacteriol. 46, 397^402. K4 H P O (aq)+H O(l)H2H PO (aq)+2O (aq) 4 2 7 2 3 2 2 [181] Greene, A.C., Patel, B.K.C. and Sheehy, A.J. (1997) Deferribacter K5 H PO (aq)HH PO (aq)+0.5O (aq) 3 3 3 2 2 thermophilus gen. nov. sp. nov., a novel thermophilic manganese- and iron-reducing bacterium isolated from a petroleum reservoir. Int. J. Syst. Bacteriol. 47, 505^509. Heterogeneity of deep subsurface microorganisms and correlations [182] Clark, D.A. and Norris, P.R. (1996) Acidimicrobium ferrooxidans to hydrogeological and geochemical parameters. Geomicrobiol. J. 12, gen. nov., sp. nov. mixed-culture ferrous iron oxidation with Sulfo- 37^51. bacillus species. Microbiology 142, 785^790. [168] Brown, D.A., Kamineni, D.C., Sawicki, J.A. and Beveridge, T.J. [183] Bridge, T.A.M. and Johnson, B. (1998) Reduction of soluble iron (1994) Minerals associated with bio¢lms occurring on exposed and reductive dissolution of ferric iron-containing minerals by mod- rock in a granitic underground research laboratory. Appl. Environ. erately thermophilic iron oxidizing bacteria. Appl. Environ. Micro- Microbiol. 60, 3182^3191. biol. 64, 2181^2186. [169] Brown, D.A. and Sherri¡, B.L. (1997) Active ultramicrobacterial [184] Wisotzkey, J.D., Jurtshuk Jr., P., Fox, G.E., Deinhard, G. and alteration of iron in granite. Proc. SPIE-Int. Soc. Opt. Eng. 3111, Poralla, K. (1992) Comparitive sequence analyses on the 16S 510^518. rRNA (rDNA) of Bacillus acidocaldarius, Bacillus acidoterrestris, [170] Love, C.A., Patel, B.K.C., Nichols, P.D. and Stackebrandt, E. and Bacillus cycloheptanicus and proposal for creation of a new (1993) Desulfotomaculum australicum, sp. nov., a thermophilic sul- genus, Alicyclobacillus gen. nov. Int. J. Syst. Bacteriol. 42, 263^ fate-reducing bacterium isolated from the Great Artesian basin of 269. Australia. Syst. Appl. Microbiol. 16, 244^251. [185] Darland, G. and Brock, T.D. (1971) Bacillus acidocaldarius sp. nov., [171] Wynter, C., Patel, B.K.C., Bain, P., Jersey, J.d., Hamilton, S. and an acidophilic thermophilic spore-forming bacterium. J. Gen. Mi- Inkerman, P.A. (1996) A novel thermostable dextranase from a crobiol. 67, 9^15. Thermoanaerobacter species cultured from the geothermal waters [186] Nicolaus, B., Improta, R., Manca, M.C., Lama, L., Esposito, E. of the Great Artesian Basin of Australia. FEMS Microbiol. Lett. and Gambacorta, A. (1998) Alicyclobacilli from an unexplored geo- 140, 271^276. thermal soil in Antarctica: Mount Rittmann. Polar Biol. 19, 131^ [172] Byers, H.K., Stackebrandt, E., Hayward, C. and Balckall, L.L. 141. (1998) Molecular investigation of a associated with [187] Huber, R., Rossnagel, P., Woese, C.R., Rachel, R., Langworthy, the Great Artesian Basin. FEMS Microb. Ecol. 25, 391^403. T.A. and Stetter, K.O. (1996) Formation of ammonium from nitrate [173] Ekendahl, S. and Pedersen, K. (1994) Carbon transformation by during chemolithoautotrophic growth of the extremely thermophilic attached bacterial populations in granitic groundwater from deep bacterium Ammonifex degensii gen. nov. sp. nov. Syst. Appl. Micro- crystalline bed-rock of the Stripa research mine. Microbiology biol. 19, 40^49. 140, 1565^1573. [188] Engle, M., Li, Y., Woese, C. and Wiegel, J. (1995) Isolation and [174] Olson, G.J., Dockins, W.S., McFeters, G.A. and Iverson, W.P. characterization of a novel alkalitolerant thermophile, Anaerobranca (1981) Sulfate-reducing and methanogenic bacteria from deep aqui- horikoshii gen. nov., sp. nov. Int. J. Syst. Bacteriol. 45, 454^461. fers in Montana. Geomicrobiol. J. 2, 327^340. [189] Schenk, A. and Aragno, M. (1979) Bacillus schlegelii, a new species [175] Liu, Y., Karnauchow, T.M., Jarrell, K.F., Balkwill, D.L., Drake, of thermophilic, facultatively chemolithoautotrophic bacterium oxi- G.R., Ringelberg, D., Clarno, R. and Boone, D.R. (1997) Descrip- dizing molecular hydrogen. J. Gen. Microbiol. 115, 333^341. tion of two new thermophilic Desulfotomaculum spp., Desulfotomac- [190] Nicolaus, B., Lama, L., Esposito, E., Manca, M.C., Di Prisco, G. ulum putei sp. nov., from a deep terrestrial subsurface, and Desulfo- and Gambacorta, A. (1996) Bacillus thermoantarcticus sp. nov., tomaculum luciae sp. nov., from a hot spring. Int. J. Syst. Bacteriol. from Mount Melbourne, Antarctica a novel thermophilic species. 47, 615^621. Polar Biol. 16, 101^104. [176] Grossman, D. and Schulman, S. (1995) The biosphere below, Earth, [191] Nicolaus, B., Marsiglia, F., Esposito, E., Trincone, A., Lama, L., June 4, 35^40. Sharp, R., Di Prisco, G. and Gambacorta, A. (1991) Isolation of [177] Daumas, S., Lombart, R. and Bianchi, A. (1986) A Bacteriological ¢ve strains of thermophilic eubacteria in Antarctica. Polar Biol. 11, study of geothermal spring waters dating from the Dogger and Trias 425^429. Period in the Paris Basin. Geomicrobiol. J. 4, 423^433. [192] Sunna, A., Tokajian, S., Burghardt, J., Rainey, F., Antranikian, G. [178] Tardy-Jacquenod, C., Magot, M., Patel, B.K.C., Matheron, R. and and Hashwa, F. (1997) Identi¢cation of Bacillus kaustophilus, Bacil- Caumette, P. (1998) Desulfotomaculum halophilum sp. nov., a halo- lus thermocatenulatus and Bacillus strain HSR as members of Bacil- philic sulfate-reducing bacterium isolated from oil production facili- lus thermoleovorans. Syst. Appl. Microbiol. 20, 232^237. ties. Int. J. Syst. Bacteriol. 48, 333^338. [193] Anderson, M., Laukkanen, M., Nurmiaho-Lassila, E.-L., Rainey, [179] Onstott, T.C., Phelps, T.J., Colwell, F.S., Ringelberg, D., White, F.A., Niemela, S.I. and Salkinoja-Salonen, M. (1995) Bacillus ther-

Table A.11 0 31 Values of vGr (kJ mol )atPSAT as a function of temperature for the reactions given in Table A.10 Reaction T (³C) 218253745557085100115150200 K1 295.71 294.57 294.04 293.08 292.40 291.53 290.17 288.73 287.24 285.68 281.82 275.75 K2 575.14 573.07 572.13 570.47 569.33 567.87 565.63 563.32 560.94 558.49 552.54 543.45 K3 637.98 636.49 635.78 634.48 633.57 632.37 630.50 628.51 626.42 624.24 618.79 610.17 K4 1259.69 1256.89 1255.59 1253.27 1251.65 1249.56 1246.29 1242.87 1239.31 1235.61 1226.48 1212.27 K5 342.27 341.91 341.73 341.40 341.16 340.84 340.33 339.77 339.18 338.56 336.97 334.41

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 233

Table A.12 0 31 Values of vG (kJ mol )atPSAT as a function of temperature for compounds in the system H^O^halogen Compound T (³C) 2 18 25 37 45 55 70 85 100 115 150 200 HCl(aq) 3127.04 3127.15 3127.24 3127.42 3127.58 3127.81 3128.21 3128.69 3129.24 3129.86 3131.59 3134.75 Cl3 3129.86 3130.88 3131.29 3131.94 3132.35 3132.83 3133.48 3134.07 3134.58 3135.03 3135.78 3136.04 ClO3 335.73 336.52 336.82 337.30 337.58 337.92 338.38 338.79 339.14 339.44 339.90 339.91 HClO(aq) 376.69 378.93 379.92 381.63 382.78 384.23 386.43 388.66 390.93 393.22 398.67 3106.72 3 ClO2 19.57 17.87 17.15 15.95 15.18 14.22 12.81 11.44 10.11 8.82 5.96 2.38 HClO2(aq) 10.08 7.16 5.85 3.57 2.01 0.04 32.97 36.06 39.20 312.42 320.14 331.73 3 ClO3 34.16 36.81 37.95 39.89 311.17 312.76 315.13 317.47 319.80 322.10 327.36 334.51 3 ClO4 34.32 37.26 38.54 310.72 312.17 313.98 316.69 319.41 322.13 324.84 331.15 339.97 Br3 3102.02 3103.47 3104.06 3105.02 3105.64 3106.37 3107.42 3108.39 3109.31 3110.15 3111.83 3113.47 BrO3 332.41 333.18 333.47 333.93 334.21 334.54 334.98 335.36 335.69 335.97 336.38 336.31 HBrO(aq) 379.21 381.44 382.43 384.13 385.28 386.73 388.92 391.15 393.40 395.68 3101.12 3109.14 3 BrO3 22.43 19.76 18.61 16.69 15.43 13.87 11.57 9.30 7.07 4.88 30.08 36.68 3 BrO4 122.60 119.38 117.98 115.60 114.01 112.03 109.07 106.11 103.16 100.22 93.41 83.93 I3 349.35 351.17 351.93 353.18 353.99 354.97 356.38 357.72 358.99 360.20 362.72 365.55 IO3 338.47 338.52 338.49 338.39 338.29 338.13 337.83 337.46 337.02 336.52 335.06 332.20 HIO(aq) 396.92 398.49 399.16 3100.30 3101.05 3101.98 3103.37 3104.75 3106.12 3107.49 3110.68 3115.20 3 IO3 3125.24 3127.20 3128.03 3129.44 3130.36 3131.50 3133.19 3134.84 3136.46 3138.05 3141.62 3146.27 HIO3(aq) 3128.87 3131.47 3132.64 3134.66 3136.03 3137.76 3140.40 3143.09 3145.83 3148.62 3155.30 3165.26 3 IO4 353.47 357.03 358.58 361.24 363.02 365.23 368.55 371.88 375.20 378.53 386.24 397.09

Table A.13 and characterization of Caldicellulosiruptor lactoaceticus sp. nov., an Metabolic reactions involving Cl extremely thermophilic, cellulolytic, anaerobic bacterium. Arch. Mi- crobiol. 163, 223^230. L1 ClO3+acetic acid(aq)HCl3+2CO (aq)+2H O(l) 4 2 2 [197] Huang, C.-Y., Patel, B., Mah, R. and Baresi, L. (1998) Caldicellu- L2 2ClO3+acetic acid(aq)H2ClO3+2CO (aq)+2H O(l) 4 2 2 2 losiruptor owensensis sp. nov., an anaerobic, extremely thermophilic, L3 ClO3HCl3+2O (aq) 4 2 xylanolytic bacterium. Int. J. Syst. Bacteriol. 48, 91^97. L4 4ClO3+3acetic acid(aq)H4Cl3+6CO (aq)+6H O(l) 3 2 2 [198] Rainey, F.A., Donnison, A.M., Janssen, P.H., Saul, D., Rodrigo, L5 4ClO3+acetic acid(aq)H4ClO3+2CO (aq)+2H O(l) 3 2 2 2 A., Bergquist, P.L., Daniel, R.M., Stackebrandt, E. and Morgan, L6 ClO3HCl3+1.5O (aq) 3 2 H.W. (1994) Description of Caldicellulosiruptor saccharolyticus gen. L7 ClO3+3H (aq)HCl3+3H O(l) 3 2 2 nov., sp. nov.: An obligately anaerobic, extremely thermophilic, L8 ClO3+3H S(aq)HCl3+3S(s)+3H O(l) 3 2 2 cellulolytic bacterium. FEMS Microbiol. Let. 120, 263^266. L9 ClO3HCl3+O (aq) 2 2 [199] Chrisostomos, S., Patel, B.K.C., Dwivedi, P.P. and Denman, S.E. (1996) Caloramator indicus sp. nov., a new thermophilic anaerobic bacterium isolated from the deep-seated nonvolcanically heated mosphaericus sp. nov. a new thermophilic ureolytic Bacillus isolated waters of an Indian artesian aquifer. Int. J. Syst. Bacteriol. 46, from air. Syst. Appl. Microbiol. 18, 203^220. 497^501. [194] Bonjour, F. and Aragno, M. (1984) Bacillus tusciae, a new species of [200] Tarlera, S., Muxi, L., Soubes, M. and Stams, A.J.M. (1997) Calo- thermoacidophilic, facultatively chemolithoautotrophic, hydrogen ramator proteoclasticus sp. nov., a new moderately thermophilic an- oxidizing sporeformer from a geothermal area. Arch. Microbiol. aerobic proteolytic bacterium. Int. J. Syst. Bacteriol. 47, 651^656. 139, 397^401. [201] Pierson, B.K. and Castenholz, R.W. (1974) A phototrophic gliding [195] Kryukov, V.R., Savel'eva, N.D. and Pusheva, M.A. (1983) Caldero- ¢lamentous bacterium of hot springs, Chloro£exus aurantiacus, gen. bacterium hydrogenophilum gen. et. sp. nov., an extremely thermo- and sp. nov. Arch. Microbiol. 100, 5^24. philic hydrogen bacterium and its activity. Mikrobio- [202] Li, Y., Mandelco, L. and Wiegel, J. (1993) Isolation and character- logiya (in Russian) 52, 781^788. ization of a moderately thermophilic anaerobic , Clostri- [196] Mladenovska, Z., Mathrani, I.M. and Ahring, B. (1995) Isolation dium paradoxum sp. nov. Int. J. Syst. Bacteriol. 43, 450^460.

Table A.14 0 31 Values of vGr (kJ mol )atPSAT as a function of temperature for the reactions given in Table A.13 Reaction T (³C) 218253745557085100115150200 L1 3971.34 3972.13 3972.59 3973.53 3974.24 3975.21 3976.83 3978.61 3980.54 3982.62 3987.92 3996.45 L2 3798.02 3798.24 3798.46 3798.96 3799.37 3799.97 3801.03 3802.24 3803.61 3805.11 3809.09 3815.68 L3 387.92 389.05 389.67 390.87 391.75 392.94 394.90 397.04 399.34 3101.81 3108.12 3118.42 L4 33040.19 33041.80 33042.87 33045.13 33046.89 33049.35 33053.53 33058.23 33063.40 33069.00 33083.53 33107.25 L5 3750.87 3749.79 3749.42 3748.92 3748.68 3748.45 3748.28 3748.29 3748.45 3748.77 3750.02 3752.81 L6 397.48 398.15 398.53 399.29 399.86 3100.64 3101.94 3103.38 3104.95 3106.65 3111.03 3118.29 L7 3889.29 3888.51 3888.05 3887.14 3886.46 3885.51 3883.94 3882.18 3880.26 3878.18 3872.74 3863.59 L8 3754.87 3752.33 3751.12 3748.93 3747.39 3745.39 3742.25 3738.95 3735.52 3731.99 3723.61 3710.74 L9 3130.62 3131.47 3131.90 3132.72 3133.31 3134.09 3135.35 3136.70 3138.13 3139.65 3143.48 3149.59

FEMSRE 711 7-3-01 234 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

Table A.15 [203] Drent, W.J., Lahpor, G.A., Wiegant, W.M. and Gottschal, J.C. Mineral hydrolysis and redox reactions (1991) Fermentation of inulin by Clostridium thermosuccinogenes sp. nov., a thermophilic anaerobic bacterium isolated from various M1 magnesite(s)+H‡HMg2‡+HCO3 3 habitats. Appl. Environ. Microbiol. 57, 455^462. M2 calcite(s)+H‡HCa2‡+HCO3 3 [204] Rainey, F.A. and Stackebrandt, E. (1993) Transfer of the type spe- M3 dolomite(s)+2H‡HCa2‡+Mg2‡+2HCO3 3 cies of the genus Thermobacteroides to the genus Thermoanaero- M4 alabandite(s)+2H‡HMn2‡+H S(aq) 2 bacter as Thermoanaerobacter acetoethylicus (Ben-Bassat and Zeikus M5 rhodochrosite(s)+H‡HMn2‡+HCO3 3 1981) comb. nov., Description of Coprothermobacter gen. nov., and M6 hematite(s)+6H‡H2Fe3‡+3H O 2 reclassi¢cation of Thermobacteroides proteolyticus as Coprothermo- M7 hematite(s)+4H‡+H (aq)H2Fe2‡+3H O(l) 2 2 bacter proteolyticus (Ollivier et al., 1985) comb. nov. Int. J. Syst. M8 magnetite(s)+6H‡+H (aq)H3Fe2‡+4H O 2 2 Bacteriol. 43, 857^859. M9 pyrrhotite(s)+2H‡HFe2‡+H S(aq) 2 [205] Ferreira, A.C., Nobre, M.F., Rainey, F.A., Silva, M.T., Wait, R., M10 siderite(s)+H‡HFe2‡+HCO3 3 Burghardt, J., Ching, A.P. and Da Costa, M.S. (1997) Deinococcus M11 pyrite(s)+2H‡+H (aq)HFe2‡+2H S(aq) 2 2 geothermalis sp. nov. and sp. nov., two ex- M12 chalcopyrite(s)+4H‡HCu2‡+Fe2‡+2H S(aq) 2 tremely radiation-resistant and slightly thermophilic species from M13 covellite(s)+2H‡HCu2‡+H S(aq) 2 hot springs. Int. J. Bacteriol. 47, 939^947. M14 chalcocite(s)+2H‡H2Cu‡+H S(aq) 2 [206] Rees, G.N., Grassia, G.S., Sheehy, A.J., Dwivedi, P.P. and Patel, M15 cuprite(s)+2H‡H2Cu‡+H O(l) 2 B.K.C. (1995) Desulfacinum infernum gen. nov., sp. nov., a thermo- M16 bornite(s)+8H‡H5Cu‡+Fe3‡+4H S(aq) 2 philic sulfate-reducing bacterium from a petroleum reservoir. Int. J. M17 bornite(s)+5H‡+9.25O (aq)H5Cu2‡+Fe3‡+4SO23+2.5H O(l) 2 4 2 Syst. Bacteriol. 45, 85^89. M18 sphalerite(s)+2H‡HZn2‡+H S(aq) 2 [207] Nazina, T.N., Ivanova, A.E., Kanchaveli, L.P. and Rozanova, E.P. M19 selenium(s)+H (aq)HHSe3+H‡ 2 (1988) A new sporeforming thermophilic methylotrophic sulfate-re- M20 selenium(s)+H O(l)+1O (aq)HHSeO3+H‡ 2 2 3 ducing bacterium, Desulfotomaculum kuznetsovii sp. nov. Mikrobio- M21 molybdenite(s)+4H O(l)HMoO23+2H S(aq)+2H‡+H (aq) 2 4 2 2 logiya (in Russian) 57, 823^827. M22 silver(s)+H‡HAg‡+0.5H (aq) 2 [208] Karnauchow, T.M., Koval, S.F. and Jarrell, K.F. (1992) Isolation M23 gold(s)+H‡HAu‡+0.5H (aq) 2 and characterization of three thermophilic anaerobes from a St. M24 quicksilver(s)+2H‡HHg2‡+H (aq) 2 Lucia hot spring. Syst. Appl. Microbiol. 15, 296^310. M25 galena(s)+2H‡HPb2‡+H S(aq) 2 [209] Nazina, T.N. and Rozanova, E.P. (1978) Thermophilic sulfate-re- M26 anglesite(s)HPb2‡+SO23 4 ducing bacteria from oil strata. Mikrobiologiya (in Russian) 47, M27 uraninite(s)+2H‡HUO2‡+H (aq) 2 2 142^148. M28 uraninite(s)HUO (aq) 2 [210] Min, H. and Zinder, S.H. (1990) Isolation and characterization of a thermophilic sulfate-reducing bacterium Desulfotomaculum thermo- acetoxidans sp. nov. Arch. Microbiol. 153, 399^404. Table A.16 0 31 Values of vGr (kJ mol )atPSAT as a function of temperature for the reactions given in Table A.15 Reaction T (³C) 218253745557085100115150200 M1 315.37 313.82 313.09 311.79 310.90 39.76 37.98 36.13 34.20 32.19 2.85 11.12 M2 311.56 310.89 310.55 39.91 39.44 38.82 37.82 36.72 35.53 34.24 30.81 5.29 M3 317.56 315.39 314.34 312.44 311.11 39.38 36.64 33.74 30.67 2.57 10.93 25.13 M4 340.77 340.31 340.15 339.90 339.76 339.63 339.48 339.39 339.35 339.37 339.55 340.02 M5 32.86 31.88 31.41 30.54 0.06 0.85 2.10 3.43 4.84 6.34 10.20 16.84 M6 310.51 33.64 30.62 4.58 8.05 12.39 18.89 25.41 31.95 38.53 54.11 77.28 M7 3170.13 3167.89 3166.87 3165.08 3163.86 3162.32 3159.97 3157.57 3155.12 3152.62 3146.53 3137.02 M8 3231.43 3227.71 3226.02 3223.10 3221.14 3218.66 3214.90 3211.11 3207.26 3203.36 3193.96 3179.51 M9 319.67 318.95 318.66 318.19 317.90 317.57 317.11 316.70 316.33 316.00 315.23 314.01 M10 31.33 0.33 1.10 2.48 3.44 4.67 6.59 8.60 10.69 12.88 18.37 27.38 M11 34.14 34.61 34.85 35.28 35.60 36.02 36.70 37.44 38.22 39.03 311.05 314.02 M12 104.01 105.51 106.10 107.04 107.60 108.26 109.11 109.86 110.48 111.02 111.98 112.98 M13 89.45 90.16 90.43 90.86 91.11 91.40 91.76 92.06 92.28 92.46 92.69 92.76 M14 160.14 158.96 158.38 157.30 156.52 155.50 153.85 152.09 150.21 148.36 143.79 136.62 M15 12.10 11.26 10.87 10.13 9.61 8.92 7.81 6.63 5.37 4.05 0.72 34.47 M16 483.48 483.88 483.85 483.54 483.17 482.53 481.22 479.53 477.50 475.17 468.70 457.57 M17 33091.33 33063.58 33050.32 33026.31 33009.51 32987.69 32953.39 32917.31 32879.52 32840.04 32741.31 32583.23 M18 24.33 25.11 25.41 25.90 26.20 26.53 26.99 27.37 27.69 27.97 28.45 28.90 M19 26.02 26.09 26.21 26.52 26.79 27.20 27.94 28.82 29.85 31.02 34.27 40.25 M20 3192.49 3191.39 3190.81 3189.71 3188.90 3187.81 3186.02 3184.05 3181.92 3179.61 3173.61 3163.45 M21 335.21 335.12 335.09 335.05 335.03 335.03 335.06 335.14 335.28 335.49 336.30 338.51 M22 87.25 86.37 85.96 85.22 84.71 84.04 82.99 81.88 80.73 79.52 76.53 71.87 M23 174.03 172.65 172.04 170.96 170.23 169.29 167.86 166.39 164.88 163.34 159.62 154.02 M24 181.01 182.01 182.41 183.02 183.40 183.84 184.41 184.90 185.31 185.66 186.24 186.64 M25 46.03 45.26 44.90 44.26 43.81 43.23 42.32 41.36 40.35 39.31 36.77 32.95 M26 42.69 44.08 44.83 46.27 47.33 48.76 51.09 53.64 56.42 59.40 67.25 80.82 M27 94.08 96.09 96.93 98.30 99.19 100.27 101.81 103.30 104.73 106.12 109.24 113.51 M28 49.31 52.30 53.60 55.82 57.30 59.15 61.91 64.67 67.43 70.18 76.58 85.70

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 235

Table A.17 Cation hydrolysis reactions

2‡ ‡ ‡ 2‡ 3 ‡ N1 Mg +H2O(l)HMgOH +H N29 Ni +2H2O(l)HHNiO2 +3H 2‡ ‡ ‡ 2‡ 23 ‡ N2 Ca +H2O(l)HCaOH +H N30 Ni +2H2O(l)HNiO2 +4H 2‡ ‡ ‡ 2‡ ‡ ‡ N3 VO +H2O(l)HVOOH +H N31 Cu +H2O(l)HCuOH +H 2‡ ‡ ‡ 2‡ ‡ N4 VOH HVO +H N32 Cu +H2O(l)HCuO(aq)+2H 3‡ 2‡ ‡ 2‡ 3 ‡ N5 V +H2O(l)HVOH +H N33 Cu +2H2O(l)HHCuO2 +3H 2‡ ‡ ‡ 2‡ 23 ‡ N6 V +H2O(l)HVOH +H N34 Cu +2H2O(l)HCuO2 +4H 3‡ 3 ‡ 2‡ ‡ ‡ N7 Cr +2H2O(l)HCrO2 +4H N35 Zn +H2O(l)HZnOH +H 3‡ ‡ 2‡ ‡ N8 Cr +2H2O(l)HHCrO2(aq)+3H N36 Zn +H2O(l)HZnO(aq)+2H 3‡ ‡ ‡ 2‡ 3 ‡ N9 Cr +H2O(l)HCrO +2H N37 Zn +2H2O(l)HHZnO2 +3H 3‡ 2‡ ‡ 2‡ 23 ‡ N10 Cr +H2O(l)HCrOH +H N38 Zn +2H2O(l)HZnO2 +4H 2‡ ‡ ‡ 2‡ ‡ ‡ N11 Mn +H2O(l)HMnOH +H N39 Hg +H2O(l)HHgOH +H 2‡ ‡ 2‡ ‡ N12 Mn +H2O(l)HMnO(aq)+2H N40 Hg +H2O(l)HHgO(aq)+2H 2‡ 3 ‡ 2‡ 3 ‡ N13 Mn +2H2O(l)HHMnO2 +3H N41 Hg +2H2O(l)HHHgO2 +3H 2‡ 23 ‡ 2‡ 32 ‡ N14 Mn +2H2O(l)HMnO2 +4H N42 Hg +2H2O(l)HHgO2 +4H 3‡ 2‡ ‡ 2‡ ‡ ‡ N15 Fe +H2O(l)HFeOH +H N43 Pb +H2O(l)HPbOH +H 3‡ ‡ ‡ 2‡ ‡ N16 Fe +H2O(l)HFeO +2H N44 Pb +H2O(l)HPbO(aq)+2H 3‡ ‡ 2‡ 3 ‡ N17 Fe +2H2O(l)HHFeO2(aq)+3H N45 Pb +2H2O(l)HHPbO2 +3H 3‡ 3 ‡ 2‡ ‡ ‡ N18 Fe +2H2O(l)HFeO2 +4H N46 UO2 +H2O(l)HUO2OH +H 2‡ ‡ ‡ 2‡ ‡ N19 Fe +H2O(l)HFeOH +H N47 UO2 +H2O(l)HUO3(aq)+2H 2‡ ‡ 2‡ 3 ‡ N20 Fe +H2O(l)HFeO(aq)+2H N48 UO2 +2H2O(l)HHUO4 +3H 2‡ 3 ‡ 2‡ 23 ‡ N21 Fe +2H2O(l)HHFeO2 +3H N49 UO2 +2H2O(l)HUO4 +4H 3‡ 2‡ ‡ ‡ ‡ N22 Co +H2O(l)HCoOH +H N50 UO2 +H2O(l)HUO2OH(aq)+H 2‡ ‡ ‡ ‡ 3 ‡ N23 Co +H2O(l)HCoOH +H N51 UO2 +H2O(l)HUO3 +2H 2‡ ‡ 4‡ 3 ‡ N24 Co +H2O(l)HCoO(aq)+2H N52 U +3H2O(l)HHUO3 +5H 2‡ 3 ‡ 4‡ 2‡ ‡ N25 Co +2H2O(l)HHCoO2 +3H N53 U +H2O(l)HUO +2H 2‡ 23 ‡ 4‡ ‡ ‡ N26 Co +2H2O(l)HCoO2 +4H N54 U +2H2O(l)HHUO2 +3H 2‡ ‡ ‡ 4‡ ‡ N27 Ni +H2O(l)HNiOH +H N55 U +2H2O(l)HUO2(aq)+4H 2‡ ‡ N28 Ni +H2O(l)HNiO(aq)+2H

[211] Tasaki, M., Kamagata, Y., Nakamura, K. and Mikami, E. (1991) extremely thermophilic eubacterium belonging to the `Thermoto- Isolation and characterization of a thermophilic benzoate-degrad- gales'. Arch. Microbiol. 154, 105^111. ing, sulfate-reducing bacterium, Desulfotomaculum thermobenzoicum [219] Patel, B.K.C., Morgan, H.W. and Daniel, R.M. (1985) Fervidobac- sp. nov. Arch. Microbiol. 155, 348^352. terium nodosum gen. nov. and spec. nov., a new chemoorganotro- [212] Fardeau, M.-L., Ollivier, B., Patel, B.K.C., Dwivedi, P., Ragot, M. phic, caldoactive, anaerobic bacterium. Arch. Microbiol. 141, 63^69. and Garcia, J.-L. (1995) Isolation and characterization of a thermo- [220] Friedrich, A.B. and Antranikian, G. (1996) Keratin degradation by philic sulfate-reducing bacterium, Desulfotomaculum thermosapovo- Fervidobacterium pennavorans, a novel thermophilic anaerobic spe- rans sp. nov. Int. J. Syst. Bacteriol. 45, 218^221. cies of the order Thermotogales. Appl. Environ. Microbiol. 62, [213] Bonch-Osmolovskaya, E.A., Sokolova, T.G., Kostrikina, N.A. and 2875^2882. Zavarzin, G.A. (1990) Desulfurella acetivorans gen. nov. and sp. [221] Fiala, G., Woese, C.R., Langworthy, T.A. and Stetter, K.O. (1990) nov. ^ a new thermophilic sulfur reducing eubacterium. Arch. Mi- Flexistipes sinusarabici, a novel genus and species of eubacteria oc- crobiol. 153, 151^155. curring in the Atlantis II Deep brines of the Red Sea. Arch. Micro- [214] Miroshnichenko, M.L., Rainey, F.A., Hippe, H., Chernyh, N.A., biol. 154, 120^126. Kostrikina, N.A. and Bonch-Osmolovskaya, E.A. (1998) Desulfu- [222] Davey, M.E., Wood, W.A., Key, R., Nakamura, K. and Stahl, D.A. rella kamchatkensis sp. nov. and Desulfurella propionica sp. nov., (1993) Isolation of three species of Geotoga and Petrotoga: two new new sulfur-respiring thermophilic bacteria from Kamchatka thermal genera, representing a new lineage in the bacterial line of descent environments. Int. J. Syst. Bacteriol. 48, 475^479. distantly related to the `Thermotogales'. Syst. Appl. Microbiol. 16, [215] Miroshnichenko, M.L., Gongadze, G.A., Lysenko, A.M. and 191^200. Bonch-Osmolovskaya, E.A. (1994) Desulfurella multipotens sp. [223] Cayol, J.-L., Ollivier, B., Patel, B.K.C., Prensier, G., Guezennec, J. nov., a new sulfur-respiring thermophilic eubacterium from Raoul and Garcia, J.-L. (1994) Isolation and characterization of Halother- Island (Kermadec archipelago, New Zealand). Arch. Microbiol. 161, mothrix orenii gen. nov., sp. nov., a halophilic, thermophilic, fer- 88^93. mentative, strictly anaerobic bacterium. Int. J. Syst. Bacteriol. 44, [216] L'Haridon, S., Cilia, V., Messner, P., Raguenes, G., Gambacorta, 534^540. A., Sleytr, U.B., Prieur, D. and Jeanthon, C. (1998) Desulfurobacte- [224] Shima, S. and Suzuki, K.-I. (1993) Hydrogenobacter acidophilus sp. rium thermolithotrophum gen. nov. sp. nov., a novel autotrophic nov., a thermoacidophilic, aerobic, hydrogen-oxidizing bacterium sulphur-reducing bacterium isolated from a deep-sea hydrothermal requiring elemental sulfur for growth. Int. J. Syst. Bacteriol. 43, vent. Int. J. Syst. Bacteriol. 48, 701^711. 703^708. [217] Svetlichnii, V.A. and Svetlichnaya, T.P. (1988) Dictyoglomus tur- [225] Nishihara, H., Igarashi, Y. and Kodama, T. (1990) A new isolate of gidus sp. nov., a new extreme thermophilic eubacterium isolated Hydrogenobacter, an obligately chemolithoautotrophic, thermo- from hot springs in the Uzon volcano crater. Mikrobiologiya (in philic, halophilic and aerobic hydrogen-oxidizing bacterium from Russian) 57, 435^441. seaside saline hot spring. Arch. Microbiol. 153, 294^298. [218] Huber, R., Woese, C.R., Langworthy, T.A., Kristjansson, J. and [226] Kawasumi, T., Igarashi, Y., Kodama, T. and Minoda, Y. (1984) Stetter, K.O. (1990) Fervidobacterium islandicum sp. nov., a new Hydrogenobacter thermophilus gen. nov., sp. nov., an extremely ther-

FEMSRE 711 7-3-01 236 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

Table A.18 0 31 Values of vGr (kJ mol )atPSAT as a function of temperature for the reactions given in Table A.17 Reaction T (³C) 218253745557085100115150200 N1 66.32 66.59 66.68 66.81 66.88 66.95 67.04 67.10 67.14 67.17 67.16 66.96 N2 73.62 73.36 73.25 73.09 72.99 72.87 72.71 72.58 72.45 72.35 72.13 71.82 N3 32.01 32.10 32.17 32.31 32.42 32.59 32.89 33.23 33.62 34.05 35.18 37.03 N4 17.78 19.44 20.08 21.10 21.73 22.46 23.44 24.31 25.08 25.76 27.01 28.11 N5 15.72 13.74 12.92 11.56 10.69 9.64 8.14 6.72 5.36 4.06 1.22 32.51 N6 36.89 37.12 37.19 37.28 37.31 37.35 37.36 37.35 37.30 37.22 36.92 36.18 N7 160.05 157.47 156.38 154.56 153.39 151.96 149.89 147.91 146.02 144.20 140.21 135.07 N8 107.80 104.29 102.82 100.38 98.81 96.90 94.14 91.49 88.94 86.47 80.95 73.38 N9 58.55 56.18 55.18 53.50 52.40 51.06 49.11 47.20 45.35 43.53 39.38 33.51 N10 24.23 23.37 22.96 22.23 21.73 21.07 20.07 19.03 17.96 16.85 14.14 9.90 N11 60.61 60.61 60.62 60.63 60.65 60.68 60.74 60.82 60.92 61.03 61.31 61.72 N12 126.54 126.65 126.72 126.90 127.05 127.26 127.63 128.06 128.54 129.06 130.40 132.46 N13 196.24 197.88 198.64 200.00 200.94 202.16 204.07 206.09 208.20 210.41 215.91 224.65 N14 272.93 274.71 275.63 277.35 278.61 280.29 283.04 286.02 289.25 292.71 301.67 316.70 N15 14.94 13.30 12.59 11.38 10.58 9.60 8.14 6.71 5.29 3.89 0.64 34.02 N16 36.15 33.40 32.25 30.36 29.15 27.69 25.59 23.59 21.66 19.82 15.73 10.21 N17 74.27 70.25 68.60 65.92 64.23 62.21 59.37 56.72 54.25 51.94 47.04 40.95 N18 127.89 124.71 123.41 121.30 119.97 118.38 116.16 114.10 112.19 110.44 106.83 102.74 N19 53.01 53.13 53.17 53.24 53.28 53.33 53.40 53.47 53.54 53.61 53.74 53.82 N20 116.37 116.44 116.47 116.55 116.62 116.72 116.88 117.07 117.28 117.50 118.04 118.73 N21 164.50 166.04 166.72 167.88 168.67 169.67 171.20 172.77 174.38 176.04 180.10 186.38 N22 9.79 7.90 7.06 5.63 4.68 3.49 1.71 30.08 31.85 33.63 37.82 313.95 N23 57.12 57.17 57.17 57.14 57.11 57.06 56.97 56.86 56.73 56.58 56.16 55.32 N24 106.77 107.26 107.48 107.86 108.12 108.46 108.98 109.51 110.05 110.60 111.86 113.51 N25 176.70 178.87 179.81 181.41 182.48 183.81 185.81 187.84 189.88 191.95 196.90 204.32 N26 260.80 263.20 264.33 266.35 267.76 269.60 272.48 275.52 278.73 282.09 290.58 304.38 N27 61.17 61.54 61.66 61.84 61.93 62.02 62.13 62.19 62.22 62.20 62.04 61.44 N28 121.93 119.33 118.19 116.22 114.91 113.27 110.80 108.34 105.86 103.37 97.50 88.83 N29 173.13 175.83 176.97 178.89 180.15 181.70 184.02 186.31 188.60 190.88 196.21 203.99 N30 247.53 250.16 251.36 253.48 254.95 256.83 259.75 262.79 265.96 269.26 277.50 290.71 N31 45.27 45.25 45.24 45.22 45.21 45.20 45.20 45.20 45.22 45.24 45.30 45.37 N32 84.06 84.40 84.57 84.88 85.12 85.42 85.92 86.47 87.06 87.68 89.28 91.82 N33 156.60 157.05 157.32 157.88 158.31 158.91 159.95 161.12 162.43 163.86 167.62 173.89 N34 233.55 235.45 236.40 238.16 239.42 241.09 243.79 246.71 249.84 253.18 261.78 276.12 N35 47.12 45.48 44.76 43.53 42.72 41.71 40.21 38.72 37.25 35.79 32.38 27.48 N36 103.18 102.6 102.37 102.02 101.81 101.57 101.26 101.01 100.8 100.63 100.34 100.05 N37 156.18 157.71 158.39 159.57 160.37 161.39 162.95 164.58 166.26 167.99 172.27 178.97 N38 226.95 229.95 231.32 233.73 235.40 237.53 240.83 244.27 247.86 251.58 260.84 275.63 N39 20.07 19.61 19.36 18.90 18.57 18.14 17.44 16.70 15.91 15.09 13.00 9.61 N40 35.46 35.28 35.26 35.30 35.37 35.50 35.79 36.17 36.65 37.20 38.74 41.39 N41 118.68 119.93 120.57 121.76 122.62 123.78 125.66 127.70 129.90 132.25 138.30 148.26 N42 118.68 119.93 120.57 121.76 122.62 123.78 125.66 127.70 129.90 132.25 138.30 148.26 N43 32.47 34.45 35.35 36.92 38.00 39.38 41.49 43.68 45.92 48.20 53.74 62.04 N44 96.73 96.48 96.43 96.42 96.47 96.57 96.81 97.17 97.60 98.13 99.63 102.27 N45 157.85 158.81 159.35 160.43 161.24 162.35 164.22 166.30 168.59 171.07 177.57 188.49 N46 30.92 30.11 29.78 29.25 28.93 28.54 28.01 27.53 27.08 26.68 25.84 24.81 N47 58.39 58.69 58.86 59.20 59.45 59.79 60.35 60.97 61.63 62.34 64.09 66.68 N48 107.04 108.98 109.86 111.39 112.44 113.78 115.85 117.98 120.19 122.47 128.04 136.70 N49 185.32 187.46 188.51 190.46 191.85 193.68 196.61 199.76 203.11 206.67 215.77 230.79 N50 101.17 102.94 103.67 104.88 105.66 106.61 107.98 109.31 110.59 111.83 114.55 118.02 N51 205.31 207.38 208.27 209.78 210.78 212.02 213.87 215.72 217.57 219.44 223.88 230.56 N52 95.31 94.85 94.61 94.19 93.90 93.52 92.96 92.40 91.83 91.27 89.93 87.95 N53 16.38 12.92 11.45 9.01 7.42 5.48 2.64 30.11 32.79 35.41 311.36 319.63 N54 33.96 30.17 28.56 25.84 24.07 21.89 18.69 15.57 12.52 9.52 2.66 37.07 N55 29.97 27.23 26.05 24.05 22.73 21.11 18.72 16.37 14.04 11.73 6.31 31.77

mophilic, aerobic, hydrogen-oxidizing bacterium. Int. J. Syst. Bac- teria, similar to Hydrogenobacter thermophilus, from Icelandic hot teriol. 34, 5^10. springs. Arch. Microbiol. 140, 321^325. [227] Kristjansson, J.K., Ingason, A. and Alfredsson, G.A. (1985) Isola- [228] Hayashi, N.R., ishida, T., Yokota, A., Kodama, T. and Igarashi, Y. tion of thermophilic obligately autotrophic hydrogen-oxidizing bac- (1999) Hydrogenophilus thermoluteolus gen. nov. sp. nov. a thermo-

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 237

Table A.19 philic, halophilic bacterium from submarine hot springs in Iceland. Chemical formulas for the minerals mentioned in Tables 9.1, 9.2, 9.5 J. Gen. Microbiol., 299^306. and A.11 [239] Sako, Y., Takai, K., Ishida, Y., Uchida, A. and Katayama, Y. (1996) Rhodothermus obamensis sp. nov., a modern lineage of ex- Mineral Formula tremely thermophilic marine bacteria. Int. J. Syst. Bacteriol. 46, Magnesite MgCO3 1099^1104. Calcite CaCO3 [240] Carreto, L., Moore, E., Nobre, M.F., Wait, R., Riley, P.W., Sharp, Dolomite CaMg(CO3)2 R.J. and Da Costa, M.S. (1996) Rubrobacter xylanophilus sp. nov., a Alabandite MnS new thermophilic species isolated from a thermally polluted e¥uent. Rhodochrosite MnCO3 Int. J. Syst. Bacteriol. 46, 460^465. Hematite Fe2O3 [241] Suzuki, K., Collins, M.D., Iijima, E. and Komagata, K. (1988) Magnetite Fe3O4 Chemotaxonomic characterization of a radiotolerant bacterium, Ar- Pyrrhotite FeS throbacter radiotolerans: Description of Rubrobacter radiotolerans Siderite FeCO3 gen. nov., comb. nov. FEMS Microbiol. Let. 52, 33^40. Pyrite FeS2 [242] Demharter, W., Hensel, R., Smida, J. and Stackebrandt, E. (1989) Chalcopyrite CuFeS2 Sphaerobacter thermophilus gen. nov., sp. nov. A deeply rooting Covellite CuS member of the actinomycetes subdivision isolated from thermophili- Chalcocite Cu2S cally treated sewage sludge. Syst. Appl. Microbiol. 11, 261^266. Cuprite Cu2O [243] Pohlschroeder, M., Leschine, S.B. and Canale-Parola, E. (1994) Spi- Bornite Cu5FeS4 rochaeta caldaria sp. nov., a thermophilic bacterium that enhances Sphalerite ZnS degradation by Clostridium thermocellum. Arch. Microbiol. Molybdenite MoS2 161, 17^24. Quicksilver Hg [244] Aksenova, H.Y., Rainey, F.A., Janssen, P.H. and Zavarzin, G.A. Galena PbS (1992) Spriochaeta thermophila sp. nov., an obligately anaerobic, Anglesite PbSO4 polysaccharolytic, extremely thermophilic bacterium. Int. J. Syst. Uraninite UO2 Bacteriol. 42, 175^177. [245] Norris, P.R., Clark, D.A., Owen, J.P. and Waterhouse, S. (1996) Characteristics of Sulfobacillus acidophilus sp. nov. and other mod- philic, facultatively chemolithoautotrophic, hydrogen-oxidizing bac- erately thermophilic mineral-sulphide-oxidizing bacteria. Microbiol- terium. Int. J. Syst. Bacteriol. 49, 783^786. ogy 142, 775^783. [229] Goto, E., Kodama, T. and Minoda, Y. (1978) Growth and taxon- [246] Golovacheva, R.S. and Karavaiko, G.I. (1978) A new genus of omy of thermophilic hydrogen bacteria. Agric. Biol. Chem. 42, thermophilic spore-forming bacteria, Sulfobacillus. Mikrobiologiya 1305^1308. (in Russian) 47, 815^822. [230] Giovannoni, S.J., Schabtach, E. and Castenholz, R.W. (1987) Iso- [247] Golovacheva, R.S. (1979) Attachment of Sulfobacillus thermosul¢- sphaera pallida, gen. and comb. nov., a gliding, budding eubacte- dooxidans cells to the surface of sul¢de minerals. Mikrobiologiya (in rium from hot springs. Arch. Microbiol. 147, 276^284. Russian) 48, 528^533. [231] Chung, A.P., Rainey, F., Nobre, M.F., Burghardt, J. and Da Costa, [248] Takai, K., Inoue, A. and Hirokoshi, K. (1999) Thermaerobacter M.S. (1997) Miothermus cerbereus sp. nov., a new slightly thermo- marianensis gen. nov., sp. nov., an aerobic extremely thermophilic philic species with high levels of 3-hydroxy fatty acids. Int. J. Syst. marine bacterium from the 11 000 m deep Mariana trench. Int. J. Bacteriol. 47, 1225^1230. Syst. Bacteriol. 49, 619^628. [232] Nobre, M.F., Truper, H.G. and Da Costa, M.S. (1996) Transfer of [249] Ben-Bassat, A. and Zeikus, J.G. (1981) Thermobacteroides aceto- Thermus ruber (Loginova et al., 1984), Thermus silvanus (Tenreiro et ethylicus gen. nov. and spec. nov., a new chemoorganotrophic, an- al., 1995), and Thermus chliarophilus (Tenreiro et al., 1995) to Mio- aerobic, thermophilic bacterium. Arch. Microbiol. 128, 365^370. thermus gen. nov. as Miothermus ruber comb. nov., Miothermus [250] Cayol, J.-L., Ollivier, B., Patel, B.K.C., Ravot, G., Magot, M., silvanus comb. nov. and Miothermus chliarophilus com. nov., respec- Ageron, E., Grimont, P.A.D. and Garcia, J.-L. (1995) Description tively and emendation of the genus Thermus. Int. J. Syst. Bacteriol. of Thermoanaerobacter brockii subsp. lactiethylicus subsp. nov., iso- 46, 604^606. lated from a deep subsurface French oil well, a proposal to reclassify [233] Malashenko, Y.R., Romanovskaya, V.A., Bogachenko, V.N. and Thermoanaerobacter ¢nnii as Thermoanaerobacter brockii subsp. ¢n- Shved, A.D. (1975) Thermophilic and thermotolerant methane-as- nii comb. nov., and an emended description of Thermoanaerobacter similating bacteria. Mikrobiolgiya (in Russian) 44, 855^862. brockii. Int. J. Syst. Bacteriol. 45, 783^789. [234] Slobodkin, A., Reysenbach, A.-L., Mayer, F. and Wiegel, J. (1997) [251] Zeikus, J.G., Hegge, P.W. and Anderson, M.A. (1979) Thermo- Isolation and characterization of the homoacetogenic thermophilic anaerobium brockii gen. nov. and sp. nov., a new chemoorganotro- bacterium Moorella glycerini sp. nov. Int. J. Syst. Bacteriol. 47, 969^ phic, caldoactive anaerobic bacterium. Arch. Microbiol. 122, 41^48. 974. [252] Lee, Y.-E., Jain, M.K., Lee, C., Lowe, S.E. and Zeikus, G. (1993) [235] Fontaine, F.E., Peterson, W.H., McCoy, E., Johnson, M.J. and Taxonomic distinction of saccharolytic thermophilic anaerobes: de- Ritter, G.J. (1942) A new type of glucose fermentation by Clostri- scription of Thermoanaerobacterium xylanolyticum gen. nov., sp. dium thermoaceticum nov. sp. J. Bacteriol. 43, 701^715. nov., and Thermoanaerobacterium saccharolyticum gen. nov., sp. [236] Collins, M.D., Lawson, P.A., Willems, A., Cordoba, J.J., Fernan- nov.; reclassi¢cation of Thermoanaerobium brockii, Clostridium ther- dez-Garayzabal, J., Garcia, P., Cai, J., Hippe, H. and Farrow, mosulfurogenes, and Clostridium thermohydrosulfuricum E100-69 as J.A.E. (1994) The phylogeny of the genus Clostridium: Proposal Thermoanaerobacter brockii comb. nov., Thermoanaerobacterium of ¢ve new genera and eleven new species combinations. Int. J. thermosulfurigenes com. nov., and Thermoanaerobacter thermohydro- Syst. Bacteriol. 44, 812^826. sulfuricus comb. nov., respectively; and transfer of Clostridium ther- [237] Lien, T., Madsen, M., Rainey, F.A. and Birkeland, N.-K. (1998) mohydrosulfuricum 39E to Thermoanaerobacter ethanolicus. Int. J. Petrotoga mobilis sp. nov., from a North Sea oil-production well. Syst. Bacteriol. 43, 41^51. Int. J. Syst. Bacteriol. 48, 1007^1013. [253] Wiegel, J. and Ljungdahl, L.G. (1981) Thermoanaerobacter ethano- [238] Alfredsson, G.A., Kristjansson, J.K., Hjo«rleifsdottir, S. and Stetter, licus gen. nov., spec. nov., a new, extreme thermophilic, anaerobic K.O. (1988) Rhodothermus marinus, gen. nov., sp. nov., a thermo- bacterium. Arch. Microbiol. 128, 343^348.

FEMSRE 711 7-3-01 238 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

[254] Leigh, J.A., Mayer, F. and Wolfe, R.S. (1981) Acetogenium kivui,a and sp. nov., a bacterium obligate for thermophily and n-alkane new thermophilic hydrogen-oxidizing, acetogenic bacterium. Arch. substrates. Arch. Microbiol. 137, 286^290. Microbiol. 129, 275^280. [271] Jackson, T.J., Ramaley, R.F. and Meinschein, W.G. (1973) Ther- [255] Larsen, L., Nielsen, P. and Ahring, B.K. (1997) Thermoanaerobacter momicrobium a new genus of extremely thermophilic bacteria. Int. J. mathranii sp. nov., an ethanol-producing, extremely thermophilic Syst. Bacteriol. 23, 28^36. anaerobic bacterium from a hot spring in Iceland. Arch. Microbiol. [272] Tenreiro, S., Nobre, M.F., Rainey, F.A., Miguel, C. and Da Costa, 168, 114^119. M.S. (1997) Thermonema rossianum sp. nov., a new thermophilic [256] Bonch-Osmolovskaya, E.A., Miroshnichenko, M.L., Chernykh, and slightly halophilic species from saline hot springs in Naples, N.A., Kostrikina, N.A., Pikuta, E.V. and Rainey, F.A. (1997) Re- Italy. Int. J. Syst. Bacteriol. 47, 122^126. duction of elemental sulfur by moderately thermophilic organotro- [273] Huber, R., Woese, C.R., Langworthy, T.A., Fricke, H. and Stetter, phic bacteria and the description of Thermoanaerobacter sulfurophi- K.O. (1989) Thermosipho africanus gen. nov., represents a new genus lus sp. nov. Microbiology 66, 483^489. of thermophilic eubacteria within the `Thermotogales'. Syst. Appl. [257] Cook, G.M., Rainey, F.A., Patel, B.K.C. and Morgan, H.W. (1996) Microbiol. 12, 32^37. Characterization of a new obligately anaerobic thermophile, Ther- [274] Svetlitshnyi, V., Rainey, F. and Wiegel, J. (1996) Thermosyntropha moanaerobacter wiegelii sp. nov. Int. J. Syst. Bacteriol. 46, 123^127. lipolytica gen. nov., sp. nov., a lipolytic, anaerobic, alkalitolerant, [258] Liu, S.-Y., Rainey, F.A., Morgan, H.W., Mayer, F. and Wiegel, J. thermophilic bacterium utilizing short- and long-chain fatty acids in (1996) Thermoanaerobacterium aotearoense sp. nov., a slightly acid- syntrophic coculture with a methanogenic archaeum. Int. J. Syst. ophilic, anaerobic thermophile isoltaed from various hot springs in Bacteriol. 46, 1131^1137. New Zealand and emendation of the genus Thermoanerobacterium. [275] Slobodkin, A., Reysenbach, A.-L., Strutz, N., Dreier, M. and Wie- Int. J. Syst. Bacteriol. 46, 388^396. gel, J. (1997) Thermoterrabacterium ferrireducens gen. nov., sp. nov., [259] Itoh, T., Suzuki, K.-i. and Nakase, T. (1998) Thermocladium mo- a thermophilic anaerobic dissimilatory Fe(III)-reducing bacterium destius gen. nov., sp. nov., a new genus of the rod-shaped, extremely from a continental hot spring. Int. J. Syst. Bacteriol. 47, 541^547. thermophilic Crenarchaeote. Int. J. Syst. Bacteriol. 48, 879^887. [276] Odinstova, E.V., Jannasch, H.W., Mamone, J.A. and Langworthy, [260] Engle, M., Li, Y., Rainey, F., DeBlois, S., Mai, V., Reichert, A., T.A. (1996) Thermothrix azorensis sp. nov., an obligately chemo- Mayer, F., Messner, P. and Wiegel, J. (1996) Thermobrachium celere lithoautotrophic, sulfur-oxidizing, thermophilic bacterium. Int. J. gen. nov. sp. nov., a rapidly growing thermophilic, alkalitolerant, Syst. Bacteriol. 46, 422^428. and proteolytic . Int. J. Syst. Bacteriol. 46, 1025^ [277] Caldwell, D.E., Caldwell, S.J. and Laycock, J.P. (1976) Thermothrix 1033. thioparus gen. et sp. nov. a facultatively anaerobic facultative che- [261] Huber, R., Dyba, D., Huber, H., Burggraf, S. and Rachel, R. (1998) molithotroph living at neutral pH and high temperature. Can. J. Sulfur-inhibited Thermosphaera aggregans sp. nov., a new genus of Microbiol. 22, 1509^1517. hyperthermophilic archaea isolated after its prediction from envi- [278] Brannan, D.K. and Caldwell, D.E. (1980) : ronmentally derived 16S rRNA sequences. Int. J. Syst. Bacteriol. growth and metabolism of a newly isolated thermophile capable 48, 31^38. of oxidizing sulfur and sulfur compounds. Appl. Environ. Micro- [262] Korn-Wendisch, F., Rainey, F., Kroppenstedt, R.M., Kempf, A., biol. 40, 211^216. Majazza, A., Kutzner, H.J. and Stackebrandt, E. (1995) Thermo- [279] Ravot, G., Magot, M., Fardeau, M.-L., Patel, B.K.C., Prensier, G., crispum gen. nov., a new genus of the order , and Egan, A., Garcia, J.-L. and Ollivier, B. (1995) Thermotoga el¢i sp. description of Thermocrispum municipale sp. nov. and Thermocris- nov., a novel thermophilic bacterium from an African oil-producing pum agreste sp. nov. Int. J. Syst. Bacteriol. 45, 67^77. well. Int. J. Syst. Bacteriol. 45, 308^314. [263] Zeikus, J.G., Dawson, M.A., Thompson, T.E., Ingvorsen, K. and [280] Fardeau, M.-L., Ollivier, B., Patel, B.K.C., Magot, M., Thomas, P., Hatchikian, E.C. (1983) of volcanic sulphidogen- Rimbault, A., Rocchiccioli, F. and Garcia, J.-L. (1997) Thermotoga esis: isolation and characterization of Thermodesulfobacterium com- hypogea sp. nov., a xylanolytic, thermophilic bacterium from an oil- mune gen. nov. and sp. nov. J. Gen. Microbiol. 129, 1159^1169. producing well. Int. J. Syst. Bacteriol. 47, 1013^1019. [264] Rozanova, E.P. and Khudyakova, A.I. (1974) A new nonspore- [281] Jeanthon, C., Reysenbach, A.-L., L'Haridon, S., Gambacorta, A., forming thermophilic sulfate-reducing organism, Desulfovibrio ther- Pace, N.R., Glenat, P. and Prieur, D. (1995) Thermotoga subterra- mophilus nov. sp. Mikrobiologiya (in Russian) 43, 1069^1075. nea sp. nov., a new thermophilic bacterium isolated from a conti- [265] Rozanova, E.P. and Pivovarova, T.A. (1988) Reclassi¢cation of nental oil reservoir. Arch. Microbiol. 64, 91^97. Desulfovibrio thermophilus (Rozanova, Khudyakova, 1974). Mikro- [282] Windberger, E., Huber, R., Trincone, A., Fricke, H. and Stetter, biologiya (in Russian) 57, 102^106. K.O. (1989) Thermotoga thermarum sp. nov. and Thermotoga nea- [266] Beeder, J., Torsvik, T. and Lien, T. (1995) Thermodesulforhabdus politana occurring in African continental solfataric springs. Arch. norvegicus gen. nov., sp. nov., a novel thermophilic sulfate-reducing Microbiol. 151, 506^512. bacterium from oil ¢eld water. Arch. Microbiol. 164, 331^336. [283] Brock, T.D. and Freeze, H. (1969) gen. nov. and [267] Henry, E.A., Devereux, R., Maki, J.S., Gilmour, C.C., Woese, C.R., sp. nov., a non-sporulating extreme thermophile. J. Bacteriol. 98, Mandelco, L., Schauder, R., Ramsen, C.C. and Mitchell, R. (1994) 289^297. Characterization of a new thermophilic sulfate-reducing bacterium [284] Williams, R.A.D., Smith, K.E., Welch, S.G. and Micallef, J. (1996) Thermodesulfovibrio yellowstonii, gen. nov. and sp. nov. its phyloge- Thermus oshimai sp. nov., isolated from hot springs in Portugal, netic relationship to Thermodesulfobacterium commune and their ori- Iceland, and the Azores, and comment on the concept of a limited gins deep within the bacterial . Arch. Microbiol. 161, 62^69. geopgraphical distribution of Thermus species. Int. J. Syst. Bacteriol. [268] Cayol, J.-L., Ducerf, S., Garcia, J.-L. and Patel, B.K.C. (1998) 46, 403^408. Thermohalobacter berrensis gen. nov., sp. nov., a novel thermophilic [285] Oshima, T. and Imahori, K. (1974) Description of Thermus thermo- strictly halophilic bacterium from a solar saltern. Int. Conf. Ther- philus (Yoshida and Oshima) comb. nov., a nonsporulating thermo- mophiles '98 Prog. Abstr. B-P2. philic bacterium from a Japanese thermal spa. Int. J. Syst. Bacteriol. [269] Zacharova, E.V., Mitrofanova, T.I., Krasilnikova, E.N. and Kon- 24, 102^112. dratieva, E.N. (1993) Thermohydrogenium kirishiense gen. nov. and [286] Egorova, A.A. and Deryugina, Z.P. (1963) The spore-forming ther- sp. nov., a new anaerobic thermophilic bacterium. Arch. Microbiol. mophilic thiobacterium. Mikrobiologiya (in Russian) 32, 439^446. 160, 492^497. [287] Huber, R., Langworthy, T.A., Ko«nig, H., Thomm, M., Woese, [270] Zarilla, K.A. and Perry, J.J. (1984) Thermophilum album gen. nov. C.R., Sleytr, U.B. and Stetter, K.O. (1986) Thermotoga maritima

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 239

sp. nov. represents a new genus of unique extremely thermophilic [305] Zhulina, T.N. and Zavarzin, G.A. (1987) Methanohalobium evesti- eubacteria growing up to 90³C. Arch. Microbiol. 144, 324^333. gatus nov. gen., nov. sp., an extreme halophilic methane-forming [288] Jannasch, H.W., Huber, R., Belkin, S. and Stetter, K.O. (1988) archaebacterium. Doklady Akad. Nauk SSSR (in Russian) 293, Thermotoga neapolitana sp. nov. of the extremely thermophilic, eu- 464^468. bacterial genus Thermotoga. Arch. Microbiol. 150, 103^104. [306] Zeikus, J.G. and Wolfe, R.S. (1972) Methanobacterium thermoauto- [289] Fuchs, T., Huber, H., Burggraf, S. and Stetter, K.O. (1996) 16S trophicus sp. nov., an anaerobic, autotrophic, extreme thermophile. rDNA-based phylogeny of the Archaeal order and re- J. Bacteriol. 109, 707^713. classi¢cation of Desulfurolobus ambivalens as Acidianus ambivalens [307] Winter, J., Lerp, C., Zabel, H.-P., Wildenauer, F.X., Ko«nig, H. and comb. nov. Syst. Appl. Microbiol. 19, 56^60. Schindler, F. (1984) Methanobacterium wolfei, sp. nov., a new tung- [290] Zillig, W., Yeats, S., Holz, I., Bock, A., Gropp, F., Rettenberger, sten-requiring, thermophilic, autotrophic methanogen. Syst. Appl. M. and Lutz, S. (1985) -related anaerobic autotrophy of the Microbiol. 5, 457^466. novel archaebacterium Sulfolobus ambivalens. Nature 313, 789^791. [308] Kamagata, Y., Kawasaki, H., Oyzizu, H., Nakamura, K., Mikami, [291] Zillig, W., Yeats, S., Holz, I., Bock, A., Rettenberger, M., Gropp, E., Endo, G., Koga, Y. and Yamasato, K. (1992) Characterization F. and Simon, G. (1986) Desulfurolobus ambivalens, gen. nov., sp. of three thermophilic strains of Methanothrix (`Methanosaeta') ther- nov., an autotrophic archaebacterium facultatively oxidizing or re- mophila sp. nov. and rejection of Methanothrix (`Methanosaeta') ducing sulfur. Syst. Appl. Microbiol. 8, 197^203. thermoacetophila. Int. J. Syst. Bacteriol. 42, 463^468. [292] Segerer, A., Neuner, A., Kristjansson, J. and Stetter, K.O. (1986) [309] Takai, K., Sugai, A., Itoh, T. and Horikoshi, K. (2000) Palaeococ- Acidianus infernus gen. nov., sp. nov., and Acidianus brierleyi comb. cus ferrophilus gen. nov., sp. nov., a barophilic, hyperthermophilic nov. facultatively aerobic, extremely acidophilic thermophilic sulfur- archaeon from a deep-sea hydrothermal vent chimney. Int. J. Syst. metabolizing archaebacteria. Int. J. Syst. Bacteriol. 36, 559^564. Evol. Microbiol. 50, 489^500. [293] Huber, G., Drobner, E., Huber, H. and Stetter, K.O. (1992) Growth [310] Schleper, C., Puehler, G., Holz, I., Gambacorta, A., Janekovic, D., by aerobic oxidation of molecular hydrogen in Archaea ^ a meta- Santarius, U., Klenk, H.-P. and Zillig, W. (1995) Picrophilus gen. bolic property so far unknown for this domain. Syst. Appl. Micro- nov., fam. nov. a novel aerobic, heterotrophic, thermoacidophilic biol. 15, 502^504. genus and family comprising archaea capable of growth around [294] Brierley, C.L. and Brierley, J.A. (1973) A chemoautotrophic and pH 0. J. Bacteriol. 177, 7050^7059. thermophilic microorganism isolated from an acid hot spring. [311] Schleper, C., Puhler, G., Klenk, H.-P. and Zillig, W. (1996) Picro- Can. J. Microbiol. 19, 183^188. philus oshimae and Picrophilus torridus fam. nov., gen. nov., sp. [295] Huber, H., Jannasch, H., Rachel, R., Fuchs, T. and Stetter, K.O. nov., two species of hyperacidophilic, thermophilic, heterotrophic, (1997) Archaeoglobus vene¢cus sp. nov., a novel facultative chemo- aerobic archaea. Int. J. Syst. Bacteriol. 46, 814^816. lithoautotrophic hyperthermophilic sul¢te reducer, isolated from [312] Segerer, A.H., Trincone, A., Gahrtz, M. and Stetter, K.O. (1991) abyssal black smokers. Syst. Appl. Microbiol. 20, 374^380. Stygiolobus azoricus gen. nov., sp. nov. represents a novel genus of [296] Fuchs, T., Huber, H., Teiner, K., Burggraf, S. and Stetter, K.O. anaerobic, extremely thermoacidophilic archaebacteria of the order (1995) Metallosphaera prunae, sp. nov., a novel metal-mobilizing, Sulfolobales. Int. J. Syst. Bacteriol. 41, 495^501. thermoacidophilic archaeum, isolated from a uranium mine in Ger- [313] Brock, T.D., Brock, K.M., Belly, R.T. and Weiss, R.L. (1972) Sul- many. Syst. Appl. Microbiol. 18, 560^566. folobus: a new genus of sulfur-oxidizing bacteria living at low pH [297] Huber, G., Spinnler, C., Gambacorta, A. and Stetter, K.O. (1989) and high temperature. Arch. Microbiol. 84, 54^68. Metallosphaera sedula gen. and sp. nov. represents a new genus of [314] Segerer, A., Stetter, K.O. and Klink, F. (1985) Two contrary modes aerobic, metal-mobilizing, thermoacidophilic archaebacteria. Syst. of chemolithotrophy in the same archaebacterium. Nature 313, 787^ Appl. Microbiol. 12, 38^47. 789. [298] Kotelnikova, S.V., Obraztsova, A.Y., Gongadze, G.M. and Lauri- [315] Brock, T.D., Cook, S., Petersen, S. and Mosser, J.L. (1976) Biogeo- navichius, K.S. (1993) Methanobacterium thermo£exum sp. nov. and chemistry and bacteriology of ferrous iron oxidation in geothermal Methanobacterium de£uvii sp. nov., thermophilic rod-shaped meth- habitats. Geochim. Cosmochim. Acta 40, 493^500. anogens isolated from anaerobic digestor sludge. Syst. Appl. Micro- [316] Takayanagi, S., Kawasaki, H., Sugimori, K., Yamada, T., Sugai, biol. 16, 427^435. A., Ito, T., Yamasato, K. and Shioda, M. (1996) Sulfolobus hako- [299] Blotevogel, K.-H. and Fischer, U. (1985) Isolation and character- nensis sp. nov., a novel species of acidothermophilic archaeon. Int. J. ization of a new thermophilic and autotrophic methane producing Syst. Bacteriol. 46, 377^382. bacterium: Methanobacterium thermoaggregans spec. nov. Arch. Mi- [317] Huber, G. and Stetter, K.O. (1991) Sulfolobus metallicus, sp. nov., a crobiol. 142, 218^222. novel strictly chemolithoautotroph thermophilic archaeal species of [300] Blotevogel, K.-H., Fischer, U., Mocha, M. and Jannsen, S. (1985) metal-mobilizers. Syst. Appl. Microbiol. 14, 372^378. Methanobacterium thermoalcaliphilum spec. nov., a new moderately [318] Grogan, D., Palm, P. and Zillig, W. (1990) Isolate B12, which har- alkaliphilic and thermophilic autotrophic methanogen. Arch. Micro- bors a -like element, represents a new species of the archaebac- biol. 142, 211^217. terial genus Sulfolobus, Sulfolobus shibatae, sp. nov. Arch. Micro- [301] Laurinavichyus, K.S., Kotel'nikova, S.V. and Obraztsova, A.Y. biol. 154, 594^599. (1988) New species of thermophilic methane-producing bacteria. [319] Grogan, D.W. (1989) Phenotypic characterization of the archaebac- Mikrobiologiya (in Russian) 57, 1035^1041. terial genus Sulfolobus: comparison of ¢ve wild-type strains. J. Bac- [302] Huber, H., Thomm, M., Ko«nig, H., Thies, G. and Stetter, K.O. teriol. 171, 6710^6719. (1982) Methanococcus thermolithotrophicus, a novel thermophilic [320] Zillig, W., Stetter, K.O., Wunderl, S., Schulz, W., Priess, H. and lithotrophic methanogen. Arch. Microbiol. 132, 47^50. Scholz, I. (1980) The Sulfolobus ^ `Caldariella' group: taxonomy on [303] Jeanthon, C., L'Haridon, S., Reysenbach, A.L., Corre, E., Vernet, the basis of the structure of DNA-dependent RNA . M., Messner, P., Sleytr, U.B. and Prieur, D. (1999) Methanococcus Arch. Microbiol. 125, 259^269. vulcanius sp. nov., a novel hyperthermophilic methanogen isolated [321] Golovacheva, R.S., Val'ekho-Roman, K.M. and Troitskii, A.V. from East Paci¢c Rise, and identi¢cation of Methanococcus sp. (1987) Sulfurococcus mirabilis gen. nov., sp. nov., a new thermo- DSM 4213T as Methanococcus fervens sp. nov. Int. J. Syst. Bacter- philic archaebacterium with the ability to oxidize sulfur. Mikrobio- iol. 49, 583^589. logiya (in Russian) 56, 100^107. [304] Boone, D.R., Whitman, W.B. and Rouviere, P., (1993) in: Metha- [322] Karavaiko, G.I., Golyshina, O.V., Troitskii, A.V., Valieho-Roman, nogenesis ^ Ecology, Physiology, Biochemistry and Genetics (Ferry, K.M., Golovacheva, R.S. and Pivovarova, T.A. (1994) Sulfurococ- J.G., Ed.), pp. 35^80. Chapman and Hall, New York. cus yellowstonii sp. nov., a new species of iron and sulfur oxidizing

FEMSRE 711 7-3-01 240 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

thermoacidophilic archaebacteria. Mikrobiologiya (in Russian) 63, [340] Burggraf, S., Fricke, H., Neuner, A., Kristjansson, J., Rouvier, P., 668^682. Mandelco, L., Woese, C.R. and Stetter, K.O. (1990) Methanococcus [323] Ronimus, R.S., Reysenbach, A.-L., Musgrave, D.R. and Morgan, igneus sp. nov., a novel hyperthermophilic methanogen from a shal- H.W. (1997) The phylogenetic position of the Thermococcus isolate low submarine hydrothermal vent. Syst. Appl. Microbiol. 13, 263^ AN1 based on 16S rRNA gene sequence analysis: a proposal that 269. AN1 represents a new species, Thermococcus zilligii sp. nov. Arch. [341] Jeanthon, C., L'Haridon, S., Reysenbach, A.L., Vernet, M., Mess- Microbiol. 168, 245^248. ner, P., Sleytr, U.B. and Prieur, D. (1998) Methanococcus infernus [324] Klages, K.U. and Morgan, H.W. (1994) Characterization of an ex- sp. nov., a novel hyperthermophilic lithotrophic methanogen iso- tremely thermophilic sulphur-metabolizing archaebacterium belong- lated from a deep-sea hydrothermal vent. Int. J. Syst. Bacteriol. ing to the . Arch. Microbiol. 162, 261^266. 48, 913^918. [325] Segerer, A., Langworthy, T.A. and Stetter, K.O. (1988) Thermoplas- [342] Huber, R., Kurr, M., Jannasch, H.W. and Stetter, K.O. (1989) A ma acidophilum and Thermoplasma volcanium sp. nov. from solfa- novel group of abyssal methanogenic archaebacteria (Methanopyrus) tara ¢elds. Syst. Appl. Microbiol. 10, 161^171. growing at 110³C. Nature 342, 833^834. [326] Darland, G., Brock, T.D., Samsono¡, W. and Conti, S.F. (1970) A [343] Stetter, K.O., Thomm, M., Winter, J., Wildgruber, G., Huber, H., thermophilic, acidophilic, mycoplasma isolated from a coal refuse Zillig, W., Janecovic, D., Ko«nig, H., Palm, P. and Wunderl, S. pile. Science 170, 1416^1418. (1981) Methanothermus fervidus, sp. nov., a novel extremely thermo- [327] Sako, Y., Nomura, N., Uchida, A., Ishida, Y., Morii, H., Koga, Y., philic methanogen isolated from an Icelandic hot spring. Zent.bl. Hoaki, T. and Maruyama, T. (1996) Aeropyrum pernix gen. nov., sp. Bakteriol. Mikrobiol. Hyg. 1 Abt. Originale C 2, 166^178. nov., a novel aerobic hyperthermophilic archaeon growing at tem- [344] Lauerer, G., Kristjansson, J.K., Langworthy, T.A., Ko«nig, H. and peratures up to 100³C. Int. J. Syst. Bacteriol. 46, 1070^1077. Stetter, K.O. (1986) Methanothermus sociabilis sp. nov., a second [328] Stetter, K.O., Lauerer, G., Thomm, M. and Neuner, A. (1987) Iso- species within the growing at 97³C. Syst. lation of extremely thermophilic sulfate reducers: evidence for a Appl. Microbiol. 8, 100^105. novel branch of archaebacteria. Science 236, 822^824. [345] Vo«lkl, P., Huber, R., Drobner, E., Rachel, R., Burggraf, S., Trin- [329] Stetter, K.O. (1988) Archaeoglobus fulgidus gen. nov., sp. nov. a new cone, A. and Stetter, K.O. (1993) Pyrobaculum aerophilum sp. nov., taxon of extremely thermophilic archaebacteria. Syst. Appl. Micro- a novel nitrate-reducing hyperthermophilic archaeum. Appl. Envi- biol. 10, 172^173. ron. Microbiol. 1993, 2918^2926. [330] Beeder, J., Nilsen, R.K., Rosnes, J.T., Torsvik, T. and Lien, T. [346] Huber, R., Kristjansson, J.K. and Stetter, K.O. (1987) Pyrobaculum (1994) Archaeoglobus fulgidus isolated from hot North Sea oil ¢eld gen. nov., a new genus of neutrophilic rod-shaped archaebacteria waters. Appl. Environ. Microbiol. 60, 1227^1231. from continental solfataras growing optimally at 100³C. Arch. Mi- [331] Burggraf, S., Jannasch, H.W., Nicolaus, B. and Stetter, K.O. (1990) crobiol. 149, 95^101. Archaeoglobus profundus sp. nov., represents a new species within [347] Erauso, G., Reysenbach, A.-L., Godfroy, A., Muenier, J.-R., the sulfate-reducing archaebacteria. Syst. Appl. Microbiol. 13, 24^ Crump, B., Partensky, F., Baross, J.A., Marteinsson, V., Barbier, 28. G., Pace, N.R. and Prieur, D. (1993) Pyrococcus abyssi sp. nov., a [332] Itoh, T., Suzuki, K.-I., Sanchez, P.C. and Nakase, T. (1999) Caldi- new hyperthermophilic archaeon isolated from a deep-sea hydro- virga maquilingensis gen. nov., sp. nov., a new genus of rod-shaped thermal vent. Arch. Microbiol. 160, 338^349. crenarchaeote isolated from a hot spring in the Philippines. Int. J. [348] Pledger, R.J. and Baross, J.A. (1991) Preliminary description and Syst. Bacteriol. 49, 1157^1163. nutritional characterization of a chemoorganotrophic archaeobacte- [333] Svetlitshnyi, V.A., Slesarev, A.I., Svetlichnaya, T.P. and Zavarzin, rium growing at temperatures of up to 100³C isolated from a sub- G.A. (1987) Caldococcus litoralis gen. nov. sp. nov., a new marine marine hydrothermal vent environment. J. Gen. Microbiol. 137, extremely thermophilic archaebacterium reducing elemental sulfur. 203^211. Mikrobiologiya (in Russian) 56, 831^838. [349] Fiala, G. and Stetter, K.O. (1986) sp. nov. rep- [334] Aoshima, M., Yamagishi, A. and Oshima, T. (1996) Eubacteria-type resents a novel genus of marine heterotrophic archaebacteria grow- from an archaeon: cloning, sequencing, ing optimally at 100³C. Arch. Microbiol. 145, 56^61. and expression of a gene encoding isocitrate dehyrogenase from a [350] Gonzalez, J.M., Masuchi, Y., Robb, F.T., Ammerman, J.W., hyperthermophilic archaebacterium, Caldococcus noboribetus. Arch. Maeder, D.L., Yanagibayashi, M., Tamaoka, J. and Kato, C. Biochem. Biophys. 336, 77^85. (1998) Pyrococcus horikoshii sp. nov., a hyperthermophilic archaeon [335] Aoshima, M. and Oshima, T. (1997) Puri¢cation and characteriza- isolated from a hydrothermal vent at the Okinawa Trough. Extrem- tion of isocitrate dehydrogenase from a hyperthermophilic archae- ophiles 2, 123^130. bacterium, Caldococcus noboribetus. Biochim. Biophys. Acta 1340, [351] Zillig, W., Holz, I., Klenk, H.-P., Trent, J., Wunderl, S., Janekovic, 227^234. D., Imsel, E. and Haas, B. (1987) Pyrococcus woesei, sp. nov., an [336] Bonch-Osmolovskaya, E.A., Slesarev, A.I., Miroshnichenko, M.L., ultra-thermophilic marine archaebacterium, representing a novel or- Svetlichnaya, T.P. and Alekseev, V.A. (1988) Characteristics of De- der, Thermococcales. Syst. Appl. Microbiol. 9, 62^70. sulfurococcus amylolyticus nov. sp. ^ a new extremely thermophilic [352] Pley, U., Schipka, J., Gambacorta, A., Jannasch, H.W., Fricke, H., archaebacterium isolated from thermal springs of Kamchatka and Rachel, R. and Stetter, K.O. (1991) Pyrodictum abyssi sp. nov. rep- Kunashir Island. Mikrobiologiya (in Russian) 57, 94^101. resents a novel heterotrophic marine archaeal hyperthermophile [337] Zillig, W., Stetter, K.O., Prangishvilli, D., Scha«fer, W., Wunderl, S., growing at 110³C. Syst. Appl. Microbiol. 14, 245^253. Janekovic, D., Holz, I. and Palm, P. (1982) , the [353] Stetter, K.O., Ko«nig, H. and Stackebrandt, E. (1983) Pyrodictium second family of extremely thermophilic, anaerobic, sulfur-respiring gen. nov., a new genus of submarine disc-shaped sulphur reducing . Zentralblatt Bakteriol. Mikrobiol. Hyg. 1 Abt. archaebacteria growing optimally at 105³C. Syst. Appl. Microbiol. Originale C 3, 304^317. 4, 535^551. [338] Zillig, W., Holz, I., Janekovic, D., Klenk, H.-P., Imsel, E., Trent, J., [354] Fiala, G., Stetter, K.O., Jannasch, H.W., Langworthy, T.A. and Wunderl, S., Forjaz, V.H., Coutinho, R. and Ferreira, T. (1990) Madon, J. (1986) Staphylothermus marinus sp. nov. represents a Hyperthermus butylicus, a hyperthermophilic sulfur-reducing archae- novel genus of extremely thermophilic submarine heterotrophic bacterium that ferments peptides. J. Bacteriol. 172, 3959^3965. archaebacteria growing up to 98³C. Syst. Appl. Microbiol. 8, 106^ [339] Zhao, H., Wood, A.G., Widdel, F. and Bryant, M.P. (1988) An 113. extremely thermophilic Methanococcus from a deep sea hydrother- [355] Jochimsen, B., Peinemann-Simon, S., Volker, H., Stuben, D., Botz, mal vent and its plasmid. Arch. Microbiol. 150, 178^183. R., Sto¡ers, P., Dando, P.R. and Thomm, M. (1997) Stetteria hy-

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 241

drogenophila, gen. nov. and sp. nov., a novel mixotrophic sulfur- peptonophilus sp. nov., a fast-growing, extremely thermophilic arch- dependent crenarchaeote isolated from Milos, Greece. Extremophiles aebacterium isolated from deep-sea hydrothermal vents. Arch. Mi- 1, 67^73. crobiol. 164, 159^164. [356] Hensel, R., Matussek, K., Michalke, K., Tacke, L., Tindall, B.J., [371] Kobayashi, T., Kwak, Y.S., Akiba, T., Kudo, T. and Horikoshi, K. Kohlho¡, M., Siebers, B. and Dielenschneider, J. (1997) Sulfopho- (1994) Thermococcus profundus sp. nov., a new hyperthermophilic bococcus zilligii gen. nov., spec. nov. a novel hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent. Syst. Appl. Archaeum isolated from hot alkaline springs of Iceland. Syst. Microbiol. 17, 232^236. Appl. Microbiol. 20, 102^110. [372] Grote, R., Li, L., Tamaoka, J., Kato, C., Horikoshi, K. and An- [357] Kurosawa, N., Itoh, Y.H., Iwai, T., Sugai, A., Uda, I., Kimura, N., tranikian, G. (1999) Thermococcus siculi sp. nov., a novel hyper- Horiuchi, T. and Itoh, T. (1998) Sulfurisphaera ohwakuensis gen. thermophilic archaeon isolated from a deep-sea hydrothermal vent nov., sp. nov., a novel extremely thermophilic acidophile of the at the Mid-Okinawa trough. Extremophiles 3, 55^62. order Sulfolobales. Int. J. Syst. Bacteriol. 48, 451^456. [373] Miroshnichenko, M.L., Bonch-Osmolovskaya, E.A., Neuner, A., [358] Dirmeier, R., Keller, M., Hafenbradl, D., Braun, F.-J., Rachel, R., Kostrikina, N.A., Chernych, N.A. and Alekseev, V.A. (1989) Ther- Burggraf, S. and Stetter, K.O. (1998) Thermococcus acidaminovorans mococcus stetteri sp. nov., a new extremely thermophilic marine sp. nov., a new hyperthermophilic alkalophilic archaeon growing on sulfur-metabolizing archaebacterium. Syst. Appl. Microbiol. 12, amino acids. Extremophiles 2, 109^114. 257^262. [359] Canganella, F., Jones, W.J., Gambacorta, A. and Antranikian, G. [374] Stetter, K.O., Fiala, G., Huber, G., Huber, R. and Segerer, A. (1998) Thermococcus guaymasensis sp. nov. and Thermococcus ag- (1990) Hyperthermophilic microorganisms. FEMS Microbiol. Rev. gregans sp. nov., two novel thermophilic archaea isolated from 75, 117^124. Guaymas Basin hydrothermal vent site. Int. J. Syst. Bacteriol. 48, [375] Fischer, F., Zillig, W., Stetter, K.O. and Schreiber, G. (1983) Che- 1181^1185. molithoautotrophic metabolism of anaerobic extremely thermophilic [360] Keller, M., Braun, F.-J., Dirmeier, R., Hafenbradl, D., Burggraf, S., archaebacteria. Nature 301, 511^513. Rachel, R. and Stetter, K.O. (1995) Thermococcus alcaliphilus sp. [376] Zillig, W., Gierl, A., Schreiber, G., Wunderl, S., Janekovic, D., nov., a new hyperthermophilic archaeum growing on polysul¢de at Stetter, K.O. and Klenk, H.P. (1983) The archaebacterium Thermo- alkaline pH. Arch. Microbiol. 164, 390^395. ¢lum pendens represents a novel genus of thermophilic, anaerobic [361] Marteinsson, V.T., Birrien, J.-L., Reysenbach, A.-L., Vernet, M., sulfur respiring Thermoproteales. Syst. Appl. Microbiol. 4, 79^87. Marie, D., Gambacorta, A., Messner, P., Sleytr, U.B. and Prieur, [377] Zillig, W., Stetter, K.O., Scha«fer, W., Janekovic, D., Wunderl, S., D. (1999) Thermococcus barophilus sp. nov., a new barophilic and Holz, I. and Palm, P. (1981) Thermoproteales: a novel type of ex- hyperthermophilic archaeon isolated under high hydrostatic pres- tremely thermoacidophilic anaerobic archaebacteria isolated from sure from a deep-sea hydrothermal vent. Int. J. Syst. Bacteriol. 49, Icelandic solfataras. Zent.bl. Bakteriol. Mikrobiol. Hyg. 1. Abt. 351^359. Originale C 2, 205^227. [362] Du¡aud, G.D., D'Hennezel, O.B., Peek, A.S., Reysenbach, A.-L. [378] Bonch-Osmolovskaya, E.A., Miroshnichenko, M.L., Kostrikina, and Kelly, R.M. (1998) Isolation and characterization of Thermo- N.A., Chernych, N.A. and Zavarzin, G.A. (1990) Thermoproteus coccus barossii, sp. nov., a hyperthermophilic archaeon isolated uzoniensis sp. nov., a new extremely thermophilic archaebacterium from a hydrothermal vent £ange formation. Syst. Appl. Microbiol. from Kamchatka continental hot springs. Arch. Microbiol. 154, 21, 40^49. 556^559. [363] Zillig, W., Holz, I., Janekovic, D., Schafer, W. and Reiter, W.D. [379] The : A Handbook on the Biology of Bacteria: Eco- (1983) The archaebacterium Thermococcus celer represents a novel physiology, Isolation, Identi¢cation, Applications, vol. 1 (Balows genus within the thermophilic branch of the archaebacteria. Syst. A., Truper, H.G., Dworkin, M., Harder, W. and Schleifer, K.-H., Appl. Microbiol. 4, 88^94. Eds.), Springer-Verlag, (1992) New York. [364] Huber, R., Stohr, J., Hohenhaus, S., Rachel, R., Burggraf, S., Jan- [380] Finster, K., Liesack, W. and Tindall, B.J. (1997) Sulfurospirillum nasch, H.W. and Stetter, K.O. (1995) Thermococcus chitonophagus arachanense sp. nov., a new microaerophilic sulfur reducing bacte- sp. nov., a novel, -degrading, hyperthermophilic archaeum rium. Int. J. Syst. Bacteriol. 47, 1212^1217. from a deep-sea hydrothermal vent environment. Arch. Microbiol. [381] Doelle, H.W. (1969) Bacterial Metabolism, Academic Press, New 164, 255^264. York. [365] Godfroy, A., Meunier, J.-R., Guezennec, J., Lesongeur, F., Ra- [382] Plyasunov, A.V., O'Connell, J.P., Wood, R.H. and Shock, E.L. guenes, G., Rimbault, A. and Barbier, G. (1996) Thermococcus fu- (2000) In¢nite dilution partial molar properties of aqueous solutions micolans sp. nov., a new hyperthermophilic archaeon isolated from a on nonelectrolytes. II. Equations for the standard thermodynamic deep-sea hydrothermal vent in the North Fiji Basin. Int. J. Syst. functions of hydration of volatile nonelectrolytes over wide ranges Bacteriol. 46, 1113^1119. of conditions including subcritical temperatures. Geochim. Cosmo- [366] Miroshnichenko, M.L., Gongadze, G.M., Rainey, F.A., Kostyuko- chim. Acta 64, 2779^2795. va, A.S., Lysenko, A.M., Chernyh, N.A. and Bonch-Osmolovskaya, [383] Drozd, J.W. (1976) Energy coupling and respiration in Nitrosomo- E.A. (1998) Thermococcus gorgonarius sp. nov. and Thermococcus nas europea. Arch. Microbiol. 110, 257^262. paci¢cus sp. nov. heterotrophic extremely thermophilic archaea from [384] Suzuki, I., Dular, U. and Kwok, S.C. (1974) Ammonia or ammo- New Zealand submarine hot vents. Int. J. Syst. Bacteriol. 48, 23^29. nium ion as substrate for oxidation by Nitrosomonas europaea cells [367] Godfroy, A., Lesongeur, F., Raguenes, G., Querellou, J., Antoine, and extracts. J. Bacteriol. 120, 556^558. E., Meunier, J.-R., Guezennec, J. and Barbier, G. (1997) Thermo- [385] Tamegai, H., Li, L., Masui, N. and Kato, C. (1997) A denitrifying coccus hydrothermalis sp. nov., a new hyperthermophilic archaeon bacterium from the deep sea at 11000 m depth. Extremophiles 1, isolated from a deep-sea hydrothermal vent. Int. J. Syst. Bacteriol. 207^211. 47, 622^626. [386] Petursdottir, S.K. and Kristjansson, J.K. (1997) Silicibacter lacus- [368] Neuner, A., Jannasch, H.W., Belkin, S. and Stetter, K.O. (1990) caerulensis gen. nov., sp. nov., a mesophilic moderately halophilic Thermococcus litoralis sp. nov. a new species of extremely thermo- bacterium characteristic of the Blue Lagoon geothermal in Ice- philic marine archaebacteria. Arch. Microbiol. 153, 205^207. land. Extremophiles 1, 94^99. [369] Belkin, S. and Jannasch, H.W. (1985) A new extremely thermo- [387] Gottschalk, G. (1986) Bacterial Metabolism, 2nd edn., Springer- philic, sulfur-reducing heterotrophic, marine bacterium. Arch. Mi- Verlag, New York. crobiol. 141, 181^186. [388] Murray, P.A. and Zinder, S.H. (1984) Nitrogen ¢xation by a meth- [370] Gonzalez, J.M., Kato, C. and Horikoshi, K. (1995) Thermococcus anogenic archaebacterium. Nature 312, 284^286.

FEMSRE 711 7-3-01 242 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243

[389] Postgate, J.R. and Kent, H.M. (1985) Diazotrophy within Desulfo- Beggiotoa spp. and Thiovulum spp., in O2 and H2S microgradients. vibrio. J. Gen. Microbiol. 131, 2119^2122. Appl. Environ. Microbiol. 45, 1261^1270. [390] Nazina, T.N., Rozanova, E.P. and Kalininskaya, T.A. (1979) Fix- [410] van den Ende, F.P. and van Gemerden, H. (1993) Sul¢de oxidation ation of molecular nitrogen by sulfate-reducing bacteria from oil under oxygen limitation by a Thiobacillus thioparus isolated from a strata. Mikrobiologiya (in Russian) 48, 133^136. marine microbial mat. FEMS Microbiol. Ecol. 13, 69^78. [391] Bergey's Manual of Systematic Bacteriology, vol. 3 (Holt, J.G., [411] Fossing, H., Gallardo, V.A., Jorgensen, B.B., Huttel, M., Nielsen, Staley, J.T., Bryant, M.P. and Pfennig, N., Eds.), Williams and L.P., Schulz, H., Can¢eld, D.E., Forster, S., Glud, R.N., Gunders- Wilkins, (1989) Baltimore, MD. en, J.K., Kuver, J., Ramsing, N.B., Teske, A., Thamdrup, B. and [392] Olsen, G. (1999) What's eating the free lunch? Nature 400, 403^405. Ulloa, O. (1995) Concentration and transport of nitrate by the mat [393] Newman, D.K., Kennedy, E.K., Coates, J.D., Ahmann, D., Ellis, forming sulphur bacterium Thioploca. Nature 374, 713^715. D.J., Lovley, D.R. and Morel, F.M.M. (1997) Dissimilatory arsen- [412] Ollivier, B., Fardeau, M.-L., Cayol, J.-L., Magot, M., Patel, B.K.C., ate and sulfate reduction in Desulfotomaculum auripigmentum sp. Prensier, G. and Garcia, J.-L. (1998) Methanocalculus halotolerans nov. Arch. Microbiol. 168, 380^388. gen. nov., sp. nov., isolated from an oil-producing well. Int. J. Syst. [394] Pikuta, E.V., Zhilina, T.N., Zavarzin, G.A., Kostrikina, N.A., Osi- Bacteriol. 48, 821^828. pov, G.A. and Rainey, F.A. (1998) Desulfonatronum lacustre gen. [413] Ollivier, B., Cayol, J.-L., Patel, B.K.C., Magot, M., Fardeau, M.-L. nov., sp. nov. a new alkaliphilic sulfate-reducing bacterium utilizing and Garcia, J.-L. (1997) Methanoplanus petrolearius sp. nov., a nov- ethanol. Mikrobiologiya (in Russian) 67, 123^131. el methanogenic bacterium from an oil producing well. FEMS Mi- [395] Zhilina, T.N., Zavarzin, G.A., Rainey, F.A., Pikuta, E.N., Osipov, crobiol. Lett. 147, 51^56. G.A. and Kostrikina, N.A. (1997) Desulfonatronovibrio hydrogeno- [414] Nozhevnikova, A.N. and Chudina, V.I. (1984) Morphology of the vorans gen. nov., sp. nov., an alkaliphilic, sulfate-reducing bacte- thermophilic acetate methane bacterium Methanothrix thermoaceto- rium. Int. J. Syst. Bacteriol. 47, 144^149. phila sp. nov. Mikrobiologiya (in Russian) 53, 756^760. [396] Lien, T., Madsen, M., Steen, I.H. and Gjerdevik, K. (1998) Desul- [415] Zhilina, T.N., Zavarzin, G.A., Detkova, E.N. and Rainey, F.A. fobulbus rhabdoformis sp. nov., a sulfate reducer from a water^oil (1996) Natroniella acetigena gen. nov. sp. nov., an extremely haloal- separation system. Int. J. Syst. Bacteriol. 48, 469^474. kaliphilic, homoacetic bacterium: a new member of Haloanerobiales. [397] Bak, F. and Cypionka, H. (1987) A novel type of energy metabolism Curr. Microbiol. 32, 320^326. involving fermentation of inorganic sulphur compounds. Nature [416] Downey, R.J. (1966) Nitrate reductase and respiratory adaptation in 326, 891^892. Bacillus stearothermophilus. J. Bacteriol. 91, 634^641. [398] Bak, F. and Pfennig, N. (1987) Chemolithotrophic growth of De- [417] Ni, S. and Boone, D.R. (1991) Isolation and characterization of a sulfovibrio sulfodismutans sp. nov. by disproportionation of inor- dimethyl sul¢de-degrading methanogen, Methanolobus siciliae ganic sulfur compounds. Arch. Microbiol. 147, 184^189. HI350, from an oil well, characterization of M. siliae T4/MT, and [399] Finster, K., Liesack, W. and Thamdrup, B. (1998) Elemental sulfur emendation of M. siciliae. Int. J. Syst. Bacteriol. 41, 410^416. and thiosulfate disproportionation by Desulfocapsa sulfoexigens sp. [418] Mathrani, I.M., Boone, D.R., Mah, R.A., Fox, G.E. and Lau, P.P. nov., a new anaerobic bacterium isolated from marine surface sedi- (1988) Methanohalophilus zhilinae sp. nov., an alkaliphilic, halo- ment. Appl. Environ. Microbiol. 64, 119^125. philic, methylotrophic methanogen. Int. J. Syst. Bacteriol. 38, 139^ [400] Janssen, P.H., Schuhmann, A., Bak, F. and Liesack, W. (1996) 142. Disproportionation of inorganic sulfur compounds by sulfate-reduc- [419] Zinder, S.H. (1993) in: Methanogenesis ^ Ecology, Physiology, Bio- ing bacterium Desulfocapsa thiozymogenes gen. nov., sp. nov. Arch. chemistry, and Genetics (Ferry, J. Ed.), Chapman and Hall, New Microbiol. 166, 184^192. York. [401] Durand, P., Reysenbach, A.-L., Prieur, D. and Pace, N. (1993) [420] Widdel, F. (1986) Growth of methanogenic bacteria in pure culture Isolation and characterization of Thiobacillus hydrothermalis sp. with 2-propanol and other alcohols as hydrogen donors. Appl. En- nov., a mesophilic obligately chemolithotrophic bacterium isolated viron. Microbiol. 51, 1056^1062. from a deep-sea hydrothermal vent in Fiji Basin. Arch. Microbiol. [421] Zellner, G. and Winter, J. (1987) Secondary alcohols as hydrogen

159, 39^44. donors for CO2-reduction by methanogenesis. FEMS Microbiol. [402] Jannasch, H.W., Wirsen, C.O., Nelson, D.C. and Robertson, L.A. Lett. 44, 323^328. (1985) Thiomicrospira crunogena sp. nov., a colorless, sulfur-oxidiz- [422] Lovley, D.R. and Phillips, E.J.P. (1988) Novel mode of microbial ing bacterium from a deep-sea hydrothermal vent. Int. J. Syst. Bac- energy metabolism: organic carbon oxidation coupled to dissimila- teriol. 35, 422^424. tory reduction of iron or manganese. Appl. Environ. Microbiol. 54, [403] Brinkho¡, T., Muyzer, G., Wirsen, C. and Kuever, J. (1999) Thio- 1472^1480. microspira chilensis sp. nov., a mesophilic obligately chemolithoau- [423] Lovley, D.R., Giovannoni, S.J., White, D.C., Champine, J.E., Phil- totrophic sulfur-oxidizing bacterium isolated from a Thioploca mat. lips, E.J.P., Gorby, Y.A. and Goodwin, S. (1993) Geobacter metal- Int. J. Syst. Bacteriol. 49, 875^879. lireducens gen. nov. sp. nov., a microorganism capable of coupling [404] Ehrlich, H.L. (1996) Geomicrobiology, 3rd edn., Marcel Dekker, the complete oxidation of organic compounds to the reduction of New York. iron and other metals. Arch. Microbiol. 159, 336^344. [405] Pollock, M.R. and Knox, R. (1943) Bacterial reduction of tetrathi- [424] Oremland, R.S., Blum, J.S., Culbertson, C.W., Visscher, P.T., onate. Biochem. J. 37, 476^481. Miller, L.G., Dowdle, P. and Strohmaier, F.E. (1994) Isolation, [406] Huber, H. and Stetter, K.O. (1989) Thiobacillus prosperus sp. nov., growth and metabolism of an obligately anaerobic selenate-respiring represents a new group of halotolerant metal-mobilizing bacteria bacterium, strain SES-3. Appl. Environ. Microbiol. 60, 3011^ isolated from a marine geothermal ¢eld. Arch. Microbiol. 151, 3019. 479^485. [425] Blum, J.S., Bindi, A.B., Buzzelli, J., Stolz, J.F. and Oremland, R.S. [407] The Prokaryotes: A Handbook on Habitats, Isolation and Identi- (1998) Bacillus arsenicoselenatis, sp. nov., and Bacillus selenitiredu- ¢cation of Bacteria, vol. 1 (Starr, M.P., Stolp, H., Truper, H.G., cens, sp. nov. two haloalkaliphiles from Mono Lake, California that Belows, A. and Schlegel, H.G., Eds.), Springer-Verlag, (1981) New respire oxyanions of selenium and arsenic. Arch. Microbiol. 171, York. 19^30. [408] Gundersen, J.K., Jorgensen, B.B., Larsen, E. and Jannasch, H.W. [426] Laverman, A., Blum, J.S., Shaefer, J.K., Phillips, E.J.P., Lovley, (1992) Mats of giant sulphur bacteria on deep-sea sediments due to D.R. and Oremland, R.S. (1995) Growth of strain SES-3 with ar- £uctuating hydrothermal £ow. Nature 360, 454^456. senate and other diverse electron acceptors. Appl. Environ. Micro- [409] Jorgensen, B.B. and Revsbech, N.P. (1983) Colorless sulfur bacteria, biol. 61, 3556^3561.

FEMSRE 711 7-3-01 J.P. Amend, E.L. Shock / FEMS Microbiology Reviews 25 (2001) 175^243 243

[427] Hippe, H., Caspari, D., Fiebig, K. and Gottschalk, G. (1979) Uti- [440] Sawers, G. (1998) The anaerobic degredation of L-serine and L- lization of and other N-methyl compounds for threonine in enterobacteria: networks of pathways and regulatory growth and methane formation by Methanosarcina barkeri. Proc. signals. Arch. Microbiol. 171, 1^5. Natl. Acad. Sci. USA 76, 494^498. [441] Madigan, M.T., Martinko, J.M. and Parker, J. (1997) Brock Biol- [428] Rabus, R. and Widdel, F. (1995) Anaerobic degradation of ethyl- ogy of Microorganisms, edn. 8, Prentice Hall, Upper Saddle River, benzene and other aromatic hydrocarbons by new denitrifying bac- NJ. teria. Arch. Microbiol. 163, 96^103. [442] Brock, T.D. and Gustafson, J. (1976) Ferric iron reduction by sul- [429] Hinrichs, K.-U., Hayes, J.M., Sylva, S.P., Brewer, P.G. and De- fur-and iron-oxidizing bacteria. Appl. Environ. Microbiol. 32, 567^ Long, E.F. (1999) Methane-consuming archaebacteria in marine 571. sediments. Nature 398, 802^805. [443] Thermophiles: General, Molecular and Applied Microbiology [430] Coates, J.D., Lonergan, D.J., Philips, E.J.P., Jenter, H. and Lovely, (Brock, T.D., Ed.), John Wiley and Sons, (1986) New York. D.R. (1995) Desulfuromonas palmitatis sp. nov., a marine dissimila- [444] Extremophiles: Microbial Life in Extreme Environments (Hori- tory Fe(III) reducer that can oxidize long-chain fatty acids. Arch. koshi, K. and Grant, W.D. Eds.), Wiley-Liss, (1998) New York. Microbiol. 164, 406^413. [445] Oremland, R.S., Hollibaugh, J.T., Maest, A.S., Presser, T.S., Miller, [431] Pfennig, N. and Biebl, H. (1976) Desulfuromonas acetoxidans gen. L.G. and Culbertson, C.W. (1989) Selenate reduction to elemental nov. and sp. nov., a new anaerobic, sulfur-reducing, acetate-oxidiz- selenium by anaerobic bacteria in sediments and culture: biogeo- ing bacterium. Arch. Microbiol. 110, 3^12. chemical signi¢cance of a novel sulfate-independent respiration. [432] Caccavo Jr., F., Lonergan, D.J., Lovley, D.R., Davis, M., Stolz, J. Appl. Environ. Microbiol. 55, 2333^2343. and McInerney, M.J. (1994) Geobacter sulfurreducens sp. nov., a [446] Shock, E.L. (2001) Corrections to standard partial molal enthalpies hydrogen- and acetate-oxidizing dissimilatory metal-reducing micro- of formation of aqueous species. Geochim. Cosmochim. Acta, in organism. Appl. Environ. Microbiol. 60, 3752^3759. preparation. [433] Isaksen, M.F. and Teske, A. (1996) Desulforhopalus vacuolatus gen. [447] Robie, R.A. and Hemingway, B.S. (1995) Thermodynamic Proper- nov., sp. nov., a new moderately psychrophilic sulfate-reducing bac- ties of Minerals and Related Substances at 298.15 K and 1 Bar (105 terium with gas vacuoles isolated from a temperate estuary. Arch. Pa) Pressure and at Higher Temperatures, US Geological Survey Microbiol. 166, 160^168. Bulletin, vol. 2131, United States Government Printing O¤ce, [434] Rabus, R., Nordhaus, R., Ludwig, W. and Widdel, F. (1993) Com- Washington, DC. plete oxidation of toluene under strictly anoxic conditions by a new [448] Fredrickson, D.R. and Chasanov, M.G. (1971) The enthalpy of sulfate redcuing bacterium. Appl. Environ. Microbiol. 59, 1444^ molybdenum disul¢de to 1200 K by drop calorimetry. J. Chem. 1451. Thermo. 3, 693^696. [435] Newman, D.K., Beveridge, T.J. and Morel, F.M.M. (1997) Precip- [449] O'Hare, P.A.G., Lewis, B.M. and Parkinson, B.A. (1988) Standard itation of arsenic trisul¢de by Desulfotomaculum auripigmentum. molar enthalpy of formation by £ourine-combustion calorimetry of

Appl. Environ. Microbiol. 63, 2022^2028. tungsten diselenide (WSe2). Thermodynamics of high-temperature [436] Rueter, P., Rabus, R., Wilkes, H., Aeckersberg, F., Rainey, F.A., vaporization of WSe2. Revised value of the standard molar enthalpy Jannasch, H.W. and Widdel, F. (1994) Anaerobic oxidation of hy- of formation of molybdenite (MoS2). J. Chem. Thermo. 20, 681^ drocarbons in crude oil by new types of sulphate-reducing bacteria. 691. Nature 372, 455^458. [450] McCollom, T.M. and Shock, E.L. (1997) Geochemical constraints [437] Aeckersberg, F., Bak, F. and Widdel, F. (1991) Anaerobic oxidation on chemolithoautotrophic metabolism by microorganisms in sea-

of saturated hydrocarbons to CO2 by a new type of sulfate-reducing £oor hydrothermal systems. Geochim. Cosmochim. Acta 61, 4375^ bacterium. Arch. Microbiol. 156, 5^14. 4391. [438] Yamada, K., Kinoshita, S., Tsunoda, T. and Aida, K. (1972) The [451] Stull, D.R., Westrum, E.F., Jr. and Sinke, G.C. (1969) The Chem- Microbial Production of Amino Acids, Halsted Press, New York. ical Thermodynamics of Organic Compounds, John Wiley and [439] Magot, M., Ravot, G., Campaignolle, X., Ollivier, B., Patel, B.K.C., Sons, New York. Fardeau, M.L., Thomas, P., Crolet, J.L. and Garcia, J.L. (1997) [452] Plyasunov, A.V., O'Connell, J.P., Wood, R.H. and Shock, E.L. Dethiosulfovibrio peptidovorans gen. nov., sp. nov., a new anaerobic, (2001) In¢nite dilution partial molar properties of aqueous nonelec- slightly halophilic, thiosulfate-reducing bacterium from corroding trolytes. III. Prediction algorithm and parameters for some inor- o¡shore oil wells. Int. J. Syst. Bacteriol. 47, 818^824. ganic solutes. Geochim. Cosmochim. Acta, in preparation.

FEMSRE 711 7-3-01