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Energetics of Overall Metabolic Reactions of Thermophilic and Hyperthermophilic Archaea and Bacteria

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Energetics of Overall Metabolic Reactions of Thermophilic and Hyperthermophilic Archaea and Bacteria FEMS Microbiology Reviews 25 (2001) 175^243 www.fems-microbiology.org Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and Bacteria Jan P. Amend *, Everett L. Shock Department of Earth 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 redox reactions include H2, 2 23 23 Fe ,H2S, S, S2O3 ,S4O6 , sulfide minerals, CH4, various mono-, di-, and hydroxy-carboxylic acids, alcohols, 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 microorganisms, 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 metabolism. 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 sulfur and nitrate reduction, and autotrophic methanogenesis), 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; Thermodynamics; Thermophile; Hyperthermophile; High temperature Contents 1. Introduction .......................................................... 176 2. Thermophiles and hyperthermophiles . ....................................... 177 2.1. Life 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 autotrophs and heterotrophs . .................. 178 3.2. Comparisons with mesophiles . ....................................... 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 kingdom. 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 genomes, 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 methane (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 enzyme. Therefore, the organism containing the appro- organism if
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