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Minireview Chemolithotrohic Bacteria

Minireview Chemolithotrohic Bacteria

Microbes Environ. Vol. 22, No. 4, 309–319, 2007 http://wwwsoc.nii.ac.jp/jsme2/ Minireview

Chemolithotrohic : Distributions, Functions and Significance in Volcanic Environments

GARY M. KING1*

1 Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA

(Received August 21, 2007—Accepted September 11, 2007)

A mosaic of environments comprises most volcanic ecosystems. Whether terrestrial or submarine, many of these environments contain large deposits of reduced minerals, or experience large fluxes of reduced substrates, especially -containing compounds. These , which also are typically characterized by temperature and pH extremes, have yielded a rich variety of chemolithotrophic bacteria, and contributed much to our under- standing of chemolithotroph and . However, volcanic ecosystems also consist of environ- ments where inorganic and organic substrates are limiting. In these cases, chemolithotrophs may still play impor- tant roles by scavenging monoxide, hydrogen or both. These gases can support of facultative chemolithotrophs, a functional group that includes many -fixing bacteria. Facultative chemolithotrophs may not only represent important early colonists on fresh volcanic substrates (e.g., basalts lacking sulfides), they may also contribute significantly to ecosystem succession through and interactions with vascu- lar . Analyses of CO and hydrogen consumption by recent deposits on Kilauea volcano show that both sub- strates support significant activity, while molecular approaches show a high diversity of . Collectively, these and other observations indicate that chemolithotrophic metabolism is more widespread than generally acknowledged, and likely to play fundamental roles in shaping ecosystem dynamics.

Key words: volcanic, rubisco, carbon monoxide,

Introduction be used chemolithotrophically grew to include carbon mon- oxide (CO), molecular hydrogen (H2) and with some contro- Winogradski, one of the pioneers of modern microbial versy, ferrous iron (Fe2+). In the last several decades, how- , first deduced the basic principles of chemo- ever, a number of groups have substantially expanded the lithotrophic metabolism, including both sulfur- and ammo- horizons of chemolithotrophy well beyond those that could nium-driven processes44). His work involved analyses of ter- have been imagined in the late 19th and early 20th restrial and aquatic bacteria, and his insights remain a centuries2,7,27,28,44,54,71). foundation for contemporary understanding of sulfur and nitrogen biogeochemistry. A. Chemolithotrophs: a brief overview Subsequent to Winogradski’s initial studies, advances in By definition, chemolithotrophs oxidize reduced inor- the microbial biology of chemolithotrophy were relatively ganic substrates as a source of for ATP synthesis, slow in coming, even though the list of substrates that could but carbon may or may not be derived from autotrophic CO2 fixation (Table 1, Fig. 1). In the former case, the term * Corresponding author. E-mail address: [email protected]; Tel.: +225– “chemolithoautotrophy” applies, and in the latter instance, 578–1901. “chemolithoheterotrophy” is used. Chemolithotrophy may 310 KING

Table 1. Selected examples of chemolithotrophic metabolism. Obligate chemolithotrophs are defined as that use only inorganic energy sources (electron donors) and inorganic carbon for , but some, e.g., Brocadia anammoxidans, can supplement inorganic carbon with organics for biosynthesis. This may be a more common phenomenon than recognized and represents a form of mixotropy. Facultative chemolithotrophs use either inorganic energy and carbon sources or (often preferentially), organic energy and biosynthetic sources; many may grow mixotrophically in situ. Chemolithoheterotrophs use inorganic energy sources and organic carbon for biosyn- thesis; metabolism may also be mixotrophic in situ.

Metabolic mode Energy source Oxidant Example Reference

Obligate O2 Nitrosomonas europea 12 ammonium Brocadia anammoxidans 42 sulfide, thiosulfate O2, Thiobacillus denitrificans 7 CO, H2 O2 Streptomyces thermoautotrophicus 29 CO H+ Carboxydothermus hydrogenoformans 88 Fe2+ O2 Acidithiobacillus ferrooxidans 44 2− H2 SO4 Desulfobacterium autotrophicum 51 H2 CO2 Methanobacterium thermoautotrophicum 72 Facultative nitrite O2 Nitrobacter vulgaris 8 sulfide, thiosulfate O2 Thioclava pacifica 74 sulfide, thiosulfate O2, nitrate Paracoccus pantotrophus 43 thiocyanate O2 Paracoccus thiocyanatus 43 elemental sulfur O2 Mesorhizobium thiogangeticum 31 Fe2+ nitrate Beta-proteobacterium strain 2002 84 CO O2, nitrate Bradyrhizobium japonicum USDA 6 48, 49 H2 O2, nitrate Paracoccus denitrificans 44 2− H2 SO4 Desulfonauticus submarinum 5 H2 perchlorate Dechloromonas sp. strain HZ 89 As3+ nitrate Alkalilimnicola ehrlichii 38 chemolithoheterotroph CO O2 Silicibacter pomeroyi 55

also be expressed obligately, facultatively or mixotrophi- cally, i.e., during simultaneous growth with heterotrophic and lithotrophic substrates. Autotrophy, when it occurs, may involve at least three different mechanisms for CO2 fix- ation in addition to the classic Calvin-Bassham-Benson pathway: the reductive tricarboxylic acid cycle (rTCA), the 3-hydroxypropionate cycle (3-HP) and acetyl-CoA synthesis44). While sulfide and oxidation were first described as dependent, chemolithotrophy now encompasses aerobes and anaerobes that collectively use Fig. 1. A schematic diagram illustrating major inorganic electron nearly all known electron acceptors (Table 1), as well as donors (energy sources) associated with volcanic activity and somewhat “exotic” combinations of reductants and oxi- coupling between reductants and three metabolic modes: chemo- dants, e.g., arsenite and nitrate61,68), hydrogen and lithoautotrophy, incorporating only CO2 into biomass; mixotro- perchlorate89). In the remarkable genus, Acidianus, hydro- phy, incorporating both CO2 and pre-formed organics; chemo- lithoheterotrophy, incorporating only pre-formed organics but gen can support chemolithotrophic sulfur reduction under using inorganic electron donors as a source of ATP or anaerobic conditions, while under aerobic conditions, the + NAD(P)H+H . Note that facultative chemolithotrophs may func- same organisms can oxidize sulfur chemolithotrophically44). tion as chemolithoautotrophs if pre-formed organics are limiting The various functional groups that have been identified and inorganic electron donors are available, if both are available, or chemolithoheterotrophs depending on regulatory collectively harbor an astonishing array of phylogenetically control of lithotrophic metabolism. Redrawn from Kelly and diverse lineages within the bacterial and archaeal domains, Wood44). and include numerous extremophiles44). In addition to Chemolithotrophs and Volcanic Environments 311

Winogradski’s obligately chemolithotrophic sulfide- and patterns of diversity and activity have helped shape basic ammonia-oxidizing bacteria, chemolithotrophs now include concepts, such as the reality of bacterial biogeography69,86). numerous functional groups (Table 1) and diverse modes of In most hydrothermal and solfatara systems, chemo- metabolism following the definitions above. A complete lithotrophic sulfide oxidation drives the bulk of carbon fix- listing is beyond the scope of this paper, so only representa- ation, and supports not only substantial amounts of micro- tive examples have been summarized (Table 1). The extent bial biomass, but also diverse communities that of this diversity suggests that chemolithotrophic metabo- exploit sulfide-oxidizing symbionts16,40,87). Sulfide-linked lism may play even more important ecological roles than chemolithoautotrophy thus forms the base of complex have been previously appreciated. Several chem- webs largely independent of photosyntetically-derived olithotrophic or predominantly chemolithotrophic lineages organic . Complete independence of plants does not branch deeply based on 16S rRNA gene sequences analy- occur, however, since molecular oxygen, the primary oxi- ses, suggesting that chemolithotrophy also represents an dant, is photosynthetically-derived. This may dramatically important ancient, if not ancestral, metabolic mode44). limit the relevance of ’s hydrothermal systems for Taken as a group, the spatial distribution of chemo- understanding systems that may exist on Europa, if any11). lithotrophs is analogous to their phylogenetic and functional Some of the other non-sulfur reduced substrates in hydro- 2+ breadth. Chemolithotrophs are essentially ubiquitous, includ- thermal fluids, e.g., H2, CO, and Fe , may also contribute to ing most terrestrial and aquatic (freshwater and marine) microbial food webs. For instance, Robb and colleagues , and notably, the deep sub-surface6,19,23,24,36,37,52,67,78). have proposed that anaerobic CO oxidizers, such as Car- This too provides an indication of the general significance boxydothermus carboxidovorans, may play important roles of chemolithotrophy for the dynamics of microbial commu- in certain cases88). Though activity data are few, numerous nities and biogeochemical cycling. novel H2- and CO-oxidizing strains have been isolated39,60,70,73,76,77), suggesting that these substrates are eco- B. Chemolithotrophy and reductant-rich volcanic logically relevant. systems While long regarded as a chemolithotrophic substrate, the Although much of the research on chemolithotrophy has ability of Fe2+ to sustain microbial communities by support- involved readily accessible environments and isolates from ing autotrophic biosynthesis in non-acidic or anaerobic sys- them44), numerous important advances have been derived tems has been documented only recently18,21,22,58,84). The sub- from extreme systems, especially those characterized by marine volcano, Loihi (Hawai’i) provides an important and high temperatures or low pH. Acidithiobacillus ferrooxi- dramatic example. Loihi supports substantial microbial dans, for example, has been obtained from environments mats that oxidize Fe2+ 22), and both culture and culture-inde- acidified by metal sulfide oxidation, and has yielded a pendent methods have shown that these mats contain chemo- mechanistic understanding of chemolithotroph interactions lithotrophic iron oxidizers22). Microbial iron oxidation at with minerals64). The latter have proven valuable in com- Loihi appears to be a consequence of reduced ambient - mercial efforts to use microbes to mine (or leach) metals water oxygen concentrations and slightly acidic, iron-rich, such as copper, gold and uranium64). sulfide-poor hydrothermal fluids, in which Fe2+ is suffi- Yet in spite of their relative inaccessibility, the discovery ciently stable that circumneutral iron-oxidizing bacteria can of submarine hydrothermal vents has clearly had a transfor- compete kinetically with molecular oxygen58,85). In nor- mative impact on chemolithotrophy research. It has become moxic, alkaline seawater, chemical Fe2+ oxidation is simply almost axiomatic that chemolithotrophs play major roles in too rapid for bacteria constrained by kinetics and the microbial biology of hydrothermal systems, as well as in thermodynamics58). the biology of solfatara associated with active and quiescent Both visual observations and models of biosynthetic rates terrestrial volcanic environments. suggest significant levels of chemosynthetic production22) at These systems have yielded a rich variety of novel Loihi. Interestingly, Fe-based microbial mats do not appear chemolithotrophs1,9,15,57,65,76,77,79,87) capable of exploiting the to support complex animal communities or Fe-based typically high concentrations of reduced inorganic sub- symbioses41) as do sulfide- and -based systems30,53). strates (especially various sulfur ) associated with This likely reflects constraints imposed by copious iron many volcanic environments. The properties of many of oxyhydroxide (rust) deposition. these isolates have been unexpected, and opened new hori- While Loihi may be somewhat unique, Fe2+-based chemo- zons in microbial biology35,39,70,84). Similarly, analyses of lithotrophy may occur routinely in association with sub- 312 KING marine volcanic systems17). Edwards and co-workers have lism, and supports a proposal that facultatively lithotrophic proposed that iron-rich basalts in marine crust support CO and H2 oxidizers, perhaps growing mixotrophically with chemolithotrophs, and presented mineralogical, bio- inputs of organics in precipitation, can colonize barren geochemical and microbiological evidence consistent with material and contribute to ecosystem succession46). Though this proposal19). The latter has included isolation of novel not yet demonstrated for CO oxidizers, mixotrophy may psychrophilic, obligately chemolithotrophic iron oxidizers offer competitive advantages as have been documented for that can use iron minerals (e.g., basaltic glass) as mixotrophic sulfide oxidizers34). substrates18). Further support for this proposal has been obtained from In these basaltic systems, chemolithotrophy may be sup- ongoing analyses of microbial succession on recently ported by direct use of Fe2+ as documented by Edwards and deposited lava fragments that initially did not consume CO colleagues, or indirectly through hydrogen production dur- at detectable rates. Within 6 months after transplanting the ing chemical hydrolysis of ferrous oxide minerals6). Esti- material on a 57-year old tephra deposit (described in more mates of potential biosynthetic rates coupled to Fe2+ oxida- detail by King46)), active CO uptake could be readily tion directly and supported by hydrolytically-formed H2, detected, indicating significant colonization by CO oxidiz- while necessarily speculative, could rival rates supported by ers. Curiously, hydrogen uptake has remained undetectable buried in deep-sea sediments6). for more than one year, suggesting that CO oxidizers may Clearly, sulfide- and metal-dependent chemolithotrophs colonize lava deposits more rapidly than hydrogen oxidiz- play important roles in hydrothermal vents associated with ers, even though long-term succession may result in greater submarine volcanic systems and terrestrial volcanic envi- activity by the latter. ronments with significant localized sources of reductants, CO consumption has also been detected for recent volca- e.g., fumaroles, solfatara, and hot springs. The latter, how- nic deposits on Miyake-jima, Japan (King and Weber, ever, usually account for only a small fraction of the surface unpubl. data) and for somewhat older (ca. 100 yr) deposits area impacted by eruptive activity, which often produces at 3200–3300 m elevation on Mauna Loa volcano (King and expansive fields of lava and tephra (material ejected into the Weber, unpubl. data). These observations collectively sug- atmosphere) that lack direct contact with reduced sulfur or gest that CO oxidizers colonize organic-poor volcanic reduced volcanic gases. What roles do chemolithotrophs deposits generally, and actively express genes for CO dehy- play in these systems? drogenase. Whether they also actively fix CO2 for biosyn- thesis has not yet been determined. C. Chemolithotrophy and reductant-poor volcanic Aside from the direct impacts of colonization per se (e.g., systems biofilm formation, carbon accumulation, - Recent observations suggest that even in the absence of ing), CO oxidizers may also contribute to nitrogen dynam- high substrate concentrations, chemolithotrophs play signif- ics and the of nitrogen cycling on volcanic depos- icant roles on relatively young volcanic deposits46). Since its. Thus far, many of the known CO-oxidizing isolates have recently emplaced lava and tephra lack significant levels of been reported to fix nitrogen or to harbor nitrogenase organic carbon and nitrogen, they represent habitats that can genes47). Further, some CO oxidizers form nitrogen-fixing 49) select for facultatively chemolithotrophic CO and H2 oxi- symbioses with plants (e.g., Bradyrhizobium ), and others dizers that derive substrates for energy from the atmo- may have the potential to do so (e.g., Burkholderia spp.49)). sphere. While atmospheric CO and H2 concentrations are Since newly formed volcanic deposits contain little or no low (about 50–350 and 550 parts per billion, biologically available nitrogen, nitrogen fixation plays a respectively45)), they are continuously available, and rela- critical in ecosystem successional development on tively high rates of uptake have been reported for soils45). them63,66). A comparison of acetylene reduction rates, an Both in situ and ex situ assays of CO and H2 uptake by index of nitrogenase activity, and maximum CO uptake recent Kilauea volcano (Hawaii) deposits have revealed potential reveals a positive correlation for sites on a succes- rates comparable to those for mature terrestrial soils46). sional gradient at Kilauea volcano (King and Weber, unpub- Comparisons of these activities with rates of CO2 produc- lished data). This suggests that both processes respond to tion have suggested that H2 could account for 20–25% of related variables, although nitrogen fixation activity by CO respiratory reducing equivalent flow, while CO could oxidizers specifically remains to be demonstrated. Develop- account for about 2–10%. This represents a significant con- ment of a suitable stable isotope probing approach (SIP62)) tribution of atmospheric trace gases to microbial metabo- may help resolve this issue. Chemolithotrophs and Volcanic Environments 313

SIP and reverse transcriptase-polymerase chain reaction ing. (rtPCR) approaches may also help determine the diversity The fact that consistent methanotrophic activity is associ- of CO oxidizers active in situ. In the first analyses of CO ated with mature, vegetated sites (King and Nanba, unpub- oxidizer diversity in any , Dunfield and King14) lished data) suggests that some conditioning of volcanic applied primers for the large sub-unit of CO deposits is a prerequisite for methanotrophs. Among other dehydrogenase47) to develop clone libraries from several possibilities, this may involve the physical-chemical sites representing diverse habitats on Kilauea volcano. The of the deposits per se, availability of methanol or required results revealed an unexpectedly high degree of CO oxi- micronutrients (e.g., Fe or Cu), or interactions with other dizer diversity (defined on the basis of unique sequences), bacterial groups. In addition, CO (and H2) oxidizers can and a battery of statistical analyses applied for the first benefit from a wide range of heterotrophic substrates that to functional genes showed substantial differentiation methanotrophs do not use. This may amount to a subsidy for among geographically close, but successionally distinct the biomass and activity of the former. Resolution of the sites (Fig. 2). dynamics of methanotrophs on volcanic deposits may pro- Many sequences could be associated with broad phyloge- vide valuable insights for the response of methanotrophs to netic groups, e.g., sub-groups of the Proteobacteria, but a disturbances in other systems and for their ecological large number of sequences appeared to represent novel, as behavior more generally. yet unidentified CO-oxidizing lineages, possibly including There is also little indication of significant activity by some Actinobacteria and Firmicutes, but likely also repre- iron-oxidizing chemolithotrophs on Kilauea volcanic depos- senting phyla not yet known to harbor CO oxidizers (Fig. 2; its, or at least on superficial deposits, even though ferrous see also 14). Notably, the phylogenetic distribution of CO iron is a major component of the basalts that form them. oxidizers among sites reflects patterns for the communities Perhaps activity is limited by water availability, as a whole; in particular proteobacterial CO oxidizers for oxygen, or other constraints on microbial interactions appear to dominate in mature forested sites, a pattern also with mineral surfaces. Nonetheless, a recent report of basal- observed during analyses of 16S rRNA gene sequences33). tic iron oxidation in liquid cultures18) suggests that closer Ongoing efforts to isolate and characterize novel CO oxi- examination of the role of chemolithotrophs in the weather- dizers from these sites will not only help in understanding ing of routinely wetted deposits may be fruitful. Although the ecology of CO oxidation on volcanic deposits, but will chemical processes have been proposed as the mechanism aid in understanding the phylogeny and evolution of aerobic for very rapid basalt in areas with high precipi- CO oxidation per se. tation, bacterial iron oxidation may also be a significant Although CO oxidizers (and likely H2 oxidizers) form contributing factor. robust and diverse groups of facultative chemolithotrophs on at least some recent Kilauea volcanic deposits, the same D. Ribulose-1,5-bisphosphate oxygenase/carboxylase cannot be said for other lithotrophs. To date there is little genes as a tool for exploring chemolithotroph diversity indication that ammonia or nitrite oxidizers contribute sig- Phylogenetic and functional breadth pose serious chal- nificantly to nitrogen dynamics at the same sites. Activity is lenges for using molecular approaches to understand the limited and inconsistent even for somewhat older (e.g., 300- distribution and diversity of chemolithotrophs in most sys- yr old) forested sites46). This may be due to slow rates of tems, not just volcanic environments. Genetic markers that nitrogen accumulation that decrease ammonium availabil- can be applied to the full range of known taxa have not yet ity, as well as a general acidification of as they develop been described. There are no known signature 16S rRNA over time. genes for chemolithotrophs, for instance, and functional Somewhat more perplexing are slow rates and a patchy genes (e.g., amoC, coxL, soxC) necessarily capture only distribution for atmospheric methane uptake by recent specific groups. Kilauea volcanic deposits, observations that imply that Nonetheless, the large sub-unit gene (cbbL) for ribulose- methanotrophs are relatively few in number. Except for the 1,5-bisphosphate carboxylase/oxygenase (rubisco) offers definition of methane as an organic compound, methanotro- some useful general insights, even though some chemo- phs otherwise appear to function as chemolithotrophs. Since lithotrophs fix CO2 by pathways other than CBB, while methane is more abundant in the atmosphere than CO or H2, others do not fix CO2 at all. Rubsico is now known to occur and more favorable thermodynamically as a substrate, the in three distinct forms that catalyze CO2 fixation: forms I, II, lack of methanotrophy relative to CO oxidation is surpris- and III. Forms I and II occur in the domains Bacteria and 314 KING

Fig. 2. Phylogenetic distribution of partial sequences of the large sub-unit gene (coxL) for carbon monoxide dehydrogenase obtained after poly- merase chain reaction amplification of genomic extracts from four sites on Kilauea volcano, Hawai’I (redrawn from 14). Assignments to spe- cific clades are based on congruent relationships between coxL phylogenies and 16S rRNA gene sequence phylogenies. See King47) and Dun- and King14) for details. Chemolithotrophs and Volcanic Environments 315

Fig. 3. Phylogenetic distribution of partial sequences of the large sub-unit gene (cbbL also rbcL) for ribulose-1,5-bisphosphate carboxylase/oxy- genase obtained after polymerase chain reaction amplification of genomic extracts from four sites on Kilauea volcano, Hawai’I (redrawn from 56). Open symbols refer to clone sequences; closed symbols refer to Caldera Rim clone sequences; hatched symbols refer to Pu’u Puai clone sequences; open square represents a Halema‘uma’u clone sequence. Note that none of the observed sequences cluster with form IA cbbL sequences. See Nanba et al.56) for details.

Eukarya, while form III appears restricted to While several factors mitigate against using environmen- Archaea3,4,75,83). Form I has been further subdivided into four tal sequences to infer the presence of specific chem- groups, A–D, that represent phylogenetically distinct olithotrophic functional groups13,23,25,50,81), empirical results groups71). Of these, form IA has been observed primarily in thus far indicate that the relative of form IA ver- some , obligate chemolithotrophs (hydrogen, sus form IC phylotypes is a sensitive indicator of to the iron, sulfur, ammonia, and nitrite oxidizers), sulfide-oxidiz- extent to which reduced sulfur and nitrogen species drive ing mixotrophs, and a single CO oxidizer71,75,81). Form IC chemolithotrophic processes59,80). For example, using cbbL occurs primarily in facultatively lithotrophic CO and H2 primers developed by King to target both form IA and IC oxidizers, facultatively lithotrophic oxidizers sequences simultaneously, Nigro and King59) found an over- and in a phylogenetically distinct clade of ammonia-oxidiz- whelming of form IA phylotypes in sulfide-rich ing Nitrosospira26,71,82). intertidal marine sediments and form IC phylotypes in sul- 316 KING fide-poor freshwater sediments. Similarly, Nanba et al.56) ther our understanding of chemolithotrophy and volcanic found only form IC sequences at sites on Kilauea volcano ecosytems, they provide will deeper insights into the funda- lava and tephra that were not impacted by reduced sulfur mental properties of microbial systems more generally. (Fig. 3), and Tolli and King80) reported dominance by form Some of these observations may yet prove relevant for IC for low-sulfur agricultural soils. In contrast, Weber and understanding the prospects for beyond Earth. King (unpubl. results) have observed dominance by form IA phylotypes in sulfide-rich hydrothermal springs. Several Acknowledgements additional studies, though they did not emphasize form IC cbbL, have also yield results consist with those form analy- Support from NSF 0348100 for the Kilauea Microbial ses of King and colleagues20,32). Collectively, these results Observatory is acknowledged gratefully. I thank C. Weber suggest that cbbL may be used as a target for molecular for numerous discussions and contributions to the KMO, “explorations” of the and dynamics of at least a Dr. K. Nanba for past and continued collaborations and portion of the chemolithotroph communities in a variety of Prof. H. Ohta for support and collaboration during work on environments. Analyses of other genes, e.g., form III cbbL Mt. Oyama, Miyake-jima, Japan. and ATP-citrate lyase, may further expand understanding of chemolithotrohic communities by targeting and ε- Proteobacteria, respectively10,83). References

E. Summary and conclusions 1) Aguiar, P., T.J. Beveridge, and A.-L. Reysenbach. 2004. Sulfuri- hydrogenibium azorense, sp. nov., a thermophilic hydrogen-oxi- Winogradski’s pioneering work opened doors to a rich dizing microaerophile from terrestrial hot springs in the Azores. variety of metabolic and phylogenetic groups that play Int. J. Syst. Evol. Microbiol. 54:33–39. 2) Argano, M. 1991. Aerobic chemolithotrophic bacteria. p. 7–103. numerous roles in the biogeochemical cycles of carbon, In J.K. Kristjansson (ed.), Thermophilic bacteria. CRC Press, nitrogen, sulfur, metals, and various trace elements. What Boca Raton, FL. once seemed an easily demarcated group of organisms with 3) Atomi, H., S. Ezaki, and T. Imanaka. 2001. Ribulose-1,5-bispho- clearly defined has increasingly become estab- sphate carboxylase/oxygenase from Thermococcus kodakaraen- sis KOD1. Meth. Enzymol. 331:353–365. lished as remarkably diverse, widely distributed and funda- 4) Atomi, H. 2002. Microbial enzymes involved in mentally important. fixation. J. Biosci. Bioengr. 94:497–505. Volcanic ecosystems represent exceptional environments 5) Audriffin, C., J.-L. Cayol, C. Joulian, L. Casalot, P. Thomas, J.-L. that support chemolithotrophs in most, if not all, of their Garcia, and B. Ollivier. 2003. Desulfonauticus submarines gen. forms. This is due to the fact that these environments consist nov., sp., nov., a novel sulfate-reducing bacterium isolated from a deep-sea . Int. J. Syst. Evol. Microbiol. of a mosaic of habitats, some with essentially unlimited sup- 53:1585–1590. plies of reduced substrates, and others that are acutely oligo- 6) Bach, W., and K.J. Edwards. 2003. Iron and sulfide oxidation trophic. Gradients between these two extremes are often within the basaltic crust: implications for chemolithoau- very steep and accompanied by equally steep gradients in totrophic microbial biomass production. Geochim. Cosmochim. Acta 67:3871–3887. variables such as pH, temperature and electron acceptors. 7) Beller, H.R., P.S.G. Chain, T.E. Letain, A. Chakicherla, F.W. Although certain terrestrial and submarine volcanic sys- Larimer, P.M. Richardson, M.A. Coleman, A.P. Wood, and D.P. tems have been the subject of relatively extensive analyses, Kelly. 2006. The genome sequence of the obligately chem- much remains unknown about the distribution and activities olithoautotrophic, facultatively anaerobic bacterium Thiobacillus denitrificans. J. Bacteriol. 188:1473–1488. of chemolithotrophs. Analyses of microbial dynamics over 8) Bock, E., H.-P. Koops, U.C. Möller, and M. Rudert. 1990. A new time on newly formed surfaces offer potentially exceptional facultatively nitrite oxidizing bacterium, Nitrobacter vulgaris sp. opportunities for novel insights. What governs the diversity nov. Arch. Microbiol. 153:105–110. in and time of chemolithotroph (and other) popula- 9) Campbell, B.J., C. Heanthon, J.E. Kostka, G.W. Luther, III, and S.C. Cary. 2001. Growth and phylogenetic properties of novel tions? What factors control colonization rates? How do bacteria belonging to the epsilon subdivision of the Proteobacte- chemolithotrophs generally and mixotrophs specific ally ria enriched from Alvinella pompejana and deep-sea hydrother- interact with microbial and multicellular mal vents. Appl. Environ. Microbiol. 67:4566–4572. organisms throughout succession? Are microbial communi- 10) Campbell, B.J., A.S. Engel, M.L. Porter, and K. Takai. 2006. The ε-Proteobacteria: key players in sulfidic habitats. Nature Rev. ties and biogeochemical patterns assembled stochastically Microbiol. 4:458–468. or deterministically? 11) Chyba, C., and C.B. Phillips. 1998. Possible ecosystems and the Answers to these and related questions will not only fur- search for life on Europa. Proc. Natl. Acad. Sci. USA 98:801– Chemolithotrophs and Volcanic Environments 317

804. 28) Friedrich, C.G., D. Rother, F. Bardischewsky, A. Quentmeier, 12) Codd, A., and J.G. Kuenen. 1987. Physiology and biochemistry and J. Fischer. 2001. Oxidation of reduced inorganic sulfur com- of autotrophic bacteria. . v. Leeuw. 53:3–14. pounds by bacteria: of a common mechanism? Appl. 13) Delwiche, C.F., and J.D. Palmer. 1996. Rampant horizontal trans- Environ. Microbiol. 67:2873–2882. fer and duplication of rubisco genes in eubacteria and plastids. 29) Gadkari, D., G. Mörsdorf, and O. Meyer. 1990. Streptomyces Mol. Biol. Evol. 13:873–882. thermoautotrophicus sp. nov., a thermophilic CO- and H2-oxidiz- 14) Dunfield, K., and G.M. King. 2004. Molecular analysis of carbon ing obligate chemolithotroph. Appl. Environ. Microbiol. monoxide-oxidizing bacteria associated with recent Hawaiian 56:3727–3734. volcanic deposits. Appl. Environ. Microbiol. 70:4242–4248. 30) Gatehouse, L.N., A. Shannon, E.P.J. Burgess, J.T. Christeller, M. 15) Durand, P., A.-L. Reysenbach, D. Prieur, and N. Pace. 1993. Iso- Sibuet, and K. Olu. 1998. Biogeoraphy, and fluid lation and characterization of Thiobacillus hydrothermalis sp. dependence of deep-sea cold- communities at active and pas- nov., a mesophilic obligately chemolithotrophic bacterium iso- sive margins. Res., Part II: Topical Studies in Ocean- lated from a deep-sea hydrothermal vent in Fiji Basin. Arch. ogr. 45:517–567. Microbiol. 159:39–44. 31) Ghosh, W., and P. Roy. 2006. Mesorhizobium thiogangeticum, 16) Eberhard, C., C.O. Wirsen, and H.W. Jannasch. 1995. Oxidation sp. nov., a novel sulfur-oxidizing chemolithoautotroph form of polymetal sulfides by chemolithoautotrophic bacteria from rhizosphere of an Indian tropical leguminous . Int. J. deep-sea hydrothermal vents. Geomicrobiol. J. 13:145–164. Syst. Evol. Microbiol. 56:91–97. 17) Edwards, K.J., W. Bach, and D.R. Rogers. 2003. Geomicrobiol- 32) Giri, B.J., N. Bano, and J.T. Hollibaugh. 2004. Distribution of ogy of the ocean crust: a role for chemoautotrophic Fe-bacteria. RuBisCO along a redox gradient in , Cali- Biol. Bull. 204:180–185. fornia. Appl. Environ. Microbiol. 70:3443–3448. 18) Edwards, K.J., D.R. Rogers, C.O. Wirsen, and T.M. McCollom. 33) Gomez-Alvarez, V., G.M. King, and K. Nüsslein. 2007. Compar- 2003. Isolation and characterization of novel psychrophilic, neu- ative bacterial diversity in recent Hawaiian volcanic deposits of trophilic, Fe-oxidizing, chemolithoautotrophic α- and γ-Proteo- different ages. FEMS Microbiol. Ecol. 60:60–73. bacteria from the deep sea. Appl. Environ. Microbiol. 69:2906– 34) Gottschal, J.C., S. de Vreies, and G. Kuenen. 1979. Competition 2913. between the facultatively chemolithotrophic Thiobacillus and a 19) Edwards, K.J., W. Bach, T.M. McCollum, and D.R. Rogers. heterotrophic Spirillum for inorganic and organic substrates. 2004. Neutrophilic iron-oxidizing bacteria in the ocean: their hab- Arch. Microbiol. 121:241–249. itats, diversity and roles in mineral deposition, rock alteration, 35) Hafenbrandl, D., M. Keller, R. Dirmeier, R. Rachel, P. Ronagel, and biomass production in the deep-sea. Geomicrobiol. J. S. Burggraf, H. Huber, and K.O. Stetter. 1996. Ferroglobus 21:393–404. placidus gen. nov., sp. nov., a novel hyperthermophilic archaeum 20) Elsaied, H., and T. Naganuma. 2001. Phylogenetic diversity of that oxidizes Fe2+ at neutral pH under anoxic conditions. Arch. ribulose-1,5-bisphosphate carboxylase/oxygenase large-subunit Microbiol. 166:308–314. genes from deep-sea . Appl. Environ. Microbiol. 36) Hagin, K.D., and D.C. Nelson. 1997. Use of reduced sulfur com- 67:1751–1765. pounds by Beggiotoa spp.: enzymology and physiology of marine 21) Emerson, D., and C.L. Moyer. 1997. Isolation and characteriza- and freshwater strains in homogeneous and gradient cultures. tion of novel iron-oxidizing bacteria that grow at circumneutral Appl. Environ. Microbiol. 63:3957–3964. pH. Appl. Environ. Microbiol. 63:4784–4792. 37) Hirayama, H., T. Takai, F. Inagaki, K.H. Nealson, and K. Horiko- 22) Emerson, D., and C.L. Moyer. 2002. Neutrophilic Fe-oxidizing shi. 2005. Thiobacter subterraneus gen. nov., sp. nov., an obli- bacteria are abundant at the Loihi seamount hydrothermal vents gately chemolithoautotrophic, thermophilic, sulfur-oxidizing bac- and play a major role in Fe oxide deposition. Appl. Environ. terium from a subsurface hot aquifer. Int. J. Syst. Evol. Microbiol. 68:3085–3093. Microbiol. 55:467–472. 23) Engel, A.S., N. Lee, M.L. Porter, L.A. Stern, P.C. Bennett, and 38) Hoeft, S.E., J.S. Blum, J.F. Stolz, F.R. Tabita, B. Witte, G.M. M. Wagner. 2003. Filamentous “Epsilonproteobacteria” domi- King, J.M. Santini, and R.S. Oremland. 2007. Alkalilimnicola nate microbial mats in sulfidic caves. Appl. Environ. Microbiol. ehrlichii sp. nov., a novel arsenite-oxidizing haloalkaliphilic 69:5503–5511. gammaproteobacterium capable of chemoautotrophic or het- 24) Engel, A.S., M.L. Porter, L.A. Stern, S. Quinlan, and P.C. Ben- erotrophic growth with nitrate or oxygen as the electron acceptor. nett. 2004. Bacterial diversity and ecosystem function of filamen- Int. J. Syst. Evol. Microbiol. 57:504–512. tous microbial mats from aphotic (cave) sulfidic springs domi- 39) Huber, R., T. Wilharm, D. Huber, A. Trincone, S. Burggraf, H. nated by chemolithoautotrophic “Epsilonproteobacteria”. FEMS Konig, R. Rachel, I. Rockinger, H. Fricke, and K.O. Stetter. 1992. Microbiol. Ecol. 51:31–53. Aquifex pyrophilus, gen. nov., sp. nov. represents a novel group 25) English, R.S., C.A. Williams, S.C. Lorbach, and J.M. Shively. of marine hyperthermophilic hydrogen-oxidizing bacteria. Syst. 1992. Two forms of ribulose-1,5-bisphosphate carboxylase/oxy- Appl. Microbiol. 15:340–351. genase from Thiobacillus denitrificans. FEMS Microbiol. Lett. 40) Jannasch, H.W. 1985. The chemosynthetic support of life and 73:111–119. microbial diversity at deep-sea hydrothermal vents. Proc. R. Soc. 26) Francis, C.A., E. Co, and B.M. Tebo. 2001. Enzymatic manga- London B 225:277–297. nese (II) oxidation by a marine α-proteobacterium. Appl. Envi- 41) Karl, D.M., G.M. McMurtry, G.M. Malahoff, and M.O. Garcia. ron. Microbiol. 67:4024–4029. 1988. Loihi seamount, Hawaii: a mid-plate volcano with a dis- 27) Friedrich, B., and E. Schwartz. 1993. of tinctive hydrothermal system. Nature (Lond.) 335:532–535. hydrogen utilization in aerobic chemolithotrophs. Annu. Rev. 42) Kartal, B., L. van Niftrik, O. Sliekers, M.C. Schmid, I. Schmidt, Microbiol. 47:351–383. K. van de Pas-Schoonen, I. Cirpus, W. van der Star, M. van Loos- 318 KING

drecht, W. Abma, J.G. Kuenen, J.-W. Mulder, M.S.M. Jetten, 58) Neubauer, S.C., D. Emerson, and J.P. Megonigal. 2002. Life at H.O. den Camp, M. Strous, and J. van de Vossenberg. 2004. the energetic edge: kinetics of circumneutral iron-oxidizing bac- Application, eco-physiology and biodiversity of anaerobic teria isolated form the -plant rhizosphere. Appl. Environ. ammonium-oxidizing bacteria. Rev. Environ. Sci. Biotechnol. Microbiol. 68:3988–3995. 3:255–264. 59) Nigro, L.M., and G.M. King. 2007. Disparate distributions of 43) Katayama, Y., A. Hiraishi, and H. Kuraishi. 1995. Paracoccus chemolithotrophs containing form IA or IC large sub-unit genes thiocyanatus sp. nov., a new species of thiocyanate-utilizing fac- for ribulose-1,5-bisphosphate carboxylase/oxygenase in intertidal ultative chemolithotroph, and transfer of Thiobacillus versutus to marine and littoral lake sediments. FEMS. Microbiol. Ecol. the genus Paracoccus as Paracoccus versutus comb. nov. with 60:113–125. emendation of the genus. Microbiol. 141:1469–1477. 60) Nishihara, H., Y. Igarashi, and T. Kodama. 1990. A new isolate 44) Kelly, D.P., and A.P. Wood. 2002. The chemolithotrophic of Hydrogenobacter, an obligately chemolithotrophic, thermo- . The Prokaryotes (Dworkin M., ed.), http:// philic, halophilic and aerobic hydrogen-oxidizing bacterium from 141.150.157.117:8080/prokPUB/chaprender/jsp/showchap.jsp? a seaside saline hot spring. Arch. Microbiol. 153:294–298. %20chapnum=246 61) Oremland, R.S., S.E. Hoeft, J.M. Santini, N. Bano, R.A. Holli- 45) King, G.M. 1999. Characteristics and significance of atmospheric baugh, and J.T. Hollibaugh. 2002. Anaerobic oxidation of arsen- carbon monoxide consumption by soils. Chemosphere: Global ite in Mono Lake water by a facultative arsenite-oxidizing Change Sci. 1:53–63. chemoautotroph strain MLHE-1. Appl. Environ. Microbiol. 46) King, G.M. 2003. Contributions of atmospheric CO and hydro- 68:4795–4802. gen uptake to microbial dynamics on recent Hawaiian volcanic 62) Radajewski, S., P. Ineson, N.R. Parekh, and J.C. Murrell. 2000. deposits. Appl. Environ. Microbiol. 69:4067–4075. Stable-isotope probing as a tool in . Nature 47) King, G.M. 2003. Molecular and culture-based analyses of aero- (Lond.) 403:646–649. bic carbon monoxide oxidizer diversity. Appl. Environ. Micro- 63) Raich, J.W., A.E. Russell, and P.M. Vitousek. 1996. Both nitro- biol. 69:7257–7265. gen and limit plant production on young Hawaiian 48) King, G.M. 2007. Nitrate-dependent anaerobic oxidation of car- lava flows. Biogeochem. 32:1–14. bon monoxide. FEMS Microbiol. Ecol. 59:2–9. 64) Rawling, D.E. 2002. Heavy metal mining using microbes. Annu. 49) King, G.M., and C.F. Weber. 2007. Distribution, diversity and Rev. Microbiol. 56:65–91. ecology of aerobic CO-oxidizing bacteria. Nature Reviews 65) Reysenbach, A.-L., Y. Liu, A.B. Banta, T.J. Beveridge, J.D. Kir- Microbiol. 5:107–118. shtein, S. Schouten, M.K. Tivey, K.L. Von Damm, and M.A. 50) Kusano, T., T. Takeshima, C. Inoue, and K. Sugawara. 1991. Evi- Voytek. 2006. A ubiquitous thermoacidophilic archaeon from dence of two sets of structural genes coding for ribulose bisphos- deep-sea hydrothermal vents. Nature (Lond.) 442:444–447. phate carboxylase/oxygenase in Thiobacillus ferrooxidans. J. 66) Riley, R.H., and P.M. Vitousek. 1995. Nutrient dynamics and Bacteriol. 173:7313–7323. nitrogen trace gas flux during ecosystem development in montane 51) Länge, S., R. Scholtz, and G. Fuchs. 1989. Oxidative and reduc- forest. Ecol. 76:292–304. tive acetyl CoA/carbon monoxide dehydrogenase pathway in 67) Rossetti, S., L.L. Blackall, C. Levantesi, D. Uccelletti, and V. Desulfobacterium autotrophicum. Arch. Microbiol. 151:77–83. Tandoi. 2003. Phylogenetic and physiological characterization of 52) Larkin, J.M., and W.R. Strohl. 1983. Beggiotoa, Thiothrix, and a heterotrophic, chemolithoautotrophic Thiothrix strain isolated Thioploca. Annu. Rev. Microbiol. 37:341–367. from activated sludge. Int. J. Syst. Evol. Microbiol. 53:1271– 53) Lutz, R.A., and M.J. Kennish. 1993. Ecology of deep-sea hydro- 1276. thermal vent communities: a review. Rev. Geophys. 31:211–242. 68) Santini, J.M., L.I. Sly, R.D. Schnagl, and J.M. Macy. 2000. A 54) Moissl, C., C. Rudolph, and R. Huber. 2002. Natural communi- new chemolithotrophic arsenite-oxidizing bacterium isolated ties of novel archaea and bacteria with a string-of-pearls-like from a gold mine: phylogenetic, physiological and preliminary morphology: molecular analysis of the bacterial partners. Appl. biochemical studies. Appl. Environ. Microbiol. 66:92–97. Environ. Microbiol. 68:933–937. 69) Sievert, S.M., T. Brinkhoff, G. Muyzer, W. Ziebis, and J. Kuever. 55) Moran, M.A., A. Buchan, J.M. Gonzalez, J.F. Heidelberg, W.B. 1999. of bacterial along an Whitman, R.P. Kiene, J.R. Henriksen, G.M. King, R. Belas, C. environmental gradient at a shallow submarine hydrothermal vent Fuqua, L. Brinkac, M. Lewis, S. Johri, B. Weaver, G. Pai, J.A. near Milos (Greece). Appl. Environ. Microbiol. 3834– Eisen, E. Rahe, W.M. Sheldon, W. Ye, T.R. Miller, J. Carlton, 3842. D.A. Rasko, I.T. Paulsen, Q. Ren, S.C. Daughterty, R.T. Deboy, 70) Shima, S., and K. Suzuki. 1993. Hydrogenobacter acidophilus sp. R.J. Dodson, A.S. Durkin, R. Madupu, W.C. Nelson, S.A, Sulli- nov., a thermoacidophilic, aerobic, hydrogen-oxidizing bacterium van, M.J. Rosovitz, D.H. Haft, J. Selengut, and N. Ward. 2004. requiring elemental sulfur for growth. Int. J. Syst. Bacteriol. Genome sequence of Silicibacter pomeroyi reveals to 43:703–708. the marine environment. Nature (Lond.) 432:910–913. 71) Shively, J.M., G. van Keulen, and W.G. Meijer. 1998. Something 56) Nanba, K., G.M. King, and K. Dunfield. 2004. Analysis of facul- from almost nothing: Carbon dioxide fixation in chemoautotro- tative distribution and diversity on volcanic deposits by phs. Annu. Rev. Microbiol. 52:191–230. use of the large subunit of ribulose-1,5-bisphosphate carboxylase/ 72) Smith, D.R., L.A. Doucette-Stamm, C. Deloughery, H. Lee, J. oxygenase. Appl. Environ. Microbiol. 70:2245–2253. Dubois, et al. 1997. Complete genome sequence of Methanobac- 57) Nelson, D.C., C.O. Wirsen, and H.W. Jannasch. 1989. Character- terium thermoautotrophicum DH: functional analysis and com- ization of large autotrophic Beggiatoa spp. abundant at hydro- parative genomics. J. Bacteriol. 179:7135–7155. thermal vents of the Guaymas Basin. Appl. Environ. Microbiol. 73) Sokolova, T.G., J.M. Gonzalez, N.A. Kostrikina, N.A. Chernyh, 55:2909–2917. T.V. Slepova, E.A. Bonch-Osmolovskaya, and F.T. Robb. 2004. Chemolithotrophs and Volcanic Environments 319

Thermosinus carboxidovorans gen. nov., sp. nov., a new anaero- 81) Uchino, Y., and A. Yokota. 2003. “Green-like” and “red-like” bic, thermophilic carbon-monoxide-oxidizing, hydrogenogenic RuBisCO cbbL genes in Rhodobacter azotoformans. Mol. Biol. bacterium from a hot pool of Yellowstone National Park. Int. J. Evol. 20:821–830. Syst. Evol. Microbiol. 54:2353–2359. 82) Utaker, J.B., K. Anderson, A. Aakra, B. Moen, and L.F. Nes. 74) Sorokin, D.Y., T.P. Tourova, E.M. Spiridonova, F.A. Rainey, and 2002. Phylogeny and functional expression of ribulose 1,5-bis- G. Muyzer. 2005. Thioclava pacifica gen. nov., sp. nov., a novel phosphate carboxylase/oxygenase from autotrophic ammonia- facultatively autotrophic, marine, sulfur-oxidizing bacterium oxidation bacterium Nitrosopira sp. isolate 40KI. J. Bacteriol. from a near-shore sulfide hydrothermal area. Int. J. Syst. Evol. 184:468–478. Microbiol. 55:1069–1075. 83) Watson, G.M.F., J.P. Yu, and F.R. Tabita. 1999. Unusual ribu- 75) Tabita, F.R. 1999. Microbial ribuolise 1,5-bisphosphate carboxy- lose-1,5-bisphosphate carboxylase/oxygenase of anoxic archaea. lase/oxygenase: A different perspective. Photosyn. Res. 60:1–28. J. Bacteriol. 181:1569–1575. 76) Takai, K., K.H. Nealson, and K. Horikoshi. 2004. Hydrogenimo- 84) Weber, K.A., J. Pollock, K.A. Cole, S.M. O’Conner, L.A. Achen- nas thermophila gen. nov., sp. nov., a novel thermophilic, hydro- bach, and J.D. Coates. 2006. Anaerobic nitrate-dependent iron gen-oxidizing chemolithotroph within the ε-Proteobacteria, iso- (II) bio-oxidation by a novel lithoautotrophic betaproteobacte- lated from a black smoker in a Central Indian Ridge hydrothermal rium, strain 2002. Appl. Environ. Microbiol. 72:686–694. field. Int. J. Syst. Evol. Microbiol. 54:25–32. 85) Wheat, G.C., H.W. Jannasch, J.N. Plant, C.L. Moyer, F.J. San- 77) Takai, K., H. Hirayama, T. Nakagawa, Y. Suzuki, K.H. Nealson, sone, and G.M. McMurtry. 2000. Continuous sampling of hydro- and K. Horikoshi. 2005. Lebetimonas acidiphila gen. nov., sp. thermal fluids from Loihi seamount after the 1996 event. J. Geo- nov., a novel thermophilic, acidiphilic, hydrogen-oxidizing chem- phys. Res. 105:19353–19367. olithoautotroph within the “Epsilonproteobacteria”, isolated 86) Whitaker, R.J., D.W. Grogan, and J.W. Taylor. 2003. Geographic from a deep-sea hydrothermal fumarole in the Mariana Arc. Int. J. barriers isolate endemic populations of hyperthermophilic Syst. Evol. Microbiol. 55:183–189. Archaea. Science 301:976–978. 78) Taylor, G.T., M. Iabichella, T.-Y. Ho, M.I. Scranton, R.C. 87) Wirsen, C.O., H.W. Jannasch, and S.J. Molyneaux. 1993. Thunell, F. Mueller-Karger, and R. Varela. 2001. Chemoautotro- Chemosynthetic microbial activity at Mid-Atlantic Ridge hydro- phy in the redox transition zone of the Cariaco Basin: a signifi- thermal vent sites. J. Geophys. Res. 98:9693–9703. cant midwater source of organic carbon production. Limnol. 88) Wu, M., Q. Ren, A.S. Durkin, S.C. Daugherty, L.M. Brinkac, R.J. Oceanogr. 46:148–163. Dodson, R. Madupu, S.A. Sullivan, J.F. Kolonay, W.C. Nelson, 79) Teske, A., T. Brinkhoff, G. Muyzer, D.P. Moser, J. Rethmeier, L.J. Tallon, K.M. Jones, L.E. Ulrich, J.M. Gonzalez, I.B. Zhulin, and H.W. Jannasch. 2000. Diversity of thiosulfate-oxidizing bac- F.T. Robb, and J.A. Eisen. 2005. Life in hot carbon monoxide: teria from marine sediments and hydrothermal vents. Appl. Envi- the complete genome sequence of Carboxydothermus hydrogeno- ron. Microbiol. 66:3125–3133. formans Z-290. 1:563–574. 80) Tolli, J., and G.M. King. 2005. Diversity and structure of bacte- 89) Zhang, H., M.A. Bruns, and B.E. Logan. 2002. Perchlorate reduc- rial chemolithotrophic communities in pine forest and agroeco- tion by a novel chemolithoautotrophic, hydrogen-oxidizing bacte- system soils. Appl. Environ. Microbiol. 71:8411–8418. rium. Environ. Microbiol. 4:570–576.