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Minireview Chemolithotrohic Bacteria Microbes Environ. Vol. 22, No. 4, 309–319, 2007 http://wwwsoc.nii.ac.jp/jsme2/ Minireview Chemolithotrohic Bacteria: 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 sulfur-containing compounds. These systems, 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 ecology and physiology. 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 carbon monoxide, hydrogen or both. These gases can support metabolism of facultative chemolithotrophs, a functional group that includes many nitrogen-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 nitrogen fixation and interactions with vascu- lar plants. 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 lithotrophs. 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, biogeochemistry 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- biology, 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 energy for ATP synthesis, slow in coming, even though the list of substrates that could but cell 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 organisms that use only inorganic energy sources (electron donors) and inorganic carbon for biomass, 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 ammonium O2 Nitrosomonas europea 12 ammonium nitrite Brocadia anammoxidans 42 sulfide, thiosulfate O2, nitrate 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 ammonia oxidation were first described as oxygen 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, mixotrophs 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 animal 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 food have been previously appreciated. Several chem- webs largely independent of photosyntetically-derived olithotrophic or predominantly chemolithotrophic lineages organic matter. 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 Earth’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 habitats, 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
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