View metadata, citation and similar papers at core.ac.uk brought to you by CORE MINI REVIEW ARTICLE published: 20 September 2011 provided by PubMed Central doi: 10.3389/fmicb.2011.00192 Sulfur metabolisms in epsilon- and gamma- in deep-sea hydrothermal fields

MasahiroYamamoto1,2* and KenTakai 1,2

1 Subsurface Geobiology Advanced Research Project, Japan Agency for Marine-Earth Science and Technology, Yokosuka, Japan 2 Precambrian Ecosystem Laboratory, Japan Agency for Marine-Earth Science and Technology, Yokosuka, Japan

Edited by: In deep-sea hydrothermal systems, super hot and reduced vent fluids from the subseafloor Niels-Ulrik Frigaard, University of blend with cold and oxidized seawater. Very unique and dense ecosystems are formed Copenhagen, Denmark within these environments. Many molecular ecological studies showed that chemoau- Reviewed by: Masaharu Ishii, University of Tokyo, totrophic epsilon- and gamma-Proteobacteria are predominant primary producers in both Japan free-living and symbiotic microbial communities in global deep-sea hydrothermal fields. Biswarup Mukhopadhyay, Virginia Inorganic sulfur compounds are important substrates for the energy conservative meta- Bioinformatics Institute, USA bolic pathways in these microorganisms. Recent genomic and metagenomic analyses and *Correspondence: biochemical studies have contributed to the understanding of potential sulfur metabolic Masahiro Yamamoto, Institute of Biogeosciences, Japan Agency for pathways for these chemoautotrophs. Epsilon-Proteobacteria use sulfur compounds for Marine-Earth Science and Technology, both electron-donors and -acceptors. On the other hand, gamma-Proteobacteria utilize two 2-15 Natsushima-cho, 237-0061 different sulfur-oxidizing pathways. It is hypothesized that differences between the meta- Yokosuka, Japan. bolic pathways used by these two predominant proteobacterial phyla are associated with e-mail: [email protected] different ecophysiological strategies; extending the energetically feasible habitats with ver- satile energy metabolisms in the epsilon-Proteobacteria and optimizing energy production rate and yield for relatively narrow habitable zones in the gamma-Proteobacteria.

Keywords: deep-sea hydrothermal vents, energy metabolism, chemoautotroph

INTRODUCTION sulfide abundantly contained in the hydrothermal fluids repre- The deep-sea hydrothermal system is one of the most extreme sented the dominating energy source in the mesophilic deep-sea environments on Earth. It is characterized by darkness, high pres- vent chemoautotrophic ecosystems (McCollom and Shock, 1997). sures, and steep physical and chemical gradients formed in mixing In addition, partially oxidized inorganic sulfur compounds such zones between hot hydrothermal vent fluid and cold deep-sea as polysulfide, elemental sulfur, and thiosulfate are generated in water. Very unique and dense communities of invertebrates are the in situ mixing zones, and serve as both electron donor and sustained in absence of a photosynthetic energy source (Dubilier acceptor in a variety of energy metabolisms. The chemical and et al., 2008). Almost all vent-endemic animals are strongly asso- microbial oxidation and reduction reactions of sulfur compounds ciated with the primary production of the endo- and/or epi- probably establish the overall complex sulfur metabolism network symbiotic chemoautotrophic microorganisms (Jeanthon, 2000). in the ecosystem. This article reviews the representative microbial With the discovery of deep-sea hydrothermal ecosystem in 1977, components capable of utilizing the inorganic sulfur compounds it had been proposed that hydrogen sulfide-oxidizing and oxygen- as the energy sources in the deep-sea hydrothermal environments reducing chemoautotrophs potentially sustain the primary pro- and highlights the biochemical and genetic components of their duction in these unique ecosystems (Kvenvolden et al., 1979). metabolisms. In addition, the possible segregation of different However, anoxic hydrothermal fluids contain several reduced sulfur metabolic pathways and their host chemoautotrophic Pro- compounds such as H2,CH4, and reduced metal ions in addition teobacteria associated with the physical and chemical transition in to H2S(Jannasch and Mottl, 1985). Recent cultivation studies have the mixing zones of the deep-sea hydrothermal environments is demonstrated that these chemicals are all used as energy sources discussed. for chemoautotrophs (Jannasch and Mottl, 1985; Nakagawa et al., 2005; Campbell et al., 2006; Emerson et al., 2007), indicating the MICROBIAL COMMUNITIES IN DEEP-SEA HYDROTHERMAL great diversity of chemoautotrophic energy metabolic processes FIELDS in the ecosystems. Hydrogen gas (H2) is one of the most impor- Recent culture-independent analyses of the both symbiotic tant energy sources, and the hydrogen-dependent ecosystems may and free-living microbial communities in the various deep-sea represent analogs for the earliest biological communities on Earth hydrothermal environments have revealed a great phylogenetic (Takai et al., 2004, 2006b; Nealson et al., 2005). diversity of Archaea and (Takai et al., 2006a); these Hydrogen sulfide or sulfide is primarily supplied via high analyses have also indicated a predominance in biomass of mem- temperatures of seawater–rock interactions in the subseafloor bers within the gamma-Proteobacteria and epsilon-Proteobacteria hydrothermal reaction zones (Jannasch and Mottl, 1985). (Stewart et al., 2005; Suzuki et al., 2005; Urakawa et al., 2005; Thermodynamic modeling indicated that the hydrogen sulfide or Campbell et al., 2006; Nakagawa and Takai, 2008; Table 1). Based

www.frontiersin.org September 2011 | Volume 2 | Article 192 | 1 Yamamoto and Takai Sulfur metabolism in hydrothermal epsilon- and gamma-Proteobacteria (2010) Nakagawa et al. (2005, 2007) Nakagawa et al. (2005, 2007) Campbell et(2001, 2009) al. Inagaki et(2003) al. Sievert et(2008) al. Yamamoto et al. Sulfide oxidation Sulfite oxidation Sulfide oxidation SUN0049-0052SUN0058, 1338 Sox system SUN0047, 0073, Sox system (?) 0192 SUN1104-1103, 1476-1477 SUN0510-0508 Sulfur respiration SUN0497-0501 Sox system NIS0573-0571 Sulfur respiration NIS1832-1828NIS0034-0035 Sox system NIS0032 Sox system NIS0146, 0158, 0326 NAMH1518-1520 Sox system (?) Sulfur respiration Saut1622-1644 Sulfur respiration Saut0991-0995Saut2096-2099 Sox system Saut1356 Sox system Saut0503, 1543Saut1022-1023 Sulfide oxidation Suden0500-0498 Sox system (?) Sulfite oxidation Sulfur respiration Suden0260-0264 SoxSuden2060-2057 system SoxSuden2049 system Suden0619 Sox system (?) Sulfide oxidation Genes Locus tag Pathways soxJ sqr sorAB soxCDYZ psrACB psrACB soxYZ soxJ sqr psrABC psrACB soxCDYZ soxJ sqr sorAB psrACB soxCDYZ soxJ sqr soxXYZAB soxXYZAB soxXYZAB soxXYZAB 2 2 ,O ,O - - 3 3 - 3 ,NO ,NO 2 0 0 0 Electron acceptor S S O NO − − 2 3 2 3 O O 2 2 , 0 ,S ,S 0 0 − − 2 3 2 3 ,S ,S , formate S S, S O O 2 2 2 2 2 2 Electron donor S isolated or identified from deep-sea hydrothermal fields. Growth tem- perature (˚C) Proteobacteria 1 Genome accession number* CP000153 25 S CP001279 45 H CP002205 25 H AP009179 30–37 H AP009178 55 H AmH *2 sp. SB155-2 sp. NBC37-1 PROTEOBACTERIA tube, East Pacific EPSILON- Sulfurovum Sediment, Mid-Okinawa Organism, isolation, or observation site Nitratiruptor Sediment, Mid-Okinawa Rise Nautilia profundicola Sulfurimonas denitrificans DSM1251 Tidal flat mud, Dutch Wadden Sea Sulfurimonas autotrophica DSM16294 Sediment, Mid-Okinawa Trough Alvinella Trough Trough Table 1 | Sulfur metabolic genes in epsilon- and gamma-

Frontiers in Microbiology | Microbial Physiology and Metabolism September 2011 | Volume 2 | Article 192 | 2 Yamamoto and Takai Sulfur metabolism in hydrothermal epsilon- and gamma-Proteobacteria (Continued) Grzymski et(2008) al. Kuwahara et(2007) al. Scott et al. (2006) Robidart et(2008) al. Newton et(2007) al. Reverse sulfate reduction reduction Reverse sulfate reduction reduction reduction Reverse sulfate reduction reduction Reverse sulfate reduction Reverse sulfate reduction ND Sulfur respiration COSY0733-0730 SoxCOSY system 0161COSY0750COSY0953COSY0795-0794 Sox system Sox system (?) Sulfide oxidation NDND Sox system Sox system (?) ND Reverse sulfate COSY0092-0091 ND Sox system ND Reverse sulfate Rmag0156Rmag0824Rmag1053Rmag0870-0869 Sox system Sox system (?) Sulfide oxidation COSY0089Rmag0808-0805 Reverse sulfate Sox system ND Reverse sulfate Rmag0088-0087 Rmag0085 Tcr0604-0601 Sox system Tcr1549Tcr0156-0157Tcr0619 Sox system Sox system Sulfide oxidation *4 psrAB soxXYZA soxB soxJ sqr dsrAB soxXYZABCD D soxJ soxXYZA dsrAB soxB soxCD sqr aprAB aprAB soxB soxJ sqr dsrAB sat soxXYZA sat aprAB sat soxXAB 2 O , 0 S, S 2 − 2 3 ,H O 2 2 S *3 *3 CP000109 33 H 01000000 00000001 CP000488 ND ND ND AAUQ 10-65 ND ND AP009247 ND ND ND AASF ND ND ND PROTEOBACTERIA episymbiont East Vesicomyosocious GAMMA- XCL-2 Galapagos Rift vent Pacific Rise CoSym symbiont Ruthia magnifica Calyptogena symbiont Endoriftia persephone Riftia symbiont Alvinella Thiomicrospira crunogena

www.frontiersin.org September 2011 | Volume 2 | Article 192 | 3 Yamamoto and Takai Sulfur metabolism in hydrothermal epsilon- and gamma-Proteobacteria Mußmann et al. (2007) -phosphosulfate reductase; reduction reduction reduction respiration y sulfite reductase; apr, adenosine 5 NDNDND Sox system Sulfide oxidation Sulfide oxidation NDNDND Reverse sulfate ND ReverseND sulfate Reverse sulfate DMSO respiration Thiosulfate soxXYZAB fccAB sqr Genes Locus tag Pathways dsrAB aprAB sat dmsABC phsABC Electron acceptor Electron donor Growth tem- perature (˚C) *5 1 00000000, Genome accession number* 00000000 ABBYABBBZ ND ND ND spp. Sediment, Deposited in DDBJ/EMBL/GenBank databases. It is not a hydrothermal field. For which the metagenome sequence isSoxXAB published. were detected, but not SoxYZ. Sequence assembles were incomplete. sat, sulfate adenylyltransferase; dms, dimethyl sulfoxide reductase; phs, thiosulfate reductase. Organism, isolation, or observation site Beggiatoa ND no data, psr, polysulfide reductase; sox, Sox multi enzyme system;*1 sqr, sulfide:quinone oxidoreductase; fcc, flavocytochrome c; dsr,*2 dissimilator *3 *4 *5 Baltic Sea Table 1 | Continued

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on the culture-dependent characterization and genetic compo- sulfur-oxidation pathways that will not be further described here nents analyses, these Proteobacteria are found to be chemoau- (see Ghosh and Dam, 2009). totrophs strongly associated with utilization of inorganic sulfur Sulfur-reduction pathways can be classified into two types compounds (Durand et al., 1993; Inagaki et al., 2003, 2004; Takai based on the substrates: (1) sulfur-reduction (sulfur respiration), et al., 2003b, 2006a,c). Therefore, the sulfur-related energy metab- and (2) sulfate reduction (sulfate respiration). Sulfur-reduction olisms in these Proteobacteria are important traits for understand- pathways have been intensively studied in gastrointestinal epsilon- ing ecology and biogeochemistry in deep-sea hydrothermal vent Proteobacterium, Wolinella succinogenes (Wolin et al., 1961; Hed- ecosystems. derich et al., 1999). Sulfur-reduction is catalyzed by polysulfide reductase (Psr), in which the actual substrate of the reaction is MICROBIAL SULFUR METABOLIC PATHWAYS FOR ENERGY polysulfide but not elemental sulfur (Pfennig and Biebel, 1986). CONSERVATION Sulfate reducing bacteria are found in several different phylo- Inorganic sulfur compounds are used as both electron donor and genetic lines (e.g., delta-Proteobacteria, Clostridia, Thermodesul- acceptor by microorganisms. Sulfur-oxidation pathways have been fobacteria, and Nitrospirae; Muyzer and Stams, 2008). Sat, Apr, well studied biochemically in anaerobic phototrophs (e.g., Chloro- and Dsr catalyze the reduction of sulfate to sulfide. bium and Allochromatium), facultatively chemoautotrophic Pro- teobacteria (e.g., Acidithiobacillus and Paracoccus) and Sulfolobales SULFUR METABOLISM IN EPSILON-PROTEOBACTERIA IN (e.g., Sulfolobus and Acidianus; Friedrich, 1998; Kletzin et al., 2004; DEEP-SEA HYDROTHERMAL FIELDS Friedrich et al., 2005; Frigaard and Dahl, 2009). Bacterial sulfur- The most well known epsilon-Proteobacteria are gastrointesti- oxidation pathways under the neutral pH are generally classified nal pathogens such as Helicobacter and Campylobacter.Theyare into two different types: (1) reverse sulfate reduction, and (2) Sox heterotrophic and do not have inorganic sulfur metabolic path- multienzyme system. Reverse sulfate reduction is reversal of sulfate ways. The genus Wolinella isolated from cattle rumen can reduce reduction pathway,in which sulfide is oxidized to sulfate via sulfite. elemental sulfur to hydrogen sulfide (Wolin et al., 1961). This pathway uses the same families of enzymes as of the sulfate There are many reports that chemoautotrophic epsilon- reduction pathway, such as dissimilatory sulfite reductase (Dsr), Proteobacteria are predominant in sulfidic environments such adenylphosphosulfate reductase (Apr), and sulfate adenylyltrans- as deep-sea hydrothermal and subsurface environments (Takai ferase (Sat; Kappler and Dahl, 2001). Sox multienzyme complex et al., 2004; Campbell et al., 2006; Nakagawa and Takai, 2008). catalyzes oxidation of inorganic sulfur compounds. Four protein Recently, whole genome sequences of five strains of marine components, SoxYZ, SoxXA, SoxB, and SoxCD are required for epsilon-Proteobacteria,i.e.,Sulfurovum sp. NBC37-1,Nitratiruptor complete oxidation of sulfide and thiosulfate to sulfate (Com- sp. SB155-2, Nautilia profundicola AmH, Sulfurimonas autotroph- plete Sox pathway; Friedrich et al., 2001). However, the sulfur ica DSM16294 isolated from deep-sea hydrothermal fields, and S. oxidizers that possess the soxYZXAB genes but not soxCD have denitrificans DSM1251 isolated from a coastal wetland, have been oftenbeenreported(Friedrich et al., 2005). It is considered that determined (Nakagawa et al., 2007; Sievert et al., 2008; Campbell SoxCD acts as sulfur dehydrogenase. Sox system without SoxCD et al., 2009; Table 1). Moreover, the metabolism of episymbion- − is able to oxidize sulfite and sulfone group ( - SO3 ) in thiosul- tic epsilon-Proteobacterium in a polychaete worm was analyzed by fate, but not sulfide, elemental sulfur, and sulfane sulfur (-S−) metagenomic analysis (Grzymski et al., 2008). In addition, sev- in thiosulfate (Friedrich et al., 2001). In addition to these two eral biochemical studies on sulfur metabolic pathways in deep-sea sulfur-oxidation pathways, several enzymes have been proposed epsilon-Proteobacteria have also been reported (Takai et al., 2005; to oxidize inorganic sulfur compounds, including sulfide:quinone Yamamoto et al., 2010). oxidoreductase (Sqr), flavocytochrome c (Fcc), and sulfite oxidase Genetic and enzymatic components characterized by the (SO), though the exact physiological functions are still debated. genomic and biochemical analyses of deep-sea epsilon- Sqr is a single-subunit flavoprotein that catalyzes oxidation of sul- Proteobacteria have facilitated considerable progress in determin- fide to elemental sulfur (Shahak and Hauska, 2008; Frigaard and ing the possible sulfur metabolism pathways of the deep-sea Dahl, 2009). Recent protein structural study divided Sqr family chemoautotrophic epsilon-Proteobacteria (Table 1). The deep-sea into six groups (Marcia et al., 2010). These different types of Sqr epsilon-Proteobacteria characterized so far possess (1) a hydrogen- probably have different mechanisms and physiological roles (Chan oxidizing sulfur respiration pathway using hydrogenase and poly- et al., 2009; Gregersen et al., 2011; Holkenbrink et al., 2011). Fcc sulfide reductase (Psr). And the epsilon-Proteobacteria except for also catalyzes oxidation of sulfide to elemental sulfur, but elec- N. profundicola AmH, possess (2) a sulfur compounds-oxidizing trons are transferred to the level of cytochrome c (Oh-oka and oxygen/nitrate-respiration pathway using the Sox multienzyme Blankenship, 2004). Fcc consists of a flavoprotein subunit, FccB, system. Both of the Sox systems coupled with and without SoxCD and a c-type cytochrome subunit, FccA (Kusai and Yamanaka, have been found. The sox genes are not organized in a single 1973; Reinartz et al., 1998). The soxEF genes conserved in the sox region, but at least in two separated regions of the soxXYZAB gene clusters are homologous genes of the fccAB genes (Friedrich and sox(CD)YX genes. One or more soxF gene was conserved et al., 2008). The soxJ gene is a homologous gene of fccB/soxF, in each sox gene cluster. Sulfurovum sp., Nitratiruptor sp., and S. that does not cluster with a homolog of fccA/soxE (Gregersen autotrophica have several sqr genes. Two sets and one set of the et al., 2011). SO is a molybdenum enzyme and catalyzes the sorAB genes coding SO were observed in Sulfurovum sp. and S. direct oxidation of sulfite to sulfate (Kappler and Dahl, 2001). autotrophica, respectively. No gene for sulfur-oxidation pathways Acidophilic sulfur-oxidizing bacteria and archaea use different was found in N. profundicola. In addition to the sulfur metabolic

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pathways, many deep-sea epsilon-Proteobacteria are capable of published (Kuwahara et al., 2007; Newton et al., 2007; Table 1). chemoautotrophic growth without sulfur compounds using a Moreover, the metabolisms of symbiont in tubeworm were ana- third metabolic pathway: (3) a hydrogen-oxidizing oxygen/nitrate- lyzed by metagenomic analysis (Robidart et al., 2008). In addition, reduction pathway (Figure 1). The bacterial members that can use a whole genome sequence of free-living sulfur-oxidizing gamma- sulfur compounds as both electron acceptors and donors are iden- Proteobacterium, Thiomicrospira crunogena XCL-2 was also pub- tified only in the phyla of epsilon-Proteobacteria and Aquificae, lished (Scott et al.,2006). Putative metabolic pathways in Beggiatoa both of which predominantly inhabit in deep-sea hydrothermal sp. from marine sediments had also analyzed by using incomplete environments. This may provide an important clue into how genome sequence (Mußmann et al., 2007). From these genome- the versatile energy metabolic pathways are associated with the based genetic characteristics, we can develop a preliminary outline energetic advantages adapted to the dynamic and transient envi- of representative sulfur-related energy metabolisms in the deep- ronmental conditions in the mixing zones of the hydrothermal sea hydrothermal gamma-Proteobacteria,which possess two differ- vent environments. ent sulfur-oxidization pathways: (1) the reverse sulfate reduction using Dsr, Apr, and Sat, and (2) the Sox multienzyme system with- SULFUR METABOLISM IN GAMMA-PROTEOBACTERIA IN out SoxCD (Figure 1). T. crunogena XCL-2, however, is an excep- DEEP-SEA HYDROTHERMAL FIELDS tion, in which no gene for the reverse sulfate reduction pathway Gamma-proteobacterial symbionts with invertebrates have never was found. Moreover, this organism has the soxCD genes separated been isolated from deep-sea hydrothermal vents. Furthermore from other sox genes. In contrast, functional genes amplifica- only a couple of free-living sulfur-oxidizing gamma-Proteobacteria tion studies suggested that hydrothermal gamma-Proteobacteria have been isolated from deep-sea hydrothermal fields (Kuever use the reverse sulfate reduction pathway, but not the Sox path- et al., 2002; Takai et al., 2006c, 2009). Unculturable gamma- way (Hügler et al., 2010). These results indicate that either of the proteobacterial sulfur-oxidizing endosymbionts are classified into two distinct sulfur-oxidization pathways is dispensable. Both of three groups based on their host invertebrates: symbionts of (1) these pathways require O2 as a terminal electron acceptor in most Bathymodiolus mussels and Calyptogena clams, (2) Alvinicon- cases. This fact indicates that the relatively reductive environment cha gastropods, and (3) gastropods (e.g., Ifremeria) and tube- (O2-depleted condition) is inhibitory for the growth of deep-sea worms (Nakagawa and Takai, 2008). In recent years, two genome chemoautotrophic gamma-Proteobacteria due to the limitation sequences of sulfur-oxidizing symbionts in Calyptogena have been of primary electron acceptor despite an increasing abundance of electron-donors (reduced sulfur compounds). Thus, it is predicted that the metabolically habitable spaces of deep-sea chemoau- totrophic gamma-Proteobacteria strictly requiring co-existence of reduced sulfur compounds and O2 are much more limited than those of deep-sea epsilon-Proteobacteria in the mixing zones of hydrothermal environments. Conversely, however, it seems likely that the genomic installation and the biochemical operation of two different sulfur-oxidizing pathways in the deep-sea chemoau- totrophic gamma-Proteobacteria are kinetically advantageous if both the reduced sulfur compounds and O2 are steadily sup- plied into the habitats. Particularly for the gamma-proteobacterial sulfur-oxidizing symbionts, the host invertebrates would prepare the metabolically suitable habitats in and around the bodies in the mixing zones of deep-sea hydrothermal environments (Arp and Childress, 1983; Zal et al., 1998; Numoto et al., 2005). This may be one of the possible rationales for the domination of deep- sea gamma-proteobacterial sulfur-oxidizing chemoautotrophs in symbiotic communities in deep-sea hydrothermal environments. All deep-sea sulfur-oxidizing gamma-Proteobacteria possess one sqr gene in the genome, except for the metagenome of Riftia symbiont. Therefore, Sqr probably has an important role for the sulfur-oxidation in the organisms. It is interesting that genes for FIGURE 1 | Energy metabolic pathways and habitat area of sulfur compound (thiosulfate and dimethyl sulfoxide) respiration epsilon-Proteobacteria and gamma-Proteobacteria in deep-sea were found in genome of Beggiatoa sp. (Mußmann et al., 2007). hydrothermal fields. From left to right on the diagram, the redox conditions shift from reductive to oxidative states. Broken lines in the This is in accordance with previous results in Beggiatoa alba that rectangle indicate inclines in concentration of hydrogen gas, hydrogen can reduce stored elemental sulfur to overcome short-term anoxic sulfide, oxidized sulfur compounds, and oxygen gas, respectively. Two gray conditions (Nelson and Castenholz, 1981; Schmidt et al., 1987). bars indicate habitat area of epsilon-Proteobacteria and gamma-Proteobacteria, respectively. Psr, polysulfide reductase; Sox, Sox CONCLUDING REMARKS multienzyme system; Dsr, dissimilatory sulfite reductase; Apr, adenosine 5-phosphosulfate reductase; Sat, sulfate adenylyltransferase. In this review, we described the sulfur-related energy metabolisms of epsilon- and gamma-Proteobacteria dominating the microbial

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communities in the global deep-sea hydrothermal environments. and Desulfurococcaceae) will be important for understanding the Most of the metabolic characteristics summarized in this article are biogeochemical processes and energy- and elemental fluxes of based on the reconstruction of genetic components in the genomes sulfur compounds in the deep-sea hydrothermal environments determined for only a few representative . Further genetic (Reysenbach et al., 2000, 2002; Teske et al., 2002; Takai et al., and biochemical variability associated with the sulfur-related 2003a). Recently, genetic information has been rapidly accumu- energy metabolisms will be clarified in many species of deep- lating and has been providing the important genetic potential for sea hydrothermal vent epsilon- and gamma-Proteobacteria in the understanding the complex sulfur-related metabolic networks in future. Surely, the investigation of other inorganic sulfur metab- deep-sea hydrothermal vent ecosystems. In contrast, enzymatic olizing groups of microbial components such as sulfate-reducers and biochemical data are highly insufficient to clarify the in vivo (delta-Proteobacteria, Thermodesulfobacteria, and Deferribacteres) and in situ kinetics, operation and control of metabolic pathways. and sulfur-reducing thermophiles (Aquificae, Thermococcaceae, These will be an important focus for future studies.

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H., and Kumagai, H. (2006b). 2:192. doi: 10.3389/fmicb.2011.00192 Sulfide oxidation in the pho- Microbiol. 74, 1145–1156. Ultramafics-Hydrothermalism- This article was submitted to Frontiers in totrophic sulfur bacterium Chro- Stewart, F. J., Newton, I. L., and Hydrogenesis-HyperSLiME Microbial Physiology and Metabolism, a matium vinosum. Arch. Microbiol. Cavanaugh, C. M. (2005). (UltraH3) linkage: a key insight specialty of Frontiers in Microbiology. 170, 59–68. Chemosynthetic endosym- into early microbial ecosystem in Copyright © 2011 Yamamoto and Takai. Reysenbach, A. L., Gotz, D., Banta, A., bioses: adaptations to oxic-anoxic the Archean deep-sea hydrothermal This is an open-access article subject Jeanthon, C., and Fouquet,Y.(2002). interfaces. Trends Microbiol. 13, systems. Paleontol. Res. 10, 269–282. to a non-exclusive license between the Expanding the distribution of the 439–448. Takai, K., Miyazaki, M., Nunoura, authors and Frontiers Media SA, which Aquificales to the deep-sea vents Suzuki, Y., Sasaki, T., Suzuki, M., T., Hirayama, H., Oida, H., permits use, distribution and reproduc- on Mid-Atlantic Ridge and Central Nogi, Y., Miwa, T., Takai, K., Furushima, Y., Yamamoto, H., tion in other forums,provided the original Indian Ridge. Cah. Biol. Mar. 43, Nealson, K. H., and Horikoshi, and Horikoshi, K. (2006c). Sul- authors and source are credited and other 425–428. K. (2005). Novel chemoautotrophic furivirga caldicuralii gen. nov., Frontiers conditions are complied with.

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