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Sulfur Metabolisms in Epsilon- and Gamma-Proteobacteria in Deep-Sea Hydrothermal Fields

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Sulfur Metabolisms in Epsilon- and Gamma-Proteobacteria in Deep-Sea Hydrothermal Fields 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-Proteobacteria 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 Bacteria (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 Frontiers in Microbiology Table 1 | Sulfur metabolic genes in epsilon- and gamma-Proteobacteria isolated or identified from deep-sea hydrothermal fields. Organism, isolation, or Genome accession Growth tem- Electron Electron Genes Locus tag Pathways observation site number*1 perature (˚C) donor acceptor EPSILON-PROTEOBACTERIA 0 2− 0 - Sulfurovum sp. NBC37-1 AP009179 30–37 H2,S ,S2O3 S ,NO3 ,O2 psrACB SUN0510-0508 Sulfur respiration Nakagawa et al. | Microbial Physiology and Metabolism Sediment, Mid-Okinawa (2005, 2007) Trough soxXYZAB SUN0497-0501 Sox system Yamamoto et al. (2010) soxCDYZ SUN0049-0052 Sox system soxJ SUN0058, 1338 Sox system (?) sqr SUN0047, 0073, Sulfide oxidation 0192 sorAB SUN1104-1103, Sulfite oxidation 1476-1477 0 2− 0 - Nitratiruptor sp. SB155-2 AP009178 55 H2,S ,S2O3 S ,NO3 ,O2 psrACB NIS0573-0571 Sulfur respiration Nakagawa et al. Sediment, Mid-Okinawa (2005, 2007) Trough soxXYZAB NIS1832-1828 Sox system soxYZ NIS0034-0035 Sox system soxJ NIS0032 Sox system (?) sqr NIS0146, 0158, Sulfide oxidation 0326 Sulfur metabolism in hydrothermal epsilon- and gamma- 0 Nautilia profundicola AmH CP001279 45 H2, formate S psrABC NAMH1518-1520 Sulfur respiration Campbell et al. Alvinella tube, East Pacific (2001, 2009) Rise 0 Sulfurimonas autotrophica CP002205 25 H2S, S , O2 psrACB Saut1622-1644 Sulfur respiration Inagaki et al. 2− DSM16294 Sediment, S2O3 (2003) Mid-Okinawa Trough soxXYZAB Saut0991-0995 Sox system September 2011 | Volume 2 | Article 192 | soxCDYZ Saut2096-2099 Sox system soxJ Saut1356 Sox system (?) sqr Saut0503, 1543 Sulfide oxidation sorAB Saut1022-1023 Sulfite oxidation 2− - Sulfurimonas denitrificans CP000153 25 S2O3 NO3 psrACB Suden0500-0498 Sulfur respiration Sievert et al. DSM1251 Tidal flat mud, (2008) Dutch Wadden Sea*2 soxXYZAB Suden0260-0264 Sox system Proteobacteria soxCDYZ Suden2060-2057 Sox system soxJ Suden2049 Sox system (?) sqr Suden0619 Sulfide oxidation 2 Yamamoto and Takai www.frontiersin.org Alvinella episymbiont East AAUQ 10-65 ND ND psrAB ND Sulfur respiration Grzymski et al. Pacific Rise (2008) 01000000*3 soxXYZABCD ND Sox system D ND Sox system (?) soxJ GAMMA-PROTEOBACTERIA 0 Thiomicrospira crunogena CP000109 33 H2,H2S, S , O2 soxXYZA Tcr0604-0601 Sox system Scott et al. (2006) 2− XCL-2 Galapagos Rift vent S2O3 soxB Tcr1549 Sox system soxCD Tcr0156-0157 Sox system sqr Tcr0619 Sulfide oxidation CoSym Vesicomyosocious AP009247 ND ND ND soxXYZA COSY0733-0730 Sox system Kuwahara et al. symbiont (2007) soxB COSY 0161 Sox system soxJ COSY0750 Sox system (?) sqr COSY0953 Sulfide oxidation dsrAB COSY0795-0794 Reverse sulfate reduction aprAB COSY0092-0091 Reverse sulfate reduction sat COSY0089 Reverse sulfate reduction Ruthia magnifica Calyptogena CP000488 ND ND ND soxXYZA Rmag0808-0805 Sox system Newton et al. symbiont (2007) Sulfur metabolism in hydrothermal epsilon- and gamma- soxB Rmag0156 Sox system soxJ Rmag0824 Sox system (?) sqr Rmag1053 Sulfide oxidation dsrAB Rmag0870-0869 Reverse sulfate reduction aprAB Rmag0088-0087 Reverse sulfate reduction September 2011 | Volume 2 | Article 192 | sat Rmag0085 Reverse sulfate reduction Endoriftia persephone Riftia AASF ND ND ND soxXAB*4 ND Sox system Robidart et al. symbiont (2008) 00000001*3 dsrAB ND Reverse sulfate reduction aprAB ND Reverse sulfate reduction Proteobacteria sat ND Reverse sulfate reduction (Continued) 3 Yamamoto and Takai Frontiers in Microbiology | Microbial Physiology and Metabolism Table 1 | Continued Organism, isolation, or Genome accession Growth tem- Electron Electron Genes Locus tag Pathways observation site number*1 perature (˚C) donor acceptor Beggiatoa spp. Sediment, ABBY ND ND ND soxXYZAB ND Sox system Mußmann et al. Baltic Sea (2007) 00000000, fccAB ND Sulfide oxidation ABBBZ sqr ND Sulfide oxidation 00000000*5 dsrAB ND Reverse sulfate reduction aprAB
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