Abstract
At deep-sea hydrothermal vents, primary production is carried out by chemolithoautotrophic microorganisms, with the oxidation of reduced sulfur compounds being a major driver for microbial carbon fixation. Dense and highly diverse assemblies of sulfur-oxidizing bacteria (SOB) are observed, yet the principles of niche differentiation between the different SOB across geochemical gradients remain poorly understood. In this study niche differentiation of the key SOB was addressed by extensive sampling of active sulfidic vents at six different hydrothermal venting sites in the Manus Basin, off Papua New Guinea. We subjected 33 diffuse fluid and water column samples and 23 samples from surfaces of chimneys, rocks and fauna to a combined analysis of 16S rRNA gene sequences, metagenomes and real-time in situ measured geochemical parameters. We found Sulfurovum Epsilonproteobacteria mainly attached to surfaces exposed to diffuse venting, while the SUP05-clade dominated the bacterioplankton in highly diluted mixtures of vent fluids and seawater. We propose that the high diversity within Sulfurimonas- and Sulfurovum-related Epsilonproteobacteria observed in this study derives from the high variation of environmental parameters such as oxygen and sulfide concentrations across small spatial and temporal scales.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Akerman NH, Butterfield DA, Huber JA . (2013). Phylogenetic diversity and functional gene patterns of sulfur-oxidizing subseafloor Epsilonproteobacteria in diffuse hydrothermal vent fluids. Front Microbiol 4: 185.
Alain K, Rolland S, Crassous P, Lesongeur F, Zbinden M, le Gall C et al. (2003). Desulfurobacterium crinifex sp. nov., a novel thermophilic, pinkish-streamer forming, chemolithoautotrophic bacterium isolated from a Juan de Fuca Ridge hydrothermal vent and amendment of the genus Desulfurobacterium. Extremophiles 7: 361–370.
Amend JP, McCollom TM, Hentscher M, Bach W . (2011). Catabolic and anabolic energy for chemolithoautotrophs in deep-sea hydrothermal systems hosted in different rock types. Geochim Cosmochim Acta 75: 5736–5748.
Anantharaman K, Breier JA, Dick GJ . (2016). Metagenomic resolution of microbial functions in deep-sea hydrothermal plumes across the Eastern Lau Spreading Center. ISME J 10: 225–239.
Anderson MJ . (2001). A new method for non-parametric multivariate analysis of variance. Austral Ecol 26: 32–46.
Anderson RE, Beltran MT, Hallam SJ, Baross JA . (2013). Microbial community structure across fluid gradients in the Juan de Fuca Ridge hydrothermal system. FEMS Microbiol Ecol 83: 324–339.
Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA et al. (2008). The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9: 75.
Bach W, Edwards KJ, Hayes JM, Huber JA, Sievert SM, Sogin ML . (2006). Energy in the dark: fuel for life in the deep ocean and beyond. Eos Trans Am Geophys Union 87: 73–78.
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS et al. (2012). SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19: 455–477.
Baross JA, Hoffman SE . (1985). Submarine hydrothermal vents and associated gradient environments as sites for the origin and evolution of life. Origins Life Evol Biosph 15: 327–345.
Beier C, Bach W, Turner S, Niedermeier D, Woodhead J, Erzinger J et al. (2015). Origin of silicic magmas at spreading centres - an example from the South East Rift, Manus Basin. J Petrol 56: 255–271.
Bemis K, Lowell RP, Farough A . (2012). Diffuse flow on and around hydrothermal vents at mid-ocean ridges. Oceanography 25: 182–191.
Binns RA, Scott SD . (1993). Actively forming polymetallic sulfide deposits associated with felsic volcanic-rocks in the Eastern Manus back-arc basin, Papua-New-Guinea. Econ Geol 88: 2226–2236.
Bourbonnais A, Juniper SK, Butterfield DA, Devol AH, Kuypers MMM, Lavik G et al. (2012). Activity and abundance of denitrifying bacteria in the subsurface biosphere of diffuse hydrothermal vents of the Juan de Fuca Ridge. Biogeosciences 9: 4661–4678.
Brazelton WJ, Baross JA . (2010). Metagenomic comparison of two Thiomicrospira lineages inhabiting contrasting deep-sea hydrothermal environments. PLoS One 5: e13530.
Brazelton WJ, Mehta MP, Kelley DS, Baross JA . (2011). Physiological differentiation within a single-species biofilm fueled by serpentinization. MBio 2: e00127-11.
Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K et al. (2009). BLAST+: architecture and applications. BMC Bioinformatics 10: 421.
Campbell BJ, Engel AS, Porter ML, Takai K . (2006). The versatile epsilon-Proteobacteria: key players in sulphidic habitats. Nat Rev Microbiol 4: 458–468.
Canfield DE, Raiswell R . (1999). The evolution of the sulfur cycle. Am J Sci 299: 697–723.
Conell JH . (1978). Diversity in tropical rain forests and coral reefs. Science 199: 1302–1310.
Dahle H, Roalkvam I, Thorseth IH, Pedersen RB, Steen IH . (2013). The versatile in situ gene expression of an Epsilonproteobacteria-dominated biofilm from a hydrothermal chimney. Environ Microbiol Rep 5: 282–290.
Duperron S, Nadalig T, Caprais JC, Sibuet M, Fiala-Medioni A, Amann R et al. (2005). Dual symbiosis in a Bathymodiolus sp. mussel from a methane seep on the Gabon continental margin (Southeast Atlantic): 16S rRNA phylogeny and distribution of the symbionts in gills. Appl Environ Microbiol 71: 1694–1700.
Eddy SR . (2011). Accelerated profile HMM searches. PLoS Comput Biol 7: e1002195.
Engel AS, Lee N, Porter ML, Stern LA, Bennett PC, Wagner M . (2003). Filamentous "Epsilonproteobacteria" dominate microbial mats from sulfidic cave springs. Appl Environ Microbiol 69: 5503–5511.
Eren AM, Morrison HG, Lescault PJ, Reveillaud J, Vineis JH, Sogin ML . (2015). Minimum entropy decomposition: Unsupervised oligotyping for sensitive partitioning of high-throughput marker gene sequences. ISME J 9: 968–979.
Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR et al. (2014). Pfam: the protein families database. Nucleic Acids Res 42: D222–D230.
Flöder S, Sommer U . (1999). Diversity in planktonic communities: an experimental test of the intermediate disturbance hypothesis. Limnol Oceanogr 44: 1114–1119.
Flores GE, Shakya M, Meneghin J, Yang ZK, Seewald JS, Geoff Wheat C et al. (2012). Inter-field variability in the microbial communities of hydrothermal vent deposits from a back-arc basin. Geobiology 10: 333–346.
Flores GE, Campbell JH, Kirshtein JD, Meneghin J, Podar M, Steinberg JI et al. (2011). Microbial community structure of hydrothermal deposits from geochemically different vent fields along the Mid-Atlantic Ridge. Environ Microbiol 13: 2158–2171.
Friedrich CG, Bardischewsky F, Rother D, Quentmeier A, Fischer J . (2005). Prokaryotic sulfur oxidation. Curr Opin Microbiol 8: 253–259.
Friedrich CG, Quentmeier A, Bardischewsky F, Rother D, Kraft R, Kostka S et al. (2000). Novel genes coding for lithotrophic sulfur oxidation of Paracoccus pantotrophus GB17. J Bacteriol 182: 4677–4687.
Glaubitz S, Kiesslich K, Meeske C, Labrenz M, Jurgens K . (2013). SUP05 dominates the gammaproteobacterial sulfur oxidizer assemblages in pelagic redoxclines of the central Baltic and Black Seas. Appl Environ Microbiol 79: 2767–2776.
Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM . (2007). DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57: 81–91.
Grote J, Jost G, Labrenz M, Herndl GJ, Jurgens K . (2008). Epsilonproteobacteria represent the major portion of chemoautotrophic bacteria in sulfidic waters of pelagic redoxclines of the Baltic and Black Seas. Appl Environ Microbiol 74: 7546–7551.
Grote J, Schott T, Bruckner CG, Glockner FO, Jost G, Teeling H et al. (2012). Genome and physiology of a model epsilonproteobacterium responsible for sulfide detoxification in marine oxygen depletion zones. Proc Natl Acad Sci USA 109: 506–510.
Grünke S, Felden J, Lichtschlag A, Girnth AC, De Beer D, Wenzhofer F et al. (2011). Niche differentiation among mat-forming, sulfide-oxidizing bacteria at cold seeps of the Nile Deep Sea Fan (Eastern Mediterranean Sea). Geobiology 9: 330–348.
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O . (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59: 307–321.
Harmsen HJM, Prieur D, Jeanthon C . (1997). Distribution of microorganisms in deep-sea hydrothermal vent chimneys investigated by whole-cell hybridization and enrichment culture of thermophilic subpopulations. Appl Environ Microbiol 63: 2876–2883.
Headd B, Engel AS . (2013). Evidence for niche partitioning revealed by the distribution of sulfur oxidation genes collected from areas of a terrestrial sulfidic spring with differing geochemical conditions. Appl Environ Microbiol 79: 1171–1182.
Huber JA, Cantin HV, Huse SM, Welch DB, Sogin ML, Butterfield DA . (2010). Isolated communities of Epsilonproteobacteria in hydrothermal vent fluids of the Mariana Arc seamounts. FEMS Microbiol Ecol 73: 538–549.
Huber JA, Mark Welch DB, Morrison HG, Huse SM, Neal PR, Butterfield DA et al. (2007). Microbial population structures in the deep marine biosphere. Science 318: 97–100.
Hugler M, Wirsen CO, Fuchs G, Taylor CD, Sievert SM . (2005). Evidence for autotrophic CO2 fixation via the reductive tricarboxylic acid cycle by members of the epsilon subdivision of Proteobacteria. J Bacteriol 187: 3020–3027.
Hugler M, Huber H, Molyneaux SJ, Vetriani C, Sievert SM . (2007). Autotrophic CO2 fixation via the reductive tricarboxylic acid cycle in different lineages within the phylum Aquificae: evidence for two ways of citrate cleavage. Environ Microbiol 9: 81–92.
Huston M . (1979). A general hypothesis of species diversity. Am Natural 113: 81–101.
Inagaki F, Takai K, Nealson KH, Horikoshi K . (2004). Sulfurovum lithotrophicum gen. nov.,sp. nov., a novel sulfur-oxidizing chemolithoautotroph within the epsilon-Proteobacteria isolated from Okinawa Trough hydrothermal sediments. Int J Syst Evol Microbiol 54: 1477–1482.
Inagaki F, Takai K, Kobayashi H, Nealson KH, Horikoshi K . (2003). Sulfurimonas autotrophica gen. nov., sp. nov., a novel sulfur-oxidizing epsilon-proteobacterium isolated from hydrothermal sediments in the Mid-Okinawa Trough. Int J Syst Evol Microbiol 53: 1801–1805.
Jannasch HW, Wirsen CO . (1979). Chemosynthetic primary production at East Pacific sea floor spreading centers. Bioscience 29: 592–598.
Jannasch HW, Nelson DC, Wirsen CO . (1989). Massive natural occurrence of unusually large bacteria (Beggiatoa sp.) at a hydrothermal deep-sea vent site. Nature 342: 834–836.
Jannasch HW, Wirsen CO, Nelson DC, Robertson LA . (1985). Thiomicrospira crunogena sp. nov., a colorless, sulfur-oxidizing bacterium from a deep-sea hydrothermal vent. Int J Syst Bacteriol 35: 422–424.
Jørgensen BB, Revsbech NP . (1983). Colorless sulfur bacteria, Beggiatoa spp. and Thiovulum spp., in O2 and H2S microgradients. Appl Environ Microbiol 45: 1261–1270.
Jørgensen BB, Des Marais DJ . (1986). Competition for sulfide among colorless and purple sulfur bacteria in cyanobacterial mats. FEMS Microbiol Ecol 38: 179–186.
Katoh K, Standley DM . (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30: 772–780.
Konstantinidis KT, Tiedje JM . (2005). Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci USA 102: 2567–2572.
Kunin V, Engelbrektson A, Ochman H, Hugenholtz P . (2010). Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ Microbiol 12: 118–123.
Labrenz M, Jost G, Jurgens K . (2007). Distribution of abundant prokaryotic organisms in the water column of the central Baltic Sea with an oxic-anoxic interface. Aquat Microb Ecol 46: 177–190.
Lesniewski RA, Jain S, Anantharaman K, Schloss PD, Dick GJ . (2012). The metatranscriptome of a deep-sea hydrothermal plume is dominated by water column methanotrophs and lithotrophs. ISME J 6: 2257–2268.
Li L, Stoeckert SJJ, Roos DS . (2003). OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13: 2178–2189.
Lopez-Garcia P, Duperron S, Philippot P, Foriel J, Susini J, Moreira D . (2003). Bacterial diversity in hydrothermal sediment and epsilonproteobacterial dominance in experimental microcolonizers at the Mid-Atlantic Ridge. Environ Microbiol 5: 961–976.
Lücker S, Wagner M, Maixner F, Pelletier E, Koch H, Vacherie B et al. (2010). A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria. Proc Natl Acad Sci USA 107: 13479–13484.
Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar et al. (2004). ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363–1371.
Macalady JL, Dattagupta S, Schaperdoth I, Jones DS, Druschel GK, Eastman D . (2008). Niche differentiation among sulfur-oxidizing bacterial populations in cave waters. ISME J 2: 590–601.
Magrane M,, Consortium, U. (2011). UniProt Knowledgebase: a hub of integrated protein data. Database 2011: bar009.
Mahe F, Rognes T, Quince C, de Vargas C, Dunthorn M . (2015). Swarm v2: highly-scalable and high-resolution amplicon clustering. PeerJ 3: e1420.
Marshall KT, Morris RM . (2013). Isolation of an aerobic sulfur oxidizer from the SUP05/Arctic96BD-19 clade. ISME J 7: 452–455.
McCollom TM, Shock EL . (1997). Geochemical constraints on chemolithoautotrophic metabolism by microorganisms in seafloor hydrothermal systems. Geochim Cosmochim Acta 61: 4375–4391.
McDermott JM, Ono S, Tivey MK, Seewald JS, Shanks WC, Solow AR . (2015). Identification of sulfur sources and isotopic equilibria in submarine hot-springs using multiple sulfur isotopes. Geochim Cosmochim Acta 160: 169–187.
Meier DV, Bach W, Girguis PR, Gruber-Vodicka HR, Reeves EP, Richter M et al. (2016). Heterotrophic Proteobacteria in the vicinity of diffuse hydrothermal venting. Environ Microbiol 18: 4348–4368.
Meyer F, Goesmann A, McHardy AC, Bartels D, Bekel T, Clausen J et al. (2003). GenDB - an open source genome annotation system for prokaryote genomes. Nucleic Acids Res 31: 2187–2195.
Meyer JL, Akerman NH, Proskurowski G, Huber JA . (2013). Microbiological characterization of post-eruption 'snowblower' vents at Axial Seamount, Juan de Fuca Ridge. Front Microbiol 4: 153.
Moore LR, Rocap G, Chisholm SW . (1998). Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 393: 464–467.
Muyzer G, Teske A, Wirsen CO, Jannasch HW . (1995). Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Arch Microbiol 164: 165–172.
Nakagawa S, Takai K . (2008). Deep-sea vent chemoautotrophs: diversity, biochemistry and ecological significance. FEMS Microbiol Ecol 65: 1–14.
Nakagawa S, Takaki Y, Shimamura S, Reysenbach AL, Takai K, Horikoshi K . (2007). Deep-sea vent epsilon-proteobacterial genomes provide insights into emergence of pathogens. Proc Natl Acad Sci USA 104: 12146–12150.
Nakagawa S, Takai K, Inagaki F, Hirayama H, Nunoura T, Horikoshi K et al. (2005). Distribution, phylogenetic diversity and physiological characteristics of epsilon-Proteobacteria in a deep-sea hydrothermal field. Environ Microbiol 7: 1619–1632.
Oksanen J, Blanchet FG, Kindt R, Legendre P, Michin PR, O'Hara RB et al. (2013). vegan: Community Ecology Package. R package version 2.0-10. Available at http://CRAN.R-project.org/package=vegan.
Opatkiewicz AD, Butterfield DA, Baross JA . (2009). Individual hydrothermal vents at Axial Seamount harbor distinct subseafloor microbial communities. FEMS Microbiol Ecol 70: 413–424.
Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW . (2015). CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 25: 1043–1055.
Price MN, Dehal PS, Arkin AP . (2009). FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26: 1641–1650.
Price MN, Dehal PS, Arkin AP . (2010). FastTree 2 - approximately maximum-likelihood trees for large alignments. PLoS ONE 5: e9490.
Pruesse E, Peplies J, Glockner FO . (2012). SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28: 1823–1829.
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P et al. (2013). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41: D590–D596.
Quentmeier A, Friedrich CG . (2001). The cysteine residue of the SoxY protein as the active site of protein-bound sulfur oxidation of Paracoccus pantotrophus GB17. FEBS Lett 503: 168–172.
Quince C, Lanzen A, Curtis TP, Davenport RJ, Hall N, Head IM et al. (2009). Accurate determination of microbial diversity from 454 pyrosequencing data. Nat Method 6: 639–641.
Reeves EP, Prieto X, Hentscher M, Rosner M, Seewald JS, Hinrichs KU et al. (2011a). Phase separation, degassing and anomalous methane at the Menez Gwen hydrothermal field. Mineral Mag 75: 1702.
Reeves EP, Yoshinaga MY, Pjevac P, Goldenstein NI, Peplies J, Meyerdierks A et al. (2014). Microbial lipids reveal carbon assimilation patterns on hydrothermal sulfide chimneys. Environ Microbiol 16: 3515–3532.
Reeves EP, Seewald JS, Saccocia P, Bach W, Craddock PR, Shanks WC et al. (2011b). Geochemistry of hydrothermal fluids from the PACMANUS, Northeast Pual and Vienna Woods hydrothermal fields, Manus Basin, Papua New Guinea. Geochim Cosmochim Acta 75: 1088–1123.
Reysenbach AL . (2001) Phylum BI. Aquificae phy. nov. In: Boone DR, Castenholz RW, Garrity GM (eds). Bergey’s Manual of Systematic Bacteriology. Springer: New York, NY, USA.
Richter M, Rossello-Mora R, Oliver Glockner F, Peplies J . (2015). JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 32: 929–931.
Richter M, Lombardot T, Kostadinov I, Kottmann R, Duhaime MB, Peplies J et al. (2008). JCoast - a biologist-centric software tool for data mining and comparison of prokaryotic (meta)genomes. BMC Bioinformatics 9: 177.
Roxburgh SH, Shea K, Wilson JB . (2004). The intermediate disturbance hypothesis: patch dynamics and mechanisms of species coexistence. Ecology 85: 359–371.
Sauve V, Bruno S, Berks BC, Hemmings AM . (2007). The SoxYZ complex carries sulfur cycle intermediates on a peptide swinging arm. J Biol Chem 282: 23194–23204.
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB et al. (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537–7541.
Schmidt K, Koschinsky A, Garbe-Schönberg D, de Carvalho LM, Seifert R . (2007). Geochemistry of hydrothermal fluids from the ultramafic-hosted Logatchev hydrothermal field, 15 degrees N on the Mid-Atlantic Ridge: temporal and spatial investigation. Chem Geol 242: 1–21.
Schmidtova J, Hallam SJ, Baldwin SA . (2009). Phylogenetic diversity of transition and anoxic zone bacterial communities within a near-shore anoxic basin: Nitinat Lake. Environ Microbiol 11: 3233–3251.
Scott SD, Binns RA . (1995). Hydrothermal processes and contrasting styles of mineralization in the western Woodlark and eastern Manus basins of the western Pacific. Geol Soc Lond Spec Publ 87: 191–205.
Seewald JS, Reeves EP, Bach W, Saccocia PJ, Craddock PR, Shanks WC et al. (2015). Submarine venting of magmatic volatiles in the Eastern Manus Basin, Papua New Guinea. Geochim Cosmochim Acta 163: 178–199.
Shah V, Morris RM . (2015). Genome sequence of “Candidatus Thioglobus autotrophica” strain EF1, a chemoautotroph from the SUP05 clade of marine Gammaproteobacteria. Genome Announce 3: e01156–e01115.
Sheik CS, Anantharaman K, Breier JA, Sylvan JB, Edwards KJ, Dick GJ . (2015). Spatially resolved sampling reveals dynamic microbial communities in rising hydrothermal plumes across a back-arc basin. ISME J 9: 1434–1445.
Sievert SM, Hügler M, Taylor CD, Wirsen CO . (2008a). Sulfur oxidation at deep-sea hydrothermal vents. In: Dahl C, Friedrich CG (eds), Microbial Sulfur Metabolism. Springer: Berlin, Heidelberg, pp 238–258.
Sievert SM, Scott KM, Klotz MG, Chain PS, Hauser LJ, Hemp J et al. (2008b). Genome of the epsilonproteobacterial chemolithoautotroph Sulfurimonas denitrificans. Appl Environ Microbiol 74: 1145–1156.
Sikorski J, Munk C, Lapidus A, Ngatchou Djao OD, Lucas S, Glavina Del Rio T et al. (2010). Complete genome sequence of Sulfurimonas autotrophica type strain (OK10T). Stand Genomic Sci 3: 194–202.
Stamatakis A . (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313.
Stokke R, Dahle H, Roalkvam I, Wissuwa J, Daae FL, Tooming-Klunderud A et al. (2015). Functional interactions among filamentous Epsilonproteobacteria and Bacteroidetes in a deep-sea hydrothermal vent biofilm. Environ Microbiol 17: 4063–4077.
Strous M, Kraft B, Bisdorf R, Tegetmeyer HE . (2012). The binning of metagenomic contigs for microbial physiology of mixed cultures. Front Microbiol 3: 410.
Sunamura M, Higashi Y, Miyako C, Ishibashi J, Maruyama A . (2004). Two Bacteria phylotypes are predominant in the Suiyo seamount hydrothermal plume. Appl Environ Microbiol 70: 1190–1198.
Takai K, Hirayama H, Nakagawa T, Suzuki Y, Nealson KH, Horikoshi K . (2004). Thiomicrospira thermophila sp. nov., a novel microaerobic, thermotolerant, sulfur-oxidizing chemolithomixotroph isolated from a deep-sea hydrothermal fumarole in the TOTO caldera, Mariana Arc, Western Pacific. Int J Syst Evol Microbiol 54: 2325–2333.
Tivey MK . (2004) Environmental conditions within active seafloor vent structures: sensitivity to vent fluid composition and fluid flow. In: Wilcock WSD, DeLong EF, Kelley DS, Baross JA, Cary SC (eds). The Subseafloor Biosphere at Mid-ocean Ridges. American Geophysical Union: Washington D. C., pp 137–152.
Urbach E, Scanlan DJ, Distel DL, Waterbury JB, Chisholm SW . (1998). Rapid diversification of marine picophytoplankton with dissimilar light-harvesting structures inferred from sequences of Prochlorococcus and Synechococcus (Cyanobacteria). J Mol Evol 46: 188–201.
Wankel SD, Joye SB, Samarkin VA, Shah SR, Friederich G, Melas-Kyriazi J et al. (2010). New constraints on methane fluxes and rates of anaerobic methane oxidation in a Gulf of Mexico brine pool via in situ mass spectrometry. Deep Sea Res 57: 2022–2029.
Yamamoto M, Arai H, Ishii M, Igarashi Y . (2006). Role of two 2-oxoglutarate:ferredoxin oxidoreductases in Hydrogenobacter thermophilus under aerobic and anaerobic conditions. FEMS Microbiol Lett 263: 189–193.
Yarza P, Yilmaz P, Pruesse E, Glockner FO, Ludwig W, Schleifer KH et al. (2014). Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 12: 635–645.
Yeats CJ, Parr JM, Binns RA, Gemmell JB, Scott SD . (2014). The SuSu Knolls hydrothermal field, eastern Manus Basin, Papua New Guinea: an active submarine high-sulfidation copper-gold system. Econ Geol 109: 2207–2226.
Acknowledgements
We would like to thank officers, crew, shipboard scientific party and the technical team of the ROV Quest 4000 m (MARUM) on R/V Sonne cruise SO216, for their invaluable assistance. The cruise SO216 with R/V Sonne was an integral part of the Cluster of Excellence of the MARUM ‘The Ocean in the Earth System, Research Area GB: Geosphere-Biosphere Interactions’ funded by the German Research Foundation (DFG). We thank Richard Reinhard, Bruno Huettel and the team of the Max Planck Genome Centre in Cologne for sequencing, and Harald Gruber-Vodicka and Hanno Teeling for help with computational analyses. Further, we thank Nicole Krombholz and Kathrin Büttner for excellent technical assistance in the Molecular Ecology department. This work was supported by the Max Planck Society. This work was further supported by U.S. National Science Foundation under Grant Nos. IOS-1257755 and OCE-1536653 to Girguis.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no conflict of interest.
Additional information
Supplementary Information accompanies this paper on The ISME Journal website
Supplementary information
Rights and permissions
About this article
Cite this article
Meier, D., Pjevac, P., Bach, W. et al. Niche partitioning of diverse sulfur-oxidizing bacteria at hydrothermal vents. ISME J 11, 1545–1558 (2017). https://doi.org/10.1038/ismej.2017.37
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1038/ismej.2017.37
This article is cited by
-
The chemosynthetic biofilm microbiome of deep-sea hydrothermal vents across space and time
Environmental Microbiome (2025)
-
Metagenomic binning reveals community and functional characteristics of sulfur- and methane-oxidizing bacteria in cold seep sponge ground
Environmental Microbiome (2025)
-
Elevated heterotrophic activity in Guaymas Basin hydrothermal plumes influences deep-sea carbon cycling
Nature Communications (2025)
-
Microbial Sulfur Pathways and Outcomes in Tailings Impoundments: A Mesocosm Study
Mine Water and the Environment (2024)
-
Exploring the long-term impact of a cadmium pollution accident on microbial communities in river ecosystems
Biogeochemistry (2024)