Abstract
Submarine hydrothermal vents are among the least-understood habitats on Earth but have been the intense focus of research in the past 30 years. An active hydrothermal sulfide chimney collected from the Dudley site in the Main Endeavour vent Field (MEF) of Juan de Fuca Ridge was investigated using mineralogical and molecular approaches. Mineral analysis indicated that the chimney was composed mainly of Fe-, Zn-and Cu-rich sulfides. According to phylogenetic analysis, within the Crenarchaeota, clones of the order Desulfurococcales predominated, comprising nearly 50% of archaeal clones. Euryarchaeota were composed mainly of clones belonging to Thermococcales and deep-sea hydrothermal vent Euryarchaeota (DHVE), each of which accounted for about 20% of all clones. Thermophilic or hyperthermophilic physiologies were common to the predominant archaeal groups. More than half of bacterial clones belonged to ɛ-Proteobacteria, which confirmed their prevalence in hydrothermal vent environments. Clones of Proteobacteria (γ-, δ-, β-), Cytophaga-Flavobacterium-Bacteroides (CFB) and Deinococcus-Thermus occurred as well. It was remarkable that methanogens and methanotrophs were not detected in our 16S rRNA gene library. Our results indicated that sulfur-related metabolism, which included sulfur-reducing activity carried out by thermophilic archaea and sulfur-oxidizing by mesophilic bacteria, was common and crucial to the vent ecosystem in Dudley hydrothermal site.
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Amann, R.I., W. Ludwig, and K.H. Schleifer. 1995. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59, 143–169.
Bae, S.S., Y.J. Kim, and S.H. Yang. 2006. Thermococcus onnurineus sp. nov., a hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent area at the PACMANUS field. J. Microbiol. Biotechnol. 16, 1826–1831.
Bano, N., S. Ruffin, B. Ransom, and J.T. Hollibaugh. 2004. Phylogenetic composition of Arctic Ocean archaeal assemblages and comparison with Antarctic assemblages. Appl. Environ. Microbiol. 70, 781–789.
Blöchl, E., R. Rachel, S. Burggraf, D. Hafenbradl, H.W. Jannasch, and K.O. Stetter. 1997. Pyrolobus fumarii, gen. and sp. nov., represents a novel group of archaea, extending the upper temperature limit for life to 113°C. Extremophiles 1, 14–21.
Boetius, A., C. Schubert, and D. Rickert. 2000. A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 407, 623–626.
Bond, P.L. and J.F. Banfield. 2001. Design and performance of rRNA targeted oligonucleotide probes for in situ detection and phylogenetic identification of microorganisms inhabiting acid mine drainage environments. Microbiol. Ecol. 41, 149–161.
Brazelton, W., M. Schrenk, D. Kelley, and J. Baross. 2006. Methaneand sulfur-metabolizing microbial communities dominate the lost city hydrothermal field ecosystem. Appl. Environ. Microbiol. 72, 6257–6270.
Butterfield, D.A., R.E. McDuff, M.J. Mottl, M.D. Lilley, J.E. Lupton, and G.J. Massoth. 1994. Gradients in the composition of hydrothermal fluids from the endeavour segment vent field: Phase seperation and brine loss. J. Geophys. Res. 99, 9561–9583.
Corlis, J.B., J. Dymon, L.I. Gordon, J.M. Edmond, and R.P. Von Herzen. 1979. Submarine thermal springs on the Galapagos Rift. Science 203, 1073–1083.
Corre, E., A.L. Reysenbach, and D. Prieur. 2001. Epsilon-Proteobacterial diversity from a deep-sea hydrothermal vent on the Mid-Atlantic Ridge. FEMS Microbiol. Lett. 205, 329–335.
Cowen, J.P. 2004. The microbial biosphere of sediment buried oceanic basement. Res. Microbiol. 155, 497–506.
Delaney, J.R., V. Robigou, R.E. McDuff, and M.K. Tivey. 1992. Geology of a vigorous hydrothermal system on the Endeavour Segment, Juan de Fuca Ridge. J. Geophys. Res. 97, 19663–19682.
Delong, E.F. 1992. Archaea in coastal marine environments. Proc. Natl. Acad. Sci. USA 89, 5685–5689.
Dilly, O., J. Bloem, A. Vos, and J.C. Munch. 2004. Bacterial diversity in agricultural soils during litter decomposition. Appl. Environ. Microbiol. 70, 468–474.
Donval, J.P., J.L. Charlou, and E. Douville. 1997. High H2 and CH4 content in hydrothermal fluids from Rainbow site newly sampled at 36°14′N on the AMAR segment, Mid-Atlantic Ridge (diving FLORES cruise, 1997). Comparison with other MAR sites. EOS Trans. 78, 832.
Ehrhardt, C.J., R.M. Haymon, M.G. Lamontagne, and P.A. Holden. 2007. Evidence for hydrothermal Archaea within the basaltic flanks of the East Pacific Rise. Environ. Microbiol. 9, 900–912.
Finster, K., W. Liesack, and B. Tindall. 1997. Sulfurospirillum arcachonense sp. nov., a new microaerophilic sulfur reducing bacterium. Int. J. Syst. Bacteriol. 47, 1212–1217.
Goffredi, S.K., A. Warén, V.J. Orphan, C.L. van Dover, and R.C. Vrijenhoek. 2004. Novel forms of structural integration between microbes and a hydrothermal vent gastropod from the Indian Ocean. Appl. Environ. Microbiol. 70, 3082–3090.
Hao, X. and K. Ma. 2003. Minimal sulfur requirement for growth and sulfur-dependent metabolism of the hyperthermophilic archaeon Staphylothermus marinus. Archaea 1, 191–197.
Harmsen, H.J.M., D. Prieur, and C. Jeanthon. 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.
He, J.Z., J.P. Shen, L.M. Zhang, and Y.G. Zhu. 2007. Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ. Microbiol. 9, 2364–2374.
Hoek, J., A. Banta, F. Hubler, and A.L. Reysenbach. 2003. Microbial diversity of a sulphide spire located in the Edmond deep-sea hydrothermal vent filed on the central indian ridge. Geobiology 1, 119–127.
Huber, H. and K.O. Stetter. 1998. Hyperthermophiles and their possible potential in biotechnology. J. Bacteriol. 64, 39–52.
Huber, H. and K.O. Stetter. 2001. Order I. Thermoproteales, p. 170–179. In D.R. Boone and R.W. Castenholz (eds.), Bergey’s Manual of Systematic Bacteriology: The Archaea and the Deeply Branching and Phototrophic Bacteria. Springer, New York, N.Y., USA.
Huber, J.A., P.H. Johnson, D.A. Butterfield, and J.A. Baross. 2006. Microbial life in ridge flank crustal fluids. Environ. Microbiol. 8, 88–99.
Inagaki, F., K. Takai, H. Kobayashi, K.H. Nealson, and K. Horikoshi. 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.
Inagaki, F., K. Takai, K.H. Nealson, and K. Horikoshi. 2004. Sulfurovum lithotrophicum gen. nov., sp. nov., a novel sulfur-oxidizing chemolithoautotroph within the epsilon-Proteobacteria isolated from the Okinawa Trough hydrothermal sediments. Int. J. Syst. Evol. Microbiol. 54, 1477–1482.
Kashefi, K. and D.R. Lovely. 2003. Extending the upper temperature limit for life. Science 301, 934.
Kelley, D.S., J.A. Baross, and J.R. Delaney. 2002. Volcanoes, fluids, and life at mid-ocean ridge spreading centers. Annu. Rev. Earth Planet Sci. 30, 385–491.
Kelley, D.S., J.A. Karson, and D.K. Blackman. 2001. An off-axis hydrothermal vent field near the Mid-Atlantic Ridge at 30°N. Nature 412, 145–149.
Kormas, K.A., M.K. Tivey, K.V. Damm, and A. Teske. 2006. Bacterial and archaeal phylotypes associated with distinct mineralogical layers of a white smoker spire from a deep-sea hydrothermal vent site (9°N, East Pacific Rise). Environ. Microbiol. 8, 909–920.
Kuwabara, T., M. Minaba, N. Ogi, and M. Kamekura. 2007. Thermococcus celericrescens sp. nov., a fastgrowing and cell-fusing hyperthermophilic archaeon from a deep-sea hydrothermal vent. Int. J. Syst. Evol. Microbiol. 57, 437–443.
Lane, D.J. 1991. 16S/23S rRNA sequencing, p. 115–175. In E. Stackebrandt and M. Goodfellow (eds.), Nucleic acid techniques in bacterial systematics. Wiley, Chichester, UK.
Lathe, R. 1985. Synthetic oligonucleotide probes deduced from amino acid sequence data. Theoretical and practical considerations. J. Mol. Biol. 183, 1–12.
Lepage, E., E. Marguet, C. Geslin, O. Matte-Tailliez, W. Zillig, P. Forterre, and P. Tailliez. 2004. Molecular diversity of new Thermococcales isolates from a single area of hydrothermal deep-sea vents as revealed by randomly amplified polymorphic DNA fingerprinting and 16S rRNA gene sequence analysis. Appl. Environ. Microbiol. 70, 1277–1286.
Lilley, M.D., D.A. Butterfield, J.E. Lupton, and E.J. Olson. 2003. Magmatic events can produce rapid changes in hydrothermal vent chemistry. Nature 422, 878–881.
Lilley, M.D., D.A. Butterfield, E.J. Olson, J.E. Lupton, S.A. Macko, and R.E. Mcduff. 1993. Anomalous CH4 and NH4 + concentrations at an unsedimented mid-ocean-ridge hydrothermal system. Nature 364, 45–47.
Longnecker, K. and A.L. Reysenbach. 2001. Expansion of the geographic distribution of a novel lineage of epsilon-Proteobacteria to a hydrothermal vent site on the Southern East Pacific Rise. FEMS Microbiol. Ecol. 35, 287–293.
López-García, P., S. Duperron, P. Philippot, J. Foriel, J. Susini, and D. Moreira. 2003. Bacterial diversity in hydrothermal sediment and epsilon-proteobacterial dominance in experimental microcolonizers at the Mid-Atlantic Ridge. Environ. Microbiol. 5, 961–976.
López-García, P., F. Gaill, and D. Moreira. 2002. Wide bacterial diversity associated with tubes of the vent worm Riftia pachyptila. Environ. Microbiol. 4, 204–215.
Maidak, B.L., J.R. Cole, T.G. Lilburn, C.T. Parker, P.R. Saxman, R.J. Farris, G.M. Garrity, G.L. Olsen, T.M. Schmidt, and J.M. Tiedje. 2001. The RDP-II (Ribosomal Database Project). Nucleic Acids Res. 29, 173–174.
McCollom, T.M. and E.L. Shock. 1997. Geochemical constraints on chemolithoautotrophic metabolism by microorganisms in seafloor hydrothermal systems. Geochim. Cosmochim. Acta 61, 4375–4391.
Miroshnichenko, M.L., S.L. Haridon, and C. Jeanthon. 2003. Oceanithermus profundus gen. nov., sp. nov., a thermophilic, microaerophilic, facultatively chemolithoheterotrophic bacterium from a deep-sea hydrothermal vent. Int. J. Syst. Evol. Microbiol. 53, 747–752.
Nakagawa, S., K. Takai, F. Inagaki, K. Horikoshi, and Y. Sako. 2005. Nitratiruptor tergarcus gen. nov., sp. nov. and Nitratifractor salsuginis gen. nov., sp. nov., nitrate-reducing chemolithoautotrophs of the e-Proteobacteria isolated from a deep-sea hydrothermal system in the Mid-Okinawa Trough. Int. J. Syst. Evol. Microbiol. 55, 925–933.
Nercessian, O., M. Prokofeva, A. Lebedinski, S. L’Haridon, C. Cary, D. Prieur, and C. Jeanthon. 2004. Design of 16S rRNA-targeted oligonucleotide probes for detecting cultured and uncultured archaeal lineages in hightemperature environments. Environ. Microbiol. 6, 170–182.
Nercessian, O., A.L. Reysenbach, D. Prieur, and C. Jeanthon. 2003. Archaeal diversity associated with in situ samplers deployed on hydrothermal vents on the East Pacific Rise. Environ. Microbiol. 5, 492–502.
Page, A., S.K. Juniper, M. Olagnon, K. Alain, G. Desrosiers, J. Querellou, and M.A. Cambon-Bonavita. 2004. Microbial diversity associated with a Paralvinella sulfincola tube and the adjacent substratum on an active deep-sea vent chimney. Geobiology 2, 225–238.
Page, A., M.K. Tivey, D.S. Stakes, and A.L. Reysenbach. 2008. Temporal and spatial archaeal colonization of hydrothermal vent deposits. Environ. Microbiol. 10, 874–884.
Perner, M., J. Kuever, and R. Seifert. 2007. The influence of ultramafic rocks on microbial communities at the Logatchev hydrothermal field, located 15N on the Mid-Atlantic Ridge. FEMS Microbiol. Ecol. 61, 97–109.
Poltz, M.F. and C.M. Cavanaugh. 1995. Dominance of one bacterial phylotype at a Mid-Atlantic Ridge hydrothermal vent site. Proc. Natl. Acad. Sci. USA 92, 7232–7236.
Prieur, D. 1997. Microbiology of deep-sea hydrothermal vents. Trends Biotechnol. 15, 242–244.
Reysenbach, A.L., Y.T. Liu, A.B. Banta, and T.J. Beveridge. 2006. Isolation of a ubiquitous obligate thermoacidophilic archaeon from deep-sea hydrothermal vents. Nature 442, 444–447.
Reysenbach, A.L., K. Longnecker, and J. Kirshtein. 2000. Novel bacterial and archaeal lineages from an in situ growth chamber deployed at a mid-atlantic ridge hydrothermal vent. Appl. Environ. Microbiol. 66, 3798–3806.
Schrenk, M.O., D.S. Kelley, J.R. Delaney, and J.A. Baross. 2003. Incidence and diversity of microorganisms within the walls of an active deep-sea sulfide chimney. Appl. Environ. Microbiol. 69, 3580–3592.
Takai, K. and K. Horikoshi. 1999. Genetic diversity of Archaea in deep-sea hydrothermal vent environments. Genetics 152, 1285–1297.
Takai, K., F. Inagaki, S. Nakagawa, H. Hirayama, T. Nunoura, and Y. Sako. 2003. Isolation and phylogenetic diversity of members of previously uncultivated ɛ-Proteobacteria in deep-sea hydrothermal vents. FEMS Microbiol. Lett. 218, 167–174.
Takai, K., T. Komatus, F. Inagaki, and K. Horikoshi. 2001. Distribution of archaea in a black smoker chimney structure. Appl. Environ. Microbiol. 67, 3618–3629.
Teske, A., K.U. Hinrichs, and V. Edgcomb. 2002. Microbial diversity of hydrothermal sediments in the Guaymas Basin: evidence for anaerobic methanotrophic communities. Appl. Environ. Microbiol. 68, 1994–2007.
Tivey, M.K. and J.R. Delaney. 1986. Growth of large sulfide structures on the endeavour segment of the Juan de Fuca Ridge. Earth Planet. Sci. Lett. 77, 303–317.
Tivey, M.K., D.S. Stakes, T.L. Cook, M.D. Hannington, and S. Petersen. 1999. A model for growth of steep-sided vent structures on the endeavour segment of the Juan de Fuca Ridge: results of a petrologic and geochemical study. J. Geophys. Res. 104, 22859–22883.
Urakawa, H., N. Dubilier, Y. Fujiwara, D.E. Cunningham, S. Kojima, and D.A. Stahl. 2005. Hydrothermal vent gastropods from the same family (Provannidae) harbour ɛ- and γ-proteobacterial endosymbionts. Environ. Microbiol. 7, 750–754.
Van Dover, C.L., S.E. Humphris, and D. Fornari. 2001. Biogeography and ecological setting of Indian Ocean hydrothermal vents. Science 294, 818–823.
Von Dam, K.L. and M.D. Lilley. 2004. Diffuse flow hydrothermal fluids from 9°50′N East Pacific Rise: orgin, evolution and biogeochemical controls, p. 245–268. In W.S.D. Wilcock, E.F. Delong, D.S. Kelley, J.A. Baross, and S.C. Cary (eds.), The subseafloor Biosphere at Mid-Ocean Ridges. Geophys Union Monogr Ser, Washington, D.C., USA.
Zerkle, A.L., C.H. House, and S.L. Brantley. 2005. Biogeochemical signatures through time as inferred from whole microbial genomes. Am. J. Sci. 305, 467–502.
Zhou, J., M. Bruns, and J. Tiedje. 1996. DNA recovery from soils of diverse composition. Appl. Environ. Microbiol. 62, 316–322.
Zillig, W. and A.L. Reysenbach. 2001. Thermococcaceae fam. nov., p. 341–348. In D.R. Boone and R.W. Castenholz (eds.), Bergey’s Manual of Systematic Bacteriology. Springer, New York, N.Y., USA.
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Zhou, H., Li, J., Peng, X. et al. Microbial diversity of a sulfide black smoker in main endeavour hydrothermal vent field, Juan de Fuca Ridge. J Microbiol. 47, 235–247 (2009). https://doi.org/10.1007/s12275-008-0311-z
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DOI: https://doi.org/10.1007/s12275-008-0311-z