Sulfur Oxidation at Deep-Sea Hydrothermal Vents

  • Stefan M. Sievert
  • Michael Hügler
  • Craig D. Taylor
  • Carl O. Wirsen

Microbial oxidation of geothermally produced reduced sulfur compounds is at the nexus of the biogeochemical carbon and sulfur cycles at deep-sea hydrothermal vents. Available information indicates that microbial symbionts and free- living gammaproteobacteria of the genera Thiomicrospira, Halothiobacillus, and Beggiatoa are important sulfur-oxidizers above the seafloor at these systems. In addition, bacteria belonging to the Epsilonproteobacteria have been identified as a major component of microbial communities at deep-sea vents. We have previously identified a novel sulfuroxidizing epsilonproteobacterium, Candidatus Arcobacter sulfidicus, which produces sulfur in filamentous form that is morphologically and chemically similar to material observed before and after submarine volcanic eruptions. In the meantime, many autotrophic epsilonproteobacteria have been isolated and characterized from deep-sea vents, providing further evidence that these organisms play an important role in sulfur and carbon cycling in these environments.

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References

  1. Brinkhoff, T, Kuever, J, Muyzer, G, Jannasch, HW (2005) The genus Thiomicrospira. In: Brenner DJ, Krieg NR, Staley JT (eds) Bergey’s manual of systematic bacteriology, vol 2, 2nd edn. Springer, New York, pp 193–199.Google Scholar
  2. Campbell BJ, Engel AS, Porter ML, Takai K (2006) The versatile epsilonproteobacteria: Key players in sulphidic habitats. Nat Rev Microbiol 4:458–468.CrossRefPubMedGoogle Scholar
  3. Cavanaugh CM (2006) Comparative genomics of chemosynthetic symbionts. In: American Society for Microbiology, General Meeting, Orlando.Google Scholar
  4. Desbruyeres, D, Alayse-Danet A-M, Ohta S, and the Scientific Parties of BIOLAU and STARMER Cruises (1994) Deep-sea hydrothermal communities in southwestern Pacific back-arc basins (the North Fiji and Lau Basins): composition, microdistribution, and food web. Mar Geol 116:227–242.CrossRefGoogle Scholar
  5. Durand P, Reysenbach A-L, Prieur D, Pace N (1993) Isolation and characterization of Thiobacillus hydrothermalis sp. nov., a mesophilic obligately chemolithoautotrophic bacterium isolated from a deep-sea hydrothermal vent in Fiji Basin. Arch Microbiol 159:39–44.CrossRefGoogle Scholar
  6. Eisen JA, Nelson KE, Paulsen IT, Heidelberg JF, Wu M, Dodson RJ, Deboy R, Gwinn ML, Nelson WC, Haft DH, Hickey EK, Peterson JD, Durkin AS, Kolonay JL, Yang F, Holt I, Umayam LA, Mason T, Brenner M, Shea TP, Parksey D, Nierman WC, Feldblyum TV, Hansen CL, Craven MB, Radune D, Vamathevan J, Khouri H, White O, Gruber TM, Ketchum KA, Venter JC, Tettelin H, Bryant DA, Fraser CM (2002) The complete genome sequence of Chlorobium tepidum TLS a photosynthetic, anaerobic, green-sulfur bacterium. Proc Natl Acad Sci USA 99:9509–9514.CrossRefPubMedGoogle Scholar
  7. Friedrich CG, Rother D, Bardischewsky F, Quentmeier A, Fischer J (2001) Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism. Appl Environ Microbiol 67:2873–2882.CrossRefPubMedGoogle Scholar
  8. Goffredi SK, Warén A, Orphan VJ, Van Dover CL, Vrijenhoek RC (2004) Novel forms of structural integration between microbes and a hydrothermal vent gastropod in the Indian Ocean. Appl Environ Microbiol 70:3082–3090.CrossRefPubMedGoogle Scholar
  9. Gordon and Betty Moore Foundation (2007) Microbial genome sequencing project. http://www.moore.org/microgenome/.
  10. Götz D, Banta A, Beveridge TJ, Rushdi AI, Simoneit BRT, Reysenbach A-L (2002) Persephonella marina gen. nov., sp. nov. and Persephonella guaymasensis sp. nov., two novel, thermophilic, hydrogen-oxidizing microaerophiles from deep-sea hydrothermal vents. Int J Syst Evol Microbiol 52:1349–1359.CrossRefPubMedGoogle Scholar
  11. Gray ND, Head IM (2001) Linking genetic identity and function in communities of uncultured bacteria. Environ Microbiol 3:481–492.CrossRefPubMedGoogle Scholar
  12. Hagen KD, Nelson DC (1997) Use of reduced sulfur compounds by Beggiatoa spp.: enzymology and physiology of marine and freshwater strains in homogeneous and gradient cultures. Appl Environ Microbiol 63:3957–3964.PubMedGoogle Scholar
  13. Haymon RM, Fornari DJ, Von Damm KL, Lilley MD, Perfit M, Edmond JM (1993) Volcanic eruption of the mid-ocean ridge along the East Pacific Rise crust at 9°45–52eN: Direct submersible observations of seafloor phenomena associated with an eruption event in April, (1991). Earth Plant Sci Lett 119:85–101.CrossRefGoogle Scholar
  14. Hensen D, Sperling D, Trüper HG, Brune DC, Dahl C (2006) Thiosulphate oxidation in the phototrophic sulphur bacterium Allochromatium vinosum. Mol Microbiol 62:794–810.CrossRefPubMedGoogle Scholar
  15. Holland ME, Baross JA, Holden JF (2004) Illuminating the subseaflloor ecosystem using microbial tracers. In: Wilcock WSD, DeLong EF, Kelley DS, Baross JA, Cary SC (eds) The subseafloor biosphere at mid-ocean ridges. Geophysics monographs 144. American Geological Union, Washington, pp 291–304.Google Scholar
  16. Huber JA, Butterfield DA, Baross JA (2003) Bacterial diversity in a subseafloor habitat following a deep-sea volcanic eruption. FEMS Microbiol Ecol 43:393–204.CrossRefPubMedGoogle Scholar
  17. Hügler M, Wirsen CO, Fuchs G, Taylor CD, Sievert SM (2005) Evidence for autotrophic CO2 fixation via the reductive tricarboxylic acid cycle in members of the epsilon-Proteobacteria. J Bacteriol 187:3020–3027.CrossRefPubMedGoogle Scholar
  18. Hügler 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.CrossRefPubMedGoogle Scholar
  19. Inagaki F, Takai K, Kobayashi H, Nealson KH, Horikoshi K (2003) Sulfurimonas autotrophica gen. nov., sp. nov., a novel sulfur-oxidizing -proteobacterium isolated from hydrothermal sediments in the Mid-Okinawa Trough. Int J Syst Evol Microbiol 53:1801–1805.CrossRefPubMedGoogle Scholar
  20. Inagaki F, Takai K, Nealson KH, and Horikoshi K (2004). Sulfurovum lithotrophicum gen. nov., sp. nov., a novel sulfur-oxidizing chemolithoautotroph within the -Proteobacteria isolated from Okinawa Trough hydrothermal sediments. Int J Syst Evol Microbiol 54: 1477–1482.CrossRefPubMedGoogle Scholar
  21. Jannasch HW (1995) Microbial interactions with hydrothermal fluids. In: Humphris SE, Zierenberg RA, Mullineaux LS, Thomson RE (eds) Seafloor hydrothermal systems. Geophysics monographs 91. American Geological Union, Washington, pp 273–296.Google Scholar
  22. Jannasch HW, Mottl MJ (1985) Geomicrobiology of deep-sea hydrothermal vents. Science 229:717–725.CrossRefPubMedGoogle Scholar
  23. 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.CrossRefGoogle Scholar
  24. Javor BJ, Wilmot DB, Vetter RD (1990) pH-dependent metabolism of thiosulfate and sulfur globules in the chemolithotrophic marine bacterium Thiomicrospira crunogena. Arch Microbiol 154:231–238.CrossRefGoogle Scholar
  25. Kappler U, Dahl C (2001) Enzymology and molecular biology of prokaryotic sulfite oxidation. FEMS Microbiol Lett 203:1–9.PubMedGoogle Scholar
  26. Karl DM (1995) Ecology of free-living, hydrothermal vent microbial communities. In: Karl DM (ed) Microbiology of deep-sea hydrothermal vents. CRC, Boca Raton, pp 35–124.Google Scholar
  27. Kelly DP, Shergill JK, Lu W-P, Wood AP (1997) Oxidative metabolism of inorganic sulfur compounds by bacteria. Antonie Van Leuwenhoek 71:95–107.CrossRefGoogle Scholar
  28. Markert S, Arndt C, Felbeck H, Feldman RA, Becher D, Sievert SM, Hügler M, Albrecht D, Robidart J, Bench S, Hecker M, Schweder T (2007) Approaching the uncultivable endosymbiont of Riftia pachyptila by physiological proteomics. Science 315:247–250.CrossRefPubMedGoogle Scholar
  29. Martinez RJ, Mills HJ, Story S, Sobecky PA (2006) Prokaryotic diversity and metabolically active microbial populations in sediments from an active mud volcano in the Gulf of Mexico. Environ Microbiol 8:1783–1796.CrossRefPubMedGoogle Scholar
  30. McCollom T, Shock EL (1997) Geochemical constraints on chemolithoautotrophic metabolism by microorganisms in seafloor hydrothermal systems. Geochim Cosmochim Acta 61:4375–4391.CrossRefPubMedGoogle Scholar
  31. Moussard H, Corre E, Cambon-Bonavita M-A, Fouquet Y, Jeanthon C (2006) Novel uncultured Epsilonproteobacteria dominate a filamentous sulphur mat from the 13°N hydrothermal vent field, East Pacific Rise. FEMS Microbiol Ecol 58:449–463.CrossRefPubMedGoogle Scholar
  32. Nakagawa S, Takai K, Inagaki F, Hirayama H, Nunoura T, Horikoshi K, Sako Y (2005) Distribution, phylogenetic diversity and physiological characteristics of epsilon-Proteobacteria in a deep-sea hydrothermal field. Environ Microbiol 7:1619–1632.CrossRefPubMedGoogle Scholar
  33. Nelson DC, Fisher CR (1995) Chemoautotrophic and methanotrophic endosymbiotic bacteria at deep-sea vents and seeps. In: Karl DM (ed) Microbiology of deep-sea hydrothermal vents. CRC, Boca Raton, pp 125–167.Google Scholar
  34. Nelson DC, Wirsen CO, Jannasch HW (1989) Characterization of large, autotrophic Beggiatoa spp. abundant at hydrothermal vents of the Guaymas Basin. Appl Environ Microbiol 55:2909–2917.PubMedGoogle Scholar
  35. Nelson D, Haymon RM, Lilley M, Lutz R (1991) Rapid growth of unusual hydrothermal bacteria observed at new vents during ADVENTURE dive program to the EPR crest at 9°45V–52–N. EOS Trans Am Geophys Union 72:481.Google Scholar
  36. Newton ILG, Woyke T, Auchtung TA, Dilly GF, Dutton RJ, Fisher MC, Fontanez KM, Lau E, Stewart FJ, Richardson PM, Barry KW, Saunders E, Detter JC, Wu D, Eisen JA, Cavanaugh CM (2007) The Calyptogena magnifica chemoautotrophic symbiont genome. Science 315:998–1000.CrossRefPubMedGoogle Scholar
  37. Orphan VJ, House CH, Hinrichs K-U, McKeegan KD, DeLong EF (2001) Methane-consuming archaea revealed by directly coupled isotopic and phylogenetic analysis. Science 293:484–487.CrossRefPubMedGoogle Scholar
  38. Petri R, Podgorsek L, Imhoff JF (2001) Phylogeny and distribution of the soxB gene among thiosulfate-oxidizing bacteria. FEMS Microbiol Lett 197:171–178.CrossRefPubMedGoogle Scholar
  39. Pott AS, Dahl C (1998) Sirohaem-sulfite reductase and other proteins encoded in the dsr locus of Chromatium vinosum are involved in the oxidation of intracellular sulfur. Microbiol 144:1881–1894.CrossRefGoogle Scholar
  40. Richardson DJ, Watmough NJ (1999) Inorganic nitrogen metabolism in bacteria. Curr Opin Chem Biol 3:207–219.CrossRefPubMedGoogle Scholar
  41. Ruby EG, Jannasch HW (1982) Physiological characteristics of Thiomicrospira sp. strain L-12 isolated from deep-sea hydrothermal vents. J Bacteriol 149:161–165.PubMedGoogle Scholar
  42. Shahak Y, Schütz M, Bronstein M, Hauska G, Padan E (1999) Sulfide-dependent anoxygenic photosynthesis in prokaryotes: sulfide:quinone reductase (SQR), the intial step. In: Peshek GA, Löffelhardt W, Schmetterer C (eds) The phototrophic prokaryotes. Kluwer/Plenum, New York, pp 211–228.Google Scholar
  43. Scott KM, Sievert SM, Abril FN, Ball LA, Barrett CJ, Blake RA, Boller AJ, Chain PSG, Clark JA, Davis CR, Detter C, Do KF, Dobrinski KP, Faza BI, Fitzpatrick KA, Freyermuth SK, Harmer TL, Hauser LJ, Hügler M, Kerfeld CA, Klotz MG, Kong MW, Land M, Lapidus A, Larimer FW, Longo DL, Lucas S, Malfatti SA, Massey SE, Martin DD, McCuddin Z, Meyer F, Moore JL, Ocampo LH Jr, Paul JH, Paulsen IT, Reep DK, Ren Q, Ross RL, Sato PY, Thomas P, Tinkham LE, Zeruth GT (2006) The genome of deep-sea vent chemolithoautotroph Thiomicrospira crunogena XCL-2. PLoS Biol 4:e383. doi:10.1371/journal.pbio.0040383.CrossRefPubMedGoogle Scholar
  44. Sievert SM (2006) The genome of the sulfur-oxidizing bacterium Thiomicrospira denitrificans: a model for epsilonproteobacterial autotrophs at vents and other redox interfaces. In: American Society for Microbiology, General Meeting, Orlando.Google Scholar
  45. Sievert SM, Wieringa EBA, Wirsen CO, Taylor CD (2007) Growth and mechanism of filamentous-sulfur formation by Candidatus Arcobacter sulfidicus in opposing oxygen-sulfide gradients. Environ Microbiol 9:271–276.CrossRefPubMedGoogle Scholar
  46. Stein JL, Cary SC, Hessler RR, Ohta S, Vetter RD, Childress JJ, Felbeck H (1988) Chemoautotrophic symbiosis in a hydrothermal vent gastropod. Biol Bull 174:373–378.CrossRefGoogle Scholar
  47. Stewart FJ, Newton ILG, Cavanaugh CM (2005) Chemosynthetic endosymbioses: adaptations to oxic-anoxic interfaces. Trends Microbiol 13:439–448.CrossRefPubMedGoogle Scholar
  48. Sturt HF, Summons RE, Smith K, Elvert M, Hinrichs KU (2004) Intact polar membrane lipids in prokaryotes and sediments deciphered by high-performance liquid chromatography/electrospray ionization multistage mass spectrometry–new biomarkers for biogeochemistry and microbial ecology. Rapid Commun Mass Spectrom 18:617–628.CrossRefPubMedGoogle Scholar
  49. Summit M, Baross JA (2001) A novel microbial habitat in the mid-ocean ridge subseafloor. Proc Nat Acad Sci USA 98:2158–2163.CrossRefPubMedGoogle Scholar
  50. Suzuki Y, Sasaki T, Suzuki M, Nogi Y, Miwa T, Takai K, Nealson KH, Horikoshi K (2005a) Novel chemoautotrophic endosymbiosis between a member of the Epsilonproteobacteria and the hydrothermal-vent gastropod Alviniconcha aff. hessleri (Gastropoda: Provannidae) from the Indian Ocean. Appl Environ Microbiol 71:5440–5450.CrossRefPubMedGoogle Scholar
  51. Suzuki Y, Sasaki T, Suzuki M, Tsuchida S, Nealson KH, Horikoshi K (2005b) Molecular phylogenetic and isotopic evidence of two lineages of chemoautotrophic endosymbionts distinct at the subdivision level harbored in one host-animal type: the genus Alviniconcha (Gastropoda: Provannidae). FEMS Microbiol Lett 249:105–112.CrossRefPubMedGoogle Scholar
  52. Suzuki Y, Kojima S, Sasaki T, Suzuki M, Utsumi T, Watanabe H, Urakawa H, Tsuchida S, Nunoura T, Hirayama H, Takai K, Nealson KH, Horikoshi K (2006) Host-symbiont relationships in hydrothermal vent gastropods of the genus Alviniconcha from the southwest Pacific. Appl Environ Microbiol 72:1388–1393.CrossRefPubMedGoogle Scholar
  53. Takai K, Inagaki F, Nakagawa S, Hirayama H, Nunoura T, Sako Y, Nealson KH, Horikoshi K (2003) Isolation and phylogenetic diversity of members of previously uncultivated epsilon-proteobacteria in deep-sea hydrothermal fields. FEMS Microbiol Lett 218:167–174.PubMedGoogle Scholar
  54. 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.CrossRefPubMedGoogle Scholar
  55. Takai K, Campbell BJ, Cary SC, Suzuki M, Oida H, Nunoura T, Hirayama H, Nakagawa S, Suzuki Y, Inagaki F, Horikoshi K (2005) Enzymatic and genetic characterization of carbon and energy metabolisms by deep-sea hydrothermal chemolithoautotrophic isolates of Epsilonproteobacteria. Appl Environ Microbiol 71:7310–7320.CrossRefPubMedGoogle Scholar
  56. Takai K, Suzuki M, Nakagawa S, Miyazaki M, Suzuki Y, Inagaki F, Horikoshi K (2006) Sulfurimonas paralvinellae sp. nov., a novel mesophilic, hydrogen- and sulfur-oxidizing chemolithoautotroph within the Epsilonproteobacteria isolated from a deep-sea hydrothermal vent polychaete nest, reclassification of Thiomicrospira denitrificans as Sulfurimonas denitrificans comb. nov. and emended description of the genus Sulfurimonas. Int J Syst Evol Microbiol 56:1725–1733.CrossRefPubMedGoogle Scholar
  57. Taylor CD, Wirsen CO (1997) Microbiology and ecology of filamentous sulfur formation. Science 277:1483–1485.CrossRefGoogle Scholar
  58. Taylor CD, Wirsen CO, Gaill F (1999) Rapid microbial production of filamentous sulfur mats at hydrothermal vents. Appl Environ Microbiol 65:2253–2255.PubMedGoogle Scholar
  59. Technische Universität München (2007) The ARB project. http://www.arb-home.de.
  60. Teske A, Nelson D (2006) The genera Beggiatoa and Thioploca. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) Proteobacteria: gamma subclass. The prokaryotes. A handbook on the biology of bacteria, vol 6, 3rd edn. Springer, New York, pp 784–812.Google Scholar
  61. Teske A, Brinkhoff T, Muyzer G, Moser DP, Rethmeier J, Jannasch HW (2000) Diversity of thiosulfate-oxidizing bacteria form marine sediments and hydrothermal vents. Appl Environ Microbiol 66:3125–3133.CrossRefPubMedGoogle Scholar
  62. Timmer-Ten Hoor A (1975) A new type of thiosulphate oxidizing, nitrate reducing microorganisms: Thiomocrospira denitrificans sp. nov. Neth J Sea Res 9:344–350.CrossRefGoogle Scholar
  63. Tivey MK (2004) The remarkable diversity of seafloor vents. Oceanus 42:60–65.Google Scholar
  64. Urakawa H, Dubilier N, Fujiwara Y, Cunningham DE, Kojima S, Stahl DA (2005) Hydrothermal vent gastropods from the same family (Provannidae) harbor epsilon and gammaproteobacterial endosymbionts. Environ Microbiol 7:750–754.CrossRefPubMedGoogle Scholar
  65. Wilcock WSD, DeLong EF, Kelley DS, Baross JA, Cary SC (eds) (2004) The subseafloor biosphere at mid-ocean ridges. Geophysics monographs 144. American Geological Union, Washington.Google Scholar
  66. Wirsen (2004) Is life thriving deep beneath the seafloor? Oceanus 42:72–77.Google Scholar
  67. Wirsen CO, Brinkhoff T, Kuever J, Muyzer G, Molyneaux S, Jannasch HW (1998) A new Thiomicrospira strain from the Mid-Atlantic Ridge compared to known hydrothermal vent isolates. Appl Environ Microbiol 64:4057–4059.PubMedGoogle Scholar
  68. Wirsen CO, Sievert SM, Cavanaugh CM, Molyneaux SJ, Ahmad A, Taylor LT, DeLong EF, Taylor CD (2002) Characterization of an autotrophic sulfide-oxidizing marine Arcobacter sp. that produces filamentous sulfur. Appl Environ Microbiol 68:316–325.CrossRefPubMedGoogle Scholar
  69. Xu J (2006) Microbial ecology in the age of genomics and metagenomics: concepts, tools, and recent advances. Mol Ecol 15:1713–1731.CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2008

Authors and Affiliations

  • Stefan M. Sievert
    • 1
  • Michael Hügler
    • 1
  • Craig D. Taylor
    • 1
  • Carl O. Wirsen
    • 1
  1. 1.Biology DepartmentWoods Hole Oceanographic InstitutionWoods HoleUSA

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