Skip to main content

Advertisement

SpringerLink
Log in

Geochemical and microbiological evidence for a hydrogen-based, hyperthermophilic subsurface lithoautotrophic microbial ecosystem (HyperSLiME) beneath an active deep-sea hydrothermal field

  • Original Paper
  • Published:
Extremophiles Aims and scope Submit manuscript

Abstract

Subsurface microbial communities supported by geologically and abiologically derived hydrogen and carbon dioxide from the Earth’s interior are of great interest, not only with regard to the nature of primitive life on Earth, but as potential analogs for extraterrestrial life. Here, for the first time, we present geochemical and microbiological evidence pointing to the existence of hyperthermophilic subsurface lithoautotrophic microbial ecosystem (HyperSLiME) dominated by hyperthermophilic methanogens beneath an active deep-sea hydrothermal field in the Central Indian Ridge. Geochemical and isotopic analyses of gaseous components in the hydrothermal fluids revealed heterogeneity of both concentration and carbon isotopic compositions of methane between the main hydrothermal vent (0.08 mM and −13.8‰ PDB, respectively) and the adjacent divergent vent site (0.2 mM and −18.5‰ PDB, respectively), representing potential subsurface microbial methanogenesis, at least in the divergent vent emitting more 13C-depleted methane. Extremely high abundance of magmatic energy sources such as hydrogen (2.5 mM) in the fluids also encourages a hydrogen-based, lithoautotrophic microbial activity. Both cultivation and cultivation-independent molecular analyses suggested the predominance of Methanococcales members in the superheated hydrothermal emissions and chimney interiors along with the other major microbial components of Thermococcales members. These results imply that a HyperSLiME, consisting of methanogens and fermenters, occurs in this tectonically active subsurface zone, strongly supporting the existence of hydrogen-driven subsurface microbial communities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1a, b
Fig. 2a–e

Similar content being viewed by others

References

  • Anderson RT, Chapelle FH, Lovley DR (1998) Evidence against hydrogen-based microbial ecosystems in basalt aquifers. Science 281:976–977

    Article  CAS  PubMed  Google Scholar 

  • Baross JA, Lilley MD, Gordon LI (1982) Is the CH4, H2 and CO venting from submarine hydrothermal systems produced by thermophilic bacteria? Nature 298:366–368

    CAS  Google Scholar 

  • Blöchl E, Rachel R, Burggraf S, Hafenbradl D, Jannasch HW, Stetter KO (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

    Article  CAS  PubMed  Google Scholar 

  • Chapelle FH, O’Neil K, Bradley PM, Methe BA, Ciufo SA, Knobel LL, Lovley DR (2002) A hydrogen-based subsurface microbial community dominated by methanogens. Nature 415:312–315

    PubMed  Google Scholar 

  • Charlou JL, Donval JP, Fouquet Y, Jean-Baptiste P, Holm N (2002) Geochemistry of high H2 and CH4 vent fluids issuing from ultramafic rocks at the Rainbow hydrothermal field (36°14′N, MAR). Chem Geol 191:345–359

    Article  CAS  Google Scholar 

  • Delaney JR, Kelley DS, Lilley MD, Butterfield DA, Baross JA, Wilcock WS, Embley RW, Summit M (1998) The quantum event of oceanic crustal accretion: impacts of diking at mid-ocean ridges. Science 281:222–230

    Article  CAS  Google Scholar 

  • DeMets C, Gordon RG, Argus DF (1988) Intra plate deformation and closure of the Australia–Antarctica–Africa plate circuit. J Geophys Res 93:11877–11897

    Google Scholar 

  • Deming JW, Baross JA (1993) Deep-sea smokers: windows to a subsurface biosphere? Geochim Cosmochim Acta 57:3219–3230

    Article  CAS  PubMed  Google Scholar 

  • Fisk MR, Giovannoni SJ (1999) Sources of nutrients and energy for a deep biosphere on Mars. J Geophys Res 104:11805–11815

    Article  CAS  Google Scholar 

  • Gamo T, Chiba H, Yamanaka T, Okudaira T, Hashimoto J, Tsuchida S, Ishibashi J, Kataoka S, Tsunogai U, Okamura K, Sano Y, Shinjo R (2001) Chemical characteristics of newly discovered black smoker fluids and associated hydrothermal plumes at the Rodriguez Triple Junction, Central Indian Ridge. Earth Planet Sci Lett 193:371–379

    Article  CAS  Google Scholar 

  • Hashimoto J, Ohta S, Gamo T, Chiba H, Yamaguchi T, Tsuchida S, Okudaira T, Watabe H, Yamanaka T, Kitazawa M (2001) First hydrothermal vent communities from the Indian Ocean discovered. Zool Sci 18:717–721

    Google Scholar 

  • Horita J, Berndt ME (1999) Abiogenic methane formation and isotopic fractionation under hydrothermal conditions. Science 285:1055–1057

    Article  PubMed  Google Scholar 

  • House CH, Schopf JW, Stetter KO (2003) Carbon isotopic fractionation by Archaea and other thermophilic prokaryotes. Org Geochem 34:345–356

    Article  CAS  Google Scholar 

  • Jannasch HW, Wirsen CO, Molyneaux SJ, Langworthy TA (1992) Comparative physiological studies on hyperthermophilic Archaea isolated from deep-sea hot vents with emphasis on Pyrococcus strain GB-D. Appl Environ Microbiol 58:3472–3481

    CAS  Google Scholar 

  • Kelly DS, Karson JA, Blackman DK, Früh-Green GL, Butterfield DA, Lilley MD, Olson EJ, Schrenk MD, Roe KK, Lebon GT, Rivizzigno P, the AT3-60 shipboard party (2001) An off-axis hydrothermal vent field near the Mid-Atlantic Ridge at 30°N. Nature 412:145–149

    Article  PubMed  Google Scholar 

  • Kimura H, Asada R, Masta A, Naganuma T (2003) Distribution of microorganisms in the subsurface of the Manus basin hydrothermal vent field in Papua New Guinea. Appl Environ Microbiol 69:644–648

    Article  CAS  PubMed  Google Scholar 

  • Maidak BL, Cole JR, Lilburn TG, Parker Jr CT, Saxman PR, Stredwick JM, Garrity GM, Li B, Olsen GJ, Pramanik S, Schmidt TM, Tiedje JM (2000) The RDP (Ribosomal Database Project) continues. Nucleic Acids Res 28:173–174

    PubMed  Google Scholar 

  • McCollom TM (1999) Methanogenesis as a potential source of chemical energy for primary biomass production by autotrophic organisms in hydrothermal systems on Europa. J Geophys Res 104:30729–30742

    Article  CAS  Google Scholar 

  • Nakagawa S, Takai K, Horikoshi K, Sako Y (2003) Persephonella hydrogeniphila sp. nov., a novel thermophilic, hydrogen-oxidizing bacterium from a deep-sea hydrothermal vent chimney. Int J Syst Evol Microbiol 53:863–869

    Article  CAS  PubMed  Google Scholar 

  • Nakagawa S, Takai K, Horikoshi K, Sako Y (2004b) Aeropyrum camini sp. nov., a strictly aerobic, hyperthermophilic archaeon from a deep-sea hydrothermal vent chimney. Int J Syst Evol Microbiol 54:329–335 (http://dx.doi.org/10.1099/ijs.0.02826-0)

    Article  PubMed  Google Scholar 

  • Sako Y, Takai K, Uchida A, Ishida Y, Katayama Y (1996) Rhodothermus obamensis sp. nov., a modern lineage of extremely thermophilic marine bacterium. Int J Syst Bacteriol 46:1099–1104

    CAS  PubMed  Google Scholar 

  • Schrenk MO, Kelly DS, Delaney JR, Baross JA (2003) Incidence and diversity of microorganisms within the walls of an active deep-sea sulfide chimney. Appl Environ Microbiol 69:3580–3592

    Article  CAS  PubMed  Google Scholar 

  • Seiler W, Giehl H, Roggendorf P (1980) Detection of carbon monoxide and hydrogen by conversion of mercury oxide to mercury vapor. Atmos Technol 12:40–45

    Google Scholar 

  • Shanks WC (2001) Stable isotopes in seafloor hydrothermal systems: vent fluids, hydrothermal deposits, hydrothermal alteration, and microbial processes. In: Valley JW, Cole DR (eds) Stable isotope geochemistry. Mineralogical Society of America, Washington, DC, pp 469–525

  • Stevens TO, McKinley JP (1995) Lithoautotrophic microbial ecosystems in deep basalt aquifers. Science 270:450–454

    CAS  Google Scholar 

  • Straube WL, Deming JW, Somerville CC, Colwell RR, Baross JA (1990) Particulate DNA in smoker fluids: evidence for existence of microbial populations in hot hydrothermal systems. Appl Environ Microbiol 56:1440–1447

    CAS  Google Scholar 

  • Summit M, Baross JA (1998) Thermophilic subseafloor microorganisms from the 1996 North Gorda Ridge eruption. Deep-Sea Res Part II 45:2751–2766

    Article  Google Scholar 

  • Takai K, Horikoshi K (1999) Genetic diversity of Archaea in deep-sea hydrothermal vent environments. Genetics 152:1285–1297

    CAS  PubMed  Google Scholar 

  • Takai K, Horikoshi, K (2000a) Rapid detection and quantification of members of the archaeal community by quantitative PCR using fluorogenic probes. Appl Environ Microbiol 66:5066–5072

    Article  CAS  PubMed  Google Scholar 

  • Takai K, Horikoshi K (2000b) Thermosipho japonicus sp. nov., an extremely thermophilic bacterium isolated from a deep-sea hydrothermal vent in Japan. Extremophiles 4:9–17

    CAS  PubMed  Google Scholar 

  • Takai K, Fujiwara Y (2002) Hydrothermal vents: biodiversity in deep-sea hydrothermal vents. In: Bitton G (ed) Encyclopedia of environmental microbiology. Wiley, New York, pp 1604–1617

  • Takai K, Inoue A, Horikoshi K (1999) Thermaerobacter marianensis gen. nov., sp. nov., an aerobic extremely thermophilic marine bacterium from the 11,000-m deep Mariana Trench. Int J Syst Bacteriol 49:619–628

    CAS  Google Scholar 

  • Takai K, Sugai A, Itoh Y, Horikoshi K (2000) Palaeococcus ferrophilus gen. nov., sp. nov., a barophilic, hyperthermophilic archaeon from a deep-sea hydrothermal vent chimney. Int J Syst Evol Microbiol 50:489–500

    CAS  PubMed  Google Scholar 

  • Takai K, Komatsu T, Inagaki F, Horikoshi K (2001a) Distribution of Archaea in a black smoker chimney structure. Appl Environ Microbiol 67:3618–3629

    CAS  PubMed  Google Scholar 

  • Takai K, Moser DP, Deflaun M, Onstott TC, Fredrickson JK (2001b) Archaeal diversity in waters from deep South African gold mines. Appl Environ Microbiol 67:5750–5760

    Google Scholar 

  • Takai K, Inoue A, Horikoshi K (2002) Methanothermococcus okinawensis sp. nov., a thermophilic, methane-producing archaeon isolated from a Western Pacific deep-sea hydrothermal vent system. Int J Syst Evol Microbiol 52:1089–1095

    Article  CAS  PubMed  Google Scholar 

  • Takai K, Inagaki F, Nakagawa S, Hirayama H, Nunoura T, Sako Y, Nealson KH, Horikoshi K (2003a) Isolation and phylogenetic diversity of members of previously uncultivated ε-Proteobacteria in deep-sea hydrothermal fields. FEMS Microbiol Lett 218:167–174

    Article  CAS  PubMed  Google Scholar 

  • Takai K, Kobayashi H, Nealson KH, Horikoshi K (2003b) Deferribacter desulfuricans sp. nov., a novel sulfur-, nitrate- and arsenate-reducing thermophile isolated from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol 53:839–846

    Article  CAS  PubMed  Google Scholar 

  • Takai K, Mormile MR, McKinley JP, Brockman FJ, Holben WE, Kovacik WP Jr, Fredrickson JK (2003c) Shifts in archaeal communities associated with lithological and geochemical variations in subsurface Cretaceous rock. Environ Microbiol 5:309–320

    Article  CAS  PubMed  Google Scholar 

  • Takai K, Nakagawa S, Sako Y, Horikoshi K (2003d) Balnearium lithotrophicum gen. nov., sp. nov., a novel thermophilic, strictly anaerobic, hydrogen-oxidizing chemolithoautotroph isolated from a black smoker chimney in the Suiyo Seamount hydrothermal system. Int J Syst Evol Microbiol 53:1947–1954

    Article  CAS  PubMed  Google Scholar 

  • Tanner MA, Grobel BM, Dojka MA, Pace NR (1998) Specific ribosomal DNA sequences from diverse environmental settings correlate with experimental contaminants. Appl Environ Microbiol 64:3110–3113

    CAS  PubMed  Google Scholar 

  • Tsunogai U, Ishibashi J, Wakita H, Gamo T, Watanabe K, Kajimura T, Kanayama S, Sakai H (1994) Peculiar features of Suiyo Seamount hydrothermal fluids, Izu-Bonin arc: differences from subaerial volcanism. Earth Planet Sci Lett 126:289–301

    CAS  Google Scholar 

  • Tsunogai U, Yoshida N, Ishibashi J, Gamo T (2000) Carbon isotopic distribution of methane in deep-sea hydrothermal plume, Myojin Knoll Caldera, Izu-Bonin arc: implications for microbial methane oxidation in ocean and applications to heat flux estimation. Geochim Cosmochim Acta 64:2439–2452

    CAS  Google Scholar 

  • Tsunogai U, Kouzuma F, Nakayama N, Gamo T, Kaneko T (2002a) Development of multi-bottle gas-tight water sampler WHATS for sampling sea-floor venting fluids (in Japanese with English abstract). JAMSTEC J Deep Sea Res 21:91–95

    Google Scholar 

  • Tsunogai U, Nakagawa F, Komatsu D, Gamo T (2002b) Stable carbon and oxygen isotopic analysis of atmospheric carbon monoxide using CF-IRMS by isotope-ratio monitoring of CO. Anal Chem 74:5695–5700

    Article  CAS  PubMed  Google Scholar 

  • Van Dover CL, Humphris SE, Fornari D, Cavanaugh CM, Collier R, Goffredi SK, Hashimoto J, Lilly MD, Reysenbach AL, Shank TM, Von Damm KL, Banta A, Gallant RM, Götz D, Green D, Hall J, Harmer TL, Hurtado LA, Johnson P, McKiness ZP, Meredith C, Olson E, Pan IL, Turnipseed M, Won Y, Young III CR, Vrijenhoek RC (2001) Biogeography and ecological setting of Indian Ocean hydrothermal vents. Science 294:818–823

    PubMed  Google Scholar 

  • Von Damm KL (1995) Controls on the chemistry and temporal variability of seafloor hydrothermal fluids. In: Humphris SE, Zierenberg RA, Mullineaux LS, Tompson RE (eds) Geophysical monograph 91 seafloor hydrothermal system. American Geographical Union, Washington, DC, pp 222–247

Download references

Acknowledgements

We would like to thank Dr. Katsuyuki Uematsu for assistance in preparing SEM-EDS analyses. We would like to thank Dr. Kei Okamura at Kyoto University for coordinating ICP measurements of hydrothermal fluid. We are very grateful to the crews of R/V Yokosuka and the operation team of DSV Shinkai 6500 for helping us to collect deep-sea hydrothermal vent samples. This research was partly supported by the following grants: MEXT Grant-in Aid for the 21st Century COE Program “Neo-Science of Natural History” at Hokkaido University, MEXT Special Coordination Fund “Archaean Park” project, and NEDO Proposal Based Research and Development Project (ID 02A53002d).

Author information

Authors and Affiliations

  1. Subground Animalcule Retrieval (SUGAR) Project, Frontier Research System for Extremophiles, Japan Marine Science and Technology Center (JAMSTEC), 2-15 Natsushima-cho, Yokosuka 237-0061, Japan

    Ken Takai, Hisako Hirayama, Kenneth H. Nealson & Koki Horikoshi

  2. Division of Earth and Planetary Sciences, Graduate School of Science, Hokkaido University, N10, W8, Sapporo 060-0810, Japan

    Toshitaka Gamo, Urumu Tsunogai & Noriko Nakayama

  3. Department of Earth Sciences, University of Southern California, 3651 Trousdale Pkwy., Los Angeles, CA, 90089-0740, USA

    Kenneth H. Nealson

Authors
  1. Ken Takai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Toshitaka Gamo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Urumu Tsunogai
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Noriko Nakayama
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hisako Hirayama
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kenneth H. Nealson
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Koki Horikoshi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ken Takai.

Additional information

Communicated by W.D. Grant

Rights and permissions

Reprints and permissions

About this article

Cite this article

Takai, K., Gamo, T., Tsunogai, U. et al. Geochemical and microbiological evidence for a hydrogen-based, hyperthermophilic subsurface lithoautotrophic microbial ecosystem (HyperSLiME) beneath an active deep-sea hydrothermal field. Extremophiles 8, 269–282 (2004). https://doi.org/10.1007/s00792-004-0386-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-004-0386-3

Keywords

Search

Navigation