Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Hydrogen is an energy source for hydrothermal vent symbioses


The discovery of deep-sea hydrothermal vents in 1977 revolutionized our understanding of the energy sources that fuel primary productivity on Earth. Hydrothermal vent ecosystems are dominated by animals that live in symbiosis with chemosynthetic bacteria. So far, only two energy sources have been shown to power chemosynthetic symbioses: reduced sulphur compounds and methane. Using metagenome sequencing, single-gene fluorescence in situ hybridization, immunohistochemistry, shipboard incubations and in situ mass spectrometry, we show here that the symbionts of the hydrothermal vent mussel Bathymodiolus from the Mid-Atlantic Ridge use hydrogen to power primary production. In addition, we show that the symbionts of Bathymodiolus mussels from Pacific vents have hupL, the key gene for hydrogen oxidation. Furthermore, the symbionts of other vent animals such as the tubeworm Riftia pachyptila and the shrimp Rimicaris exoculata also have hupL. We propose that the ability to use hydrogen as an energy source is widespread in hydrothermal vent symbioses, particularly at sites where hydrogen is abundant.

This is a preview of subscription content

Access options

Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: Hydrogen consumption in Bathymodiolus gills.
Figure 2: The sulphur-oxidizing symbiont has the gene for hydrogen uptake, which it expresses.
Figure 3: Hydrogen is consumed in mussel beds of B. puteoserpentis.

Accession codes

Data deposits

All hupL sequences have been deposited at NCBI under accession numbers FR851255–FR851274. The sequences that make up the genome fragment and the RAST annotation can be found at NCBI under project identification 65421 (accession numbers CAEB01000001–CAEB01000078).


  1. Corliss, J. B. et al. Submarine thermal springs in the Galapagos Rift. Science 203, 1073–1083 (1979)

    ADS  CAS  Article  PubMed  Google Scholar 

  2. Cavanaugh, C. M., Gardiner, S. L., Jones, M. L., Jannasch, H. W. & Waterbury, J. B. Prokaryotic cells in the hydrothermal vent tube worm Riftia pachyptila Jones: possible chemoautotrophic symbionts. Science 213, 340–342 (1981)

    ADS  CAS  Article  PubMed  Google Scholar 

  3. Felbeck, H. Chemoautotrophic potential of the hydrothermal vent tube worm, Riftia pachyptila Jones (Vestimentifera). Science 213, 336–338 (1981)

    ADS  CAS  Article  PubMed  Google Scholar 

  4. Childress, J. J. et al. A methanotrophic marine molluscan (Bivalvia, Mytilidae) symbiosis: mussels fueled by gas. Science 233, 1306–1308 (1986)

    ADS  CAS  Article  PubMed  Google Scholar 

  5. Cavanaugh, C. M., Levering, P. R., Maki, J. S., Mitchell, R. & Lidstrom, M. E. Symbiosis of methylotrophic bacteria and deep-sea mussels. Nature 325, 346–348 (1987)

    ADS  Article  Google Scholar 

  6. Dubilier, N., Bergin, C. & Lott, C. Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nature Rev. Microbiol. 6, 725–740 (2008)

    CAS  Article  Google Scholar 

  7. Tivey, M. K. Generation of seafloor hydrothermal vent fluids and associated mineral deposits. Oceanography (Wash. D.C.) 20, 50–65 (2007)

    Article  Google Scholar 

  8. Fisher, C. R., Takai, K. & Le Bris, N. Hydrothermal vent ecosystems. Oceanography (Wash. D.C.) 20, 14–23 (2007)

    Article  Google Scholar 

  9. Takai, K., Nakagawa, S., Reysenbach, A.-L. & Hock, J. In Back-Arc Spreading Systems—Geological, Biological, Chemical, and Physical Interactions (eds Christie, D. M. et al.) 185–213 (American Geophysical Union, 2006)

    Book  Google Scholar 

  10. Perner, M. et al. The influence of ultramafic rocks on microbial communities at the Logatchev hydrothermal field, located 15° N on the Mid-Atlantic Ridge. FEMS Microbiol. Ecol. 61, 97–109 (2007)

    CAS  Article  PubMed  Google Scholar 

  11. Schmidt, K., Koschinsky, A., Garbe-Schönberg, D., de Carvalho, L. M. & Seifert, R. Geochemistry of hydrothermal fluids from the ultramafic-hosted Logatchev hydrothermal field, 15° N on the Mid-Atlantic Ridge: temporal and spatial investigation. Chem. Geol. 242, 1–21 (2007)

    ADS  CAS  Article  Google Scholar 

  12. Amend, J. P. & Shock, E. L. Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and Bacteria. FEMS Microbiol. Rev. 25, 175–243 (2001)

    CAS  Article  PubMed  Google Scholar 

  13. Gebruk, A. V., Chevaldonné, P., Shank, T., Lutz, R. A. & Vrijenhoek, R. C. Deep-sea hydrothermal vent communities of the Logatchev area (14° 45′ N, Mid-Atlantic Ridge): diverse biotopes and high biomass. J. Mar. Biol. Assoc. UK 80, 383–393 (2000)

    Article  Google Scholar 

  14. Duperron, S. et al. A dual symbiosis shared by two mussel species, Bathymodiolus azoricus and Bathymodiolus puteoserpentis (Bivalvia: Mytilidae), from hydrothermal vents along the northern Mid-Atlantic Ridge. Environ. Microbiol. 8, 1441–1447 (2006)

    CAS  Article  PubMed  Google Scholar 

  15. Petersen, J. M. & Dubilier, N. Methanotrophic symbioses in marine invertebrates. Environ. Microbiol. Rep. 1, 319–335 (2009)

    CAS  Article  PubMed  Google Scholar 

  16. Wendeberg, A., Zielinski, F. U., Borowski, C. & Dubilier, N. Expression patterns of mRNAs for methanotrophy and thiotrophy in symbionts of the hydrothermal vent mussel Bathymodiolus puteoserpentis . ISME J. 10.1038/ismej.2011.81 (7 July 2011)

  17. Vignais, P. M. & Billoud, B. Occurrence, classification, and biological function of hydrogenases: an overview. Chem. Rev. 107, 4206–4272 (2007)

    CAS  Article  PubMed  Google Scholar 

  18. Bernhard, M., Schwartz, E., Rietdorf, J. & Friedrich, B. The Alcaligenes eutrophus membrane-bound hydrogenase gene locus encodes functions involved in maturation and electron transport coupling. J. Bacteriol. 178, 4522–4529 (1996)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. Meyer, O. & Schlegel, H. G. Reisolation of the carbon monoxide utilizing hydrogen bacterium Pseudomonas carboxydovorans (Kistner) comb. nov. Arch. Microbiol. 118, 35–43 (1978)

    CAS  Article  PubMed  Google Scholar 

  20. Schwartz, E. & Friedrich, B. in The Prokaryotes: A Handbook on the Biology of Bacteria (eds Dworkin, M. et al.) Vol. 2, 496–563 (Springer, 2006)

    Book  Google Scholar 

  21. Nelson, D. C., Hagan, K. D. & Edwards, D. B. The gill symbiont of the hydrothermal vent mussel Bathymodiolus thermophilus is a psychrophilic, chemoautotrophic, sulfur bacterium. Mar. Biol. 121, 487–495 (1995)

    Article  Google Scholar 

  22. Haase, K. M. et al. Diking, young volcanism and diffuse hydrothermal activity on the southern Mid-Atlantic Ridge: the Lilliput field at 9° 33′ S. Mar. Geol. 266, 52–64 (2009)

    ADS  Article  Google Scholar 

  23. Haase, K. M. et al. Young volcanism and related hydrothermal activity at 5° S on the slow-spreading southern Mid-Atlantic Ridge. Geochem. Geophys. Geosys. 8, Q11002 (2007)

    ADS  Article  Google Scholar 

  24. Friedrich, B. & Schwartz, E. Molecular biology of hydrogen utilization in aerobic chemolithotrophs. Annu. Rev. Microbiol. 47, 351–383 (1993)

    CAS  Article  PubMed  Google Scholar 

  25. Zielinski, F. U. et al. Widespread occurrence of an intranuclear bacterial parasite in vent and seep bathymodiolin mussels. Environ. Microbiol. 11, 1150–1167 (2009)

    CAS  Article  PubMed  Google Scholar 

  26. Ohmura, N., Sasaki, K., Matsumoto, N. & Saiki, H. Anaerobic respiration using Fe3+, S0, and H2 in the chemolithoautotrophic bacterium Acidithiobacillus ferrooxidans . J. Bacteriol. 184, 2081–2087 (2002)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. Imhoff, J. F., Hiraishi, A. & Sühling, J. in Bergey’s Manual of Systematic Bacteriology (eds Brenner, D. J. et al.) Vol. 2, part A, 119–132 (Springer, 2005)

    Book  Google Scholar 

  28. DiSpirito, A. A., Kunz, R. C., Choi, D.-W. & Zahn, J. A. in Respiration in Archaea and Bacteria. (ed. Zannoni, D. ) Vol. 2, 149–168 (Springer, 2004)

    Book  Google Scholar 

  29. Olson, J. W. & Maier, R. J. Molecular hydrogen as an energy source for Helicobacter pylori . Science 298, 1788–1790 (2002)

    ADS  CAS  Article  PubMed  Google Scholar 

  30. Bowien, B. & Schlegel, H. G. Physiology and biochemistry of aerobic hydrogen-oxidizing bacteria. Annu. Rev. Microbiol. 35, 405–452 (1981)

    CAS  Article  PubMed  Google Scholar 

  31. Moraru, C., Lam, P., Fuchs, B. M., Kuypers, M. M. M. & Amann, R. GeneFISH—an in situ technique for linking gene presence and cell identity in environmental microorganisms. Environ. Microbiol. 12, 3057–3073 (2010)

    CAS  Article  PubMed  Google Scholar 

  32. Constant, P., Piossant, L. & Villemur, R. Tropospheric H2 budget and the response of its soil uptake under the changing environment. Sci. Total Environ. 407, 1809–1823 (2009)

    ADS  CAS  Article  PubMed  Google Scholar 

  33. Tromp, T., Shia, R.-L., Allen, M., Eiler, J. M. & Yung, Y. L. Potential environmental impact of a hydrogen economy on the stratosphere. Science 300, 1740–1742 (2003)

    ADS  CAS  Article  PubMed  Google Scholar 

  34. Perner, M., Petersen, J. M., Zielinski, F., Gennerich, H. H. & Seifert, R. Geochemical constraints on the diversity and activity of H2-oxidizing microorganisms in diffuse hydrothermal fluids from a basalt- and an ultramafic-hosted vent. FEMS Microbiol. Ecol. 74, 55–71 (2010)

    CAS  Article  PubMed  Google Scholar 

  35. Punshon, S., Moore, R. M. & Xie, H. Net loss rates and distribution of molecular hydrogen (H2) in mid-latitude coastal waters. Mar. Chem. 105, 129–139 (2007)

    CAS  Article  Google Scholar 

  36. Welhan, J. A. & Craig, H. in Hydrothermal Processes at Seafloor Spreading Centers (eds Rona, P. A. et al.) 391–410 (Plenum, 1983)

    Book  Google Scholar 

  37. Lilley, M. D., DeAngelis, M. A. & Gordon, L. I. CH4, H2, CO and N2O in submarine hydrothermal vent waters. Nature 300, 48–50 (1982)

    ADS  CAS  Article  Google Scholar 

  38. Hügler, M., Petersen, J. M., Dubilier, N., Imhoff, J. F. & Sievert, S. M. Pathways of carbon and energy metabolism of the epibiotic community associated with the deep-sea hydrothermal vent shrimp Rimicaris exoculata . PLoS ONE 6, e16018 (2011)

    ADS  Article  PubMed  PubMed Central  Google Scholar 

  39. Zhou, J. Z., Bruns, M. A. & Tiedje, J. M. DNA recovery from soils of diverse composition. Appl. Environ. Microbiol. 62, 316–322 (1996)

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Csáki, R., Hanczár, T., Bodrossy, L., Murrell, J. C. & Kovács, K. L. Molecular characterization of structural genes coding for a membrane bound hydrogenase in Methylococcus capsulatus (Bath). FEMS Microbiol. Lett. 205, 203–207 (2001)

    Article  PubMed  Google Scholar 

  41. Petersen, J. M. et al. Dual symbiosis of the vent shrimp Rimicaris exoculata with filamentous gamma- and epsilonproteobacteria at four Mid-Atlantic Ridge hydrothermal vent fields. Environ. Microbiol. 12, 2204–2218 (2010)

    CAS  PubMed  Google Scholar 

  42. Ludwig, W. et al. ARB: a software environment for sequence data. Nucleic Acids Res. 32, 1363–1371 (2004)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  43. Katoh, K., Asimenos, G. & Toh, H. Multiple alignment of DNA sequences with MAFFT. Methods Mol. Biol. 39–64. (2009)

  44. Aziz, R. K. et al. The RAST server: Rapid annotations using subsystems technology. BMC Genomics 9, 75 (2008)

    Article  PubMed  PubMed Central  Google Scholar 

  45. Moraru, C., Moraru, G., Fuchs, B. M. & Amann, R. Concepts and software for a rational design of polynucleotide probes. Environ. Microbiol. Rep. 3, 69–78 (2011)

    CAS  Article  PubMed  Google Scholar 

  46. Pernthaler, A., Pernthaler, J. & Amann, R. Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl. Environ. Microbiol. 68, 3094–3101 (2002)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. Wankel, S. D. et al. Influence of subsurface biosphere on geochemical fluxes from diffuse hydrothermal fluids. Nature Geosci. 4, 461–468 (2011)

    ADS  CAS  Article  Google Scholar 

  48. Le Pennec, M. & Hily, A. Anatomie, structure et ultrastructure de la branchie d’un Mytilidae des sites hydrothermeaux du Pacifique oriental. Oceanol. Acta 7, 517–523 (1984)

    Google Scholar 

Download references


We thank the chief scientists, and the captains and crews of the research vessels and remotely operated vehicles involved in sampling and analyses at sea. Thank you to D. Garbe-Schönberg, K. van der Heijden and J. Stecher for on-board sampling and analysis, and S. Duperron, M.-A. Cambon-Bonavita and M. Zbinden for providing samples. We acknowledge B. Friedrich and O. Lenz for the antiserum against the C. necator uptake hydrogenase, J. Milucka for help with western blots and T. Holler for culturing C. necator. S. Wetzel provided technical assistance. This work was supported by the German Science Foundation (DFG) Priority Program 1144 “From Mantle to Ocean: Energy-, Material- and Life Cycles at Spreading Axes” (publication number 60), the DFG Cluster of Excellence “The Ocean in the Earth System” at MARUM (Center for Marine Environmental Sciences), and the Max Planck Society.

Author information

Authors and Affiliations



J.M.P., F.U.Z., T.P., R.S., C.B., D.F. and N.D. did the on-board experiments during the research cruises. F.U.Z. analysed the data from physiology experiments. J.M.P. amplified and sequenced hupL, analysed the genome data, did western blots and immunohistochemistry. C.M. and R.A. did the geneFISH. S.H., S.D.W. and P.R.G. did the in situ mass spectrometry and analysed the data. V.B. and E.P. did the genome sequencing and assembly. W.B. did the thermodynamic modelling. J.M.P., F.U.Z. and N.D. conceived the study and wrote the paper.

Corresponding author

Correspondence to Nicole Dubilier.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

The file contains, Supplementary Materials and Methods, a Supplementary Discussion, Supplementary Figures 1-7 with legends, Supplementary Tables 1-7 and additional references. (PDF 3734 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Petersen, J., Zielinski, F., Pape, T. et al. Hydrogen is an energy source for hydrothermal vent symbioses. Nature 476, 176–180 (2011).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:

Further reading


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing