Skip to main content

Thank you for visiting nature.com. 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.

  • Letter
  • Published:

A marine microbial consortium apparently mediating anaerobic oxidation of methane

Nature volume 407, pages 623–626 (2000)Cite this article

Abstract

A large fraction of globally produced methane is converted to CO2 by anaerobic oxidation in marine sediments1. Strong geochemical evidence for net methane consumption in anoxic sediments is based on methane profiles2, radiotracer experiments3 and stable carbon isotope data4. But the elusive microorganisms mediating this reaction have not yet been isolated, and the pathway of anaerobic oxidation of methane is insufficiently understood. Recent data suggest that certain archaea reverse the process of methanogenesis by interaction with sulphate-reducing bacteria5,6,7. Here we provide microscopic evidence for a structured consortium of archaea and sulphate-reducing bacteria, which we identified by fluorescence in situ hybridization using specific 16S rRNA-targeted oligonucleotide probes. In this example of a structured archaeal-bacterial symbiosis, the archaea grow in dense aggregates of about 100 cells and are surrounded by sulphate-reducing bacteria. These aggregates were abundant in gas-hydrate-rich sediments with extremely high rates of methane-based sulphate reduction, and apparently mediate anaerobic oxidation of methane.

Access through your institution
Buy or subscribe

This is a preview of subscription content, access via your institution

Access options

Access through your institution

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Depth profiles of various quantities from methane-rich sediments.
Figure 2: In situ identification of archaea/SRB aggregates with fluorescently labelled rRNA-targeted oligonucleotide probes.
Figure 3

Similar content being viewed by others

References

  1. Reeburgh, W. S. in Dynamic Environment of the Ocean Floor (eds Fanning, K. & Manheim, F. T.) 203–217 (Heath, Lexington, Massachusetts, 1982).

    Google Scholar 

  2. Martens, C. S. & Berner, R. A. Interstitial water chemistry of Long Island Sound sediments. I, Dissolved gases. Limnol. Oceanogr. 22, 10–25 ( 1977).

    Article  ADS  CAS  Google Scholar 

  3. Iversen, N. & Jørgensen, B. B. Anaerobic methane oxidation rates at the sulfate-methane transition in marine sediments from Kattegat and Skagerrak (Denmark). Limnol. Oceanogr. 30, 944–955 (1985).

    Article  ADS  CAS  Google Scholar 

  4. Alperin, M. J., Reeburgh, W. S. & Whiticar, M. J. Carbon and hydrogen isotope fractionation resulting from anaerobic methane oxidation. Glob. Biochem. Cycles 2, 279–288 (1988).

    Article  ADS  CAS  Google Scholar 

  5. Hoehler, T. M., Alperin, M. J., Albert, D. B. & Martens, C. S. Field and laboratory studies of methane oxidation in an anoxic marine sediment: Evidence for a methanogenic-sulfate reducer consortium. Glob. Biogeochem. Cycles 8, 451–463 ( 1994).

    Article  ADS  CAS  Google Scholar 

  6. Hansen, L. B., Finster, K., Fossing, H. & Iversen, N. Anaerobic methane oxidation in sulfate depleted sediments: effects of sulfate and molybdate additions. Aquat. Microb. Ecol. 14, 195– 204 (1998).

    Article  Google Scholar 

  7. Hinrichs, K. U., Hayes, J. M., Sylva, S. P., Brewer, P. G. & DeLong, E. F. Methane-consuming archaebacteria in marine sediments. Nature 398, 802– 805 (1999).

    Article  ADS  CAS  Google Scholar 

  8. Suess, E. et al. Gas hydrate destabilization: enhanced dewatering, benthic material turnover and large methane plumes at the Cascadia convergent margin. Earth Planet. Sci. Lett. 170, 1–5 (1999).

    Article  ADS  CAS  Google Scholar 

  9. Linke, P. et al. In situ measurement of fluid flow from cold seeps at active continental margins. Deep Sea Res. 41, 721– 739 (1994).

    Article  ADS  Google Scholar 

  10. Bohrmann, G., Linke, P., Suess, P. & Pfannkuche, O. RV SONNE Cruise Report SO143: TECFLUX-I-1999. GEOMAR Rep. 93, (2000).

  11. Aharon, P. & Fu, B. Microbial sulfate reduction rates and sulfur and oxygen isotope fractionations at oil and gas seeps in deepwater Gulf of Mexico. Geochim. Cosmochim. Acta 64, 233–246 (2000).

    Article  ADS  CAS  Google Scholar 

  12. Elvert, M., Suess, E. & Whiticar, M. J. Anaerobic methane oxidation associated with marine gas hydrates: superlight C-isotopes from saturated and unsaturated C 20 and C25 irregular isoprenoids. Naturwissenschaften 86, 295–300 ( 1999).

    Article  ADS  CAS  Google Scholar 

  13. Koga, Y., Morii, H., Akagawa-Matushita, M. & Ohga, M. Correlation of polar lipid composition with 16S rRNA phylogeny in methanogens. Further analysis of lipid component parts. Biosci. Biotechnol. Biochem. 62, 230–236 ( 1998).

    Article  CAS  Google Scholar 

  14. Thiel, V. et al. Highly isotopically depleted isoprenoids: molecular markers for ancient methane venting. Geochim. Cosmochim. Acta 63 , 3959–3966 (1999).

    Article  ADS  CAS  Google Scholar 

  15. Pancost, R. D. et al. Biomarker evidence for widespread anaerobic methane oxidation in Mediterranean sediments by a consortium of methanogenic archaea and bacteria. Appl. Environ. Microbiol. 66, 1126– 1132 (2000).

    Article  CAS  Google Scholar 

  16. Amann, R. I., Krumholz, L. & Stahl, D. A. Fluorescent-oligonucleotide probing of whole cells for determinative phylogenetic and environmental studies in microbiology. J. Bacteriol. 172, 762– 770 (1990).

    Article  CAS  Google Scholar 

  17. Amann, R. I. et al. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl. Environ. Microbiol. 56, 1919–1925 (1990).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Manz, W., Eisenbrecher, M., Neu, T. R. & Szewzyk, U. Abundance and spatial organization of Gram-negative sulfate-reducing bacteria in activated sludge investigated by in situ probing with specific 16S rRNA targeted oligonucleotides. FEMS Microbiol. Ecol. 25 , 43–61 (1998).

    Article  CAS  Google Scholar 

  19. Ravenschlag, K., Sahm, K., Knoblauch, C., Jørgensen, B. B. & Amann, R. Community structure, cellular rRNA content and activity of sulfate-reducing bacteria in marine Arctic sediments. Appl. Environ. Microbiol. 66, 3590–3600 (2000).

    Article  Google Scholar 

  20. Sahm, K., Knoblauch, C. & Amann, R. Phylogenetic affiliation and quantification of psychrophilic sulfate-reducing isolates in marine arctic sediments. Appl. Environ. Microbiol. 65, 3976–3981 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Devereux, R., Kane, M. D., Winfrey, J. & Stahl, D. A. Genus- and group-specific hybridization probes for determinative and environmental studies of sulfate-reducing bacteria. Syst. Appl. Microbiol. 15, 601 –609 (1992).

    Article  CAS  Google Scholar 

  22. Rabus, R., Hansen, T. A. & Widdel, F. in The Prokaryotes: An Evolving Electronic Resource for the Microbiological Community (eds Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.-H. & Stackebrandt, E.) (Springer, New York, 2000).

    Google Scholar 

  23. Fröstl, J. M. & Overmann, J. Physiology and tactic response of the phototrophic consortium “Chlorochromatium aggregatum”. Arch. Microbiol. 169, 129–135 (1998).

    Article  Google Scholar 

  24. Mobarry, B., Wagner, M., Urbain, V., Rittmann, B. E. & Stahl, D. A. Phylogenetic probes for analyzing abundance and spatial organization of nitrifying bacteria. Appl. Environ. Microb. 62, 2156–2162 (1996).

    CAS  Google Scholar 

  25. Boone, D. R., Johnson, R. L. & Liu, Y. Diffusion of the interspecies electron carriers H 2 and formate in methanogenic ecosystems and its implications in the measurement of Km and H2 or formate uptake. Appl. Environ. Microbiol. 55, 1735– 1741 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Valentine, D. L. & Reeburgh, W. S. New perspectives on anaerobic methane oxidation. Environ. Microb. 2 (in the press).

  27. Preuβ, A., Schauder, R. & Fuchs, G. Carbon isotope fractionation by autotrophic bacteria with three different CO2 fixation pathways. Z. Naturforsch. C 44, 397–402 ( 1989).

    Article  Google Scholar 

  28. Fossing, H. & Jørgensen, B. B. Measurement of bacterial sulfate reduction in sediments: Evaluation of a single-step chromium reduction method. Biogeochemistry 8, 205– 222 (1989).

    Article  CAS  Google Scholar 

  29. Snaidr, J., Amann, R., Huber, I., Ludwig, W. & Schleifer, K. H. Phylogenetic analysis and in situ identification of bacteria in activated sludge. Appl. Environ. Microbiol. 63, 2884–2896 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Stumm, W. & Morgan, J. J. Aquatic Chemistry 2nd edn (Wiley, New York, 1981).

    Google Scholar 

Download references

Acknowledgements

The expedition SO143 was performed as part of the program TECFLUX, which addresses geophysical, biogeochemical and hydrographic processes associated with fluid venting from the Cascadia continental margin. The field work of TECFLUX’99 was jointly planned, coordinated and performed by the GEOMAR Research Center for Marine Geosciences at Kiel and the College of Ocean and Atmospheric Sciences (COAS) of Oregon State University, Corvallis. We thank these institutions for the invitation to participate. The TECFLUX programme is supported in Germany by the Bundesministerium für Bildung und Forschung and in the United States by the National Science Foundation. We thank the officers, crew and shipboard scientific party of RV SONNE for support at sea during the expedition SO-143, P. Linke and M. Elvert for providing some of the sediment samples, A. Kähler, T. Lösekann, H. Löbner and G. Tsounis for help with the SRR measurements, and J. Wulf for help with the micrograph photography. We thank C. Arnosti for corrections to the manuscript, and D. Valentine and W. Reeburgh for showing us their manuscript before publication.

Author information

Authors and Affiliations

  1. Max Planck Institute for Marine Microbiology, Bremen, 28359, Germany

    Antje Boetius, Katrin Ravenschlag, Carsten J. Schubert, Friedrich Widdel, Armin Gieseke, Rudolf Amann, Bo Barker Jørgensen & Ursula Witte

  2. GEOMAR Research Center for Marine Geosciences, Kiel, 24148, Germany

    Dirk Rickert & Olaf Pfannkuche

Authors
  1. Antje Boetius
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Katrin Ravenschlag
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Carsten J. Schubert
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Dirk Rickert
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. Friedrich Widdel
    View author publications

    You can also search for this author inPubMed Google Scholar

  6. Armin Gieseke
    View author publications

    You can also search for this author inPubMed Google Scholar

  7. Rudolf Amann
    View author publications

    You can also search for this author inPubMed Google Scholar

  8. Bo Barker Jørgensen
    View author publications

    You can also search for this author inPubMed Google Scholar

  9. Ursula Witte
    View author publications

    You can also search for this author inPubMed Google Scholar

  10. Olaf Pfannkuche
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to Antje Boetius.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Cite this article

Boetius, A., Ravenschlag, K., Schubert, C. et al. A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 407, 623–626 (2000). https://doi.org/10.1038/35036572

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35036572

This article is cited by

Search

Advanced search

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