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.

  • Article
  • Published:

Aerobic production of methane in the sea

Nature Geoscience volume 1, pages 473–478 (2008)Cite this article

Abstract

Methane is a potent greenhouse gas that has contributed approximately 20% to the Earth’s warming since pre-industrial times. The world’s oceans are an important source of methane, comprising 1–4% of annual global emissions. But despite its global significance, oceanic methane production is poorly understood. In particular, methane concentrations in the surface waters of most of the world’s oceans are supersaturated with respect to atmospheric concentrations, but the origin of this methane, which has been thought to be produced exclusively in anaerobic environments, is not known. Here, we measure methane production in seawater samples amended with methylphosphonate, an organic, phosphorus-containing compound. We show that methane is produced aerobically as a by-product of methylphosphonate decomposition in phosphate-stressed waters. Methylphosphonate decomposition, and thus methane production, may be enhanced by the activity of nitrogen-fixing microorganisms. We suggest that aerobic marine methane production will be sensitive to the changes in water-column stratification and nutrient limitation that are likely to result from greenhouse-gas-induced ocean warming.

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

Access options

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: Aerobic production of methane from MPn in glucose-plus-nitrate-amended surface seawater samples collected from Station ALOHA.
Figure 2: Methane accumulation in surface seawater samples collected from Station ALOHA.
Figure 3: Schematic representation of the hypothetical greenhouse-gas balance for an iron (Fe)-stimulated, nitrogen (N2)-fixation bloom in the North Pacific gyre.

Similar content being viewed by others

References

  1. Reeburgh, W. S. Oceanic methane biogeochemistry. Chem. Rev. 107, 486–513 (2007).

    Article  Google Scholar 

  2. Quay, P. et al. The isotopic composition of atmospheric methane. Glob. Biogeochem. Cycles 13, 445–461 (1999).

    Article  Google Scholar 

  3. Lamontagne, R. A., Swinnerton, J. W., Linnenbom, V. J. & Smith, W. D. Methane concentrations in various marine environments. J. Geophys. Res. 78, 5317–5324 (1973).

    Article  Google Scholar 

  4. Scranton, M. I. & Brewer, P. G. Occurrence of methane in the near-surface waters of the western subtropical North Atlantic. Deep-Sea Res. 24, 127–138 (1977).

    Article  Google Scholar 

  5. Tilbrook, B. D. & Karl, D. M. Methane sources, distributions and sinks from California coastal waters to the oligotrophic North Pacific gyre. Mar. Chem. 49, 51–64 (1995).

    Article  Google Scholar 

  6. Rudd, J. W. M. & Taylor, C. D. Methane cycling in aquatic environments. Adv. Aquat. Microbiol. 2, 77–150 (1980).

    Google Scholar 

  7. Kiene, R. P. in Microbial Production and Consumption of Greenhouse Gases: Methane, Nitrogen Oxides, and Halomethanes (eds Rogers, J. E. & Whitman, W. B.) 111–146 (ASM, Washington DC, 1991).

    Google Scholar 

  8. Karl, D. M. & Björkman, K. M. in Biogeochemistry of Marine Dissolved Organic Matter (eds Hansell, D. & Carlson, C.) 246–366 (Elsevier Science, Amsterdam, 2002).

    Google Scholar 

  9. Kittredge, J. S. & Roberts, E. A carbon–phosphorus bond in nature. Science 164, 37–42 (1969).

    Article  Google Scholar 

  10. Kittredge, J. S., Horiguchi, M. & Williams, P. M. Aminophosphonic acids: Biosynthesis by marine phytoplankton. Comput. Biochem. Physiol. 29, 859–863 (1969).

    Article  Google Scholar 

  11. Kolowith, L. C., Ingall, E. D. & Benner, R. Composition and cycling of marine organic phosphorus. Limnol. Oceanogr. 46, 309–320 (2001).

    Article  Google Scholar 

  12. Benitez-Nelson, C. R., O’Neill, L., Kolowith, L. C., Pellechia, P. & Thunell, R. Phosphonates and particulate organic phosphorus cycling in an anoxic marine basin. Limnol. Oceanogr. 49, 1593–1604 (2004).

    Article  Google Scholar 

  13. Cook, A. M., Daughton, C. G. & Alexander, M. Phosphonate utilization by bacteria. J. Bacteriol. 133, 85–90 (1978).

    Google Scholar 

  14. White, A. K. & Metcalf, W. Microbial metabolism of reduced phosphorus compounds. Ann. Rev. Microbiol. 61, 379–400 (2007).

    Article  Google Scholar 

  15. Kononova, S. V. & Nesmeyanova, M. A. Phosphonates and their degradation by microorganisms. Biochemistry 67, 184–195 (2002).

    Google Scholar 

  16. Daughton, C. G., Cook, A. M. & Alexander, M. Biodegradation of phosphonate toxicants yields methane or ethane on cleavage of the C–P bond. FEMS Microbiol. Lett. 5, 91–93 (1979).

    Article  Google Scholar 

  17. Huang, J., Su, Z. & Xu, Y. The evolution of microbial phosphonate degradative pathways. J. Mol. Evol. 61, 682–690 (2005).

    Article  Google Scholar 

  18. DeLong, E. F. et al. Community genomics among stratified microbial assemblages in the ocean’s interior. Science 311, 496–503 (2006).

    Article  Google Scholar 

  19. Venter, J. C. et al. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304, 66–74 (2004).

    Article  Google Scholar 

  20. Moran, M. A. et al. Genome sequence of Silicibacter pomeroyi reveals adaptations to the marine environment. Nature 432, 910–913 (2004).

    Article  Google Scholar 

  21. Dyhrman, S. T. et al. Phosphonate utilization by the globally important marine diazotroph Trichodesmium. Nature 439, 68–71 (2006).

    Article  Google Scholar 

  22. Oremland, R. S. Methanogenic activity in plankton samples and fish intestines: A mechanism for in situ methanogenesis in oceanic surface waters. Limnol. Oceanogr. 24, 1136–1141 (1979).

    Article  Google Scholar 

  23. Marty, D. G. Methanogenic bacteria in seawater. Limnol. Oceanogr. 38, 452–456 (1993).

    Article  Google Scholar 

  24. de Angelis, M. A. & Lee, C. Methane production during zooplankton grazing on marine phytoplankton. Limnol. Oceanogr. 39, 1298–1308 (1994).

    Article  Google Scholar 

  25. Karl, D. M. & Tilbrook, B. D. Production and transport of methane in oceanic particulate organic matter. Nature 368, 732–734 (1994).

    Article  Google Scholar 

  26. Sannigrahi, P., Ingall, E. D. & Benner, R. Nature and dynamics of phosphorus-containing components of marine dissolved and particulate organic matter. Geochim. Cosmochim. Acta 70, 5868–5882 (2006).

    Article  Google Scholar 

  27. Tilbrook, B. D. & Karl, D. M. Dissolved methane distributions, sources, and sinks in the Western Bransfield Strait, Antarctica. J. Geophys. Res. 99, 16383–16393 (1994).

    Article  Google Scholar 

  28. Crutzen, P. J. Methane’s sinks and sources. Nature 350, 380–381 (1991).

    Article  Google Scholar 

  29. Dlugokencky, E. J., Masarie, K. A., Lang, P. M. & Tans, P. P. Continuing decline in the growth rate of the atmospheric methane burden. Nature 393, 447–450 (1998).

    Article  Google Scholar 

  30. Fiore, A. M., Horowitz, L. W., Dlugokencky, E. J. & West, J. J. Impact of meteorology and emissions on methane trends, 1990–2004. Geophys. Res. Lett. 33, L12809 (2006).

    Article  Google Scholar 

  31. Karl, D. M. A sea of change: Biogeochemical variability in the North Pacific subtropical gyre. Ecosystems 2, 181–214 (1999).

    Article  Google Scholar 

  32. Björkman, K. M. & Karl, D. M. Bioavailability of dissolved organic phosphorus in the euphotic zone at Station ALOHA, North Pacific Subtropical Gyre. Limnol. Oceanogr. 48, 1049–1057 (2003).

    Article  Google Scholar 

  33. Karl, D. M. Microbial oceanography: paradigms, processes and promise. Nature Rev. Microbiol. 5, 759–769 (2007).

    Article  Google Scholar 

  34. Moore, J. K., Doney, S. C., Lindsay, K., Mahowald, N. & Michaels, A. F. Nitrogen fixation amplifies the ocean biogeochemical response to decadal timescale variations in mineral dust deposition. Tellus 58, 560–572 (2006).

    Article  Google Scholar 

  35. Hutchins, D. A. et al. CO2 control of Trichodesmium N2 fixation, photosynthesis, growth rates, and elemental ratios: Implications for past, present, and future ocean biogeochemistry. Limnol. Oceanogr. 52, 1293–1304 (2007).

    Article  Google Scholar 

  36. Polovina, J. J., Howell, E. A. & Abecassis, M. Ocean’s least productive waters are expanding. Geophys. Res. Lett. 35, L03618 (2008).

    Article  Google Scholar 

  37. Diaz, J. et al. Marine polyphosphate: A key player in geologic phosphorus sequestration. Science 320, 652–655 (2008).

    Article  Google Scholar 

  38. LaRoche, J. & Breitbarth, E. Importance of the diazotrophs as a source of new nitrogen in the ocean. J. Sea Res. 53, 67–91 (2005).

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank J. Dore for advice and assistance with methane determinations, and A. White and R. Letelier for field assistance, expertise and leadership during the August 2007 R/V Kilo Moana BloomER expedition. This research was supported by the Gordon and Betty Moore Foundation and the National Science Foundation and is a contribution from the Center for Microbial Oceanography: Research and Education (C-MORE).

Author information

Authors and Affiliations

  1. University of Hawaii, Honolulu, Hawaii 96822, USA

    David M. Karl, Lucas Beversdorf, Karin M. Björkman & Matthew J. Church

  2. Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA

    Asuncion Martinez & Edward F. Delong

Authors
  1. David M. Karl
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lucas Beversdorf
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Karin M. Björkman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Matthew J. Church
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Asuncion Martinez
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Edward F. Delong
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

D.M.K. formulated the hypothesis, directed the research and wrote the first draft of the manuscript. L.B. and K.B. carried out most of the experiments. E.F.D. and A.M. conducted and analysed the genome database search. All authors contributed to the experimental design, data interpretation and preparation of the final draft of the manuscript.

Corresponding author

Correspondence to David M. Karl.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Karl, D., Beversdorf, L., Björkman, K. et al. Aerobic production of methane in the sea. Nature Geosci 1, 473–478 (2008). https://doi.org/10.1038/ngeo234

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ngeo234

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