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:

Methanotrophic symbionts provide carbon for photosynthesis in peat bogs

Abstract

Wetlands are the largest natural source of atmospheric methane1, the second most important greenhouse gas2. Methane flux to the atmosphere depends strongly on the climate3; however, by far the largest part of the methane formed in wetland ecosystems is recycled and does not reach the atmosphere4,5. The biogeochemical controls on the efficient oxidation of methane are still poorly understood. Here we show that submerged Sphagnum mosses, the dominant plants in some of these habitats, consume methane through symbiosis with partly endophytic methanotrophic bacteria, leading to highly effective in situ methane recycling. Molecular probes revealed the presence of the bacteria in the hyaline cells of the plant and on stem leaves. Incubation with 13C-methane showed rapid in situ oxidation by these bacteria to carbon dioxide, which was subsequently fixed by Sphagnum, as shown by incorporation of 13C-methane into plant sterols. In this way, methane acts as a significant (10–15%) carbon source for Sphagnum. The symbiosis explains both the efficient recycling of methane and the high organic carbon burial in these wetland ecosystems.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Figure 1: Methane oxidation potential of different parts of submerged and non-submerged Sphagnum mosses as a measure of methanotrophs associated.
Figure 2: In situ detection of the new methanotroph in S. cuspidatum with fluorescently labelled rRNA-targeted oligonucleotide probes.
Figure 3: Incorporation of 13 C label in biological markers for Sphagnum (circles) and methanotrophic bacteria (squares).

Similar content being viewed by others

References

  1. Hein, R., Crutzen, P. J. & Heimann, M. An inverse modeling approach to investigate the global atmospheric methane cycle. Global Biogeochem. Cycles 11, 43–76 (1997)

    Article  ADS  CAS  Google Scholar 

  2. Rodhe, H. A comparison of the contribution of various gases to the greenhouse effect. Science 248, 1217–1219 (1990)

    Article  ADS  CAS  Google Scholar 

  3. Smith, L. C. et al. Siberian peatlands a net carbon sink and global methane source since the early Holocene. Science 303, 353–356 (2004)

    Article  ADS  CAS  Google Scholar 

  4. Dedysh, S. N. et al. Isolation of acidophilic methane-oxidizing bacteria from northern peat wetlands. Science 282, 281–284 (1998)

    Article  ADS  CAS  Google Scholar 

  5. Lamers, L. P. M., Farhoush, C., Van Groenendael, J. M. & Roelofs, J. G. M. Calcareous groundwater raises bogs; the concept of ombrotrophy revisited. J. Ecol. 87, 639–648 (1999)

    Article  Google Scholar 

  6. Dedysh, S. N. et al. Methylocella palustris gen. nov., sp. nov., a new methane-oxidizing acidophilic bacterium from peat bogs, representing a novel subtype of serine-pathway methanotrophs. Int. J. Syst. Evol. Microbiol. 50, 955–969 (2000)

    Article  CAS  Google Scholar 

  7. Dedysh, S. N. et al. Methylocapsa acidophila gen. nov., sp. nov., a novel methane-oxidizing and dinitrogen fixing acidophilic bacterium from Sphagnum bog. Int. J. Syst. Evol. Microbiol. 52, 251–261 (2002)

    Article  CAS  Google Scholar 

  8. Rydin, H. & Clymo, R. S. Transport of carbon and phosphorus compounds about Sphagnum. Proc. R. Soc. Lond. 237, 63–84 (1989)

    Article  ADS  CAS  Google Scholar 

  9. Yao, R., Macario, A. J. L. & Conway de Macario, E. Immunochemical differences among Methanosarcina mazei S-6 morphologic forms. J. Bacteriol. 174, 4683–4688 (1992)

    Article  CAS  Google Scholar 

  10. Rohmer, M., Bisseret, P. & Neunlist, S. in Biological Markers in Sediments and Petroleum (eds Moldowan, J. M., Albrecht, P. & Philp, R. P.) 1–17 (Prentice Hall, London, 1992)

    Google Scholar 

  11. Jahnke, L. L., Summons, R. E., Hope, J. M. & Des Marais, D. J. Carbon isotopic fractionation in lipids from methanotrophic bacteria II: The effects of physiology and environmental parameters on the biosynthesis and isotopic signatures of biomarkers. Geochim. Cosmochim. Acta 63, 79–93 (1999)

    Article  ADS  Google Scholar 

  12. Keeley, J. E. & Sandquist, D. R. Carbon: freshwater plants. Plant Cell Environ. 15, 1021–1035 (1992)

    Article  CAS  Google Scholar 

  13. Smolders, A. J. P., Tomassen, H. B. M., van Mullekom, M., Lamers, L. P. M. & Roelofs, J. G. M. Mechanisms involved in the re-establishment of Sphagnum-dominated vegetation in rewetted bog remnants. Wetlands Ecol. Manag. 11, 403–418 (2003)

    Article  Google Scholar 

  14. Post, W. M., Emanuel, W. R., Zinke, P. J. & Strangenberger, A. G. Soil carbon pools and world life zones. Nature 298, 156 (1982)

    Article  ADS  CAS  Google Scholar 

  15. Marguillier, S., van der Velde, G., Dehairs, F., Hemminga, M. A. & Rajagopal, S. Trophic relationship in an interlinked mangrove-seagrass ecosystem as traced by δ13C and δ15N. Mar. Ecol. Prog. Ser. 151, 115–121 (1997)

    Article  ADS  CAS  Google Scholar 

  16. Smolders, A. J. P., Tomassen, H. B. M., Lamers, L. P. M., Lomans, B. P. & Roelofs, J. G. M. Peat bog restoration by floating raft formation: the effects of groundwater and peat quality. J. Appl. Ecol. 39, 391–401 (2002)

    Article  CAS  Google Scholar 

  17. Lomans, B. P. et al. Microbial populations involved in cycling of dimethyl sulfide and methanethiol in freshwater sediments. Appl. Environ. Microbiol. 67, 1044–1051 (2001)

    Article  CAS  Google Scholar 

  18. Juretschko, S. et al. Combined molecular and conventional analyses of nitrifying bacterium diversity in activated sludge: Nitrosococcus mobilis and Nitrospira-like bacteria as dominant populations. Appl. Environ. Microbiol. 64, 3042–3051 (1998)

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  20. 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 

  21. Daims, H., Bruhl, A., Amann, R., Schleifer, K. H. & Wagner, M. The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: development and evaluation of a more comprehensive probe set. Syst. Appl. Microbiol. 22, 434–444 (1999)

    Article  CAS  Google Scholar 

  22. Wolters-Arts, M. et al. Water-conducting properties of lipids during pollen hydration. Plant Cell Environ. 25, 513–519 (2002)

    Article  CAS  Google Scholar 

  23. Schouten, S. et al. Biosynthetic effects on the stable carbon isotopic compositions of algal lipids: Implications for deciphering the carbon isotopic biomarker record. Geochim. Cosmochim. Acta 62, 1397–1406 (1998)

    Article  ADS  CAS  Google Scholar 

  24. Sinninghe Damsté, J. S. et al. The occurrence of hopanoids in planctomycetes: implications for the sedimentary biomarker record. Organic Geochim. 35, 561–566 (2004)

    Article  Google Scholar 

Download references

Acknowledgements

We thank K. T. van de Pas-Schoonen, A. Pol, H. P. M. Geurts, J. Eygensteyn, M. van Mullekom, J. Berk, H. Tomassen and M. M. A. van Herpen for technical support. Part of this study was supported by the Dutch Ministry of Agriculture, Nature Management and Food quality (Research Program ‘Overlevingsplan Bos en Natuur’).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Alfons J. P. Smolders or Jaap S. Sinninghe Damsté.

Ethics declarations

Competing interests

The 16S rRNA gene sequences were deposited at GenBank under accession number AY163571. Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Raghoebarsing, A., Smolders, A., Schmid, M. et al. Methanotrophic symbionts provide carbon for photosynthesis in peat bogs. Nature 436, 1153–1156 (2005). https://doi.org/10.1038/nature03802

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature03802

This article is cited by

Comments

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.

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