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.
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References
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)
Rodhe, H. A comparison of the contribution of various gases to the greenhouse effect. Science 248, 1217–1219 (1990)
Smith, L. C. et al. Siberian peatlands a net carbon sink and global methane source since the early Holocene. Science 303, 353–356 (2004)
Dedysh, S. N. et al. Isolation of acidophilic methane-oxidizing bacteria from northern peat wetlands. Science 282, 281–284 (1998)
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)
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)
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)
Rydin, H. & Clymo, R. S. Transport of carbon and phosphorus compounds about Sphagnum. Proc. R. Soc. Lond. 237, 63–84 (1989)
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)
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)
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)
Keeley, J. E. & Sandquist, D. R. Carbon: freshwater plants. Plant Cell Environ. 15, 1021–1035 (1992)
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)
Post, W. M., Emanuel, W. R., Zinke, P. J. & Strangenberger, A. G. Soil carbon pools and world life zones. Nature 298, 156 (1982)
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)
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)
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)
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)
Ludwig, W. et al. ARB: A software environment for sequence data. Nucleic Acids Res. 32, 1363–1371 (2004)
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)
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)
Wolters-Arts, M. et al. Water-conducting properties of lipids during pollen hydration. Plant Cell Environ. 25, 513–519 (2002)
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)
Sinninghe Damsté, J. S. et al. The occurrence of hopanoids in planctomycetes: implications for the sedimentary biomarker record. Organic Geochim. 35, 561–566 (2004)
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’).
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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.
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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
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DOI: https://doi.org/10.1038/nature03802
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