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Zero-valent sulphur is a key intermediate in marine methane oxidation

Abstract

Emissions of methane, a potent greenhouse gas, from marine sediments are controlled by anaerobic oxidation of methane coupled primarily to sulphate reduction (AOM). Sulphate-coupled AOM is believed to be mediated by a consortium of methanotrophic archaea (ANME) and sulphate-reducing Deltaproteobacteria but the underlying mechanism has not yet been resolved. Here we show that zero-valent sulphur compounds (S0) are formed during AOM through a new pathway for dissimilatory sulphate reduction performed by the methanotrophic archaea. Hence, AOM might not be an obligate syntrophic process but may be carried out by the ANME alone. Furthermore, we show that the produced S0—in the form of disulphide—is disproportionated by the Deltaproteobacteria associated with the ANME. Our observations expand the diversity of known microbially mediated sulphur transformations and have significant implications for our understanding of the biogeochemical carbon and sulphur cycles.

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Figure 1: Microbial activity and composition of the Isis enrichment culture.
Figure 2: Zero-valent S in ANME cells in the Isis enrichment culture.
Figure 3: Disulphide disproportionation by Isis enrichment culture.
Figure 4: Revised model of anaerobic oxidation of methane coupled to sulphate reduction.

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Acknowledgements

We want to thank G. Klockgether, K. Imhoff, S. Littmann and T. Vagner for technical support, G. Lavik and M. Formolo for analytical support and discussions, M. Schüler and T. Keil for assistance with cryosectioning, A. Boetius for providing samples, and T. Holler for the initial enrichment and maintenance of the Isis culture. This work was financially supported by the Max Planck Society and the ERC Advanced Grant 294343 (to M.W.).

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J.M., T.G.F., F.W. and M.M.M.K. designed experiments. J.M., T.G.F. and M.M.M.K. performed experiments and analysed data. J.M. performed immunolabeling and microscopy. D.F. performed CARD-FISH and nanoSIMS. L.P. analysed nanoSIMS data. M.S. and M.W. performed Raman measurements, I.L. performed energy-dispersive X-ray spectroscopy analyses, and G.W. contributed new analytical tools. J.M., T.G.F. and M.M.M.K. wrote the manuscript with contributions of all co-authors.

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Correspondence to Jana Milucka.

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Milucka, J., Ferdelman, T., Polerecky, L. et al. Zero-valent sulphur is a key intermediate in marine methane oxidation. Nature 491, 541–546 (2012). https://doi.org/10.1038/nature11656

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