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Marine methane paradox explained by bacterial degradation of dissolved organic matter

Abstract

Biogenic methane is widely thought to be a product of archaeal methanogenesis, an anaerobic process that is inhibited or outcompeted by the presence of oxygen and sulfate1,2,3. Yet a large fraction of marine methane delivered to the atmosphere is produced in high-sulfate, fully oxygenated surface waters that have methane concentrations above atmospheric equilibrium values, an unexplained phenomenon referred to as the marine methane paradox4,5. Here we use nuclear magnetic resonance spectroscopy to show that polysaccharide esters of three phosphonic acids are important constituents of dissolved organic matter in seawater from the North Pacific. In seawater and pure culture incubations, bacterial degradation of these dissolved organic matter phosphonates in the presence of oxygen releases methane, ethylene and propylene gas. Moreover, we found that in mutants of a methane-producing marine bacterium, Pseudomonas stutzeri, disrupted in the C–P lyase phosphonate degradation pathway, methanogenesis was also disabled, indicating that the C–P lyase pathway can catalyse methane production from marine dissolved organic matter. Finally, the carbon stable isotope ratio of methane emitted during our incubations agrees well with anomalous isotopic characteristics of seawater methane. We estimate that daily cycling of only about 0.25% of the organic matter phosphonate inventory would support the entire atmospheric methane flux at our study site. We conclude that aerobic bacterial degradation of phosphonate esters in dissolved organic matter may explain the marine methane paradox.

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Figure 1: Characterization of phosphorus in DOM by 31P NMR spectroscopy.
Figure 2: Hydrocarbon gas production from semi-labile DOM.
Figure 3: Production of methane and ethylene from semi-labile DOM phosphonates.

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Acknowledgements

We thank the Captain and crew of the RV Kilo Moana as well as K. Olson and the staff at the Natural Energy Laboratory, Hawaii Authority for assistance in sample collection. We also thank R. Boiteau for his assistance with mass spectrometry, A. Bate for helping with gas chromatography measurements, K. Doggett for flow cytometry analysis and the Hawaii Ocean Time-series team for facilitating part of this work. This research is a contribution of the Daniel K. Inouye Center for Microbial Oceanography: Research and Education (C-MORE) and was supported by the Gordon and Betty Moore Foundation (through Grants GBMF3298 to D.J.R. and E.F.D., GBMF3777 to E.F.D. and GBMF3794 to D.M.K.), as well as a grant from the Simons Foundation (SCOPE Award ID 329108 to D.J.R., E.F.D. and D.M.K.).

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Contributions

D.M.K., D.J.R. and E.F.D. designed the experiments with input from all co-authors. D.J.R. collected and purified DOM samples, and performed spectral analyses. S.F. performed microcosm incubations and trace gas analyses with input from D.M.K. O.A.S. isolated DOM degrading microbes, performed genomic analyses, and performed microcosm incubations and trace gas analyses with input from E.F.D. C.G.J. performed NMR spectral analyses of DOM. L.D.R. performed chemical degradation experiments and identified phosphonates in DOM. M.A. purified DOM and assisted in microcosm incubation experiments. D.J.R. drafted the manuscript with input from all authors.

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Correspondence to Daniel J. Repeta.

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Repeta, D., Ferrón, S., Sosa, O. et al. Marine methane paradox explained by bacterial degradation of dissolved organic matter. Nature Geosci 9, 884–887 (2016). https://doi.org/10.1038/ngeo2837

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