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Electric currents couple spatially separated biogeochemical processes in marine sediment

Abstract

Some bacteria are capable of extracellular electron transfer, thereby enabling them to use electron acceptors and donors without direct cell contact1,2,3,4. Beyond the micrometre scale, however, no firm evidence has previously existed that spatially segregated biogeochemical processes can be coupled by electric currents in nature. Here we provide evidence that electric currents running through defaunated sediment couple oxygen consumption at the sediment surface to oxidation of hydrogen sulphide and organic carbon deep within the sediment. Altering the oxygen concentration in the sea water overlying the sediment resulted in a rapid (<1-h) change in the hydrogen sulphide concentration within the sediment more than 12 mm below the oxic zone, a change explicable by transmission of electrons but not by diffusion of molecules. Mass balances indicated that more than 40% of total oxygen consumption in the sediment was driven by electrons conducted from the anoxic zone. A distinct pH peak in the oxic zone could be explained by electrochemical oxygen reduction, but not by any conventional sets of aerobic sediment processes. We suggest that the electric current was conducted by bacterial nanowires combined with pyrite, soluble electron shuttles and outer-membrane cytochromes. Electrical communication between distant chemical and biological processes in nature adds a new dimension to our understanding of biogeochemistry and microbial ecology.

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Figure 1: Sediment O 2 , ΣH 2 S, Fe 2+ and pH microprofiles.
Figure 2: Electric currents in sediment.
Figure 3: Time series of O 2 and H 2 S distribution in the sediment during oxic–anoxic cycles.

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Acknowledgements

This research was financially supported by the Aarhus University Research Foundation, the Danish National Research Foundation (N.R.-P.), the Max Planck Society (N.R.-P.) and the Japan Society for the Promotion of Science (M.S.).

Author Contributions The study was conceived by L.P.N. All authors contributed to the design and execution of the study, interpretation of the results and preparation of the manuscript.

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Correspondence to Lars Peter Nielsen.

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Nielsen, L., Risgaard-Petersen, N., Fossing, H. et al. Electric currents couple spatially separated biogeochemical processes in marine sediment. Nature 463, 1071–1074 (2010). https://doi.org/10.1038/nature08790

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