Electric currents couple spatially separated biogeochemical processes in marine sediment

Some microbes are capable of extracellular electron transport through so-called bacterial nanowires or electron shuttles. It is now shown that this may be a significant process in the marine sediment, allowing oxygen to oxidize compounds located centimetres away. The remains of dead algae and faeces buried in marine sediment are a good food resource for microbes, but at sediment depths greater than a few millimetres the lack of oxygen limits utilization of this resource. A study of sediment samples from the seabed off Aarhus in Denmark reveals that microbes can overcome this obstacle by making intercellular electric connections and establishing a division of labour. Cells at the surface utilize sufficient oxygen for all cells in the community, and those at depth acquire nutrients for all. It has been previously demonstrated that some microbes are capable of extracellular electron transport through so–called nanowires or electron shuttles. Here it is demonstrated that this may be a significant process in the marine sediment. 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.