Extracellular Electron Shuttling Mediated by Soluble c‑Type Cytochromes Produced by Shewanella oneidensis MR‑1

How metal-reducing bacteria transfer electrons during dissimilatory energy generation under electron acceptor-limited conditions is poorly understood. Here, we incubated the iron and manganese-reducing bacterium Shewanella oneidensis MR-1 without electron acceptors. Removal of soluble extracellular organic compounds (EOCs) dramatically retarded transfer of electrons to an experimental electron acceptor, Cr­(VI), by MR-1. However, the return of either high MW (>3000 Da) or low MW (c-type cytochromes (c-Cyts). A model of the kinetics of individual elementary reactions between cells, flavins, released c-Cyts, and Cr­(VI), including the direct reduction of flavins, released c-Cyts, and Cr­(VI) by cells and the indirect reduction of Cr­(VI) by reduced forms of flavins and released c-Cyts, was developed. Model results suggest that released c-Cyts could act as electron mediators to accelerate electron transfer from cells to Cr­(VI), and the relative contribution of this pathway was higher than that mediated by flavins. Hence, extracellular c-Cyts produced by MR-1 likely play a role in extracellular electron transfer under electron acceptor-limited conditions. These findings provide new insights into extracellular electron shuttling and the metabolic strategy of metal-reducing bacteria under electron acceptor-limited conditions.