Long-range electron conduction of Shewanella biofilms mediated by outer membrane C-type cytochromes

We investigated the role of c-type cytochromes (c-Cyts) in electron conduction across biofilms of Shewanella oneidensis MR-1 and the relevance of the electron conductivity for biological current generation. Following the formation of monolayer and multilayer biofilms on indium-tin oxide electrodes, we quantified the c-Cyts that were electrically wired with the electrode surface using whole-cell voltammetry. A multilayer biofilm with a thickness of 16 μm exhibited a redox peak with an 8-fold larger coulombic area than that of a monolayer biofilm (about 0.5-μm thickness), indicating an abundance of c-Cyts that are able to perform redox-cycling reactions with the distant electrode surface. To determine if this electron conduit of c-Cyts participated in biological current generation, we conducted slow-scan voltammetry for multilayer biofilms. A large anodic current of c-Cyts caused by microbial lactate oxidization was observed during the slow-potential scans, demonstrating the transport of respiratory electrons via the sequential redox cycling of c-Cyts. Experiments with deletion mutants deficient in outer-membrane (OM) c-Cyts (ΔmtrC/ΔomcA, ΔpilD), and the biosynthetic protein of capsular polysaccharide (ΔSO3177) suggested that cell-surface-bound c-Cyts, but those located on pili or extracellular polymeric substrates, play a predominant role in the long-range electron conduction in the biofilm of S. oneidensis MR-1.

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► The role of bacterial c-Cyts for electron conductivity across Shewanella biofilms.
► Whole-cell cyclic voltammetry quantified bacterial c-Cyts in the biofilm on electrodes.
► Multilayer biofilm showed the larger redox current of c-Cyts than monolayer biofilm.
► The long-range electron transfer contributes bacterial anode current generation.
► Mutant experiments revealed electron conduction by c-Cyts along cellular surface.