Abstract: Extracellular electron transfer (EET) plays a critical role in bioelectrochemical processes, allowing coupling between microorganisms and extracellular solid-state electrodes, metals, or other cells in energy metabolism. Previous studies have suggested a role for outer-surface c-type cytochromes in direct metal-to-microbe electron transfer by Geobacter sulfurreducens, a model electroactive bacterium. Here, we examined the possibility of other microbially produced electrical contacts by deleting the gene for PilA, the protein monomer that G. sulfurreducens assembles into electrically conductive protein nanowires (e-pili). Deleting pilA gene inhibited electron extraction from pure iron and 316L stainless steel up to 31% and 81%, respectively more than deleting the gene for the outer-surface cytochrome OmcS. This PilA-deficient phenotype, and the observation that relatively thick biofilms (21.7 μm) grew on the metal surfaces at multi-cell distances from the metal surfaces suggest that e-pili contributed significantly to microbial corrosion via direct metal-to-microbe electron transfer. These results have implications for the fundamental understanding of electron harvest via e-pili by electroactive microbes, their uses in bioenergy production, as well as in monitoring and mitigation of metal biocorrosion.

Key words: Electrically conductive protein nanowires, Direct metal-to-microbe electron transfer, Geobacter sulfurreducens, Outer-surface c-type cytochromes, Biofilm