A Bundled Antiparallel Cytochrome Nanowire Structure Suggests Roles in Cell-Cell Electron Transfer and Biofilm Formation

Abstract

Long-range extracellular electron transfer enables respiring microbes to use minerals, other organisms, or electrodes as electron acceptors by transporting electrons microns away from the cell surface. This process is primarily studied in Geobacter sulfurreducens, which produces at least three different micrometer-long, multi-heme cytochrome nanowires capable of electron transfer. However, the distribution and higher-order structure of these types of cytochrome nanowires remains largely unknown. Here, we employed cryo-electron microscopy to determine the atomic structure of a unique cytochrome nanowire from Desulfuromonas soudanensis WTL, a halophilic, iron- and electrode-reducing bacterium found in deep subsurface brine. These filaments are based on a homolog of the OmcE tetraheme cytochrome, which then assemble into highly ordered bundles of antiparallel filaments. This arrangement likely arises from the association of nanowires extending from adjacent cells. Furthermore, a similar cytochrome bundle structure was observed in Geobacter metallireducens, suggesting that this quaternary structure may be a common feature among nanowires secreted by electroactive microbes. Our findings demonstrate that cytochrome nanowires in diverse taxa can form specialized bundle interfaces, potentially facilitating conductive biofilm formation and representing a novel strategy for microbial electron exchange. More broadly, this work expands understanding of electron transfer mechanisms and demonstrates the production of multi-heme filaments across distinct lineages. These insights could guide future research into cytochrome nanowire secretion and conductive biofilm engineering, with potential applications in electrochemical technologies.