Structure of Microbial Nanowires Reveals Stacked Hemes that Transport Electrons over Micrometers

Highlights

• Geobacter nanowires are made up of micrometer-long polymerization of cytochrome OmcS

• All hemes are closely stacked (<4–6 Å), providing a continuous path for electron flow

• We show that these are the same filaments that were earlier thought as type IV pili

• This structure explains the molecular basis for electron conduction in protein wires

Summary

Long-range (>10 μm) transport of electrons along networks of Geobacter sulfurreducens protein filaments, known as microbial nanowires, has been invoked to explain a wide range of globally important redox phenomena. These nanowires were previously thought to be type IV pili composed of PilA protein. Here, we report a 3.7 Å resolution cryoelectron microscopy structure, which surprisingly reveals that, rather than PilA, G. sulfurreducens nanowires are assembled by micrometer-long polymerization of the hexaheme cytochrome OmcS, with hemes packed within ∼3.5–6 Å of each other. The inter-subunit interfaces show unique structural elements such as inter-subunit parallel-stacked hemes and axial coordination of heme by histidines from neighboring subunits. Wild-type OmcS filaments show 100-fold greater conductivity than other filaments from a ΔomcS strain, highlighting the importance of OmcS to conductivity in these nanowires. This structure explains the remarkable capacity of soil bacteria to transport electrons to remote electron acceptors for respiration and energy sharing.