Five Cytochrome ‘Nanowires’ Suffice for Prokaryotes to Breathe Rocks Microns Away

Micron-scale electron transfer through polymeric cytochrome ‘nanowires’ powers prokaryotic life from hydrothermal vents to terrestrial soils in ways not fully understood. Herein, six reduction potentials from recently reported spectroelectrochemistry are each assigned with chemical accuracy (<0.05 eV) to the cryogenic electron microscopy structure of the hexa-heme homopolymeric outer-membrane cytochrome type S (OmcS) from Geobacter sulfurreducens using hybrid quantum/classical computations. The unambiguous assignments define a bumpy but overall thermoneutral free energy landscape that is dynamically modulated by <0.1 V under the flow of electrons via redox cooperativities between adjacent hemes. A physiologically relevant ≥5 filaments are predicted to suffice for cellular respiration by pairing, in the context of non-adiabatic Marcus theory, the free energy landscape with reorganization energies that empirically account for protein-water electronic polarizability, and electronic couplings characteristic of the highly conserved heme packing motifs. General considerations on protein electron transfer and comparison to all known cytochrome ‘nanowires’ suggest the mechanistic insights are broadly applicable to multi-heme cytochromes in all kingdoms of life.