Divide-Conquer-Recombine Kinetic Monte Carlo Simulations of Electron Transfer in the Extracellular Redox Network of Shewanella oneidensis MR-1

Abstract

Metal-reducing bacteria, such as Shewanella oneidensis MR-1, have evolved extracellular electron transfer (EET) mechanisms to external surfaces, allowing them to use abundant minerals as respiratory electron acceptors, instead of oxygen or other soluble oxidants that would normally diffuse inside cells. By performing EET at electrodes, such microbes can serve as biocatalysts for converting the energy stored in fuels to electricity, or vice versa, in renewable energy technologies. Furthermore, a biophysical understanding of this phenomenon may enable the transmission of signals at cellular/synthetic interfaces, creating new materials that combine the replication and self-repair of a natural system with the vast toolbox of nanotechnology.But how can a cell transfer electrons to surface micrometers away from the cell? Microbes overcome this hurdle by deploying multiheme cytochrome complexes that form 20-30 nm conduits through the periplasm and across the outer-membrane. More recently, we learned that this cytochrome network extends along micrometer-long membrane extensions called bacterial nanowires, and even over entire bacterial biofilms. Here we report a detailed computational study of the electron transfer dynamics in microbial cytochrome networks. Using atomistically-informed kinetic Monte Carlo (KMC) simulations, we calculate the electron transport rate through the Shewanella decaheme cytochrome MtrF, and find the result to match in vitro measurements and satisfy the in vivo cellular respiration rates on electrodes. To extend this approach to multi-cytochrome complexes, we present a hierarchical framework that predicts the structure of Mtr-Omc complexes, performs KMC simulations, and visualizes electron transport. We also present a divide-conquer-recombine KMC approach, and an implementation on parallel computers, to simulate EET over much larger structures such as entire bacterial nanowires. The electron flux is found to strongly depend on the cytochrome density, topology, and orientation on membrane.