Defense: Kiriko. Terai: Structure-function relations and kinetic principles underlying multiscale electron transfer in biology

Structure-function relations and kinetic principles underlying multiscale electron transfer in biology

Electron transfer (ET) underlies fundamental biological processes such as respiration, photosynthesis, redox catalysis, and cellular signaling. This work investigates the structure-function relations and kinetic principles governing efficient and controlled ET across multiscales in biological systems. Two major research directions are explored: free energy transduction by nanoscale molecular machines and long-range extracellular ET in protein-based nanowires. The first research direction focuses on understanding free energy transduction in electron bifurcation (EB), a mechanism that couples exergonic and endergonic ET reactions. We found that many-particle correlations are essential to accurately describe EB, and, more broadly, any process involving free energy transduction. To better represent biological conditions such as spatial confinement and limited redox carrier pools, we developed an open many-particle system model that treats redox pools as finite narrow-band reservoirs. Using this framework, we identified that inverted redox potentials at the bifurcating site reduces slippage in the pre-steady-state regime. The second direction examines electron transport through bacterial nanowires, which enable extracellular ET by forming conductive protein filaments. These nanowires exhibit anti-Arrhenius behavior, with conductivity decreasing as temperature increases, a phenomenon inconsistent with conventional thermally activated hopping mechanisms. Our simulations show that electrostatic effects on the ET parameters alone cannot account for the anti-Arrhenius behavior. Instead, the physical origin of anti-Arrhenius transport lies in other factors, pointing to a more complex structural or dynamical basis for the observed temperature dependence. Together, these studies provide new insights into how biological ET systems achieve efficiency and control, emphasizing the role of physical constraints, correlations, and structural dynamics.