Heme Hopping Falls Short: What Explains Anti-Arrhenius Conductivity in a Multi-heme Cytochrome Nanowire?

Abstract

A helical homopolymer of the outer-membrane cytochrome type S (OmcS) was proposed to electrically connect a common soil bacterium, Geobacter sulfurreducens, with minerals and other microbes for biogeochemically important processes. OmcS exhibits a surprising rise in conductivity upon cooling from 300 to 270 K that has recently been attributed to a restructuring of H-bonds, which in turn modulates heme redox potentials. This proposal is more thoroughly examine herein by (1) analyzing H-bonding at 13 temperatures encompassing the entire experimental range; (2) computing redox potentials with quantum mechanics/molecular mechanics for 10-times more (3000) configurations sampled from 3-times longer (2 μs) molecular dynamics, as well as 3 μs of constant redox and pH molecular dynamics; and (3) modeling redox conduction with both single-particle diffusion and multi-particle flux kinetic schemes. Upon cooling by 30 K, the connectivity of the intra-protein H-bonding network was highly (86%) similar. An increase in the density and static dielectric constant of the filament's hydration shell caused a -0.002 V/K shift in heme redox potentials, and a factor of 2 decrease in charge mobility. Revision of a too-far negative redox potential in prior work (-0.521 V; expected = -0.350 - +0.150 V; new Calc. = -0.214 V vs. SHE) caused the mobility to be greater at high versus low temperature, opposite to the original prediction. These solution-phase redox conduction models failed to reproduce the experimental conductivity of electrode-absorbed, partially dehydrated, and possibly aggregated OmcS filaments. Some improvement was seen by neglecting reorganization energy from the solvent to model dehydration. Correct modeling of the physical state is suggested to be a prerequisite for reaching a verdict on the operative charge transport mechanism and the molecular basis of its temperature response.

Theory of Protein Charge Transfer: Electron Transfer between Tryptophan Residue and Active Site of Azurin

“…However, statistical convergence, not reachable for a large protein complex, is attained on the simulation time of 200–300 ns for small globular proteins, such as azurin considered here. Despite this convergence, the protein component of the thermal bath shows a strong separation between λ St and λ according to eq , suggesting that the jammed and frustrated protein interior promotes glassy dynamics with strong features of nonergodic sampling. − It is currently not clear if this is just the size of the protein complex or the membrane that acts to dehydrate a part of the protein to allow eq for large membrane-bound protein complexes. However, dehydration provides a natural control mechanism of protein’s activity: a small globular protein becomes redox-active when binding to a large protein complex partially eliminates its hydration shell.…”