Assessing Thermal Response of Redox Conduction for Anti-Arrhenius Kinetics in a Microbial Cytochrome Nanowire.

Abstract

A micrometers-long helical homopolymer of the outer-membrane cytochrome type S (OmcS) from Geobacter sulfurreducens is proposed to transport electrons to extracellular acceptors in an ancient respiratory strategy of biogeochemical and technological significance. OmcS surprisingly exhibits higher conductivity upon cooling (anti-Arrhenius kinetics), an effect previously attributed to H-bond restructuring and heme redox potential shifts. Herein, the temperature sensitivity of redox conductivity is more thoroughly examined with conventional and constant-redox and -pH molecular dynamics and quantum mechanics/molecular mechanics. A 30 K drop in temperature constituted a weak perturbation to electron transfer energetics, changing electronic couplings (⟨Hmn⟩), reaction free energies (ΔGmn), reorganization energies (λmn), and activation energies (Ea) by at most |0.002|, |0.050|, |0.120|, and |0.045| eV, respectively. Changes in ΔGmn reflected -0.07 ± 0.03 V shifts in redox potentials that were caused in roughly equal measure by altered electrostatic interactions with the solvent and protein. Changes in intraprotein H-bonding reproduced the earlier observations. Single-particle diffusion and multiparticle steady-state flux models, parametrized with Marcus theory rates, showed that biologically relevant incoherent hopping cannot qualitatively or quantitatively describe electrical conductivity measured by atomic force microscopy in filamentous OmcS. The discrepancy is attributed to differences between solution-phase simulations and solid-state measurements and the need to model intra- and intermolecular vibrations explicitly.