From Hot Water to Dry Dirt: Microbes Use Cytochrome ‘Nanowires’ of Similar Conductivity but Different Structure

Abstract

AbstractMicron-scale electron transfer through polymeric cytochrome ‘nanowires’ powers prokaryotic life from hydrothermal vents to terrestrial soils in ways not fully understood. How much structural diversity optimizes electrical conductivity for survival in these different habitats is challenging to assess experimentally. Herein, physiologically relevant redox conduction is computationally assessed in cytochrome filaments fromGeobacter sulfurreducens(OmcE, OmcS, and OmcZ),Pyrobaculum calidifontis(A3MW92), andArchaeoglobus veneficus(F2KMU8). A newly implemented Python program, BioDC, is used and validated against redox currents predicted from considerably more expensive molecular dynamics and quantum mechanical/molecular mechanical calculations. BioDC uses the heme solvent accessibility, stacking geometry, and redox-linked change in electrostatic energy to estimate electron transfer energetics. Leveraging this efficiency, structurally diverse cytochrome ‘nanowires’ from different organisms are shown to have similar redox conductivities. A functionally robust heme chain ‘packaged’ in habitat-customized proteins is proposed to be a general evolutionary design principle for cytochrome ‘nanowires’ widely distributed among prokaryotes.TOC Graphic