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

Abstract

Micron-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 from Geobacter sulfurreducens (OmcE, OmcS, and OmcZ), Pyrobaculum calidifontis (A3MW92), and Archaeoglobus 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 O_FIG O_LINKSMALLFIG WIDTH=198 HEIGHT=200 SRC="FIGDIR/small/544705v1_ufig1.gif" ALT="Figure 1"> View larger version (60K): org.highwire.dtl.DTLVardef@ac61d9org.highwire.dtl.DTLVardef@14c2e87org.highwire.dtl.DTLVardef@82d60corg.highwire.dtl.DTLVardef@1b2cbd6_HPS_FORMAT_FIGEXP M_FIG C_FIG