Abstract
<title>Abstract</title> <p>Microbial respiration via extracellular electron transfer (EET) drives various globally-important environmental processes and applications in bioenergy, bioremediation, and bioelectronics. However, despite ~40 years of research, the EET components and pathways have remained unclear due to their high redundancy. e.g., depending on nutrient availability, Geobacter sulfurreducens selects distinct sets of membrane-embedded porin-cytochrome complexes (PCCs) that are long-believed to transfer electrons to surface-displayed polymerized cytochrome “nanowires”. In contrast, here we show that PCC Om(abc)B and OmcS nanowires form sequential, independent EET pathways to environmentally-abundant Fe(III). Genetic studies show that PCCs enable switching from intracellular to extracellular ET and provide energy to synthesize nanowires that then perform long-range (>1 μm) EET to access ~50-times the cell’s biovolume of Fe(III) essential for replication. Surprisingly, wired cells completely shut-off PCC production without altering their expression. Our biophysical, biochemical, and coevolution analyses, using native-lipid nanodiscs, spectroelectrochemistry, UV-visible, circular dichroism, and electron paramagnetic resonance spectroscopies, reveal that Om(ab)B and OmcB protein and electronic structures (Em, -182, -167 mV, respectively) are evolutionarily-optimized for efficient EET, enabling OmcB to transfer electrons ~5 times faster than nanowires. This microbial strategy to switch from wireless to wired EET network could enable engineering and controlling EET in diverse environmentally-important species and environments.</p>