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Microbial extracellular electron transfer (EET) drives various globally-important environmental phenomena and has biotechnology applications. Diverse prokaryotes have been proposed to perform EET via surface-displayed “nanowires” composed of multi-heme cytochromes. However, the mechanism that enables only a few cytochromes to polymerize into nanowires is unclear. Here, we identify a highly-conserved omcS-companion (osc) cluster that drives the formation of OmcS cytochrome nanowires in Geobacter sulfurreducens. Through a combination of genetic, biochemical, and biophysical methods, we establish that prolyl isomerase-containing chaperon OscH, channel-like OscEFG, and β-propeller-like OscD are involved in the folding, secretion, and morphology maintenance of OmcS nanowires, respectively. OscH and OscG can interact with OmcS. Furthermore, overexpression of oscG accelerates EET by overproducing nanowires in an ATP-dependent manner. Heme loading splits OscD and ΔoscD accelerates cell growth with bundling nanowires. Our findings establish the mechanism and prevalence of a specialized and modular assembly system for nanowires across phylogenetically-diverse species and environments 

Abstract Microbial respiration via extracellular electron transfer (EET) drives several globally-important environmental processes and has applications in bioenergy, bioremediation, and bioelectronics.Geobacter sulfurreducensproduce micrometer-long cytochrome nanowires for long-range (>10 µm) EET, but also require transmembrane porin-cytochrome complexes (PCCs), which can only perform EET on the cell surface. It was unknown why cells performing long-range EET need both PCCs and nanowires. Using Om(abc)B and OmcS as a model PCC and nanowire, respectively, for EET to Fe(III), we show that PCCs and nanowires form sequential, independent EET pathways where PCCs first kickstart EET and provide energy crucial for nanowire synthesis, and then nanowires perform long-range EET. Our model explains why both PCCs and nanowires are necessary. To understand the underlying EET mechanism, we purified native Om(ab)B and OmcB and found high excitonic coupling among hemes. Their midpoint reduction potentials (-182, -167 mV, respectively) are tuned for efficient electron transport. Additionally, OmcB transfers electrons to Fe(III) ~5 times more efficiently than OmcS. Our work suggests that the metabolic trade-off between PCCs and nanowires results from efficient proteome allocation. Notably, PCCs are widespread in environmentally-important bacteria and co-evolved with OmcS nanowires. This previously-undescribed nanowire synthesis strategy could accelerate EET in diverse microbes and environments.