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Widespread extracellular electron transfer pathways for charging microbial cytochrome OmcS nanowires via periplasmic cytochromes PpcABCDE
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Resumo(s)
Extracellular electron transfer (EET) via microbial nanowires drives globally-important environmental processes and biotechnological applications for bioenergy, bioremediation, and bioelectronics. Due to highly-redundant and complex EET pathways, it is unclear how microbes wire electrons rapidly (>106s−1) from the inner-membrane through outer-surface nanowires directly to an external environment despite a crowded periplasm and slow (<105s−1) electron diffusion among periplasmic cytochromes. Here, we show that Geobacter sulfurreducens periplasmic cytochromes PpcABCDE inject electrons directly into OmcS nanowires by binding transiently with differing efficiencies, with the least-abundant cytochrome (PpcC) showing the highest efficiency. Remarkably, this defined nanowire-charging pathway is evolutionarily conserved in phylogenetically-diverse bacteria capable of EET. OmcS heme reduction potentials are within 200 mV of each other, with a midpoint 82 mV-higher than reported previously. This could explain efficient EET over micrometres at ultrafast (<200 fs) rates with negligible energy loss. Engineering this minimal nanowire-charging pathway may yield microbial chassis with improved performance.
Descrição
We thank Gary Brudvig for advice on spectroelectrochemistry measurements and M. Gubermann-Pfeffer for help with ZDOCK. This research was supported by the National Defense Science and Engineering Graduate Fellowship (to C.C.S.), the Human Frontier Science Program award no. RGP017/2023 (to N.S.M. and C.A. S.), NSF CAREER award no. 1749662 (to N.S.M.), the NSF-ANR award no. 2210473 (to N.S.M.), and the National Institutes of Health (NIH) Director’s New Innovator award (1DP2AI138259-01 to N.S.M.).
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© The Author(s) 2024
Palavras-chave
General Chemistry General Biochemistry,Genetics and Molecular Biology General Physics and Astronomy SDG 7 - Affordable and Clean Energy SDG 15 - Life on Land