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A flavin-based extracellular electron transfer mechanism in diverse Gram-positive bacteria

Samuel H. Light, Lin Su, Rafael Rivera-Lugo, Jose A. Cornejo, Alexander Louie, Anthony T. Iavarone, Caroline M. Ajo-Franklin and Daniel A. Portnoy ()
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Samuel H. Light: University of California, Berkeley
Lin Su: Lawrence Berkeley National Laboratory
Rafael Rivera-Lugo: University of California, Berkeley
Jose A. Cornejo: Lawrence Berkeley National Laboratory
Alexander Louie: University of California, Berkeley
Anthony T. Iavarone: University of California, Berkeley
Caroline M. Ajo-Franklin: Lawrence Berkeley National Laboratory
Daniel A. Portnoy: University of California, Berkeley

Nature, 2018, vol. 562, issue 7725, 140-144

Abstract: Abstract Extracellular electron transfer (EET) describes microbial bioelectrochemical processes in which electrons are transferred from the cytosol to the exterior of the cell1. Mineral-respiring bacteria use elaborate haem-based electron transfer mechanisms2–4 but the existence and mechanistic basis of other EETs remain largely unknown. Here we show that the food-borne pathogen Listeria monocytogenes uses a distinctive flavin-based EET mechanism to deliver electrons to iron or an electrode. By performing a forward genetic screen to identify L. monocytogenes mutants with diminished extracellular ferric iron reductase activity, we identified an eight-gene locus that is responsible for EET. This locus encodes a specialized NADH dehydrogenase that segregates EET from aerobic respiration by channelling electrons to a discrete membrane-localized quinone pool. Other proteins facilitate the assembly of an abundant extracellular flavoprotein that, in conjunction with free-molecule flavin shuttles, mediates electron transfer to extracellular acceptors. This system thus establishes a simple electron conduit that is compatible with the single-membrane structure of the Gram-positive cell. Activation of EET supports growth on non-fermentable carbon sources, and an EET mutant exhibited a competitive defect within the mouse gastrointestinal tract. Orthologues of the genes responsible for EET are present in hundreds of species across the Firmicutes phylum, including multiple pathogens and commensal members of the intestinal microbiota, and correlate with EET activity in assayed strains. These findings suggest a greater prevalence of EET-based growth capabilities and establish a previously underappreciated relevance for electrogenic bacteria across diverse environments, including host-associated microbial communities and infectious disease.

Keywords: Ferric Iron Reductase; Nb Fm; Ferric Ammonium Citrate; Gene Name Assignment; Brain Heart Infusion Medium (search for similar items in EconPapers)
Date: 2018
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Citations: View citations in EconPapers (2)

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DOI: 10.1038/s41586-018-0498-z

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