A flavin-based extracellular electron transfer mechanism in diverse Gram-positive bacteria
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 mechanisms2,3,4 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 andmore »
- Authors:
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1574398
- DOE Contract Number:
- AC02-05CH11231
- Resource Type:
- Journal Article
- Journal Name:
- Nature (London)
- Additional Journal Information:
- Journal Volume: 562; Journal Issue: 7725; Journal ID: ISSN 0028-0836
- Country of Publication:
- United States
- Language:
- English
Citation Formats
Light, Samuel H., Su, Lin, Rivera-Lugo, Rafael, Cornejo, Jose A., Louie, Alexander, Iavarone, Anthony T., Ajo-Franklin, Caroline M., and Portnoy, Daniel A. A flavin-based extracellular electron transfer mechanism in diverse Gram-positive bacteria. United States: N. p., 2018.
Web. doi:10.1038/s41586-018-0498-z.
Light, Samuel H., Su, Lin, Rivera-Lugo, Rafael, Cornejo, Jose A., Louie, Alexander, Iavarone, Anthony T., Ajo-Franklin, Caroline M., & Portnoy, Daniel A. A flavin-based extracellular electron transfer mechanism in diverse Gram-positive bacteria. United States. https://doi.org/10.1038/s41586-018-0498-z
Light, Samuel H., Su, Lin, Rivera-Lugo, Rafael, Cornejo, Jose A., Louie, Alexander, Iavarone, Anthony T., Ajo-Franklin, Caroline M., and Portnoy, Daniel A. Wed .
"A flavin-based extracellular electron transfer mechanism in diverse Gram-positive bacteria". United States. https://doi.org/10.1038/s41586-018-0498-z.
@article{osti_1574398,
title = {A flavin-based extracellular electron transfer mechanism in diverse Gram-positive bacteria},
author = {Light, Samuel H. and Su, Lin and Rivera-Lugo, Rafael and Cornejo, Jose A. and Louie, Alexander and Iavarone, Anthony T. and Ajo-Franklin, Caroline M. and Portnoy, Daniel A.},
abstractNote = {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 mechanisms2,3,4 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.},
doi = {10.1038/s41586-018-0498-z},
url = {https://www.osti.gov/biblio/1574398},
journal = {Nature (London)},
issn = {0028-0836},
number = 7725,
volume = 562,
place = {United States},
year = {2018},
month = {9}
}
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