Flavin Electron Shuttles Dominate Extracellular Electron Transfer by Shewanella oneidensis

Shewanella oneidensis strain MR-1 is widely studied for its ability to respire a diverse array of soluble and insoluble electron acceptors. The ability to breathe insoluble substrates is defined as extracellular electron transfer and can occur via direct contact or by electron shuttling in S. oneide...

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Main Authors: Kotloski, Nicholas J., Gralnick, Jeffrey A.
Format: Online
Language:English
Published: American Society of Microbiology 2013
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3551548/
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spelling pubmed-35515482013-02-09 Flavin Electron Shuttles Dominate Extracellular Electron Transfer by Shewanella oneidensis Kotloski, Nicholas J. Gralnick, Jeffrey A. Observation Shewanella oneidensis strain MR-1 is widely studied for its ability to respire a diverse array of soluble and insoluble electron acceptors. The ability to breathe insoluble substrates is defined as extracellular electron transfer and can occur via direct contact or by electron shuttling in S. oneidensis. To determine the contribution of flavin electron shuttles in extracellular electron transfer, a transposon mutagenesis screen was performed with S. oneidensis to identify mutants unable to secrete flavins. A multidrug and toxin efflux transporter encoded by SO_0702 was identified and renamed bfe (bacterial flavin adenine dinucleotide [FAD] exporter) based on phenotypic characterization. Deletion of bfe resulted in a severe decrease in extracellular flavins, while overexpression of bfe increased the concentration of extracellular flavins. Strains lacking bfe had no defect in reduction of soluble Fe(III), but these strains were deficient in the rate of insoluble Fe(III) oxide reduction, which was alleviated by the addition of exogenous flavins. To test a different insoluble electron acceptor, graphite electrode bioreactors were set up to measure current produced by wild-type S. oneidensis and the Δbfe mutant. With the same concentration of supplemented flavins, the two strains produced similar amounts of current. However, when exogenous flavins were not supplemented to bioreactors, bfe mutant strains produced significantly less current than the wild type. We have demonstrated that flavin electron shuttling accounts for ~75% of extracellular electron transfer to insoluble substrates by S. oneidensis and have identified the first FAD transporter in bacteria. American Society of Microbiology 2013-01-15 /pmc/articles/PMC3551548/ /pubmed/23322638 http://dx.doi.org/10.1128/mBio.00553-12 Text en Copyright © 2013 Kotloski and Gralnick. http://creativecommons.org/licenses/by-nc-sa/3.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported (http://creativecommons.org/licenses/by-nc-sa/3.0/) license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Kotloski, Nicholas J.
Gralnick, Jeffrey A.
spellingShingle Kotloski, Nicholas J.
Gralnick, Jeffrey A.
Flavin Electron Shuttles Dominate Extracellular Electron Transfer by Shewanella oneidensis
author_facet Kotloski, Nicholas J.
Gralnick, Jeffrey A.
author_sort Kotloski, Nicholas J.
title Flavin Electron Shuttles Dominate Extracellular Electron Transfer by Shewanella oneidensis
title_short Flavin Electron Shuttles Dominate Extracellular Electron Transfer by Shewanella oneidensis
title_full Flavin Electron Shuttles Dominate Extracellular Electron Transfer by Shewanella oneidensis
title_fullStr Flavin Electron Shuttles Dominate Extracellular Electron Transfer by Shewanella oneidensis
title_full_unstemmed Flavin Electron Shuttles Dominate Extracellular Electron Transfer by Shewanella oneidensis
title_sort flavin electron shuttles dominate extracellular electron transfer by shewanella oneidensis
description Shewanella oneidensis strain MR-1 is widely studied for its ability to respire a diverse array of soluble and insoluble electron acceptors. The ability to breathe insoluble substrates is defined as extracellular electron transfer and can occur via direct contact or by electron shuttling in S. oneidensis. To determine the contribution of flavin electron shuttles in extracellular electron transfer, a transposon mutagenesis screen was performed with S. oneidensis to identify mutants unable to secrete flavins. A multidrug and toxin efflux transporter encoded by SO_0702 was identified and renamed bfe (bacterial flavin adenine dinucleotide [FAD] exporter) based on phenotypic characterization. Deletion of bfe resulted in a severe decrease in extracellular flavins, while overexpression of bfe increased the concentration of extracellular flavins. Strains lacking bfe had no defect in reduction of soluble Fe(III), but these strains were deficient in the rate of insoluble Fe(III) oxide reduction, which was alleviated by the addition of exogenous flavins. To test a different insoluble electron acceptor, graphite electrode bioreactors were set up to measure current produced by wild-type S. oneidensis and the Δbfe mutant. With the same concentration of supplemented flavins, the two strains produced similar amounts of current. However, when exogenous flavins were not supplemented to bioreactors, bfe mutant strains produced significantly less current than the wild type. We have demonstrated that flavin electron shuttling accounts for ~75% of extracellular electron transfer to insoluble substrates by S. oneidensis and have identified the first FAD transporter in bacteria.
publisher American Society of Microbiology
publishDate 2013
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3551548/
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