Flavin Electron Shuttles Dominate Extracellular Electron Transfer by <named-content content-type="genus-species">Shewanella oneidensis</named-content>

ABSTRACT 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...

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Autores principales:	Nicholas J. Kotloski, Jeffrey A. Gralnick
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2013
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/604cdc3046e74e5f9f81eb180507cfde
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spelling	oai:doaj.org-article:604cdc3046e74e5f9f81eb180507cfde2021-11-15T15:40:24ZFlavin Electron Shuttles Dominate Extracellular Electron Transfer by <named-content content-type="genus-species">Shewanella oneidensis</named-content>10.1128/mBio.00553-122150-7511https://doaj.org/article/604cdc3046e74e5f9f81eb180507cfde2013-03-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00553-12https://doaj.org/toc/2150-7511ABSTRACT 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. IMPORTANCE Extracellular electron transfer by microbes is critical for the geochemical cycling of metals, bioremediation, and biocatalysis using electrodes. A controversy in the field was addressed by demonstrating that flavin electron shuttling, not direct electron transfer or nanowires, is the primary mechanism of extracellular electron transfer employed by the bacterium Shewanella oneidensis. We have identified a flavin adenine dinucleotide transporter conserved in all sequenced Shewanella species that facilitates export of flavin electron shuttles in S. oneidensis. Analysis of a strain that is unable to secrete flavins demonstrated that electron shuttling accounts for ~75% of the insoluble extracellular electron transfer capacity in S. oneidensis.Nicholas J. KotloskiJeffrey A. GralnickAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 1 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Nicholas J. Kotloski Jeffrey A. Gralnick Flavin Electron Shuttles Dominate Extracellular Electron Transfer by <named-content content-type="genus-species">Shewanella oneidensis</named-content>
description	ABSTRACT 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. IMPORTANCE Extracellular electron transfer by microbes is critical for the geochemical cycling of metals, bioremediation, and biocatalysis using electrodes. A controversy in the field was addressed by demonstrating that flavin electron shuttling, not direct electron transfer or nanowires, is the primary mechanism of extracellular electron transfer employed by the bacterium Shewanella oneidensis. We have identified a flavin adenine dinucleotide transporter conserved in all sequenced Shewanella species that facilitates export of flavin electron shuttles in S. oneidensis. Analysis of a strain that is unable to secrete flavins demonstrated that electron shuttling accounts for ~75% of the insoluble extracellular electron transfer capacity in S. oneidensis.
format	article
author	Nicholas J. Kotloski Jeffrey A. Gralnick
author_facet	Nicholas J. Kotloski Jeffrey A. Gralnick
author_sort	Nicholas J. Kotloski
title	Flavin Electron Shuttles Dominate Extracellular Electron Transfer by <named-content content-type="genus-species">Shewanella oneidensis</named-content>
title_short	Flavin Electron Shuttles Dominate Extracellular Electron Transfer by <named-content content-type="genus-species">Shewanella oneidensis</named-content>
title_full	Flavin Electron Shuttles Dominate Extracellular Electron Transfer by <named-content content-type="genus-species">Shewanella oneidensis</named-content>
title_fullStr	Flavin Electron Shuttles Dominate Extracellular Electron Transfer by <named-content content-type="genus-species">Shewanella oneidensis</named-content>
title_full_unstemmed	Flavin Electron Shuttles Dominate Extracellular Electron Transfer by <named-content content-type="genus-species">Shewanella oneidensis</named-content>
title_sort	flavin electron shuttles dominate extracellular electron transfer by <named-content content-type="genus-species">shewanella oneidensis</named-content>
publisher	American Society for Microbiology
publishDate	2013
url	https://doaj.org/article/604cdc3046e74e5f9f81eb180507cfde
work_keys_str_mv	AT nicholasjkotloski flavinelectronshuttlesdominateextracellularelectrontransferbynamedcontentcontenttypegenusspeciesshewanellaoneidensisnamedcontent AT jeffreyagralnick flavinelectronshuttlesdominateextracellularelectrontransferbynamedcontentcontenttypegenusspeciesshewanellaoneidensisnamedcontent
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Flavin Electron Shuttles Dominate Extracellular Electron Transfer by <named-content content-type="genus-species">Shewanella oneidensis</named-content>

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