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A Re-evaluation of Electron-Transfer Mechanisms in Microbial Electrochemistry: Shewanella Releases Iron that Mediates Extracellular Electron Transfer.

ABSTRACT: Exoelectrogenic bacteria can couple their metabolism to extracellular electron acceptors, including macroscopic electrodes, and this has applications in energy production, bioremediation and biosensing. Optimisation of these technologies relies on a detailed molecular understanding of extracellular electron-transfer (EET) mechanisms, and Shewanella oneidensis MR-1 (MR-1) has become a model organism for such fundamental studies. Here, cyclic voltammetry was used to determine the relationship between the surface chemistry of electrodes (modified gold, ITO and carbon electrodes) and the EET mechanism. On ultra-smooth gold electrodes modified with self-assembled monolayers containing carboxylic-acid-terminated thiols, an EET pathway dominates with an oxidative catalytic onset at 0.1?V versus SHE. Addition of iron(II)chloride enhances the catalytic current, whereas the siderophore deferoxamine abolishes this signal, leading us to conclude that this pathway proceeds via an iron mediated electron transfer mechanism. The same EET pathway is observed at other electrodes, but the onset potential is dependent on the electrolyte composition and electrode surface chemistry. EET pathways with onset potentials above -0.1?V versus SHE have previously been ascribed to direct electron-transfer (DET) mechanisms through the surface exposed decaheme cytochromes (MtrC/OmcA) of MR-1. In light of the results reported here, we propose that the previously identified DET mechanism of MR-1 needs to be re-evaluated.

SUBMITTER: Oram J

PROVIDER: S-EPMC5021177 | biostudies-literature | 2016 May

REPOSITORIES: biostudies-literature

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A Re-evaluation of Electron-Transfer Mechanisms in Microbial Electrochemistry: <i>Shewanella</i> Releases Iron that Mediates Extracellular Electron Transfer.

Oram Joseph J Jeuken Lars J C LJ

ChemElectroChem 20160219 5

Exoelectrogenic bacteria can couple their metabolism to extracellular electron acceptors, including macroscopic electrodes, and this has applications in energy production, bioremediation and biosensing. Optimisation of these technologies relies on a detailed molecular understanding of extracellular electron-transfer (EET) mechanisms, and <i>Shewanella oneidensis</i> MR-1 (MR-1) has become a model organism for such fundamental studies. Here, cyclic voltammetry was used to determine the relationsh ...[more]

PMID: 27668145

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Project description:UnlabelledShewanella 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 ?bfe 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.ImportanceExtracellular 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.

Dataset Information

A Re-evaluation of Electron-Transfer Mechanisms in Microbial Electrochemistry: Shewanella Releases Iron that Mediates Extracellular Electron Transfer.

Publications

A Re-evaluation of Electron-Transfer Mechanisms in Microbial Electrochemistry: <i>Shewanella</i> Releases Iron that Mediates Extracellular Electron Transfer.

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