title: Rate enhancement of bacterial extracellular electron transport involves bound flavin semiquinones.
abstract: Extracellular redox-active compounds, flavins and other quinones, have been hypothesized to play a major role in the delivery of electrons from cellular metabolic systems to extracellular insoluble substrates by a diffusion-based shuttling two-electron-transfer mechanism. Here we show that flavin molecules secreted by Shewanella oneidensis MR-1 enhance the ability of its outer-membrane c-type cytochromes (OM c-Cyts) to transport electrons as redox cofactors, but not free-form flavins. Whole-cell differential pulse voltammetry revealed that the redox potential of flavin was reversibly shifted more than 100 mV in a positive direction, in good agreement with increasing microbial current generation. Importantly, this flavin/OM c-Cyts interaction was found to facilitate a one-electron redox reaction via a semiquinone, resulting in a 10(3)- to 10(5)-fold faster reaction rate than that of free flavin. These results are not consistent with previously proposed redox-shuttling mechanisms but suggest that the flavin/OM c-Cyts interaction regulates the extent of extracellular electron transport coupled with intracellular metabolic activity.
authors.affiliation: Department of Applied Chemistry, School of Engineering, The University of Tokyo, Tokyo 113-8656, Japan.
authors.forename: Akihiro
authors.initials: A
authors.lastname: Okamoto
authors.forename: Kazuhito
authors.initials: K
authors.lastname: Hashimoto
authors.forename: Kenneth H
authors.initials: KH
authors.lastname: Nealson
authors.forename: Ryuhei
authors.initials: R
authors.lastname: Nakamura
mesh_terms: D018441:Biofilms; D003574:Cytochrome c Group / Q000378:metabolism*; D045304:Cytochromes c / Q000378:metabolism; D004563:Electrochemistry; D004566:Electrodes; D004578:Electron Spin Resonance Spectroscopy; D004579:Electron Transport; D005486:Flavin Mononucleotide / Q000378:metabolism; D005182:Flavin-Adenine Dinucleotide / Q000031:analogs & derivatives* / Q000378:metabolism; D006418:Heme / Q000378:metabolism; D018613:Microscopy, Confocal; D009711:Nucleotides / Q000235:genetics; D010084:Oxidation-Reduction; D020592:Shewanella / Q000378:metabolism / Q000502:physiology*
chemical_list: D003574:Cytochrome c Group; D009711:Nucleotides; D005182:Flavin-Adenine Dinucleotide; C029276:flavin semiquinone; D006418:Heme; D005486:Flavin Mononucleotide; D045304:Cytochromes c; C433527:MtrC protein, Shewanella
keywords: electromicrobiology; flavin mononucleotide; iron-reducing bacteria; microbial fuel cell; whole-cell voltammetry