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Rate enhancement of bacterial extracellular electron transport involves bound flavin semiquinones.

Okamoto A, Hashimoto K, Nealson KH, Nakamura R.

Proc Natl Acad Sci U S A. 2013 May 7;110(19):7856-61.

 

Department of Applied Chemistry, School of Engineering, The University of Tokyo, Tokyo 113-8656, Japan.

 

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 flavinmolecules secreted by Shewanella oneidensis MR-1 enhance the ability of its outer-membrane c-type cytochromes (OM c-Cyts) to transportelectrons 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.

 

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Additional Information

 

Bacteria transport electrons to solid materials in cellular exterior, such as Fe(III)- and Mn(IV)-oxide minerals and even artificial electrodes. This is called extracellular electron transport (EET), and takes a pivotal role in bacterial respiration in anaerobic biofilms such in microbial fuel cells that is capable of producing electricity by decomposing biomass and/or organic wastewater. For the EET process, researches has long believed that microbes transport electrons by a shuttling process of redox mediator, i.e. first microbes secrete an electron-carrier molecule of flavin, second the flavin receives electrons from microbes, and third the flavin diffuses to the surface of an electrode to terminate the EET via a two-electron redox reaction. Here we demonstrate 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 electrochemistry revealed that the redox potential of flavin was reversibly shifted more than 100 mV in a positive direction by the association with OM c-Cyts. Importantly, this flavin/OM c-Cyts interaction was found to facilitate a one-electron redox reaction via the semiquinone form of flavin, resulting in a 103–105-fold faster reaction rate than the two-electron reaction 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. This finding expands the strategy for the power-output improvement of microbial fuel cells, and also potentially leads to technological development for monitoring the metabolic activity of anaerobic biofilm in drug screening procedures.

Rate enhancement of bacterial extracellular electron transport involves bound flavin semiquinones