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.iron-reducing bacteria | electromicrobiology | microbial fuel cell | whole-cell voltammetry | flavin mononucleotide

Performance and recent improvement in microbial fuel cells for simultaneous carbon and nitrogen removal: A review

“…Direct electron transfer (DET) refers to electrons transferred by c-type cytochromes (CTCs), flavin bound to c-type cytochromes and conductive pili, which may serve as biological nanowires (Fig. 2) (Debabov, 2008;Yang et al, 2012;Reguera et al, 2005;Okamoto et al, 2014a;Okamoto et al, 2014b). Mediated electron transfer (MET) means the addition of external electron mediators to shuttle electrons between electrodes and microorganisms that are unable to carry electrons directly to the electrodes (Lovley, 2006;Mook et al, 2013b).…”

Electron flow in multiheme bacterial cytochromes is a balancing act between heme electronic interaction and redox potentials

“…MtrB(E) does not contain any hemes but is supposed to enable contact for ET between the periplasmic MtrA(D) and the outer membrane cytochrome MtrC(F). The latter is assumed to pass electrons on to extracellular substrates either directly or via redox mediators such as flavins (11).…”

Proton Transport in the Outer‐Membrane Flavocytochrome Complex Limits the Rate of Extracellular Electron Transport

“…These non‐covalently bound cofactors of semiquinone (Sq) in OM Cyts  c 4c–4e have an unfavorable energy level for accepting electrons from heme redox centers. Because the bound Sq cofactor has a more negative redox potential than heme cofactors in OM Cyts  c , the rate of electron transport should not be enhanced compared with the highly efficient electron transport circuit of hemes in the OM Cyts  c complex.…”