Extracellular Electron Shuttling Mediated by Soluble c-Type Cytochromes Produced by Shewanella oneidensis MR-1

Abstract

How metal-reducing bacteria transfer electrons during dissimilatory energy generation under electron acceptor-limited conditions is poorly understood. Here, we incubated the iron and manganese-reducing bacterium Shewanella oneidensis MR-1 without electron acceptors. Removal of soluble extracellular organic compounds (EOCs) dramatically retarded transfer of electrons to an experimental electron acceptor, Cr(VI), by MR-1. However, the return of either high MW (>3000 Da) or low MW (<3000 Da) soluble EOCs produced by MR-1 to washed cells restored Cr(VI) reduction though Cr(VI) reduction was fastest when both size fractions were added together. Spectral and electrochemical characterization of EOCs indicated the presence of flavins and c-type cytochromes (c-Cyts). A model of the kinetics of individual elementary reactions between cells, flavins, released c-Cyts, and Cr(VI), including the direct reduction of flavins, released c-Cyts, and Cr(VI) by cells and the indirect reduction of Cr(VI) by reduced forms of flavins and released c-Cyts, was developed. Model results suggest that released c-Cyts could act as electron mediators to accelerate electron transfer from cells to Cr(VI), and the relative contribution of this pathway was higher than that mediated by flavins. Hence, extracellular c-Cyts produced by MR-1 likely play a role in extracellular electron transfer under electron acceptor-limited conditions. These findings provide new insights into extracellular electron shuttling and the metabolic strategy of metal-reducing bacteria under electron acceptor-limited conditions.

High Current Production of Shewanella Oneidensis with Electrospun Carbon Nanofiber Anodes is Directly Linked to Biofilm Formation**

“…[12] Recently, indications for mediated electron transfer by soluble c-type cytochromes contained in culture supernatant were found. [13] Okamoto et al [14,15] suggested a different role of flavins in the extracellular electron transport: flavin mononucleotide and RF act as co-factor of the outer membrane cytochromes MtrC and OmcA respectively and enhance their extracellular electron transfer rates. This role may explain the observed current increase in the presence of low concentrations of flavins that hardly can be accounted for by diffusive MET.…”

“…However, the per cell flavin reduction rate in solution corresponding to about 2 fA [11] is only about 4 % of the current production with direct contact to the electrode of 50 fA [12] . Recently, indications for mediated electron transfer by soluble c‐type cytochromes contained in culture supernatant were found [13] . Okamoto et al [14,15] .…”

Liposoluble quinone promotes the reduction of hydrophobic mineral and extracellular electron transfer of Shewanella oneidensis MR-1

“…It was reported that ferrihydrite reduction in Shewanella relies on secreted redox mediators. 14 , 42 To explore whether the flavin-based electron mediator acts on the surface of hydrophobic minerals, we measured the secretion of water-soluble riboflavin in supernatants. In the Fh-BIC group, riboflavin accumulates rapidly at the beginning.…”

Perspectives on Microbial Electron Transfer Networks for Environmental Biotechnology

“…It could be a critical framework of METN that makes the “microcosm-to-microcosm” communication possible. However, unlike DIET, progress on IIET has been slow to sufficient, considering that the vast candidates for electron shuttles ranged from artificial additives (e.g., H 2 , biochar, and flavins) to microbial secreta (e.g., soluble c -type cytochromes) ( Liu et al, 2020 ; Wu et al, 2020 ; Zavarzina et al, 2020 ). Overall, such “top-down” strategies mainly focus on modifying and optimizing the natural-given properties of EAM, whereas how to piece together those nature-given properties is still a fundamental question awaiting an answer.…”