Theoretical exploration of optimal metabolic flux distributions for extracellular electron transfer by Shewanella oneidensis MR-1.

Wynand S Verwoerd,Longfei Mao

doi:10.1186/s13068-014-0118-6

Abstract

BackgroundShewanella oneidensis MR-1 is one of the model microorganisms used for extracellular electron transfer. In this study, to elucidate the capability and the relevant metabolic processes of S. oneidensis MR-1 involved in an electron transferring environment, we employed genome-scale modelling to model the necessary metabolic states and flux adjustments for electricity generation in the cytochrome c-based direct electron transfer (DET) mode, the NADH-linked mediated electron transfer (MET) mode and a presumable mixed mode comprising DET and flavin secretion. These are difficult to develop experimentally.ResultsThe results showed that the microbe had the potential to achieve current outputs of up to 2.610 A/gDW in the DET mode, 2.189 A/gDW in the MET mode and 2.197 A/gDW in the mixed mode. Compared with the DET mode, which relied on cytochrome c oxidase (EC: 1.1.1.2) to mediate the electron transfer, the MET mode was mainly dependent on two routes, catalysed by isocitrate dehydrogenase (NAD) (EC: 1.1.1.4) and NAD transhydrogenase, for the computed high current density value. In the mixed mode, whereas the cytochrome c-based DET accounted for most of the computed maximum current output value, the two flavins combined, riboflavin and FMN, played a much less important role in the probed current value.ConclusionsShewanella oneidensis MR-1 has the potential to sustain a high extracellular electron transfer rate similarly to Geobacter sulfurreducens, but relies on different intracellular mechanisms. Various levels of electron transfer rates are achieved by different combinations of metabolic pathways. Flavins can significantly degenerate the maximum electricity generation capability of the cell and the biomass formation, and thus should be avoided in order to achieve a high coulombic efficiency.Electronic supplementary materialThe online version of this article (doi:10.1186/s13068-014-0118-6) contains supplementary material, which is available to authorized users.

Highlights

Shewanella oneidensis MR-1 is one of the model microorganisms used for extracellular electron transfer
In this study, we integrated electron transfer mechanisms with a genome-scale metabolic mode to determine the capability of S. oneidensis MR-1 for microbial fuel cell (MFC) current production and examine the properties of alternative genotypes arising from the energy perturbation
The results show that S. oneidensis MR-1 has the potential to produce an electric current at up to 2.610 A/gDW in the direct electron transfer (DET) mode, 2.189 A/gDW in the mediated electron transfer (MET) mode and 2.197 A/gDW in a presumed mixed mode based on cytochrome c and flavins

Summary

Introduction

Shewanella oneidensis MR-1 is one of the model microorganisms used for extracellular electron transfer. To elucidate the capability and the relevant metabolic processes of S. oneidensis MR-1 involved in an electron transferring environment, we employed genome-scale modelling to model the necessary metabolic states and flux adjustments for electricity generation in the cytochrome c-based direct electron transfer (DET) mode, the NADH-linked mediated electron transfer (MET) mode and a presumable mixed mode comprising DET and flavin secretion. Two hypotheses were proposed for the electron conduction in nanowires of Geobacter: the first claims that the cytochromes mediate the electron transfer via the pilus with metallic-like conductivity, and the second suggests that the electrons are hopping between heme groups in cytochromes aligned with the pilus to reach remote electron acceptors [9] These pili were first described for Geobacter sulfurreducens [10,11,12], and afterwards for S. oneidensis [12,13]. Unlike the anaerobic Geobacter, Shewanella can use oxygen and can have wider applications

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