Analysis of Enhanced Current-Generating Mechanism of Geobacter sulfurreducens Strain via Model-Driven Metabolism Simulation

Jing Meng,Yunxia Yue,Xiao Sun,Jing Guo,Zixiang Xu,Arum Han

doi:10.1371/journal.pone.0073907

Jing Meng, Yunxia Yue + Show 4 more

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https://doi.org/10.1371/journal.pone.0073907

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Abstract

Microbial fuel cells (MFCs) are a class of ideal technologies that function via anaerobic respiration of electricigens, which bring current generation and environmental restoration together. An in-depth understanding of microbial metabolism is of great importance in engineering microbes to further improve their respiration. We employed flux balance analysis and selected Fe(iii) as a substitute for the electrode to simulate current-generating metabolism of Geobacter sulfurreducens PCA with a fixed acetate uptake rate. Simulation results indicated the fluxes of reactions directing acetate towards dissimilation to generate electrons increased under the suboptimal growth condition, resulting in an increase in the respiration rate and a decrease in the growth rate. The results revealed the competitive relationship between oxidative respiration and cell growth during the metabolism of microbe current generation. The results helped us quantitatively understand why microbes growing slowly have the potential to make good use of fuel in MFCs. At the same time, slow growth does not necessarily result in speedy respiration. Alternative respirations may exist under the same growth state due to redundant pathways in the metabolic network. The big difference between the maximum and minimum respiration mainly results from the total formate secretion. With iterative flux variability analysis, a relatively ideal model of variant of G. sulfurreducens PCA was reconstructed by deleting several enzymes in the wild model, which could reach simultaneous suboptimal growth and maximum respiration. Under this ideal condition, flux towards extracellular electron transfer rather than for biosynthesis is beneficial for the conversion of organic matter to electricity without large accumulations of biomass and electricigens may maximize utilization of limited fuel. Our simulations will provide an insight into the enhanced current-generating mechanism and identify theoretical range of respiration rates for guiding strain improvement in MFCs.

Highlights

Microbial Fuel Cells [1,2] are devices that convert a diverse range of organic matters to electricity with microbes serving as catalysts
In order to examine the impact of growth state on the current production capacity, we simulated optimal and suboptimal growth by constraining acetate uptake rate at 13.630mmol/ g.dw/h
We confined our attention to central metabolism, a coupled characterization of metabolic pathways from extending previous computational and experimental analysis of the metabolic model of G. sulfurreducens [15,22]

Summary

Introduction

Microbial Fuel Cells [1,2] are devices that convert a diverse range of organic matters to electricity with microbes serving as catalysts. Practical applications of MFCs are fascinating, including power production from waste water combined with wastewater treatment, oxidation of contaminants to harmless carbon dioxide using an electrode as the electron acceptor, reduction of toxic metals to insoluble forms with an electrode as the electron donor, and driving small-scale portable electronics, microrobots, and so on. Widespread utilization of MFCs cannot be expected because of the current bottleneck in power production and costing materials. The conductive biofilms of Geobacter sulfurreducens have been utilized to enhance the capacity for current production [3]. Electricigens can completely oxidize organic matters, resulting in extracellular electron transfer to anodes via the entire respiratory chain, and to cathodes via the external electric circuit to reduce terminal electron acceptors, such as O2Mn4+.

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