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      Microbial electro-fermentation for synthesis of chemicals and biofuels driven by bi-directional extracellular electron transfer

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          Abstract

          Electroactive bacteria could perform bi-directional extracellular electron transfer (EET) to exchange electrons and energy with extracellular environments, thus playing a central role in microbial electro-fermentation (EF) process. Unbalanced fermentation and microbial electrosynthesis are the main pathways to produce value-added chemicals and biofuels. However, the low efficiency of the bi-directional EET is a dominating bottleneck in these processes. In this review, we firstly demonstrate the main bi-directional EET mechanisms during EF, including the direct EET and the shuttle-mediated EET. Then, we review representative milestones and progresses in unbalanced fermentation via anode outward EET and microbial electrosynthesis via inward EET based on these two EET mechanisms in detail. Furthermore, we summarize the main synthetic biology strategies in improving the bi-directional EET and target products synthesis, thus to enhance the efficiencies in unbalanced fermentation and microbial electrosynthesis. Lastly, a perspective on the applications of microbial electro-fermentation is provided.

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          Most cited references66

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          Water splitting-biosynthetic system with CO₂ reduction efficiencies exceeding photosynthesis.

          Artificial photosynthetic systems can store solar energy and chemically reduce CO2 We developed a hybrid water splitting-biosynthetic system based on a biocompatible Earth-abundant inorganic catalyst system to split water into molecular hydrogen and oxygen (H2 and O2) at low driving voltages. When grown in contact with these catalysts, Ralstonia eutropha consumed the produced H2 to synthesize biomass and fuels or chemical products from low CO2 concentration in the presence of O2 This scalable system has a CO2 reduction energy efficiency of ~50% when producing bacterial biomass and liquid fusel alcohols, scrubbing 180 grams of CO2 per kilowatt-hour of electricity. Coupling this hybrid device to existing photovoltaic systems would yield a CO2 reduction energy efficiency of ~10%, exceeding that of natural photosynthetic systems.
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            Integrated electromicrobial conversion of CO2 to higher alcohols.

            One of the major challenges in using electrical energy is the efficiency in its storage. Current methods, such as chemical batteries, hydraulic pumping, and water splitting, suffer from low energy density or incompatibility with current transportation infrastructure. Here, we report a method to store electrical energy as chemical energy in higher alcohols, which can be used as liquid transportation fuels. We genetically engineered a lithoautotrophic microorganism, Ralstonia eutropha H16, to produce isobutanol and 3-methyl-1-butanol in an electro-bioreactor using CO(2) as the sole carbon source and electricity as the sole energy input. The process integrates electrochemical formate production and biological CO(2) fixation and higher alcohol synthesis, opening the possibility of electricity-driven bioconversion of CO(2) to commercial chemicals.
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              Structure of Microbial Nanowires Reveals Stacked Hemes that Transport Electrons over Micrometers

              Long-range (>10 μm) transport of electrons along networks of Geobacter sulfurreducens protein filaments, known as microbial nanowires, has been invoked to explain a wide range of globally important redox phenomena. These nanowires were previously thought to be type IV pili composed of PilA protein. Here we report a 3.7 Å resolution cryo-electron microscopy structure which surprisingly reveals that, rather than PilA, G. sulfurreducens nanowires are assembled by micrometer-long polymerization of the hexaheme cytochrome OmcS, with hemes packed within ~3.5–6 Å of each other. The inter-subunit interfaces show unique structural elements such as inter-subunit parallel-stacked hemes and axial coordination of heme by histidines from neighbouring subunits. Wild-type OmcS filaments show 100-fold greater conductivity than other filaments from an Δ omcS strain, highlighting the importance of OmcS to conductivity in these nanowires. This structure explains the remarkable capacity of soil bacteria to transport electrons to remote electron acceptors for respiration and energy sharing.
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                Author and article information

                Contributors
                Journal
                Synth Syst Biotechnol
                Synth Syst Biotechnol
                Synthetic and Systems Biotechnology
                KeAi Publishing
                2405-805X
                08 September 2020
                December 2020
                08 September 2020
                : 5
                : 4
                : 304-313
                Affiliations
                [a ]Frontier Science Center for Synthetic Biology and Key Laboratory of Systems Bioengineering (Ministry of Education), Tianjin University, Tianjin, 300072, China
                [b ]Collaborative Innovation Center of Chemical Science and Engineering (Tianjin), School of Chemical Engineering and Technology, Tianjin University, Tianjin, 300072, China
                Author notes
                []Corresponding author. Frontier Science Center for Synthetic Biology and Key Laboratory of Systems Bioengineering (Ministry of Education), Tianjin University, Tianjin, 300072, China. hsong@ 123456tju.edu.cn
                [∗∗ ]Corresponding author. Frontier Science Center for Synthetic Biology and Key Laboratory of Systems Bioengineering (Ministry of Education), Tianjin University, Tianjin, 300072, China. messilifeng@ 123456163.com
                [1]

                Co-First authors: Ziying Gong and Huan Yu.

                Article
                S2405-805X(20)30063-6
                10.1016/j.synbio.2020.08.004
                7490822
                32995586
                575f6cfb-0f78-4fd0-8c28-f3ec53b82b30
                © 2020 KeAi Communications Co.(+) Ltd

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 1 June 2020
                : 23 July 2020
                : 25 August 2020
                Categories
                Article

                unbalanced fermentation,microbial electrosynthesis,extracellular electron transfer,synthetic biology

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