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Extracellular Electron Transfer from Cathode to Microbes: Application for Biofuel Production Okkyoung Choi and Byoung‑In Sang*

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Extracellular Electron Transfer from Cathode to Microbes: Application for Biofuel Production Okkyoung Choi and Byoung‑In Sang* Choi and Sang Biotechnol Biofuels (2016) 9:11 DOI 10.1186/s13068-016-0426-0 Biotechnology for Biofuels REVIEW Open Access Extracellular electron transfer from cathode to microbes: application for biofuel production Okkyoung Choi and Byoung‑In Sang* Abstract Extracellular electron transfer in microorganisms has been applied for bioelectrochemical synthesis utilizing microbes to catalyze anodic and/or cathodic biochemical reactions. Anodic reactions (electron transfer from microbe to anode) are used for current production and cathodic reactions (electron transfer from cathode to microbe) have recently been applied for current consumption for valuable biochemical production. The extensively studied exoelectro‑ genic bacteria Shewanella and Geobacter showed that both directions for electron transfer would be possible. It was proposed that gram-positive bacteria, in the absence of cytochrome C, would accept electrons using a cascade of membrane-bound complexes such as membrane-bound Fe-S proteins, oxidoreductase, and periplasmic enzymes. Modification of the cathode with the addition of positive charged species such as chitosan or with an increase of the interfacial area using a porous three-dimensional scaffold electrode led to increased current consumption. The extracellular electron transfer from the cathode to the microbe could catalyze various bioelectrochemical reductions. Electrofermentation used electrons from the cathode as reducing power to produce more reduced compounds such as alcohols than acids, shifting the metabolic pathway. Electrofuel could be generated through artificial photosynthe‑ sis using electrical energy instead of solar energy in the process of carbon fixation. Keywords: Bioelectrochemical synthesis, Extracellular electron transfer, Cathodic electron, Electrofuel Background and/or cathodic reactions. BES has two categories An eventual replacement of fossil energy source with according to the direction of electron flow, microbial fuel sustainable energy system is unavoidable. Biofuels have cells (MFC, electricity production), and microbial elec- emerged as one of the sustainable fuels sources and it is trosynthesis (MES, electricity consumption). A microbial considered as alternatives to petroleum. Biomass cap- fuel cell uses extracellular electron transfer to an elec- tured the energy from sunlight and stored it as high- trode originating from organic compounds consumed by energy chemical bonds, which is used for biofuels. More microorganisms. Microbial electrosynthesis uses elec- recently, electrofuels have been studied for liquid fuels as tron transfer from an electrode to microorganisms pro- a means for intermittent electricity storage [1] using the ducing reduced biochemical compounds. An electrode is energy of low-potential electrons such as hydrogen gas, thus used as an electron acceptor (MFC) or an electron reduced metal, or electricity [2]. It usually uses the inter- donor (MES). action between microbes and electrode, through extra- Extracellular electron transfer has been gaining wide cellular electron transfer. interest in relation to microbial electrochemical synthesis Bioelectrochemical synthesis (BES) uses extracellular [1, 3], interspecies electron transfer [4, 5], and microbial electron transfer of microorganisms catalyzing anodic immobilization of heavy metals for bioremediation [6, 7] (Table 1). In particular, biofuels or biochemicals are reduced compounds and the reducing power is needed in *Correspondence: [email protected] Department of Chemical Engineering, Hanyang University, 222 microbial fermentation processes [8, 9]. An external sup- Wangshimni‑ro, Seongdong‑gu, Seoul 04763, South Korea ply of electrons using electricity enhances the reducing © 2016 Choi and Sang. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Choi andSang Table 1 The application of bioelectrochemical reduction Application Product Reaction conditions Key outcomes Ref. 6 3 Biofuels(2016)9:11 Biotechnol Direct reduction Cr + Cr + G. sulfurreducens, 600 mV vs. Ag/AgCl U(VI) was removed and recovered using poised [19] → − electrode Shewanella oneidensis MR‑1, 500 mV vs. Ag/AgCl Lactate and the electrode as the electron donors for [18] − Cr(VI) reduction Fumarate succinate G. sulfurreducens, 500 mV vs. Ag/AgCl Fumarate reduction dependent on current supply [48] → − Shewanella species in biocathode of microbial fuel Similar comparison under chromate reducing [102] cell condition Nitrate reduction Nitrifying and denitrifying microorganisms at Simultaneous occurrence of nitrification and denitri‑[49] 197 mV vs. SHE fication at a biocathode + Denitrifying microorganisms at 123 mV vs. SHE Long‑term stability, carbon‑free operation [51] − Indirect reduction Caproate and caprylate production from acetate Acetate fed at 0.9 V vs. NHE In situ‑produced hydrogen as electron donor, low [90] − concentration and reaction rates Ethanol production from acetate 550 mV vs. NHE, artificial mediator tested Methyl viologen increased ethanol production but [81] − inhibited butyrate and methane formation, still hydrogen was coproduced at the cathode Alcohol formation from glycerol Open circuit operation Changes in microbial community and product [87] outcomes after current supply Reduction of acetate and butyrate to mainly alco‑ 820 mV vs. Ag/AgCl Halotolerant mixed sulfate‑reducing bacteria [92] hols and acetone − culture Polyhydroxyalkanoates (PHA) from glucose 512 mV, the biocathode coupled to a bioanode in Microaerophilic microenvironment at cathode [94] an MEC enhanced PHA synthesis as alternative pathway to re‑oxidize the NADH Butyraldehyde to butanol Immobilized alcohol dehydrogenase at 400 mV Reduction to alcohol by current without supple‑ [88] vs. Ag/AgCl − ment of NADH Hydrogen production 700 mV vs. Ag/AgCl Increased cathodic hydrogen efficiency on micro‑ [103] − bial biocathode based on a naturally selected mixed culture 500 mV, the biocathode coupled to a bioanode in Operated for a long period with high current [104] an MEC density but phosphate precipitation on the biocathode 700 mV vs. SHE Desulfovibrio sp. as a dominant microorganism in [22] − the biocathode Methane production 700 mV vs. Ag/AgCl Methane production directly from current [53] − 550 mV vs. NHE CO2 reduction to CH4, need to reduce the internal [105] − resistance Improved 1,3‑propandiol production from glycerol 900 mV vs. SHE Electrical current as the driving force for a mixed [93] − population fermenting glycerol in the cathode Improved butanol production from glucose 0.045 V vs. SHE Increased alcohol production in electrofermenta‑ [24] 2of14 Page + tion with increased a ratio NADH/NAD+ Choi andSang Biotechnol Biofuels(2016)9:11 Biotechnol Table 1 continued Application Product Reaction conditions Key outcomes Ref. Electrofuel from CO2 and electricity Butyrate 800 mV vs. SHE Production of organic compounds from CO2 by [100] − hydrogen driven by a cathode Acetate 590 mV vs. SHE Higher acetate production than on unmodified [99] − graphite Acetate, 2‑oxobutyrate 400 mV vs. SHE The production of organic acids by current con‑ [106] − sumption Page 3of14 Page Choi and Sang Biotechnol Biofuels (2016) 9:11 Page 4 of 14 process in microbial metabolism. Direct electron transfer Electron transfer from a cathode to microbes is ideal in extracellular electron transfer from a cathode Multihame c-type cytochrome is a key component of the to microbes. electron transfer channel in gram-negative bacteria [10]. The two mostly extensively studied microorgan- Filamentous conductive pili are also involved in electron isms for extracellular electron transfer are Geobacter transfer in Shewanella [17] and Geobacter [11]. BES uses and Shewanella species. Geobacter and Shewanella are two directions, i.e., microbe → electrode (anode) in MFC metal-reducing and gram-negative bacteria. Extracel- and electrode (cathode) → microbe in MES, with the lular electron transfer in microorganisms is used in the same or different mode. Electrons flow from an electron metal reduction process by the microorganism and, donor with a relatively lower redox potential to an elec- in this case, the metal is used as an electron accep- tron acceptor with higher redox potential. In this light, in tor. When metal (hydr)oxides that are poorly soluble the present study we address the question that of whether in water are present as electron acceptors, extracel- it is possible to use the same electron transport chain for lular electron transfer occurs using multihaem c-type the opposite direction. cytochromes in Geobacter and Shewanella [10]. Based The redox tower in Fig. 2 shows the broad range of on this phenomenon, the microorganisms are able to redox potential for MtrC (located on an extracellular extracellularly transfer electrons and this can be applied site of the outer membrane), MrtA (a periplasmic c-type for BES. cytochrome), CymA (a link point between the inner The mode of extracellular electron transfer is broadly membrane and the periplasm), and OmcA (anchored in divided into
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