Metabolic engineering strategies to enable microbial electrosynthesis utilization of CO₂: recent progress and challenges

References

• Zhao T, Feng G, Chen W, et al. Artificial bioconversion of carbon dioxide. Chin J Catal. 2019;40(10):1421–1437.
   Web of Science ®Google Scholar
• Bian B, Bajracharya S, Xu J, et al. Microbial electrosynthesis from CO2: challenges, opportunities and perspectives in the context of circular bioeconomy. Bioresour Technol. 2020;302:122863.
   PubMed Web of Science ®Google Scholar
• Chen H, Dong F, Minteer SD. The progress and outlook of bioelectrocatalysis for the production of chemicals, fuels and materials. Nat Catal. 2020;3(3):225–244.
   Web of Science ®Google Scholar
• Bajracharya S, Sharma M, Mohanakrishna G, et al. An overview on emerging bioelectrochemical systems (BESs): technology for sustainable electricity, waste remediation, resource recovery, chemical production and beyond. Renewable Energy. 2016;98:153–170.
   Web of Science ®Google Scholar
• Prevoteau A, Carvajal-Arroyo JM, Ganigue R, et al. Microbial electrosynthesis from CO2: forever a promise? Curr Opin Biotechnol. 2020;62:48–57.
   PubMed Web of Science ®Google Scholar
• Lee SY, Oh YK, Lee S, et al. Recent developments and key barriers to microbial CO2 electrobiorefinery. Bioresour Technol. 2021;320(Pt A):124350.
   PubMedGoogle Scholar
• Zhang P, Liu J, Qu Y, et al. Nanomaterials for facilitating microbial extracellular electron transfer: recent progress and challenges. Bioelectrochemistry. 2018;123:190–200.
   PubMed Web of Science ®Google Scholar
• Shin HJ, Jung KA, Nam CW, et al. A genetic approach for microbial electrosynthesis system as biocommodities production platform. Bioresour Technol. 2017;245(Pt B):1421–1429.
   PubMedGoogle Scholar
• Jiang Y, May HD, Lu L, et al. Carbon dioxide and organic waste valorization by microbial electrosynthesis and electro-fermentation. Water Res. 2019;149:42–55.
   PubMed Web of Science ®Google Scholar
• Cao M, Tran VG, Zhao H. Unlocking nature’s biosynthetic potential by directed genome evolution. Curr Opin Biotechnol. 2020;66:95–104.
   PubMed Web of Science ®Google Scholar
• Lian J, Schultz C, Cao M, et al. Multi-functional genome-wide CRISPR system for high throughput genotype-phenotype mapping. Nat Commun. 2019;10(1):5794.
   PubMedGoogle Scholar
• Alpdagtas S, Turunen O, Valjakka J, et al. The challenges of using NAD(+)-dependent formate dehydrogenases for CO2 conversion. Crit Rev Biotechnol. 2021;42(6):953–972.
   PubMed Web of Science ®Google Scholar
• Kopke M, Held C, Hujer S, et al. Clostridium ljungdahlii represents a microbial production platform based on syngas. Proc Natl Acad Sci U S A. 2010;107(29):13087–13092.
   PubMed Web of Science ®Google Scholar
• Patankar S, Dudhane A, Paradh AD, et al. Improved bioethanol production using genome-shuffled clostridium ragsdalei (DSM 15248) strains through syngas fermentation. Biofuels. 2021;12(1):81–89.
   Web of Science ®Google Scholar
• Petrognani C, Boon N, Ganigué R. Production of isobutyric acid from methanol by Clostridium luticellarii. Green Chem. 2020;22(23):8389–8402.
   Web of Science ®Google Scholar
• Rodrigues RM, Guan X, Iñiguez JA, et al. Perfluorocarbon nanoemulsion promotes the delivery of reducing equivalents for electricity-driven microbial CO2 reduction. Nat Catal. 2019;2(5):407–414.
   Web of Science ®Google Scholar
• Aryal N, Tremblay PL, Lizak DM, et al. Performance of different Sporomusa species for the microbial electrosynthesis of acetate from carbon dioxide. Bioresour Technol. 2017;233:184–190.
   PubMed Web of Science ®Google Scholar
• Mayer F, Enzmann F, Lopez AM, et al. Performance of different methanogenic species for the microbial electrosynthesis of methane from carbon dioxide. Bioresour Technol. 2019;289:121706.
   PubMed Web of Science ®Google Scholar
• Rosenbaum M, Aulenta F, Villano M, et al. Cathodes as electron donors for microbial metabolism: which extracellular electron transfer mechanisms are involved? Bioresour Technol. 2011;102(1):324–333.
   PubMed Web of Science ®Google Scholar
• Zhang S, Yan L, Xing W, et al. Acidithiobacillus ferrooxidans and its potential application. Extremophiles. 2018;22(4):563–579.
   PubMed Web of Science ®Google Scholar
• Cai Z, Huang L, Quan X, et al. Acetate production from inorganic carbon (HCO3-) in photo-assisted biocathode microbial electrosynthesis systems using WO3/MoO3/g-C3N4 heterojunctions and Serratia marcescens species. Appl. Catal., B. 2020;267:118611.
   Web of Science ®Google Scholar
• Soussan L, Riess J, Erable B, et al. Electrochemical reduction of CO2 catalysed by Geobacter sulfurreducens grown on polarized stainless steel cathodes. Electrochem Commun. 2013;28:27–30.
   Web of Science ®Google Scholar
• Le QAT, Kim HG, Kim YH. Electrochemical synthesis of formic acid from CO2 catalyzed by Shewanella oneidensis MR-1 whole-cell biocatalyst. Enzyme Microb Technol. 2018;116:1–5.
   PubMed Web of Science ®Google Scholar
• Zhu X, Siegert M, Yates MD, et al. Alamethicin suppresses methanogenesis and promotes acetogenesis in bioelectrochemical systems. Appl Environ Microbiol. 2015;81(11):3863–3868.
   PubMed Web of Science ®Google Scholar
• Madjarov J, Soares R, Paquete CM, et al. Sporomusa ovata as catalyst for bioelectrochemical carbon dioxide reduction: a review across disciplines from microbiology to process engineering. Front Microbiol. 2022;13:913311.
   PubMed Web of Science ®Google Scholar
• Chen Z, Zhang Y, Luo Q, et al. Maghemite (gamma-Fe2O3) nanoparticles enhance dissimilatory ferrihydrite reduction by Geobacter sulfurreducens: impacts on iron mineralogical change and bacterial interactions. J Environ Sci (China). 2019;78:193–203.
   PubMedGoogle Scholar
• Strycharz SM, Glaven RH, Coppi MV, et al. Gene expression and deletion analysis of mechanisms for electron transfer from electrodes to Geobacter sulfurreducens. Bioelectrochemistry. 2011;80(2):142–150.
   PubMed Web of Science ®Google Scholar
• Li Y, Luo Q, Li H, et al. Application of 2-hydroxy-1,4-naphthoquinone-graphene oxide (HNQ-GO) composite as recyclable catalyst to enhance Cr(VI) reduction by Shewanella xiamenensis. J Chem Technol Biotechnol. 2019;94(2):446–454.
   Web of Science ®Google Scholar
• Li Y, Chen Z, Shi Y, et al. Function of c-type cytochromes of Shewanella xiamenensis in enhanced anaerobic bioreduction of Cr(VI) by graphene oxide and graphene oxide/polyvinyl alcohol films. J Hazard Mater. 2020;387:122018.
   PubMed Web of Science ®Google Scholar
• Kumar A, Hsu HH, Kavanagh P, et al. The ins and outs of microorganism-electrode electron transfer reactions. Nat Rev Chem. 2017;1(3):0024.
   Web of Science ®Google Scholar
• Singh S, Noori MT, Verma N. Efficient bio-electroreduction of CO2 to formate on a iron phthalocyanine-dispersed CDC in microbial electrolysis system. Electrochim Acta. 2020;338:135887.
   Web of Science ®Google Scholar
• Min K, Park YS, Park GW, et al. Elevated conversion of CO2 to versatile formate by a newly discovered formate dehydrogenase from Rhodobacter aestuarii. Bioresour Technol. 2020;305:123155.
   PubMed Web of Science ®Google Scholar
• Zhang L, Ong J, Liu J, et al. Enzymatic electrosynthesis of formate from CO2 reduction in a hybrid biofuel cell system. Renewable Energy. 2017;108:581–588.
   Web of Science ®Google Scholar
• Irfan M, Bai Y, Zhou L, et al. Direct microbial transformation of carbon dioxide to value-added chemicals: a comprehensive analysis and application potentials. Bioresour Technol. 2019;288:121401.
   PubMed Web of Science ®Google Scholar
• Sun M, Zhai L, Mu Y, et al. Bioelectrochemical element conversion reactions towards generation of energy and value-added chemicals. Prog. Energy Combust. Sci. 2020;77:100814.
   Web of Science ®Google Scholar
• Yishai O, Lindner SN, Gonzalez de la Cruz J, et al. The formate bio-economy. Curr Opin Chem Biol. 2016;35:1–9.
   PubMed Web of Science ®Google Scholar
• Claassens NJ, Cotton CAR, Kopljar D, et al. Making quantitative sense of electromicrobial production. Nat Catal. 2019;2(5):437–447.
   Web of Science ®Google Scholar
• Bose A, Gardel EJ, Vidoudez C, et al. Electron uptake by iron-oxidizing phototrophic bacteria. Nat Commun. 2014;5:3391.
   PubMed Web of Science ®Google Scholar
• Sadhukhan J, Lloyd JR, Scott K, et al. A critical review of integration analysis of microbial electrosynthesis (MES) systems with waste biorefineries for the production of biofuel and chemical from reuse of CO2. Renewable Sustainable Energy Rev. 2016;56:116–132.
   Web of Science ®Google Scholar
• Igarashi K, Kato S. Extracellular electron transfer in acetogenic bacteria and its application for conversion of carbon dioxide into organic compounds. Appl Microbiol Biotechnol. 2017;101(16):6301–6307.
   PubMed Web of Science ®Google Scholar
• Karthikeyan R, Singh R, Bose A. Microbial electron uptake in microbial electrosynthesis: a mini-review. J Ind Microbiol Biotechnol. 2019;46(9-10):1419–1426.
   PubMed Web of Science ®Google Scholar
• Wang M, Zhao Z, Zhang Y. Magnetite-contained biochar derived from fenton sludge modulated electron transfer of microorganisms in anaerobic digestion. J Hazard Mater. 2021;403:123972.
   PubMed Web of Science ®Google Scholar
• Kong F, Ren H-Y, Pavlostathis SG, et al. Overview of value-added products bioelectrosynthesized from waste materials in microbial electrosynthesis systems. Renewable Sustainable Energy Rev. 2020;125:109816.
   Web of Science ®Google Scholar
• Jiang Y, Jianxiong Zeng R. Expanding the product spectrum of value added chemicals in microbial electrosynthesis through integrated process design-a review. Bioresour Technol. 2018;269:503–512.
   PubMed Web of Science ®Google Scholar
• Shi L, Dong HL, Reguera G, et al. Extracellular electron transfer mechanisms between microorganisms and minerals. Nat Rev Microbiol. 2016;14(10):651–662.
   PubMed Web of Science ®Google Scholar
• Robert SH. Characterization of an electron conduit between bacteria and the extracellular environment. Proc. Natl. Acad. Sci. 2009;106:22169–22174.
   PubMed Web of Science ®Google Scholar
• Pirbadian S, Barchinger SE, Leung KM, et al. Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components. Proc Natl Acad Sci U S A. 2014;111(35):12883–12888.
   PubMed Web of Science ®Google Scholar
• Marsili E, Baron DB, Shikhare ID, et al. Shewanella secretes flavins that mediate extracellular electron transfer. Proc Natl Acad Sci U S A. 2008;105(10):3968–3973.
   PubMed Web of Science ®Google Scholar
• Leys D, Meyer TE, Tsapin AS, et al. Crystal structures at atomic resolution reveal the novel concept of “electron-harvesting” as a role for the small tetraheme cytochrome c. J Biol Chem. 2002;277(38):35703–35711.
   PubMed Web of Science ®Google Scholar
• Beblawy S, Bursac T, Paquete C, et al. Extracellular reduction of solid electron acceptors by Shewanella oneidensis. Mol Microbiol. 2018;109(5):571–583.
   PubMed Web of Science ®Google Scholar
• Mcmillan DGG, Marritt SJ, Firer-Sherwood MA, et al. Protein-protein interaction regulates the direction of catalysis and electron transfer in a redox enzyme complex. J Am Chem Soc. 2013;135(28):10550–10556.
   PubMed Web of Science ®Google Scholar
• Cordova CD, Schicklberger MFR, Yang Y, et al. Partial functional replacement of CymA by SirCD in Shewanella oneidensis MR-1. J Bacteriol. 2011;193(9):2312–2321.
   PubMed Web of Science ®Google Scholar
• Richardson DJ, Butt JN, Fredrickson JK, et al. The porin-cytochrome’ model for microbe-to-mineral electron transfer. Mol Microbiol. 2012;85(2):201–212.
   PubMed Web of Science ®Google Scholar
• Johs A, Shi L, Droubay T, et al. Characterization of the decaheme c-type cytochrome OmcA in solution and on hematite surfaces by small angle X-ray scattering and neutron reflectometry. Biophys J. 2010;98(12):3035–3043.
   PubMed Web of Science ®Google Scholar
• Jing X, Wu Y, Shi L, et al. Outer membrane c-type cytochromes OmcA and MtrC play distinct roles in enhancing the attachment of Shewanella oneidensis MR-1 cells to goethite. Appl Environ Microbiol. 2020;86(23):e01941-20.
   PubMed Web of Science ®Google Scholar
• Myers CR, Myers JM. MtrB is required for proper incorporation of the cytochromes OmcA and OmcB into the outer membrane of Shewanella putrefaciens MR-1. Appl Environ Microbiol. 2002;68(11):5585–5594.
   PubMed Web of Science ®Google Scholar
• Schuetz B, Schicklberger M, Kuermann J, et al. Periplasmic electron transfer via the c-type cytochromes MtrA and FccA of Shewanella oneidensis MR-1. Appl Environ Microbiol. 2009;75(24):7789–7796.
   PubMed Web of Science ®Google Scholar
• Paquete CM, Saraiva IH, Louro RO. Redox tuning of the catalytic activity of soluble fumarate reductases from Shewanella. Biochim Biophys Acta. 2014;1837(6):717–725.
   PubMed Web of Science ®Google Scholar
• Ross DE, Flynn JM, Baron DB, et al. Towards electrosynthesis in Shewanella: energetics of reversing the Mtr pathway for reductive metabolism. PLoS One. 2011;6(2):e16649.
   PubMed Web of Science ®Google Scholar
• Feng J, Jiang M, Li K, et al. Direct electron uptake from a cathode using the inward Mtr pathway in Escherichia coli. Bioelectrochemistry. 2020;134:107498.
   PubMed Web of Science ®Google Scholar
• Tokunou Y, Hashimoto K, Okamoto A. Extracellular electron transport scarcely accumulates proton motive force in Shewanella oneidensis MR-1. BCSJ. 2015;88(5):690–692.
   Google Scholar
• Rowe AR, Rajeev P, Jain A, et al. Tracking electron uptake from a cathode into Shewanella cells: implications for energy acquisition from solid-substrate electron donors. mBio. 2018;9(1):e02203-17.
   PubMed Web of Science ®Google Scholar
• Sun D, Wan X, Liu W, et al. Characterization of the genome from Geobacter anodireducens, a strain with enhanced current production in bioelectrochemical systems. RSC Adv. 2019;9(44):25890–25899.
   PubMed Web of Science ®Google Scholar
• Thirumurthy MA, Jones AK. Geobacter cytochrome OmcZs binds riboflavin: implications for extracellular electron transfer. Nanotechnology. 2020;31(12):124001.
   PubMed Web of Science ®Google Scholar
• Richter H, Nevin KP, Jia H, et al. Cyclic voltammetry of biofilms of wild type and mutant Geobacter sulfurreducens on fuel cell anodes indicates possible roles of OmcB, OmcZ, type IV pili, and protons in extracellular electron transfer. Energy Environ Sci. 2009;2(5):506–516.
   Web of Science ®Google Scholar
• Lovley DR, Walker DJF. Geobacter protein nanowires. Front Microbiol. 2019;10:2078.
   PubMed Web of Science ®Google Scholar
• Teixeira LR, Portela PC, Morgado L, et al. Backbone assignment of cytochrome PccH, a crucial protein for microbial electrosynthesis in Geobacter sulfurreducens. Biomol NMR Assign. 2019;13(2):321–326.
   PubMed Web of Science ®Google Scholar
• Dantas JM, Tomaz DM, Morgado L, et al. Functional characterization of PccH, a key cytochrome for electron transfer from electrodes to the bacterium Geobacter sulfurreducens. FEBS Lett. 2013;587(16):2662–2668.
   PubMed Web of Science ®Google Scholar
• Deng X, Dohmae N, Nealson KH, et al. Multi-heme cytochromes provide a pathway for survival in energy-limited environments. Sci Adv. 2018;4(2):eaao5682. Feb
   PubMed Web of Science ®Google Scholar
• Deng X, Dohmae N, Kaksonen AH, et al. Biogenic iron sulfide nanoparticles to enable extracellular electron uptake in sulfate-reducing bacteria. Angew Chem Int Ed Engl. 2020;59(15):5995–5999.
   PubMed Web of Science ®Google Scholar
• Karbelkar AA, Rowe AR, El-Naggar MY. An electrochemical investigation of interfacial electron uptake by the sulfur oxidizing bacterium Thioclava electrotropha ElOx9. Electrochim Acta. 2019;324:134838.
   Web of Science ®Google Scholar
• Lohner ST, Deutzmann JS, Logan BE, et al. Hydrogenase-independent uptake and metabolism of electrons by the archaeon Methanococcus maripaludis. Isme J. 2014;8(8):1673–1681.
   PubMed Web of Science ®Google Scholar
• Ishii T, Kawaichi S, Nakagawa H, et al. From chemolithoautotrophs to electrolithoautotrophs: CO2 fixation by Fe(II)-oxidizing bacteria coupled with direct uptake of electrons from solid electron sources. Front Microbiol. 2015;6:994.
   PubMed Web of Science ®Google Scholar
• Zhen G, Lu X, Kumar G, et al. Microbial electrolysis cell platform for simultaneous waste biorefinery and clean electrofuels generation: Current situation, challenges and future perspectives. Prog Energy Combust Sci. 2017;63:119–145.
   Web of Science ®Google Scholar
• Rosenbaum MA, Henrich AW. Engineering microbial electrocatalysis for chemical and fuel production. Curr Opin Biotechnol. 2014;29:93–98.
   PubMed Web of Science ®Google Scholar
• Jensen HM, Albers AE, Malley KR, et al. Engineering of a synthetic electron conduit in living cells. Proc Natl Acad Sci U S A. 2010;107(45):19213–19218.
   PubMed Web of Science ®Google Scholar
• Sturm-Richter K, Golitsch F, Sturm G, et al. Unbalanced fermentation of glycerol in Escherichia coli via heterologous production of an electron transport chain and electrode interaction in microbial electrochemical cells. Bioresour Technol. 2015;186:89–96.
   PubMed Web of Science ®Google Scholar
• Jensen HM, TerAvest MA, Kokish MG, et al. CymA and exogenous flavins improve extracellular electron transfer and couple it to cell growth in Mtr-expressing Escherichia coli. ACS Synth Biol. 2016;5(7):679–688.
   PubMed Web of Science ®Google Scholar
• Wu Z, Wang J, Liu J, et al. Engineering an electroactive Escherichia coli for the microbial electrosynthesis of succinate from glucose and CO2. Microb Cell Fact. 2019;18(1):15.
   PubMedGoogle Scholar
• Su L, Fukushima T, Ajo-Franklin CM. A hybrid cyt c maturation system enhances the bioelectrical performance of engineered Escherichia coli by improving the rate-limiting step. Biosens Bioelectron. 2020;165:112312.
   PubMed Web of Science ®Google Scholar
• Feng J, Lu Q, Li K, et al. Construction of an electron transfer mediator pathway for bioelectrosynthesis by Escherichia coli. Front Bioeng Biotechnol. 2020;8:590667.
   PubMed Web of Science ®Google Scholar
• Antonovsky N, Gleizer S, Noor E, et al. Sugar synthesis from CO2 in Escherichia coli. Cell. 2016;166(1):115–125.
   PubMed Web of Science ®Google Scholar
• Gleizer S, Ben-Nissan R, Bar-On YM, et al. Conversion of Escherichia coli to generate all biomass carbon from CO2. Cell. 2019;179(6):1255–1263.e12.
   PubMed Web of Science ®Google Scholar
• Satanowski A, Dronsella B, Noor E, et al. Awakening a latent carbon fixation cycle in Escherichia coli. Nat Commun. 2020;11(1):5812.
   PubMed Web of Science ®Google Scholar
• Kim SJ, Yoon J, Im DK, et al. A adaptively evolved Escherichia coli for improved ability of formate utilization as a carbon source in sugar-free conditions. Biotechnol Biofuels. 2019;12:207.
   PubMed Web of Science ®Google Scholar
• Tashiro Y, Hirano S, Matson MM, et al. Electrical-biological hybrid system for CO2 reduction. Metab Eng. 2018;47:211–218.
   PubMed Web of Science ®Google Scholar
• Kim S, Lindner SN, Aslan S, et al. Growth of E. coli on formate and methanol via the reductive glycine pathway. Nat Chem Biol. 2020;16(5):538–545.
   PubMed Web of Science ®Google Scholar
• Yishai O, Goldbach L, Tenenboim H, et al. Engineered assimilation of exogenous and endogenous formate in Escherichia coli. ACS Synth Biol. 2017;6(9):1722–1731.
   PubMed Web of Science ®Google Scholar
• Hu G, Li Z, Ma D, et al. Light-driven CO2 sequestration in Escherichia coli to achieve theoretical yield of chemicals. Nat Catal. 2021;4(5):395–406.
   Web of Science ®Google Scholar
• He H, Hoper R, Dodenhoft M, et al. An optimized methanol assimilation pathway relying on promiscuous formaldehyde-condensing aldolases in E. coli. Metab Eng. 2020;60:1–13.
   PubMed Web of Science ®Google Scholar
• Chen F, Jung H, Tsuei CY, et al. Converting Escherichia coli to a synthetic methylotroph growing solely on methanol. Cell. 2020;182(4):933–946.e14.
   PubMed Web of Science ®Google Scholar
• Lu X, Liu Y, Yang Y, et al. Constructing a synthetic pathway for acetyl-coenzyme a from one-carbon through enzyme design. Nat Commun. 2019;10(1):1378.
   PubMedGoogle Scholar
• Yu H, Liao J. A modified serine cycle in Escherichia coli coverts methanol and CO2 to two-carbon compounds. Nat Commun. 2018;9(1):3992.
   PubMedGoogle Scholar
• Mall A, Sobotta J, Huber C, et al. Reversibility of citrate synthase allows autotrophic growth of a thermophilic bacterium. Science. 2018;359(6375):563–567.
   PubMed Web of Science ®Google Scholar
• Lo S, Chiang E, Yang Y, et al. Growth enhancement facilitated by gaseous CO2 through heterologous expression of reductive tricarboxylic acid cycle genes in Escherichia coli. Fermentation. 2021;7(2):98.
   Google Scholar
• Bar-Even A. Formate assimilation: the metabolic architecture of natural and synthetic pathways. Biochemistry. 2016;55(28):3851–3863.
   PubMed Web of Science ®Google Scholar
• Cotton CA, Claassens NJ, Benito-Vaquerizo S, et al. Renewable methanol and formate as microbial feedstocks. Curr Opin Biotechnol. 2020;62:168–180.
   PubMed Web of Science ®Google Scholar
• Chen C, Tseng I, Lo S, et al. Manipulating ATP supply improves in situ CO2 recycling by reductive TCA cycle in engineered Escherichia coli. 3 Biotech. 2020;10(3):125.
   PubMedGoogle Scholar
• Logan BE. Exoelectrogenic bacteria that power microbial fuel cells. Nat Rev Microbiol. 2009;7(5):375–381.
   PubMed Web of Science ®Google Scholar
• Wu Z, Wang J, Zhang X, et al. Engineering an electroactive Escherichia coli for the microbial electrosynthesis of succinate by increasing the intracellular FAD Pool. Biochem. Eng. J. 2019;146:132–142.
   Web of Science ®Google Scholar
• Feng J, Qian Y, Wang Z, et al. Enhancing the performance of Escherichia coli-inoculated microbial fuel cells by introduction of the phenazine-1-carboxylic acid pathway. J Biotechnol. 2018;275:1–6.
   PubMed Web of Science ®Google Scholar
• Kane AL, Brutinel ED, Joo H, et al. Formate metabolism in Shewanella oneidensis generates proton motive force and prevents growth without an electron acceptor. J Bacteriol. 2016;198(8):1337–1346.
   PubMed Web of Science ®Google Scholar
• Logan BE, Rossi R, Ragab A, et al. Electroactive microorganisms in bioelectrochemical systems. Nat Rev Microbiol. 2009;17:307–319.
   Google Scholar
• Saito J, Hashimoto K, Okamoto A. Flavin as an indicator of the rate-limiting factor for microbial current oroduction in Shewanella oneidensis MR-1. Electrochim Acta. 2016;216:261–265.
   Web of Science ®Google Scholar
• Seviour TW, Hinks J. Bucking the current trend in bioelectrochemical systems: a case for bioelectroanalytics. Crit Rev Biotechnol. 2018;38(4):634–646.
   PubMed Web of Science ®Google Scholar
• Von Canstein H, Ogawa J, Shimizu S, et al. Secretion of flavins by Shewanella species and their role in extracellular electron transfer. Appl Environ Microbiol. 2008;74(3):615–623.
   PubMed Web of Science ®Google Scholar
• Min D, Cheng L, Zhang F, et al. Enhancing extracellular electron transfer of Shewanella oneidensis MR-1 through coupling improved flavin synthesis and metal-reducing conduit for pollutant degradation. Environ Sci Technol. 2017;51(9):5082–5089.
   PubMed Web of Science ®Google Scholar
• Abbas CA, Sibirny AAJM, Mmbr MBR. Genetic control of biosynthesis and transport of riboflavin and flavin nucleotides and construction of robust biotechnological producers. Microbiol Mol Biol Rev. 2011;75(2):321–360.
   PubMed Web of Science ®Google Scholar
• Yang Y, Ding Y, Hu Y, et al. Enhancing bidirectional electron transfer of Shewanella oneidensis by a synthetic flavin pathway. ACS Synth Biol. 2015;4(7):815–823.
   PubMed Web of Science ®Google Scholar
• Xiao Y, Zhang E, Zhang J, et al. Extracellular polymeric substances are transient media for microbial extracellular electron transfer. Sci Adv. 2017;3(7):e1700623.
   PubMed Web of Science ®Google Scholar
• Sharma M, Alvarez-Gallego Y, Achouak W, et al. Electrode material properties for designing effective microbial electrosynthesis systems. J Mater Chem A. 2019;7(42):24420–24436.
   Web of Science ®Google Scholar
• Jiang Y, Zeng RJ. Bidirectional extracellular electron transfers of electrode-biofilm: mechanism and application. Bioresour Technol. 2019;271:439–448.
   PubMed Web of Science ®Google Scholar
• Cheng L, Min D, Liu DF, et al. Deteriorated biofilm-forming capacity and electroactivity of shewanella oneidnsis MR-1 induced by insertion sequence (is) elements. Biosens Bioelectron. 2020;156:112136.
   PubMed Web of Science ®Google Scholar
• Liu T, Yu YY, Deng XP, et al. Enhanced Shewanella biofilm promotes bioelectricity generation. Biotechnol Bioeng. 2015;112(10):2051–2059.
   PubMed Web of Science ®Google Scholar
• Suo D, Fang Z, Yu Y, et al. Synthetic curli enables efficient microbial electrocatalysis with stainless‐steel electrode. AIChE J. 2020;66(4):e16897.
   Web of Science ®Google Scholar
• Chen X, Li S, Liu L. Engineering redox balance through cofactor systems. Trends Biotechnol. 2014;32(6):337–343.
   PubMed Web of Science ®Google Scholar
• Li F, Li YX, Cao YX, et al. Modular engineering to increase intracellular NAD(H/(+)) promotes rate of extracellular electron transfer of Shewanella oneidensis. Nat Commun. 2018;9(1):3637.
   PubMedGoogle Scholar
• Cao Y, Li X, Li F, et al. CRISPRi-sRNA: transcriptional-translational regulation of extracellular electron transfer in Shewanella oneidensis. ACS Synth Biol. 2017;6(9):1679–1690.
   PubMed Web of Science ®Google Scholar
• Li J, Tang Q, Li Y, et al. Rediverting electron flux with an engineered CRISPR-ddAsCpf1 system to enhance the pollutant degradation capacity of Shewanella oneidensis. Environ Sci Technol. 2020;54(6):3599–3608.
   PubMed Web of Science ®Google Scholar
• Rollefson JB, Stephen CS, Tien M, et al. Identification of an extracellular polysaccharide network essential for cytochrome anchoring and biofilm formation in Geobacter sulfurreducens. J Bacteriol. 2011;193(5):1023–1033.
   PubMed Web of Science ®Google Scholar
• Tan Y, Adhikari RY, Malvankar NS, et al. Expressing the Geobacter metallireducens PilA in Geobacter sulfurreducens yields pili with exceptional conductivity. mBio. 2017;8(1);e02203-16.
   PubMed Web of Science ®Google Scholar
• Ueki T, Nevin KP, Woodard TL, et al. Construction of a Geobacter strain with exceptional growth on cathodes. Front Microbiol. 2018;9(1512):1512.
   PubMedGoogle Scholar
• Zhang T, Shi XC, Ding R, et al. The hidden chemolithoautotrophic metabolism of Geobacter sulfurreducens uncovered by adaptation to formate. Isme J. 2020;14(8):2078–2089.
   PubMed Web of Science ®Google Scholar
• Jiang X, van Wonderen JH, Butt JN, et al. Which multi-heme protein complex transfers electrons more efficiently? Comparing MtrCAB from Shewanella with OmcS from Geobacter. J Phys Chem Lett. 2020;11(21):9421–9425.
   PubMed Web of Science ®Google Scholar
• Zhang L, Zhao R, Jia D, et al. Engineering Clostridium ljungdahlii as the gas-fermenting cell factory for the production of biofuels and biochemicals. Curr Opin Chem Biol. 2020;59:54–61.
   PubMed Web of Science ®Google Scholar
• Woolston BM, Emerson DF, Currie DH, et al. Rediverting carbon flux in Clostridium ljungdahlii using CRISPR interference (CRISPRi). Metab Eng. 2018;48:243–253.
   PubMed Web of Science ®Google Scholar
• Huang H, Chai C, Yang S, et al. Phage serine integrase-mediated genome engineering for efficient expression of chemical biosynthetic pathway in gas-fermenting Clostridium ljungdahlii. Metab Eng. 2019;52:293–302.
   PubMed Web of Science ®Google Scholar
• Han S, Gao X, Ying H, et al. NADH gene manipulation for advancing bioelectricity in Clostridium ljungdahlii microbial fuel cells. Green Chem. 2016;18(8):2473–2478.
   Web of Science ®Google Scholar
• Shi XC, Tremblay PL, Wan L, et al. Improved robustness of microbial electrosynthesis by adaptation of a strict anaerobic microbial catalyst to molecular oxygen. Sci Total Environ. 2021;754:142440.
   PubMed Web of Science ®Google Scholar
• Chou H, Su H, Chow T, et al. Engineering cyanobacteria with enhanced growth in simulated flue gases for high-yield bioethanol production. Biochem Eng J. 2021;165:107823.
   Web of Science ®Google Scholar
• Ates B, Koytepe S, Ulu A, et al. Chemistry, structures, and advanced applications of nanocomposites from biorenewable resources. Chem Rev. 2020;120(17):9304–9362.
   PubMed Web of Science ®Google Scholar
• Tian S, Wang H, Dong Z, et al. Mo2C-induced hydrogen production enhances microbial electrosynthesis of acetate from CO2 reduction. Biotechnol Biofuels. 2019;12:71.
   PubMed Web of Science ®Google Scholar
• Tahir K, Miran W, Jang J, et al. A novel MXene-coated biocathode for enhanced microbial electrosynthesis performance. Chem Eng J. 2020;381:122687.
   Web of Science ®Google Scholar
• Shakeel S, Anwer AH, Khan MZ. Nitric acid treated graphite granular cathode for microbial electro reduction of carbon dioxide to acetate. J Cleaner Prod. 2020;269:122391.
   Web of Science ®Google Scholar
• Chen L, Tremblay PL, Mohanty S, et al. Electrosynthesis of acetate from CO2 by a highly structured biofilm assembled with reduced graphene oxide–tetraethylene pentamine. J Mater Chem A. 2016;4(21):8395–8401.
   Web of Science ®Google Scholar
• Han S, Liu H, Zhou C, et al. Growth of carbon nanotubes on graphene as 3D biocathode for NAD+/NADH balance model and high-rate production in microbial electrochemical synthesis from CO2. J Mater Chem A. 2019;7(3):1115–1123.
   Web of Science ®Google Scholar
• Cestellos-Blanco S, Zhang H, Kim JM, et al. Photosynthetic semiconductor biohybrids for solar-driven biocatalysis. Nat Catal. 2020;3(3):245–255.
   Web of Science ®Google Scholar
• Kumar M, Sahoo PC, Srikanth S, et al. Photosensitization of electro-active microbes for solar assisted carbon dioxide transformation. Bioresour Technol. 2019;272:300–307.
   PubMed Web of Science ®Google Scholar
• Sakimoto KK, Wong AB, Yang PJS. Self-photosensitization of nonphotosynthetic bacteria for solar-to-chemical production. Science. 2016;351(6268):74–77.
   PubMed Web of Science ®Google Scholar
• Chen X, Feng Q, Cai Q, et al. Mn3O4 nanozyme coating accelerates nitrate reduction and decreases N2O emission during photoelectrotrophic denitrification by thiobacillus denitrificans-CdS. Environ Sci Technol. 2020;54(17):10820–10830.
   PubMed Web of Science ®Google Scholar
• Xiao S, Li Z, Fu Q, et al. Hybrid microbial photoelectrochemical system reduces CO2 to CH4 with 1.28% solar energy conversion efficiency. Chem Eng J. 2020;390:124530.
   Web of Science ®Google Scholar
• Jia Y, Qian D, Chen Y, et al. Intra/extracellular electron transfer for aerobic denitrification mediated by in-situ biosynthesis palladium nanoparticles. Water Res. 2021;189:116612.
   PubMed Web of Science ®Google Scholar
• Zhou S, Tang J, Yuan Y, et al. TiO2 nanoparticle-induced nanowire formation facilitates extracellular electron transfer. Environ Sci Technol Lett. 2018;5(9):564–570.
   Web of Science ®Google Scholar
• Su L, Yin T, Du H, et al. Synergistic improvement of Shewanella loihica PV-4 extracellular electron transfer using a TiO2@TiN nanocomposite. Bioelectrochemistry. 2020;134:107519.
   PubMed Web of Science ®Google Scholar
• Gildemyn S, Verbeeck K, Jansen R, et al. The type of ion selective membrane determines stability and production levels of microbial electrosynthesis. Bioresour Technol. 2017;224:358–364.
   PubMed Web of Science ®Google Scholar
• Xiang Y, Liu G, Zhang R, et al. High-efficient acetate production from carbon dioxide using a bioanode microbial electrosynthesis system with bipolar membrane. Bioresour Technol. 2017;233:227–235.
   PubMed Web of Science ®Google Scholar
• Matemadombo F, Puig S, Ganigué R, et al. Modelling the simultaneous production and separation of acetic acid from CO2 using an anion exchange membrane microbial electrosynthesis system. J Chem Technol Biotechnol. 2017;92(6):1211–1217.
   Web of Science ®Google Scholar
• Kumar P, Chandrasekhar K, Kumari A, et al. Electro-fermentation in aid of bioenergy and biopolymers. Energies. 2018;11(2):343.
   Web of Science ®Google Scholar
• Virdis B, D Hoelzle R, Marchetti A, et al. Electro-fermentation: sustainable bioproductions steered by electricity. Biotechnol Adv. 2022;59:107950.
   PubMed Web of Science ®Google Scholar