生物工程强化微生物电合成转化CO_2的研究进展
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摘要
微生物电合成(Microbial electrosynthesis,MES)可直接利用电能驱动微生物还原固定CO_2合成多碳化合物,为可再生新能源转化、精细化学品制备和生态环境保护提供新机遇。但是,微生物吸收胞外电极电子速率慢、产物合成效率低和产品品位不高,限制了MES实现工业化应用。在概述阴极电活性微生物吸收胞外电子的分子机制的基础上,重点综述近5年应用生物工程的理论和技术强化MES用于CO_2转化的策略与研究进展,包括改造和调控胞外电子传递通路和胞内代谢途径以及定向构建有限微生物混合培养菌群三方面,阐明了生物工程可有效突破MES中电子传递慢和可用代谢途径相对单一等瓶颈。针对目前生物工程在改进MES所面临的主要问题,从胞外电子传递机理研究、基因工具箱开发、组学技术与现代分析技术联用等角度展望了今后的研究方向。
Microbial electrosynthesis(MES) is able to produce polycarbon chemicals through electricity-driven reduction of CO_2 using electroactive microorganisms as biocatalysts, providing great potential for renewable energy conversion, fine chemical engineering and ecological environmental protection. However, the sluggish extracellular electron uptake rate between microorganisms and the electrode, the low productivity and value of products impede the industrial application of MES technology. After brief overview of molecular mechanism of extracellular electron transfer(EET) in cathodic electroactive microorganisms, the application strategy and progress of bioengineering in boosting MES for CO_2 conversion in recent five years, including transforming and regulating extracellular electron transfer(EET) route and intracellular metabolic pathway and constructing defined mixed culture, are reviewed comprehensively, thus expounding the commendable availability of biological engineering in breaking the bottleneck(such as low electron transport rate and few usable metabolic pathway) involved in MES. Finally, according to the present existing problems that limit the efficiency of bioengineering in improving MES, future research directions are discussed from the perspectives of exploring EET mechanism, developing genetic tools and coupling omics-techniques with advanced analysis-techniques.
Microbial electrosynthesis(MES) is able to produce polycarbon chemicals through electricity-driven reduction of CO_2 using electroactive microorganisms as biocatalysts, providing great potential for renewable energy conversion, fine chemical engineering and ecological environmental protection. However, the sluggish extracellular electron uptake rate between microorganisms and the electrode, the low productivity and value of products impede the industrial application of MES technology. After brief overview of molecular mechanism of extracellular electron transfer(EET) in cathodic electroactive microorganisms, the application strategy and progress of bioengineering in boosting MES for CO_2 conversion in recent five years, including transforming and regulating extracellular electron transfer(EET) route and intracellular metabolic pathway and constructing defined mixed culture, are reviewed comprehensively, thus expounding the commendable availability of biological engineering in breaking the bottleneck(such as low electron transport rate and few usable metabolic pathway) involved in MES. Finally, according to the present existing problems that limit the efficiency of bioengineering in improving MES, future research directions are discussed from the perspectives of exploring EET mechanism, developing genetic tools and coupling omics-techniques with advanced analysis-techniques.
引文
[1] Logan BE,Rabaey K.Conversion of wastes into bioelectricity and chemicals by using microbial electrochemical Ttechnologies[J].Science,2012,337(6095):686-690.
[2] Kumar A,Hsu LH-H,Kavanagh P,et al.The ins and outs of microorganism-electrode electron transfer reactions[J].Nature Reviews Chemistry,2017,1(3):0024.
[3] Santoro C,Arbizzani C,Erable B,et al.Microbial fuel cells:From fundamentals to applications.A review[J].Journal of Power Sources,2017,356:225-244.
[4] Zou L,Lu Z,Huang Y,et al.Nanoporous Mo2C functionalized 3D carbon architecture anode for boosting flavins mediated interfacial bioelectrocatalysis in microbial fuel cells[J].Journal of Power Sources,2017,359:549-555.
[5] Wu X,Zou L,Huang Y,et al.Shewanella putrefaciens CN32 outer membrane cytochromes MtrC and UndA reduce electron shuttles to produce electricity in microbial fuel cells[J].Enzyme and Microbial Technology,2018,115:23-28.
[6] Jafary T,Daud WRW,Ghasemi M,et al.Biocathode in microbial electrolysis cell;present status and future prospects[J].Renewable and Sustainable Energy Reviews,2015,47:23-33.
[7] Rabaey K,Rozendal RA.Microbial electrosynthesis-revisiting the electrical route for microbial production[J].Nature Reviews Microbiology,2010,8(10):706-716.
[8] Shin HJ,Jung KA,Nam CW,et al.A genetic approach for microbial electrosynthesis system as biocommodities production platform[J].Bioresource Technology,2017,245:1421-1429.
[9] 朱华伟,张延平,李寅.微生物电合成-电能驱动的CO2固定[J].中国科学:生命科学,2016,46(12):1388-1399.
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[12] 张尧,张闻杰,蒋永,等.生物电化学系统固定二氧化碳同时产生乙酸和丁酸[J].应用与环境生物学报,2014,20(2):174-178.
[13] Liu C,Colón BC,Ziesack M,et al.Water splitting-biosynthetic system with CO2 reduction efficiencies exceeding photosynthesis[J].Science,2016,352(6290):1210-1213.
[14] Schiel-Bengelsdorf B,Duerre P.Pathway engineering and synthetic biology using acetogens[J].FEBS Letters,2012,586(15):2191-2198.
[15] Tremblay P-L,Zhang T.Electrifying microbes for the production of chemicals[J].Frontiers in Microbiology,2015,6:201.
[16] Ragsdale SW,Pierce E.Acetogenesis and the Wood-Ljungdahl pathway of CO2 fixation[J].Biochimica et Biophysica Acta,2008,1784(12):1873-1898.
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[18] Cui M,Nie H,Zhang T,et al.Three-dimensional hierarchical metal oxide-carbon electrode materials for highly efficient microbial electrosynthesis[J].Sustainable Energy & Fuels,2017,1(5):1171-1176.
[19] Zou S,He Z.Efficiently "pumping out" value-added resources from wastewater by bioelectrochemical systems:A review from energy perspectives[J].Water Research,2018,131:62-73.
[20] Christodoulou X,Velasquez-Orta SB.Microbial electrosynthesis and anaerobic fermentation:an economic evaluation for acetic acid production from CO2 and CO[J].Environmental Science & Technology,2016,50(20):11234-11242.
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[22] Okkyoung C,Youngsoon U,Byoung-In S.Butyrate production enhancement by Clostridium tyrobutyricum using electron mediators and a cathodic electron donor[J].Biotechnology and Bioengineering,2012,109(10):2494-2502.
[23] Im CH,Kim C,Song YE,et al.Electrochemically enhanced microbial CO conversion to volatile fatty acids using neutral red as an electron mediator[J].Chemosphere,2018,191:166-173.
[24] Harrington TD,Tran VN,Mohamed A,et al.The mechanism of neutral red-mediated microbial electrosynthesis in Escherichia coli:menaquinone reduction[J].Bioresource Technology,2015,192:689-695.
[25] Tremblay P-L,Angenent LT,Zhang T.Extracellular electron uptake:among autotrophs and mediated by surfaces[J].Trends in Biotechnology,2017,35(4):360-371.
[26] Blanchet E,Duquenne F,Rafrafi Y,et al.Importance of the hydrogen route in up-scaling electrosynthesis for microbial CO2 reduction[J].Energy & Environmental Science,2015,8(12):3731-3744.
[27] Jourdin L,Lu Y,Flexer V,et al.Biologically induced hydrogen production drives high rate/high efficiency microbial electrosynthesis of acetate from carbon dioxide[J].ChemElectroChem,2016,3(4):581-591.
[28] Puig S,Ganigué R,Batlle-Vilanova P,et al.Tracking bio-hydrogen-mediated production of commodity chemicals from carbon dioxide and renewable electricity[J].Bioresource Technology,2017,228:201-209.
[29] Dennis PG,Harnisch F,Yeoh YK,et al.Dynamics of cathode-associated microbial communities and metabolite profiles in a glycerol-fed bioelectrochemical system[J].Applied and Environmental Microbiology,2013,79(13):4008-4014.
[30] Deutzmann JS,Sahin M,Spormann AM.Extracellular enzymes facilitate electron uptake in biocorrosion and bioelectrosynthesis[J].mBio,2015,6(2):e00496-15.
[31] Strycharz SM,Glaven RH,Coppi MV,et al.Gene expression and deletion analysis of mechanisms for electron transfer from electrodes to Geobacter sulfurreducens[J].Bioelectrochemistry,2011,80(2):142-150.
[32] Ross DE,Flynn JM,Baron DB,et al.Towards electrosynthesis in Shewanella:energetics of reversing the Mtr pathway for reductive metabolism[J].PloS One,2011,6(2):e16649.
[33] Mohanakrishna G,Seelam JS,Vanbroekhoven K,et al.An enriched electroactive homoacetogenic biocathode for the microbial electrosynthesis of acetate through carbon dioxide reduction[J].Faraday Discussions,2015,183:445-462.
[34] Cheng S,Xing D,Call DF,et al.Direct biological conversion of electrical current into methane by electromethanogenesis[J].Environmental Science & Technology,2009,43(10):3953-3958.
[35] Malvankar NS,Lovley DR.Microbial nanowires:a new paradigm for biological electron transfer and bioelectronics[J].ChemSusChem,2012,5(6):1039-1046.
[36] Torres CI,Marcus AK,Lee HS,et al.A kinetic perspective on extracellular electron transfer by anode-respiring bacteria[J].FEMS Microbiology Reviews,2010,34(1):3-17.
[37] 李锋,宋浩.微生物胞外电子传递效率的合成生物学强化[J].生物工程学报,2017,33(03):516-534.
[38] Yong XY,Shi DY,Chen YL,et al.Enhancement of bioelectricity generation by manipulation of the electron shuttles synthesis pathway in microbial fuel cells[J].Bioresource Technology,2014,152:220-224.
[39] Yang Y,Ding Y,Hu Y,et al.Enhancing bidirectional electron transfer of Shewanella oneidensis by a synthetic flavin pathway[J].ACS Synthetic Biology,2015,4(7):815-823.
[40] 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[J].Environmental Science & Technology,2017,51(9):5082-5089.
[41] Yong XY,Feng J,Chen YL,et al.Enhancement of bioelectricity generation by cofactor manipulation in microbial fuel cell[J].Biosensors & Bioelectronics,2014,56:19-25.
[42] Tao L,Xie M,Chiew GGY,et al.Improving electron trans-inner membrane movements in microbial electrocatalysts[J].Chemical Communications,2016,52(37):6292-6295.
[43] Jensen HM,Albers AE,Malley KR,et al.Engineering of a synthetic electron conduit in living cells[J].Proceedings of the National Academy of Sciences of the United States of America,2010,107(45):19213-19218.
[44] 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[J].ACS Synthetic Biology,2016,5(7):679-688.
[45] Teravest MA,Zajdel TJ,Ajo-Franklin CM.The Mtr pathway of Shewanella oneidensis MR-1 couples substrate utilization to current production in Escherichia coli[J].ChemElectroChem,2014,1(11):1874-1879.
[46] Jeon JM,Park H,Seo HM,et al.Isobutanol production from an engineered Shewanella oneidensis MR-1[J].Bioprocess and Biosystems Engineering,2015,38(11):2147-2154.
[47] Koepke M,Held C,Hujer S,et al.Clostridium ljungdahlii represents a microbial production platform based on syngas[J].Proceedings of the National Academy of Sciences of the United States of America,2010,107(29):13087-13092.
[48] Banerjee A,Leang C,Ueki T,et al.Lactose-inducible system for metabolic engineering of Clostridium ljungdahlii[J].Applied and Environmental Microbiology,2014,80(8):2410-2416.
[49] Ueki T,Nevin KP,Woodard TL,et al.Converting carbon dioxide to butyrate with an engineered strain of Clostridium ljungdahlii[J].mBio,2014,5(5):e01636-14.
[50] Grousseau E,Lu J,Gorret N,et al.Isopropanol production with engineered Cupriavidus necator as bioproduction platform[J].Applied Microbiology and Biotechnology,2014,98(9):4277-4290.
[51] Li H,Opgenorth PH,Wernick DG,et al.Integrated electromicrobial conversion of CO2 to higher alcohols[J].Science,2012,335(6076):1596-1596.
[52] Torella JP,Gagliardi CJ,Chen JS,et al.Efficient solar-to-fuels production from a hybrid microbial-water-splitting catalyst system[J].Proceedings of the National Academy of Sciences of the United States of America,2015,112(8):2337-2342.
[53] Krieg T,Sydow A,Faust S,et al.CO2 to terpenes:autotrophic and electroautotrophic α-humulene production with Cupriavidus necator[J].Angewandte Chemie International Edition,2018,57(7):1879-1882.
[54] Marshall CW,Ross DE,Handley KM,et al.Metabolic reconstruction and modeling microbial electrosynthesis[J].Scientific Reports,2017,7(1):8391.
[55] Deutzmann JS,Spormann AM.Enhanced microbial electrosynthesis by using defined co-cultures[J].ISME Journal,2017,11(3):704-714.
[56] Xiang Y,Liu G,Zhang R,et al.Acetate production and electron utilization facilitated by sulfate-reducing bacteria in a microbial electrosynthesis system[J].Bioresource Technology,2017,241:821-829.
[2] Kumar A,Hsu LH-H,Kavanagh P,et al.The ins and outs of microorganism-electrode electron transfer reactions[J].Nature Reviews Chemistry,2017,1(3):0024.
[3] Santoro C,Arbizzani C,Erable B,et al.Microbial fuel cells:From fundamentals to applications.A review[J].Journal of Power Sources,2017,356:225-244.
[4] Zou L,Lu Z,Huang Y,et al.Nanoporous Mo2C functionalized 3D carbon architecture anode for boosting flavins mediated interfacial bioelectrocatalysis in microbial fuel cells[J].Journal of Power Sources,2017,359:549-555.
[5] Wu X,Zou L,Huang Y,et al.Shewanella putrefaciens CN32 outer membrane cytochromes MtrC and UndA reduce electron shuttles to produce electricity in microbial fuel cells[J].Enzyme and Microbial Technology,2018,115:23-28.
[6] Jafary T,Daud WRW,Ghasemi M,et al.Biocathode in microbial electrolysis cell;present status and future prospects[J].Renewable and Sustainable Energy Reviews,2015,47:23-33.
[7] Rabaey K,Rozendal RA.Microbial electrosynthesis-revisiting the electrical route for microbial production[J].Nature Reviews Microbiology,2010,8(10):706-716.
[8] Shin HJ,Jung KA,Nam CW,et al.A genetic approach for microbial electrosynthesis system as biocommodities production platform[J].Bioresource Technology,2017,245:1421-1429.
[9] 朱华伟,张延平,李寅.微生物电合成-电能驱动的CO2固定[J].中国科学:生命科学,2016,46(12):1388-1399.
[10] Nevin KP,Woodard TL,Franks AE,et al.Microbial electrosynthesis:feeding microbes electricity to convert carbon dioxide and water to multicarbon extracellular organic compounds[J].mBio,2010,1(2):e00103-10.
[11] Nevin KP,Hensley SA,Franks AE,et al.Electrosynthesis of organic compounds from carbon dioxide is catalyzed by a diversity of acetogenic microorganisms[J].Applied and Environmental Microbiology,2011,77(9):2882-2886.
[12] 张尧,张闻杰,蒋永,等.生物电化学系统固定二氧化碳同时产生乙酸和丁酸[J].应用与环境生物学报,2014,20(2):174-178.
[13] Liu C,Colón BC,Ziesack M,et al.Water splitting-biosynthetic system with CO2 reduction efficiencies exceeding photosynthesis[J].Science,2016,352(6290):1210-1213.
[14] Schiel-Bengelsdorf B,Duerre P.Pathway engineering and synthetic biology using acetogens[J].FEBS Letters,2012,586(15):2191-2198.
[15] Tremblay P-L,Zhang T.Electrifying microbes for the production of chemicals[J].Frontiers in Microbiology,2015,6:201.
[16] Ragsdale SW,Pierce E.Acetogenesis and the Wood-Ljungdahl pathway of CO2 fixation[J].Biochimica et Biophysica Acta,2008,1784(12):1873-1898.
[17] Zaybak Z,Pisciotta JM,Tokash JC,et al.Enhanced start-up of anaerobic facultatively autotrophic biocathodes in bioelectrochemical systems[J].Journal of Biotechnology,2013,168(4):478-485.
[18] Cui M,Nie H,Zhang T,et al.Three-dimensional hierarchical metal oxide-carbon electrode materials for highly efficient microbial electrosynthesis[J].Sustainable Energy & Fuels,2017,1(5):1171-1176.
[19] Zou S,He Z.Efficiently "pumping out" value-added resources from wastewater by bioelectrochemical systems:A review from energy perspectives[J].Water Research,2018,131:62-73.
[20] Christodoulou X,Velasquez-Orta SB.Microbial electrosynthesis and anaerobic fermentation:an economic evaluation for acetic acid production from CO2 and CO[J].Environmental Science & Technology,2016,50(20):11234-11242.
[21] 靖宪月,陈姗姗,周顺桂.吸收胞外电子的电活性微生物[J].微生物学报,2018,58(01):19-27.
[22] Okkyoung C,Youngsoon U,Byoung-In S.Butyrate production enhancement by Clostridium tyrobutyricum using electron mediators and a cathodic electron donor[J].Biotechnology and Bioengineering,2012,109(10):2494-2502.
[23] Im CH,Kim C,Song YE,et al.Electrochemically enhanced microbial CO conversion to volatile fatty acids using neutral red as an electron mediator[J].Chemosphere,2018,191:166-173.
[24] Harrington TD,Tran VN,Mohamed A,et al.The mechanism of neutral red-mediated microbial electrosynthesis in Escherichia coli:menaquinone reduction[J].Bioresource Technology,2015,192:689-695.
[25] Tremblay P-L,Angenent LT,Zhang T.Extracellular electron uptake:among autotrophs and mediated by surfaces[J].Trends in Biotechnology,2017,35(4):360-371.
[26] Blanchet E,Duquenne F,Rafrafi Y,et al.Importance of the hydrogen route in up-scaling electrosynthesis for microbial CO2 reduction[J].Energy & Environmental Science,2015,8(12):3731-3744.
[27] Jourdin L,Lu Y,Flexer V,et al.Biologically induced hydrogen production drives high rate/high efficiency microbial electrosynthesis of acetate from carbon dioxide[J].ChemElectroChem,2016,3(4):581-591.
[28] Puig S,Ganigué R,Batlle-Vilanova P,et al.Tracking bio-hydrogen-mediated production of commodity chemicals from carbon dioxide and renewable electricity[J].Bioresource Technology,2017,228:201-209.
[29] Dennis PG,Harnisch F,Yeoh YK,et al.Dynamics of cathode-associated microbial communities and metabolite profiles in a glycerol-fed bioelectrochemical system[J].Applied and Environmental Microbiology,2013,79(13):4008-4014.
[30] Deutzmann JS,Sahin M,Spormann AM.Extracellular enzymes facilitate electron uptake in biocorrosion and bioelectrosynthesis[J].mBio,2015,6(2):e00496-15.
[31] Strycharz SM,Glaven RH,Coppi MV,et al.Gene expression and deletion analysis of mechanisms for electron transfer from electrodes to Geobacter sulfurreducens[J].Bioelectrochemistry,2011,80(2):142-150.
[32] Ross DE,Flynn JM,Baron DB,et al.Towards electrosynthesis in Shewanella:energetics of reversing the Mtr pathway for reductive metabolism[J].PloS One,2011,6(2):e16649.
[33] Mohanakrishna G,Seelam JS,Vanbroekhoven K,et al.An enriched electroactive homoacetogenic biocathode for the microbial electrosynthesis of acetate through carbon dioxide reduction[J].Faraday Discussions,2015,183:445-462.
[34] Cheng S,Xing D,Call DF,et al.Direct biological conversion of electrical current into methane by electromethanogenesis[J].Environmental Science & Technology,2009,43(10):3953-3958.
[35] Malvankar NS,Lovley DR.Microbial nanowires:a new paradigm for biological electron transfer and bioelectronics[J].ChemSusChem,2012,5(6):1039-1046.
[36] Torres CI,Marcus AK,Lee HS,et al.A kinetic perspective on extracellular electron transfer by anode-respiring bacteria[J].FEMS Microbiology Reviews,2010,34(1):3-17.
[37] 李锋,宋浩.微生物胞外电子传递效率的合成生物学强化[J].生物工程学报,2017,33(03):516-534.
[38] Yong XY,Shi DY,Chen YL,et al.Enhancement of bioelectricity generation by manipulation of the electron shuttles synthesis pathway in microbial fuel cells[J].Bioresource Technology,2014,152:220-224.
[39] Yang Y,Ding Y,Hu Y,et al.Enhancing bidirectional electron transfer of Shewanella oneidensis by a synthetic flavin pathway[J].ACS Synthetic Biology,2015,4(7):815-823.
[40] 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[J].Environmental Science & Technology,2017,51(9):5082-5089.
[41] Yong XY,Feng J,Chen YL,et al.Enhancement of bioelectricity generation by cofactor manipulation in microbial fuel cell[J].Biosensors & Bioelectronics,2014,56:19-25.
[42] Tao L,Xie M,Chiew GGY,et al.Improving electron trans-inner membrane movements in microbial electrocatalysts[J].Chemical Communications,2016,52(37):6292-6295.
[43] Jensen HM,Albers AE,Malley KR,et al.Engineering of a synthetic electron conduit in living cells[J].Proceedings of the National Academy of Sciences of the United States of America,2010,107(45):19213-19218.
[44] 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[J].ACS Synthetic Biology,2016,5(7):679-688.
[45] Teravest MA,Zajdel TJ,Ajo-Franklin CM.The Mtr pathway of Shewanella oneidensis MR-1 couples substrate utilization to current production in Escherichia coli[J].ChemElectroChem,2014,1(11):1874-1879.
[46] Jeon JM,Park H,Seo HM,et al.Isobutanol production from an engineered Shewanella oneidensis MR-1[J].Bioprocess and Biosystems Engineering,2015,38(11):2147-2154.
[47] Koepke M,Held C,Hujer S,et al.Clostridium ljungdahlii represents a microbial production platform based on syngas[J].Proceedings of the National Academy of Sciences of the United States of America,2010,107(29):13087-13092.
[48] Banerjee A,Leang C,Ueki T,et al.Lactose-inducible system for metabolic engineering of Clostridium ljungdahlii[J].Applied and Environmental Microbiology,2014,80(8):2410-2416.
[49] Ueki T,Nevin KP,Woodard TL,et al.Converting carbon dioxide to butyrate with an engineered strain of Clostridium ljungdahlii[J].mBio,2014,5(5):e01636-14.
[50] Grousseau E,Lu J,Gorret N,et al.Isopropanol production with engineered Cupriavidus necator as bioproduction platform[J].Applied Microbiology and Biotechnology,2014,98(9):4277-4290.
[51] Li H,Opgenorth PH,Wernick DG,et al.Integrated electromicrobial conversion of CO2 to higher alcohols[J].Science,2012,335(6076):1596-1596.
[52] Torella JP,Gagliardi CJ,Chen JS,et al.Efficient solar-to-fuels production from a hybrid microbial-water-splitting catalyst system[J].Proceedings of the National Academy of Sciences of the United States of America,2015,112(8):2337-2342.
[53] Krieg T,Sydow A,Faust S,et al.CO2 to terpenes:autotrophic and electroautotrophic α-humulene production with Cupriavidus necator[J].Angewandte Chemie International Edition,2018,57(7):1879-1882.
[54] Marshall CW,Ross DE,Handley KM,et al.Metabolic reconstruction and modeling microbial electrosynthesis[J].Scientific Reports,2017,7(1):8391.
[55] Deutzmann JS,Spormann AM.Enhanced microbial electrosynthesis by using defined co-cultures[J].ISME Journal,2017,11(3):704-714.
[56] Xiang Y,Liu G,Zhang R,et al.Acetate production and electron utilization facilitated by sulfate-reducing bacteria in a microbial electrosynthesis system[J].Bioresource Technology,2017,241:821-829.