Carbon dioxide and organic waste valorization by microbial electrosynthesis and electro-fermentation.

Carbon-rich waste materials (solid, liquid, or gaseous) are largely considered to be a burden on society due to the large capital and energy costs for their treatment and disposal. However, solid and liquid organic wastes have inherent energy and value, and similar as waste CO2 gas they can be reused to produce value-added chemicals and materials. There has been a paradigm shift towards developing a closed loop, biorefinery approach for the valorization of these wastes into value-added products, and such an approach enables a more carbon-efficient and circular economy. This review quantitatively analyzes the state-of-the-art of the emerging microbial electrochemical technology (MET) platform and provides critical perspectives on research advancement and technology development. The review offers side-by-side comparison between microbial electrosynthesis (MES) and electro-fermentation (EF) processes in terms of principles, key performance metrics, data analysis, and microorganisms. The study also summarizes all the processes and products that have been developed using MES and EF to date for organic waste and CO2 valorization. It finally identifies the technological and economic potentials and challenges on future system development.

[1]  S. K. Brar,et al.  Enhancement of biobutanol production by electromicrobial glucose conversion in a dual chamber fermentation cell using C. pasteurianum. , 2016 .

[2]  Valeria Mapelli,et al.  Enhancement of anaerobic lysine production in Corynebacterium glutamicum electrofermentations. , 2017, Bioelectrochemistry.

[3]  S. Papanikolaou,et al.  Valorization of industrial waste and by-product streams via fermentation for the production of chemicals and biopolymers. , 2014, Chemical Society reviews.

[4]  Janaka N. Edirisinghe,et al.  Metabolic Reconstruction and Modeling Microbial Electrosynthesis , 2016, bioRxiv.

[5]  Hubertus V. M. Hamelers,et al.  Bioelectrochemical Production of Caproate and Caprylate from Acetate by Mixed Cultures , 2013 .

[6]  S. Puig,et al.  Bio-electrorecycling of carbon dioxide into bioplastics , 2018 .

[7]  Nicolas Bernet,et al.  Electro-Fermentation: How To Drive Fermentation Using Electrochemical Systems. , 2016, Trends in biotechnology.

[8]  C. Santoro,et al.  Microbial fuel cells: From fundamentals to applications. A review , 2017, Journal of power sources.

[9]  Tian Zhang,et al.  Extracellular Electron Uptake: Among Autotrophs and Mediated by Surfaces. , 2017, Trends in biotechnology.

[10]  D. Pant,et al.  Dual‐Function Electrocatalytic and Macroporous Hollow‐Fiber Cathode for Converting Waste Streams to Valuable Resources Using Microbial Electrochemical Systems , 2018, Advanced materials.

[11]  Yong Jiang,et al.  Bioelectrochemical systems for simultaneously production of methane and acetate from carbon dioxide at relatively high rate , 2013 .

[12]  Heming Wang,et al.  A comprehensive review of microbial electrochemical systems as a platform technology. , 2013, Biotechnology advances.

[13]  A. Estéve-Núñez,et al.  Geobacter Dominates the Inner Layers of a Stratified Biofilm on a Fluidized Anode During Brewery Wastewater Treatment , 2018, Front. Microbiol..

[14]  R. Sheldon.  Green and sustainable manufacture of chemicals from biomass: state of the art , 2014 .

[15]  Xing Xie,et al.  Design and fabrication of bioelectrodes for microbial bioelectrochemical systems , 2015 .

[16]  O. Choi,et al.  Butyrate production enhancement by Clostridium tyrobutyricum using electron mediators and a cathodic electron donor , 2012, Biotechnology and bioengineering.

[17]  Sylvia Gildemyn,et al.  Interfacing anaerobic digestion with (bio)electrochemical systems: Potentials and challenges. , 2018, Water research.

[18]  Lisa H. Orfe,et al.  The mechanism of neutral red-mediated microbial electrosynthesis in Escherichia coli: menaquinone reduction. , 2015, Bioresource technology.

[19]  Booki Min,et al.  Bioelectrochemical reduction of volatile fatty acids in anaerobic digestion effluent for the production of biofuels. , 2015, Water research.

[20]  Xia Huang,et al.  Microbial electrochemical nutrient recovery in anaerobic osmotic membrane bioreactors. , 2017, Water research.

[21]  R. Zeng,et al.  Bidirectional extracellular electron transfers of electrode-biofilm: Mechanism and application. , 2019, Bioresource technology.

[22]  Sven Kerzenmacher,et al.  Unbalanced fermentation of glycerol in Escherichia coli via heterologous production of an electron transport chain and electrode interaction in microbial electrochemical cells. , 2015, Bioresource technology.

[23]  Rashmi Saini,et al.  CO₂ utilizing microbes--a comprehensive review. , 2011, Biotechnology advances.

[24]  D. Pant,et al.  An overview of cathode materials for microbial electrosynthesis of chemicals from carbon dioxide , 2017 .

[25]  Dirk Holtmann,et al.  CO2 to Terpenes: Autotrophic and Electroautotrophic α-Humulene Production with Cupriavidus necator. , 2018, Angewandte Chemie.

[26]  Y. Rafrafi,et al.  Importance of the hydrogen route in up-scaling electrosynthesis for microbial CO2 reduction , 2015 .

[27]  Yong Jiang,et al.  Expanding the product spectrum of value added chemicals in microbial electrosynthesis through integrated process design-A review. , 2018, Bioresource technology.

[28]  Kwang Myung Cho,et al.  Integrated Electromicrobial Conversion of CO2 to Higher Alcohols , 2012, Science.

[29]  A. Spormann,et al.  Hydrogenase-independent uptake and metabolism of electrons by the archaeon Methanococcus maripaludis , 2014, The ISME Journal.

[30]  M. Zaiat,et al.  Effect of the electric supply interruption on a microbial electrosynthesis system converting inorganic carbon into acetate. , 2018, Bioresource technology.

[31]  Liviu Mihai Dumitru,et al.  Bio‐Electrocatalytic Application of Microorganisms for Carbon Dioxide Reduction to Methane , 2016, ChemSusChem.

[32]  K. Rabaey,et al.  Membrane Electrolysis Assisted Gas Fermentation for Enhanced Acetic Acid Production , 2018, Front. Energy Res..

[33]  S. Freguia,et al.  Development of bioelectrocatalytic activity stimulates mixed-culture reduction of glycerol in a bioelectrochemical system , 2015, Microbial biotechnology.

[34]  Irini Angelidaki,et al.  Simultaneous biogas upgrading and biochemicals production using anaerobic bacterial mixed cultures. , 2018, Water research.

[35]  Shungui Zhou,et al.  Thermophilic Moorella thermoautotrophica-immobilized cathode enhanced microbial electrosynthesis of acetate and formate from CO2. , 2017, Bioelectrochemistry.

[36]  Mauro Majone,et al.  Bioelectrochemical reduction of CO(2) to CH(4) via direct and indirect extracellular electron transfer by a hydrogenophilic methanogenic culture. , 2010, Bioresource technology.

[37]  Frederik Golitsch,et al.  Electrode-assisted acetoin production in a metabolically engineered Escherichia coli strain , 2017, Biotechnology for Biofuels.

[38]  P. Liang,et al.  Electrochemical Control of Redox Potential Arrests Methanogenesis and Regulates Products in Mixed Culture Electro-Fermentation , 2018, ACS Sustainable Chemistry & Engineering.

[39]  Kazuya Watanabe,et al.  Electrochemically active bacteria sense electrode potentials for regulating catabolic pathways , 2018, Nature Communications.

[40]  Danielle A. Salvatore,et al.  Electrolytic CO2 Reduction in a Flow Cell. , 2018, Accounts of chemical research.

[41]  C. Buisman,et al.  Continuous Long‐Term Bioelectrochemical Chain Elongation to Butyrate , 2017 .

[42]  C. Buisman,et al.  In situ acetate separation in microbial electrosynthesis from CO2 using ion-exchange resin , 2017 .

[43]  Pier-Luc Tremblay,et al.  Production of long chain alkyl esters from carbon dioxide and electricity by a two-stage bacterial process. , 2017, Bioresource technology.

[44]  Deepak Pant,et al.  Recent advances in the use of different substrates in microbial fuel cells toward wastewater treatment and simultaneous energy recovery , 2016 .

[45]  B. Rittmann,et al.  Changes in Glucose Fermentation Pathways as a Response to the Free Ammonia Concentration in Microbial Electrolysis Cells. , 2017, Environmental science & technology.

[46]  K. Mayrhofer,et al.  Selective microbial electrosynthesis of methane by a pure culture of a marine lithoautotrophic archaeon. , 2015, Bioelectrochemistry.

[47]  Bruce E Logan,et al.  Enhanced start-up of anaerobic facultatively autotrophic biocathodes in bioelectrochemical systems. , 2013, Journal of biotechnology.

[48]  Andrea Schievano,et al.  Electro-Fermentation - Merging Electrochemistry with Fermentation in Industrial Applications. , 2016, Trends in biotechnology.

[49]  Christoph Wittmann,et al.  Anodic electro‐fermentation: Anaerobic production of L‐Lysine by recombinant Corynebacterium glutamicum , 2018, Biotechnology and bioengineering.

[50]  Korneel Rabaey,et al.  Carbon and electron fluxes during the electricity driven 1,3-propanediol biosynthesis from glycerol. , 2013, Environmental science & technology.

[51]  K. Rabaey,et al.  Continuous long-term electricity-driven bioproduction of carboxylates and isopropanol from CO2 with a mixed microbial community , 2017 .

[52]  S. Srikanth,et al.  Microaerophilic microenvironment at biocathode enhances electrogenesis with simultaneous synthesis of polyhydroxyalkanoates (PHA) in bioelectrochemical system (BES). , 2012, Bioresource technology.

[53]  Derek R. Lovley,et al.  Microbial Electrosynthesis: Feeding Microbes Electricity To Convert Carbon Dioxide and Water to Multicarbon Extracellular Organic Compounds , 2010, mBio.

[54]  W. Bentley,et al.  Electronic control of gene expression and cell behaviour in Escherichia coli through redox signalling , 2017, Nature Communications.

[55]  Derek R Lovley,et al.  A shift in the current: new applications and concepts for microbe-electrode electron exchange. , 2011, Current opinion in biotechnology.

[56]  Jeffrey A. Gralnick,et al.  Enabling Unbalanced Fermentations by Using Engineered Electrode-Interfaced Bacteria , 2010, mBio.

[57]  Gordon G Wallace,et al.  High Acetic Acid Production Rate Obtained by Microbial Electrosynthesis from Carbon Dioxide. , 2015, Environmental science & technology.

[58]  W. D. de Vos,et al.  Harnessing the power of microbial autotrophy , 2016, Nature Reviews Microbiology.

[59]  P. Westermann,et al.  Microbial Production of Short Chain Fatty Acids from Lignocellulosic Biomass: Current Processes and Market , 2016, BioMed research international.

[60]  Fan Lü,et al.  Exploit Carbon Materials to Accelerate Initiation and Enhance Process Stability of CO Anaerobic Open-Culture Fermentation , 2018 .

[61]  P. He,et al.  Significant enhancement by biochar of caproate production via chain elongation. , 2017, Water research.

[62]  Hao Song,et al.  Enzyme-Assisted Microbial Electrosynthesis of Poly(3-hydroxybutyrate) via CO2 Bioreduction by Engineered Ralstonia eutropha , 2018 .

[63]  Hubertus V. M. Hamelers,et al.  Bioelectrochemical ethanol production through mediated acetate reduction by mixed cultures. , 2010, Environmental science & technology.

[64]  Valeria Mapelli,et al.  Electrochemical startup increases 1,3-propanediol titers in mixed-culture glycerol fermentations , 2015 .

[65]  G. Reguera,et al.  Stimulation of electro-fermentation in single-chamber microbial electrolysis cells driven by genetically engineered anode biofilms , 2017 .

[66]  Cees Buisman,et al.  Bioelectrochemical Power-to-Gas: State of the Art and Future Perspectives. , 2016, Trends in biotechnology.

[67]  S. Velasquez-Orta,et al.  Microbial Electrosynthesis and Anaerobic Fermentation: An Economic Evaluation for Acetic Acid Production from CO2 and CO. , 2016, Environmental science & technology.

[68]  K. Rabaey,et al.  Microbial electrosynthesis — revisiting the electrical route for microbial production , 2010, Nature Reviews Microbiology.

[69]  D. Gang,et al.  Neutral red-mediated microbial electrosynthesis by Escherichia coli, Klebsiella pneumoniae, and Zymomonas mobilis. , 2015, Bioresource technology.

[70]  Jongwoo Lim,et al.  Physical Biology of the Materials-Microorganism Interface. , 2018, Journal of the American Chemical Society.

[71]  Justin C. Biffinger,et al.  Biochar Based Microbial Fuel Cell for Enhanced Wastewater Treatment and Nutrient Recovery , 2016 .

[72]  Alfred M Spormann,et al.  Enhanced microbial electrosynthesis by using defined co-cultures , 2016, The ISME Journal.

[73]  E. Trably,et al.  Electro‐fermentation triggering population selection in mixed‐culture glycerol fermentation , 2017, Microbial biotechnology.

[74]  S. Freguia,et al.  Bringing High-Rate, CO2-Based Microbial Electrosynthesis Closer to Practical Implementation through Improved Electrode Design and Operating Conditions. , 2016, Environmental science & technology.

[75]  Z. Ren,et al.  Nickel based catalysts for highly efficient H2 evolution from wastewater in microbial electrolysis cells , 2016 .

[76]  K. Rabaey,et al.  Integrated Production, Extraction, and Concentration of Acetic Acid from CO2 through Microbial Electrosynthesis , 2015 .

[77]  M. Hermansson,et al.  Effect of Start-Up Strategies and Electrode Materials on Carbon Dioxide Reduction on Biocathodes , 2017, Applied and Environmental Microbiology.

[78]  A. Elmekawy,et al.  Bioelectrochemical synthesis of caproate through chain elongation as a complementary technology to anaerobic digestion , 2018, Biofuels, Bioproducts and Biorefining.

[79]  Sai Kishore Butti,et al.  A Circular Bioeconomy with Biobased Products from CO2 Sequestration. , 2016, Trends in biotechnology.

[80]  Nilay Shah,et al.  The role of CO 2 capture and utilization in mitigating climate change , 2017 .

[81]  K. Rabaey,et al.  The type of ion selective membrane determines stability and production levels of microbial electrosynthesis. , 2017, Bioresource technology.

[82]  J. Krömer,et al.  Microbial Electrosynthesis of Isobutyric, Butyric, Caproic Acids, and Corresponding Alcohols from Carbon Dioxide , 2018, ACS Sustainable Chemistry & Engineering.

[83]  C. Buisman,et al.  Application of gas diffusion biocathode in microbial electrosynthesis from carbon dioxide , 2016, Environmental Science and Pollution Research.

[84]  Benjamin Erable,et al.  Electrochemical reduction of CO2 catalysed by Geobacter sulfurreducens grown on polarized stainless steel cathodes , 2013 .

[85]  Yong Jiang,et al.  Removal of Sulfide and Production of Methane from Carbon Dioxide in Microbial Fuel Cells–Microbial Electrolysis Cell (MFCs–MEC) Coupled System , 2014, Applied Biochemistry and Biotechnology.

[86]  M. Kumar,et al.  Electro-biocatalytic conversion of carbon dioxide to alcohols using gas diffusion electrode. , 2018, Bioresource technology.

[87]  Wenjuan Zhang,et al.  Efficient bioconversion of organic wastes to high optical activity of l-lactic acid stimulated by cathode in mixed microbial consortium. , 2018, Water research.

[88]  R. Zengerle,et al.  Revisiting methods to characterize bioelectrochemical systems: The influence of uncompensated resistance (iRu-drop), double layer capacitance, and junction potential , 2017 .

[89]  R. Norman,et al.  Electrosynthesis of Commodity Chemicals by an Autotrophic Microbial Community , 2012, Applied and Environmental Microbiology.

[90]  Lei Wang,et al.  Engineering exoelectrogens by synthetic biology strategies , 2018, Current Opinion in Electrochemistry.

[91]  K. Chandrasekhar,et al.  Solid phase bio-electrofermentation of food waste to harvest value-added products associated with waste remediation. , 2015, Waste management.

[92]  J. Liao,et al.  Fuelling the future: microbial engineering for the production of sustainable biofuels , 2016, Nature Reviews Microbiology.

[93]  Permani C Weerasekara,et al.  The United Nations World Water Development Report 2017 Wastewater: The Untapped Resource , 2017 .

[94]  H. May,et al.  Energy Efficiency and Productivity Enhancement of Microbial Electrosynthesis of Acetate , 2017, Front. Microbiol..

[95]  Lu Lu,et al.  Microbial electrolysis cells for waste biorefinery: A state of the art review. , 2016, Bioresource technology.

[96]  D. Lovley.  Syntrophy Goes Electric: Direct Interspecies Electron Transfer. , 2017, Annual review of microbiology.

[97]  Peng Liang,et al.  One-year operation of 1000-L modularized microbial fuel cell for municipal wastewater treatment. , 2018, Water research.

[98]  S. Mohan,et al.  Microbial electrosynthesis of carboxylic acids through CO2 reduction with selectively enriched biocatalyst: Microbial dynamics , 2017 .

[99]  E. Marsili,et al.  Weak electricigens: A new avenue for bioelectrochemical research. , 2018, Bioresource technology.

[100]  Doris Hafenbradl,et al.  Integrating electrochemical, biological, physical, and thermochemical process units to expand the applicability of anaerobic digestion. , 2018, Bioresource technology.

[101]  K. Nealson,et al.  Electromicrobiology: realities, grand challenges, goals and predictions , 2016, Microbial biotechnology.

[102]  Youngsoon Um,et al.  Electricity-driven metabolic shift through direct electron uptake by electroactive heterotroph Clostridium pasteurianum , 2014, Scientific Reports.

[103]  Jack A. Gilbert,et al.  Influence of Acidic pH on Hydrogen and Acetate Production by an Electrosynthetic Microbiome , 2014, PloS one.

[104]  Zhen He,et al.  Efficiently "pumping out" value-added resources from wastewater by bioelectrochemical systems: A review from energy perspectives. , 2018, Water research.

[105]  S. Venkata Mohan,et al.  Synergistic yield of dual energy forms through biocatalyzed electrofermentation of waste: Stoichiometric analysis of electron and carbon distribution , 2015 .

[106]  J. Gralnick,et al.  Acetoin production via unbalanced fermentation in Shewanella oneidensis , 2017, Biotechnology and bioengineering.

[107]  K. Zengler,et al.  Production of organics from CO2 by microbial electrosynthesis (MES) at high temperature , 2017 .

[108]  A. Stams,et al.  Microbial Community Analysis of a Methane-Producing Biocathode in a Bioelectrochemical System , 2013, Archaea.

[109]  Deepak Pant,et al.  Bioelectrocatalyzed reduction of acetic and butyric acids via direct electron transfer using a mixed culture of sulfate-reducers drives electrosynthesis of alcohols and acetone. , 2013, Chemical communications.

[110]  Dirk Weuster-Botz,et al.  Reaction engineering analysis of hydrogenotrophic production of acetic acid by Acetobacterium woodii. , 2011, Biotechnology and bioengineering.

[111]  A. Kondo,et al.  Increase in lactate yield by growing Corynebacterium glutamicum in a bioelectrochemical reactor. , 2014, Journal of bioscience and bioengineering.

[112]  T. Zhang,et al.  More efficient together , 2015, Science.

[113]  Tian Zhang,et al.  Improved cathode materials for microbial electrosynthesis , 2013 .

[114]  D. Pant,et al.  Biotransformation of carbon dioxide in bioelectrochemical systems: State of the art and future prospects , 2017 .

[115]  H. May,et al.  The bioelectrosynthesis of acetate. , 2016, Current opinion in biotechnology.

[116]  D. Pant,et al.  Influence of headspace composition on product diversity by sulphate reducing bacteria biocathode. , 2014, Bioresource technology.

[117]  Jens O Krömer,et al.  Balancing cellular redox metabolism in microbial electrosynthesis and electro fermentation - A chance for metabolic engineering. , 2018, Metabolic engineering.

[118]  C. Buisman,et al.  Critical Biofilm Growth throughout Unmodified Carbon Felts Allows Continuous Bioelectrochemical Chain Elongation from CO2 up to Caproate at High Current Density , 2018, Front. Energy Res..

[119]  Kelly P. Nevin,et al.  Electrosynthesis of Organic Compounds from Carbon Dioxide Is Catalyzed by a Diversity of Acetogenic Microorganisms , 2011, Applied and Environmental Microbiology.

[120]  M. Majone,et al.  Electrochemically Driven Fermentation of Organic Substrates with Undefined Mixed Microbial Cultures. , 2017, ChemSusChem.

[121]  Bruce E Logan,et al.  Direct biological conversion of electrical current into methane by electromethanogenesis. , 2009, Environmental science & technology.

[122]  K. Rabaey,et al.  Porous nickel hollow fiber cathodes coated with CNTs for efficient microbial electrosynthesis of acetate from CO2 using Sporomusa ovata , 2018 .

[123]  Korneel Rabaey,et al.  Dynamics of Cathode-Associated Microbial Communities and Metabolite Profiles in a Glycerol-Fed Bioelectrochemical System , 2013, Applied and Environmental Microbiology.

[124]  Yong Jiang,et al.  Production of acetate from carbon dioxide in bioelectrochemical systems based on autotrophic mixed culture. , 2013, Journal of microbiology and biotechnology.

[125]  M. Alves,et al.  Methane Production and Conductive Materials: A Critical Review. , 2018, Environmental science & technology.

[126]  Justin C. Biffinger,et al.  Graphitic biochar as a cathode electrocatalyst support for microbial fuel cells. , 2015, Bioresource technology.

[127]  Yung-Hun Yang,et al.  A Hierarchically Modified Graphite Cathode with Au Nanoislands, Cysteamine, and Au Nanocolloids for Increased Electricity-Assisted Production of Isobutanol by Engineered Shewanella oneidensis MR-1. , 2017, ACS applied materials & interfaces.

[128]  Korneel Rabaey,et al.  Metabolic and practical considerations on microbial electrosynthesis. , 2011, Current opinion in biotechnology.

[129]  Jiujun Zhang,et al.  A review of catalysts for the electroreduction of carbon dioxide to produce low-carbon fuels. , 2014, Chemical Society reviews.

[130]  E. Trably,et al.  Cooperative growth of Geobacter sulfurreducens and Clostridium pasteurianum with subsequent metabolic shift in glycerol fermentation , 2017, Scientific Reports.

[131]  Kun Guo,et al.  Selective Enrichment Establishes a Stable Performing Community for Microbial Electrosynthesis of Acetate from CO₂. , 2015, Environmental science & technology.

[132]  Karsten Zengler,et al.  A logical data representation framework for electricity-driven bioproduction processes. , 2015, Biotechnology advances.

[133]  Frauke Kracke,et al.  Identifying target processes for microbial electrosynthesis by elementary mode analysis , 2014, BMC Bioinformatics.

[134]  Peng Liang,et al.  A novel pilot-scale stacked microbial fuel cell for efficient electricity generation and wastewater treatment. , 2016, Water research.

[135]  A. Spormann,et al.  Extracellular Enzymes Facilitate Electron Uptake in Biocorrosion and Bioelectrosynthesis , 2015, mBio.

[136]  S. Atsumi,et al.  Electrical-biological hybrid system for CO2 reduction. , 2018, Metabolic engineering.

[137]  Sai Gu,et al.  Life cycle, techno-economic and dynamic simulation assessment of bioelectrochemical systems: A case of formic acid synthesis. , 2018, Bioresource technology.

[138]  I. Angelidaki,et al.  Salinity-gradient energy driven microbial electrosynthesis of value-added chemicals from CO2 reduction. , 2018, Water research.

[139]  K. Ishihara,et al.  Extracellular Electron Transfer Enhances Polyhydroxybutyrate Productivity in Ralstonia eutropha , 2014 .

[140]  E. Papoutsakis,et al.  Stoichiometric and energetic analyses of non-photosynthetic CO2-fixation pathways to support synthetic biology strategies for production of fuels and chemicals , 2012 .

[141]  Gunda Mohanakrishna,et al.  Technological advances in CO2 conversion electro-biorefinery: A step toward commercialization. , 2016, Bioresource technology.

[142]  Hajime Kobayashi,et al.  Bioelectrochemical analyses of the development of a thermophilic biocathode catalyzing electromethanogenesis. , 2015, Environmental science & technology.

[143]  Sai Kishore Butti,et al.  Electrofermentation of food waste – Regulating acidogenesis towards enhanced volatile fatty acids production , 2018 .

[144]  Gemma Reguera,et al.  Fermentation of glycerol into ethanol in a microbial electrolysis cell driven by a customized consortium. , 2014, Environmental science & technology.