Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

The progress and outlook of bioelectrocatalysis for the production of chemicals, fuels and materials

Nature Catalysis volume 3, pages 225–244 (2020)Cite this article

Subjects

Abstract

Bioelectrocatalysis is a green, sustainable, efficient method to produce value-added chemicals, clean biofuels and degradable materials. As an alternative approach to modern biomanufacturing technology, bioelectrocatalysis fully combines the merits of both biocatalysis and electrocatalysis to realize the green, efficient production of target products from electricity. Here, we review the development status of bioelectrocatalysis, discussing the current challenges and looking toward future development directions. First, we detail the structure, function and modification methods of bioelectrocatalysis. Next, we describe the mechanism of electron transfer, including mediated electron transfer and directed electron transfer. Third, we discuss the impact of the electrode on bioelectrocatalysis. Then we analyse and summarize the application of bioelectrocatalysis methods in the production of chemicals, biofuels and materials. Finally, we detail future developments and perspectives on bioelectrocatalysis for electrosynthesis.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: The structural basis of electroactive microbial cells for electron transfer.
Fig. 2: Three modification strategies of oxidoreductase to enhance the electron transfer.
Fig. 3: The MET and DET of oxidoreductase and electroactive microbial cell.
Fig. 4: Bioelectrocatalytic N2 fixation based on isolated nitrogenase and microbial cells.
Fig. 5: The bioelectrochemical preparation of chiral alcohol based on isolated P450cam and engineered E. coli cells.
Fig. 6: Bioelectrochemical cell design and reaction process of (R)-methylphenylsulfoxide preparation.
Fig. 7: Upgraded bioelectrocatalytic N2 fixation.
Fig. 8: Sustainable bioelectrosynthesis of the bioplastic PHB.

Similar content being viewed by others

References

  1. Wong, T. S. & Schwaneberg, U. Protein engineering in bioelectrocatalysis. Curr. Opin. Biotechnol. 14, 590–596 (2003).

    Article  CAS  PubMed  Google Scholar 

  2. Lapinsonnière, L., Picot, M. & Barrière, F. Enzymatic versus microbial bio-catalyzed electrodes in bio-electrochemical systems. ChemSusChem 5, 995–1005 (2012).

    Article  CAS  PubMed  Google Scholar 

  3. Ikeda, T. & Kano, K. An electrochemical approach to the studies of biological redox reactions and their applications to biosensors, bioreactors, and biofuel cells. J. Biosci. Bioeng. 92, 9–18 (2001).

    Article  CAS  PubMed  Google Scholar 

  4. Sakai, K. et al. Direct electron transfer-type bioelectrocatalytic interconversion of carbon dioxide/formate and NAD+/NADH redox couples with tungsten-containing formate dehydrogenase. Electrochim. Acta 228, 537–544 (2017).

    Article  CAS  Google Scholar 

  5. Milton, R. D. & Minteer, S. D. Direct enzymatic bioelectrocatalysis: differentiating between myth and reality. J. R. Soc. Interface 14, 20170253 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Wu, R. & Zhu, Z. Self-powered enzymatic electrosynthesis of l-3, 4-dihydroxyphenylalanine in a hybrid bioelectrochemical system. ACS Sustain. Chem. Eng. 6, 12593–12597 (2018). This study demonstrated a self-powered bioelectrochemical system for the enzymatic electrosynthesis of high-value-added pharmaceuticals.

    Article  CAS  Google Scholar 

  7. Moser, C. C., Page, C. C., Farid, R. & Dutton, P. L. Biological electron transfer. J. Bioenerg. Biomembr. 27, 263–274 (1995).

    Article  CAS  PubMed  Google Scholar 

  8. Tsujimura, S. From fundamentals to applications of bioelectrocatalysis: bioelectrocatalytic reactions of FAD-dependent glucose dehydrogenase and bilirubin oxidase. Biosci. Biotechnol. Biochem. 83, 39–48 (2019).

    Article  CAS  PubMed  Google Scholar 

  9. Karyakin, A. A. Principles of direct (mediator free) bioelectrocatalysis. Bioelectrochemistry 88, 70–75 (2012).

    Article  CAS  PubMed  Google Scholar 

  10. Schmid, A. et al. Industrial biocatalysis today and tomorrow. Nature 409, 258–268 (2001).

    Article  CAS  PubMed  Google Scholar 

  11. Sheldon, R. A. & Woodley, J. M. Role of biocatalysis in sustainable chemistry. Chem. Rev. 118, 801–838 (2017).

    Article  CAS  PubMed  Google Scholar 

  12. De Carvalho, C. C. Enzymatic and whole cell catalysis: finding new strategies for old processes. Biotechnol. Adv. 29, 75–83 (2011).

    Article  CAS  PubMed  Google Scholar 

  13. Steckhan, E. et al. Environmental protection and economization of resources by electroorganic and electroenzymatic syntheses. Chemosphere 43, 63–73 (2001).

    Article  CAS  PubMed  Google Scholar 

  14. Freguia, S., Virdis, B., Harnisch, F. & Keller, J. Bioelectrochemical systems: microbial versus enzymatic catalysis. Electrochim. Acta 82, 165–174 (2012).

    Article  CAS  Google Scholar 

  15. Harnisch, F. & Holtmann, D. Bioelectrosynthesis (Springer, 2019).

  16. Bajracharya, S. et al. An overview on emerging bioelectrochemical systems (BESs): technology for sustainable electricity, waste remediation, resource recovery, chemical production and beyond. Renew. Energy 98, 153–170 (2016).

    Article  CAS  Google Scholar 

  17. MacVittie, K. & Katz, E. Self-powered electrochemical memristor based on a biofuel cell-towards memristors integrated with biocomputing systems. Chem. Commun. 50, 4816–4819 (2014).

    Article  CAS  Google Scholar 

  18. Rasmussen, M., Abdellaoui, S. & Minteer, S. D. Enzymatic biofuel cells: 30 years of critical advancements. Biosens. Bioelectron. 76, 91–102 (2016).

    Article  CAS  PubMed  Google Scholar 

  19. Pant, D. et al. Bioelectrochemical systems (BES) for sustainable energy production and product recovery from organic wastes and industrial wastewaters. RSC Adv. 2, 1248–1263 (2012).

    Article  CAS  Google Scholar 

  20. Yuan, M. et al. Creating a low‐potential redox polymer for efficient electroenzymatic CO2 reduction. Angew. Chem. Int. Ed. 130, 6692–6696 (2018). The CO 2 fixation performed by the cobaltocene functionalized poly(allylamine) redox polymer immobilized formate dehydrogenase achieved almost 100% Faradaic efficiency.

    Article  Google Scholar 

  21. Cai, R. et al. Electroenzymatic C–C bond formation from CO2. J. Am. Chem. Soc. 140, 5041–5044 (2018). This study empolyed VFe protein for electroenzymatic C–C bond formation from CO 2.

    Article  CAS  PubMed  Google Scholar 

  22. Mateos, R. et al. in Microbial Electrochemical Technology Ch. 5.4, 777–796 (Elsevier, 2019).

  23. Cai, R. & Minteer, S. D. Nitrogenase bioelectrocatalysis: from understanding electron-transfer mechanisms to energy applications. ACS Energy Lett. 3, 2736–2742 (2018).

    Article  CAS  Google Scholar 

  24. Milton, R. D. et al. Bioelectrochemical Haber–Bosch process: an ammonia-producing H2/N2 fuel cell. Angew. Chem. Int. Ed. 56, 2680–2683 (2017). Bioelectrochemical N 2 fixation based on nitrogenase powered by hydrogen fuel cells was developed in this study.

    Article  CAS  Google Scholar 

  25. Milton, R. D. et al. Nitrogenase bioelectrocatalysis: heterogeneous ammonia and hydrogen production by MoFe protein. Energy Environ. Sci. 9, 2550–2554 (2016).

    Article  CAS  Google Scholar 

  26. Milton, R. D. & Minteer, S. D. Enzymatic bioelectrosynthetic ammonia production: recent electrochemistry of nitrogenase, nitrate reductase, and nitrite reductase. ChemPlusChem 82, 513–521 (2017).

    Article  CAS  PubMed  Google Scholar 

  27. Chen, H. et al. Upgraded bioelectrocatalytic N2 fixation: from N2 to chiral amine intermediates. J. Am. Chem. Soc. 141, 4963–4971 (2019). This study proposed an upgraded bioelectrocatalytic N 2 fixation system to realize the conversion from chemically inert N 2 gas to a variety of chiral amine intermediates.

    Article  CAS  PubMed  Google Scholar 

  28. Yuan, R., Watanabe, S., Kuwabata, S. & Yoneyama, H. Asymmetric electroreduction of ketone and aldehyde derivatives to the corresponding alcohols using alcohol dehydrogenase as an electrocatalyst. J. Org. Chem. 62, 2494–2499 (1997).

    Article  CAS  PubMed  Google Scholar 

  29. Lütz, S., Steckhan, E. & Liese, A. First asymmetric electroenzymatic oxidation catalyzed by a peroxidase. Electrochem. Commun. 6, 583–587 (2004). Thioanisole is selectively oxidized to (R)-methylphenylsulfoxide with electrochemically generated hydrogen peroxide via cathodic reduction of oxygen catalysed by chloroperoxidase.

    Article  CAS  Google Scholar 

  30. Märkle, W. & Lütz, S. Electroenzymatic strategies for deracemization, stereoinversion and asymmetric synthesis of amino acids. Electrochim. Acta 53, 3175–3180 (2008).

    Article  CAS  Google Scholar 

  31. Alkotaini, B. et al. Sustainable bioelectrosynthesis of the bioplastic polyhydroxybutyrate: overcoming substrate requirement for NADH regeneration. ACS Sustain. Chem. Eng. 6, 4909–4915 (2018). A bioelectrocatalytic method combining both enzymatic and electrochemical approaches was used to regenerate NADH and further support the enzymatic synthesis of PHB.

    Article  CAS  Google Scholar 

  32. Chen, X., Cao, Y., Li, F., Tian, Y. & Song, H. Enzyme-assisted microbial electrosynthesis of poly (3-hydroxybutyrate) via CO2 bioreduction by engineered Ralstonia eutropha. ACS Catal. 8, 4429–4437 (2018). An enzyme–microorganism hybrid system was utilized to realize the bioelectrocatalytic synthesis of PHB from CO 2.

    Article  CAS  Google Scholar 

  33. Reddy, M. V. & Sun, X. in Microbial Electrochemical Technology Ch. 5.3, 757–776 (Elsevier, 2019).

  34. Grieshaber, D., MacKenzie, R., Voeroes, J. & Reimhult, E. Electrochemical biosensors-sensor principles and architectures. Sensors 8, 1400–1458 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Masa, J. & Schuhmann, W. Electrocatalysis and bioelectrocatalysis-distinction without a difference. Nano Energy 29, 466–475 (2016).

    Article  CAS  Google Scholar 

  36. Xiang, K., Qiao, Y., Ching, C. B. & Li, C. M. GldA overexpressing-engineered E. coli as superior electrocatalyst for microbial fuel cells. Electrochem. Commun. 11, 1593–1595 (2009).

    Article  CAS  Google Scholar 

  37. Schaetzle, O., Barrière, F. & Baronian, K. Bacteria and yeasts as catalysts in microbial fuel cells: electron transfer from micro-organisms to electrodes for green electricity. Energy Environ. Sci. 1, 607–620 (2008).

    Article  CAS  Google Scholar 

  38. Hickey, D. P., Gaffney, E. M. & Minteer, S. D. Electrometabolic pathways: recent developments in bioelectrocatalytic cascades. Top. Curr. Chem. 376, 43 (2018).

    Article  CAS  Google Scholar 

  39. Chiranjeevi, P., Bulut, M., Breugelmans, T., Patil, S. A. & Pant, D. Current trends in enzymatic electrosynthesis for CO2 reduction. Curr. Opin. Green. Sustain. Chem. 16, 65–70 (2019).

    Article  Google Scholar 

  40. Wu, R., Ma, C. & Zhu, Z. Enzymatic electrosynthesis as an emerging electrochemical synthesis platform. Curr. Opin. Electrochem. 19, 1–7 (2020).

    Article  Google Scholar 

  41. Dominguez-Benetton, X., Srikanth, S., Satyawali, Y., Vanbroekhoven, K. & Pant, D. Enzymatic electrosynthesis: an overview on the progress in enzyme-electrodes for the production of electricity, fuels and chemicals. J. Microb. Biochem. Technol. S6, 007 (2013).

    Google Scholar 

  42. Kumar, P., Chandrasekhar, K., Kumari, A., Sathiyamoorthi, E. & Kim, B. Electro-fermentation in aid of bioenergy and biopolymers. Energies 11, 343 (2018).

    Article  CAS  Google Scholar 

  43. Irfan, M. et al. Direct microbial transformation of carbon dioxide to value-added chemicals: a comprehensive analysis and application potentials. Bioresour. Technol. 288, 121401 (2019).

    Article  CAS  PubMed  Google Scholar 

  44. Jiang, Y. et al. Carbon dioxide and organic waste valorization by microbial electrosynthesis and electro-fermentation. Water Res. 149, 42–55 (2018).

    Article  CAS  PubMed  Google Scholar 

  45. Jiang, Y. & Zeng, R. J. Expanding the product spectrum of value added chemicals in microbial electrosynthesis through integrated process design-a review. Bioresour. Technol. 269, 503–512 (2018).

    Article  CAS  PubMed  Google Scholar 

  46. Rosenbaum, M. A. & Henrich, A. W. Engineering microbial electrocatalysis for chemical and fuel production. Curr. Opin. Biotechnol. 29, 93–98 (2014).

    Article  CAS  PubMed  Google Scholar 

  47. Sadhukhan, J. 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. Renew. Sustain. Energy Rev. 56, 116–132 (2016).

    Article  CAS  Google Scholar 

  48. Mayo, S. L., Ellis, W. R., Crutchley, R. J. & Gray, H. B. Long-range electron transfer in heme proteins. Science 233, 948–952 (1986).

    Article  CAS  PubMed  Google Scholar 

  49. Collman, J. P. et al. A cytochrome c oxidase model catalyzes oxygen to water reduction under rate-limiting electron flux. Science 315, 1565–1568 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Urlacher, V. B. & Eiben, S. Cytochrome P450 monooxygenases: perspectives for synthetic application. Trends Biotechnol. 24, 324–330 (2006).

    Article  CAS  PubMed  Google Scholar 

  51. Vlasits, J. et al. Mechanisms of catalase activity of heme peroxidases. Arch. Biochem. Biophys. 500, 74–81 (2010).

    Article  CAS  PubMed  Google Scholar 

  52. Zhang, W. et al. Mechanistic Insights into Interactions between bacterial class I P450 enzymes and redox partners. ACS Catal. 8, 9992–10003 (2018).

    Article  CAS  Google Scholar 

  53. Evans, D. J. & Pickett, C. J. Chemistry and the hydrogenases. Chem. Soc. Rev. 32, 268–275 (2003).

    Article  CAS  PubMed  Google Scholar 

  54. Lewis, E. A. & Tolman, W. B. Reactivity of dioxygen-copper systems. Chem. Rev. 104, 1047–1076 (2004).

    Article  CAS  PubMed  Google Scholar 

  55. Betancor, L., Johnson, G. R. & Luckarift, H. R. Stabilized laccases as heterogeneous bioelectrocatalysts. ChemCatChem 5, 46–60 (2013).

    Article  CAS  Google Scholar 

  56. Van Berkel, W., Kamerbeek, N. & Fraaije, M. Flavoprotein monooxygenases, a diverse class of oxidative biocatalysts. J. Biotechnol. 124, 670–689 (2006).

    Article  CAS  PubMed  Google Scholar 

  57. Krige, A., Sjöblom, M., Ramser, K., Christakopoulos, P. & Rova, U. On-line Raman spectroscopic study of cytochromes’ redox state of biofilms in microbial fuel cells. Molecules 24, E646 (2019).

    Article  CAS  PubMed  Google Scholar 

  58. Malvankar, N. S. & Lovley, D. R. Microbial nanowires for bioenergy applications. Curr. Opin. Biotechnol. 27, 88–95 (2014).

    Article  CAS  PubMed  Google Scholar 

  59. Tan, Y. et al. The low conductivity of Geobacter uraniireducens pili suggests a diversity of extracellular electron transfer mechanisms in the genus Geobacter. Front. Microbiol. 7, 980 (2016).

    PubMed  PubMed Central  Google Scholar 

  60. Malvankar, N. S. et al. Structural basis for metallic-like conductivity in microbial nanowires. mBio 6, e00084-15 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Wang, F. et al. Structure of microbial nanowires reveals stacked hemes that transport electrons over micrometers. Cell 177, 361–369.e310 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Ueki, T. et al. Decorating the outer surface of microbially produced protein nanowires with peptides. ACS Synth. Biol. 8, 1809–1817 (2019).

    Article  CAS  PubMed  Google Scholar 

  63. Lovley, D. R. & Walker, D. J. Geobacter protein nanowires. Front. Microbiol. 10, 2078 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  64. Malvankar, N., Tuominen, M. & Lovley, D. Lack of involvement of c-type cytochromes in long-range electron transport in microbial biofilms and nanowires. Energy Environ. Sci. 5, 8651–8659 (2012).

    Article  CAS  Google Scholar 

  65. Vargas, M. et al. Aromatic amino acids required for pili conductivity and long-range extracellular electron transport in Geobacter sulfurreducens. mBio 4, e00105-13 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  66. Liu, F. et al. Magnetite compensates for the lack of a pilin‐associated c-type cytochrome in extracellular electron exchange. Environ. Microbiol. 17, 648–655 (2015).

    Article  CAS  PubMed  Google Scholar 

  67. Tang, H.-Y., Holmes, D. E., Ueki, T., Palacios, P. A. & Lovley, D. R. Iron corrosion via direct metal-microbe electron transfer. mBio 10, e00303-19 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  68. Rotaru, A.-E., Woodard, T. L., Nevin, K. P. & Lovley, D. R. Link between capacity for current production and syntrophic growth in Geobacter species. Front. Microbiol. 6, 744 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  69. Flanagan, K. A., Leang, C., Ward, J. & Lovley, D. R. Improper localization of the OmcS cytochrome may explain the inability of the xapD-deficient mutant of Geobacter sulfurreducens to reduce Fe (III) oxide. Preprint at https://www.biorxiv.org/content/10.1101/114900v1 (2017).

  70. Malvankar, N. S. et al. Tunable metallic-like conductivity in microbial nanowire networks. Nat. Nanotechnol. 6, 573–579 (2011).

    Article  PubMed  Google Scholar 

  71. Hartshorne, R. S. et al. Characterization of an electron conduit between bacteria and the extracellular environment. Proc. Natl Acad. Sci. USA 106, 22169–22174 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  72. Ross, D. E., Flynn, J. M., Baron, D. B., Gralnick, J. A. & Bond, D. R. Towards electrosynthesis in Shewanella: energetics of reversing the Mtr pathway for reductive metabolism. PLoS ONE 6, e16649 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Strycharz, S. M. et al. Graphite electrode as a sole electron donor for reductive dechlorination of tetrachlorethene by Geobacter lovleyi. Appl. Environ. Microbiol. 74, 5943–5947 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Kracke, F., Vassilev, I. & Krömer, J. O. Microbial electron transport and energy conservation-the foundation for optimizing bioelectrochemical systems. Front Microbiol. 6, 575 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  75. Choi, O. & Sang, B.-I. Extracellular electron transfer from cathode to microbes: application for biofuel production. Biotechnol. Biofuels. 9, 11 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Choi, O., Kim, T., Woo, H. M. & Um, Y. Electricity-driven metabolic shift through direct electron uptake by electroactive heterotroph Clostridium pasteurianum. Sci. Rep. 4, 6961 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Sharp, R. E. & Chapman, S. K. Mechanisms for regulating electron transfer in multi-centre redox proteins. Biochim. Biophys. Acta Protein Struct. Mol. Enzymol. 1432, 143–158 (1999).

    Article  CAS  Google Scholar 

  78. Hibino, Y., Kawai, S., Kitazumi, Y., Shirai, O. & Kano, K. Protein-engineering improvement of direct electron transfer-type bioelectrocatalytic properties of d-fructose dehydrogenase. Electrochemistry 87, 47–51 (2018).

    Article  CAS  Google Scholar 

  79. Courjean, O., Gao, F. & Mano, N. Deglycosylation of glucose oxidase for direct and efficient glucose electrooxidation on a glassy carbon electrode. Angew. Chem. Int. Ed. 48, 5897–5899 (2009).

    Article  CAS  Google Scholar 

  80. Ferapontova, E., Schmengler, K., Börchers, T., Ruzgas, T. & Gorton, L. Effect of cysteine mutations on direct electron transfer of horseradish peroxidase on gold. Biosens. Bioelectron. 17, 953–963 (2002).

    Article  CAS  PubMed  Google Scholar 

  81. Presnova, G. et al. Direct heterogeneous electron transfer of recombinant horseradish peroxidases on gold. Faraday Discuss. 116, 281–289 (2000).

    Article  CAS  Google Scholar 

  82. Holland, J. T., Lau, C., Brozik, S., Atanassov, P. & Banta, S. Engineering of glucose oxidase for direct electron transfer via site-specific gold nanoparticle conjugation. J. Am. Chem. Soc. 133, 19262–19265 (2011).

    Article  CAS  PubMed  Google Scholar 

  83. Bailey, J. E. et al. Inverse metabolic engineering: a strategy for directed genetic engineering of useful phenotypes. Biotechnol. Bioeng. 52, 109–121 (1996).

    Article  CAS  PubMed  Google Scholar 

  84. Kracke, F., Lai, B., Yu, S. & Krömer, J. O. Balancing cellular redox metabolism in microbial electrosynthesis and electro fermentation-a chance for metabolic engineering. Metab. Eng. 45, 109–120 (2018).

    Article  CAS  PubMed  Google Scholar 

  85. Marshall, C. W., Ross, D. E., Fichot, E. B., Norman, R. S. & May, H. D. Electrosynthesis of commodity chemicals by an autotrophic microbial community. Appl. Environ. Microbiol. 78, 8412–8420 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Grobbler, C. et al. Use of SWATH mass spectrometry for quantitative proteomic investigation of Shewanella oneidensis MR-1 biofilms grown on graphite cloth electrodes. Syst. Appl. Microbiol. 38, 135–139 (2015).

    Article  CAS  PubMed  Google Scholar 

  87. Trinh, C. T., Wlaschin, A. & Srienc, F. Elementary mode analysis: a useful metabolic pathway analysis tool for characterizing cellular metabolism. Appl. Microbiol. Biotechnol. 81, 813 (2009).

    Article  CAS  PubMed  Google Scholar 

  88. Marcus, R. A. & Sutin, N. Electron transfers in chemistry and biology. Biochim. Biophys. Acta 811, 265–322 (1985).

    Article  CAS  Google Scholar 

  89. Lee, Y. S. et al. Construction of uniform monolayer-and orientation-tunable enzyme electrode by a synthetic glucose dehydrogenase without electron-transfer subunit via optimized site-specific gold-binding peptide capable of direct electron transfer. ACS Appl. Mater. Interfaces 10, 28615–28626 (2018).

    Article  CAS  PubMed  Google Scholar 

  90. Liu, H.-H. et al. Direct electrochemistry and electrocatalysis of heme-proteins entrapped in agarose hydrogel films. Biosens. Bioelectron. 20, 294–304 (2004).

    Article  CAS  PubMed  Google Scholar 

  91. Mazurenko, I. et al. Impact of substrate diffusion and enzyme distribution in 3D-porous electrodes: a combined electrochemical and modelling study of a thermostable H2/O2 enzymatic fuel cell. Energy Environ. Sci. 10, 1966–1982 (2017).

    Article  CAS  Google Scholar 

  92. Hickey, D. P. et al. Pyrene hydrogel for promoting direct bioelectrochemistry: ATP-independent electroenzymatic reduction of N2. Chem. Sci. 9, 5172–5177 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Schröder, U. Anodic electron transfer mechanisms in microbial fuel cells and their energy efficiency. Phys. Chem. Chem. Phys. 9, 2619–2629 (2007).

    Article  PubMed  Google Scholar 

  94. Steinbusch, K. J., Hamelers, H. V., Schaap, J. D., Kampman, C. & Buisman, C. J. Bioelectrochemical ethanol production through mediated acetate reduction by mixed cultures. Environ. Sci. Technol. 44, 513–517 (2009).

    Article  CAS  Google Scholar 

  95. Hatch, J. L. & Finneran, K. T. Influence of reduced electron shuttling compounds on biological H2 production in the fermentative pure culture Clostridium beijerinckii. Curr. Microbiol. 56, 268–273 (2008).

    Article  CAS  PubMed  Google Scholar 

  96. Park, D. & Zeikus, J. Utilization of electrically reduced neutral Red by Actinobacillus succinogenes: physiological function of neutral red in membrane-driven fumarate reduction and energy conservation. J. Bacteriol. 181, 2403–2410 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Okamoto, A., Hashimoto, K., Nealson, K. H. & Nakamura, R. Rate enhancement of bacterial extracellular electron transport involves bound flavin semiquinones. Proc. Natl Acad. Sci. USA 110, 7856–7861 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  98. Jiang, X. et al. Probing electron transfer mechanisms in Shewanella oneidensis MR-1 using a nanoelectrode platform and single-cell imaging. Proc. Natl Acad. Sci. USA 107, 16806–16810 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  99. Milton, R. D. et al. Rational design of quinones for high power density biofuel cells. Chem. Sci. 6, 4867–4875 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Wu, H. et al. Methods for the regeneration of nicotinamide coenzymes. Green. Chem. 15, 1773–1789 (2013).

    Article  CAS  Google Scholar 

  101. Hollmann, F., Arends, I. W. & Buehler, K. Biocatalytic redox reactions for organic synthesis: nonconventional regeneration methods. ChemCatChem 2, 762–782 (2010).

    Article  CAS  Google Scholar 

  102. Guo, K., Prévoteau, A., Patil, S. A. & Rabaey, K. Engineering electrodes for microbial electrocatalysis. Curr. Opin. Biotech. 33, 149–156 (2015).

    Article  CAS  PubMed  Google Scholar 

  103. Guo, K. et al. Effects of surface charge and hydrophobicity on anodic biofilm formation, community composition, and current generation in bioelectrochemical systems. Environ. Sci. Technol. 47, 7563–7570 (2013).

    Article  CAS  PubMed  Google Scholar 

  104. Saboe, P. O., Conte, E., Farell, M., Bazan, G. C. & Kumar, M. Biomimetic and bioinspired approaches for wiring enzymes to electrode interfaces. Energy Environ. Sci. 10, 14–42 (2017).

    Article  CAS  Google Scholar 

  105. Sugimoto, Y. et al. Electrostatic interaction between an enzyme and electrodes in the electric double layer examined in a view of direct electron transfer-type bioelectrocatalysis. Biosens. Bioelectron. 63, 138–144 (2015).

    Article  CAS  PubMed  Google Scholar 

  106. Murata, K., Akatsuka, W., Sadakane, T., Matsunaga, A. & Tsujimura, S. Glucose oxidation catalyzed by FAD-dependent glucose dehydrogenase within Os complex-tethered redox polymer hydrogel. Electrochim. Acta 136, 537–541 (2014).

    Article  CAS  Google Scholar 

  107. Ciobanu, M., Kincaid, H. A., Jennings, G. K. & Cliffel, D. E. Photosystem I patterning imaged by scanning electrochemical microscopy. Langmuir 21, 692–698 (2005).

    Article  CAS  PubMed  Google Scholar 

  108. Ko, B. S. et al. Effect of surface composition on the adsorption of photosystem I onto alkanethiolate self-assembled monolayers on gold. Langmuir 20, 4033–4038 (2004).

    Article  CAS  PubMed  Google Scholar 

  109. Shrier, A., Giroud, F., Rasmussen, M. & Minteer, S. D. Operational stability assays for bioelectrodes for biofuel cells: effect of immobilization matrix on laccase biocathode stability. J. Electrochem. Soc. 161, H244–H248 (2014).

    Article  CAS  Google Scholar 

  110. Neto, S. A., Minteer, S. D. & de Andrade, A. R. Developing ethanol bioanodes using a hydrophobically modified linear polyethylenimine hydrogel for immobilizing an enzyme cascade. J. Electroanal. Chem. 812, 153–158 (2018).

    Article  CAS  Google Scholar 

  111. Ikeda, T., Matsushita, F. & Senda, M. Amperometric fructose sensor based on direct bioelectrocatalysis. Biosens. Bioelectron. 6, 299–304 (1991).

    Article  CAS  Google Scholar 

  112. Zhang, L. et al. Rational design of enzyme-modified electrodes for optimized bioelectrocatalytic activity. ChemElectroChem 6, 4980–4984 (2019).

    Article  CAS  Google Scholar 

  113. Walcarius, A., Minteer, S. D., Wang, J., Lin, Y. & Merkoçi, A. Nanomaterials for bio-functionalized electrodes: recent trends. J. Mater. Chem. B 1, 4878–4908 (2013).

    Article  CAS  PubMed  Google Scholar 

  114. Guo, K. et al. Surfactant treatment of carbon felt enhances anodic microbial electrocatalysis in bioelectrochemical systems. Electrochem. Commun. 39, 1–4 (2014).

    Article  CAS  Google Scholar 

  115. Zhang, T. et al. Improved cathode materials for microbial electrosynthesis. Energy Environ. Sci. 6, 217–224 (2013).

    Article  CAS  Google Scholar 

  116. Olsson, A. L., Van der Mei, H. C., Busscher, H. J. & Sharma, P. K. Influence of cell surface appendages on the bacterium-substratum interface measured real-time using QCM-D. Langmuir 25, 1627–1632 (2008).

    Article  CAS  Google Scholar 

  117. Dingari, N. N. & Buie, C. R. Theoretical investigation of bacteria polarizability under direct current electric fields. Langmuir 30, 4375–4384 (2014).

    Article  CAS  PubMed  Google Scholar 

  118. Rizzello, L., Cingolani, R. & Pompa, P. P. Nanotechnology tools for antibacterial materials. Nanomedicine 8, 807–821 (2013).

    Article  CAS  PubMed  Google Scholar 

  119. Santoro, C., Arbizzani, C., Erable, B. & Ieropoulos, I. Microbial fuel cells: from fundamentals to applications. A review. J. Power Sources 356, 225–244 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Santoro, C. et al. The effects of carbon electrode surface properties on bacteria attachment and start up time of microbial fuel cells. Carbon 67, 128–139 (2014).

    Article  CAS  Google Scholar 

  121. Takahashi, Y., Wanibuchi, M., Kitazumi, Y., Shirai, O. & Kano, K. Improved direct electron transfer-type bioelectrocatalysis of bilirubin oxidase using porous gold electrodes. J. Electroanal. Chem. 843, 47–53 (2019).

    Article  CAS  Google Scholar 

  122. Krieg, T., Sydow, A., Schröder, U., Schrader, J. & Holtmann, D. Reactor concepts for bioelectrochemical syntheses and energy conversion. Trends Biotechnol. 32, 645–655 (2014).

    Article  CAS  PubMed  Google Scholar 

  123. Krieg, T., Hüttmann, S., Mangold, K.-M., Schrader, J. & Holtmann, D. Gas diffusion electrode as novel reaction system for an electro-enzymatic process with chloroperoxidase. Green. Chem. 13, 2686–2689 (2011).

    Article  CAS  Google Scholar 

  124. Logan, B., Cheng, S., Watson, V. & Estadt, G. Graphite fiber brush anodes for increased power production in air-cathode microbial fuel cells. Environ. Sci. Technol. 41, 3341–3346 (2007).

    Article  CAS  PubMed  Google Scholar 

  125. Flexer, V., Brun, N., Destribats, M., Backov, R. & Mano, N. A novel three-dimensional macrocellular carbonaceous biofuel cell. Phys. Chem. Chem. Phys. 15, 6437–6445 (2013).

    Article  CAS  PubMed  Google Scholar 

  126. Kipf, E. et al. Systematic screening of carbon-based anode materials for microbial fuel cells with Shewanella oneidensis MR-1. Bioresour. Technol. 146, 386–392 (2013).

    Article  CAS  PubMed  Google Scholar 

  127. Engel, A. B. et al. Enhanced performance of electrospun carbon fibers modified with carbon nanotubes: promising electrodes for enzymatic biofuel cells. Nanotechnology 24, 245402 (2013).

    Article  CAS  PubMed  Google Scholar 

  128. Soussan, L., Riess, J., Erable, B., Délia, M.-L. & Bergel, A. Electrochemical reduction of CO2 catalysed by Geobacter sulfurreducens grown on polarized stainless steel cathodes. Electrochem. commun. 28, 27–30 (2013).

    Article  CAS  Google Scholar 

  129. Guo, K., Hidalgo, D., Tommasi, T. & Rabaey, K. Pyrolytic carbon-coated stainless steel felt as a high-performance anode for bioelectrochemical systems. Bioresour. Technol. 211, 664–668 (2016).

    Article  CAS  PubMed  Google Scholar 

  130. Laheäär, A., Delpeux-Ouldriane, S., Lust, E. & Béguin, F. Ammonia treatment of activated carbon powders for supercapacitor electrode application. J. Electrochem. Soc. 161, A568–A575 (2014).

    Article  CAS  Google Scholar 

  131. Cavalcanti, I. et al. A disposable chitosan-modified carbon fiber electrode for dengue virus envelope protein detection. Talanta 91, 41–46 (2012).

    Article  CAS  PubMed  Google Scholar 

  132. Wang, L. et al. Dendritic copper-cobalt nanostructures/reduced graphene oxide-chitosan modified glassy carbon electrode for glucose sensing. Sens. Actuator B 195, 1–7 (2014).

    Article  CAS  Google Scholar 

  133. Wang, Y. & Hasebe, Y. Carbon felt-based bioelectrocatalytic flow-through detectors: Highly sensitive amperometric determination of H2O2 based on a direct electrochemistry of covalently modified horseradish peroxidase using cyanuric chloride as a linking agent. Sens. Actuator B 155, 722–729 (2011).

    Article  CAS  Google Scholar 

  134. Franzoi, A. C., Vieira, I. C., Dupont, J., Scheeren, C. W. & de Oliveira, L. F. Biosensor for luteolin based on silver or gold nanoparticles in ionic liquid and laccase immobilized in chitosan modified with cyanuric chloride. Analyst 134, 2320–2328 (2009).

    Article  CAS  PubMed  Google Scholar 

  135. Zor, E., Patir, I. H., Bingol, H. & Ersoz, M. An electrochemical biosensor based on human serum albumin/graphene oxide/3-aminopropyltriethoxysilane modified ITO electrode for the enantioselective discrimination of d-and l-tryptophan. Biosens. Bioelectron. 42, 321–325 (2013).

    Article  CAS  PubMed  Google Scholar 

  136. Tian, X. et al. Nitrogen-doped activated carbon as metal-free oxygen reduction catalyst for cost-effective rolling-pressed air-cathode in microbial fuel cells. Fuel 223, 422–430 (2018).

    Article  CAS  Google Scholar 

  137. Ma, Z., Song, H., Stoll, Z. A. & Xu, P. Melamine modified carbon felts anode with enhanced electrogenesis capacity toward microbial fuel cells. J. Energy Chem. 26, 81–86 (2017).

    Article  Google Scholar 

  138. Wei, J., Liang, P. & Huang, X. Recent progress in electrodes for microbial fuel cells. Bioresour. Technol. 102, 9335–9344 (2011).

    Article  CAS  PubMed  Google Scholar 

  139. Holzinger, M., Le Goff, A. & Cosnier, S. Carbon nanotube/enzyme biofuel cells. Electrochim. Acta 82, 179–190 (2012).

    Article  CAS  Google Scholar 

  140. Yuan, M. & Minteer, S. D. Redox polymers in electrochemical systems: from methods of mediation to energy storage. Curr. Opin. Electrochem. 15, 1–6 (2019).

    Article  CAS  Google Scholar 

  141. Badura, A. et al. Photo-induced electron transfer between photosystem 2 via cross-linked redox hydrogels. Electroanalysis 20, 1043–1047 (2008).

    Article  CAS  Google Scholar 

  142. Kato, M., Zhang, J. Z., Paul, N. & Reisner, E. Protein film photoelectrochemistry of the water oxidation enzyme photosystem II. Chem. Soc. Rev. 43, 6485–6497 (2014).

    Article  CAS  PubMed  Google Scholar 

  143. Tapia, C. et al. Wiring of photosystem I and hydrogenase on an electrode for photoelectrochemical H2 production by using redox polymers for relatively positive onset potential. ChemElectroChem 4, 90–95 (2017).

    Article  CAS  Google Scholar 

  144. Barsan, M. M., Ghica, M. E. & Brett, C. M. Electrochemical sensors and biosensors based on redox polymer/carbon nanotube modified electrodes: a review. Anal. Chim. Acta 881, 1–23 (2015).

    Article  CAS  PubMed  Google Scholar 

  145. Burgess, B. K. & Lowe, D. J. Mechanism of molybdenum nitrogenase. Chem. Rev. 96, 2983–3012 (1996).

    Article  CAS  PubMed  Google Scholar 

  146. Leddy, J. & Paschkewitz, T. M. Ammonia production using bioelectrocatalytical devices. US patent US9506085B2 (2016).

  147. Liu, C., Sakimoto, K. K., Colón, B. C., Silver, P. A. & Nocera, D. G. Ambient nitrogen reduction cycle using a hybrid inorganic-biological system. Proc. Natl Acad. Sci. USA 114, 6450–6455 (2017). The inorganic–biological hybrid bioelectrocatalytic system fixes atmospheric N 2 into NH 3 or soluble biomass with high fluxes and energy efficiency.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Ortiz-Medina, J. F., Grunden, A. M., Hyman, M. R. & Call, D. F. Nitrogen gas fixation and conversion to ammonium using microbial electrolysis cells. ACS Sustain. Chem. Eng. 7, 3511–3519 (2019).

    Article  CAS  Google Scholar 

  149. Ambrosio, R., Ortiz-Marquez, J. C. F. & Curatti, L. Metabolic engineering of a diazotrophic bacterium improves ammonium release and biofertilization of plants and microalgae. Metab. Eng. 40, 59–68 (2017).

    Article  CAS  PubMed  Google Scholar 

  150. Patel, R. N. Biocatalytic synthesis of intermediates for the synthesis of chiral drug substances. Curr. Opin. Biotechnol. 12, 587–604 (2001).

    Article  CAS  PubMed  Google Scholar 

  151. Xu, F. Applications of oxidoreductases: recent progress. Ind. Biotechnol. 1, 38–50 (2005).

    Article  CAS  Google Scholar 

  152. Leonida, M. D. Redox enzymes used in chiral syntheses coupled to coenzyme regeneration. Curr. Med. Chem. 8, 345–369 (2001).

    Article  CAS  PubMed  Google Scholar 

  153. Zhang, L., Vila, N., Kohring, G.-W., Walcarius, A. & Etienne, M. Covalent immobilization of (2,2′-bipyridyl)(pentamethylcyclopentadienyl)-rhodium complex on a porous carbon electrode for efficient electrocatalytic NADH regeneration. ACS Catal. 7, 4386–4394 (2017).

    Article  CAS  Google Scholar 

  154. Hildebrand, F. & Lütz, S. Electroenzymatic synthesis of chiral alcohols in an aqueous–organic two-phase system. Tetrahedron Asymm. 18, 1187–1193 (2007).

    Article  CAS  Google Scholar 

  155. Kazlauskaite, J., Westlake, A. C. G., Wong, L.-L. & Hill, H. A. O. Direct electrochemistry of cytochrome P450cam. Chem. Commun. 1996, 2189–2190 (1996).

    Article  Google Scholar 

  156. Kazlauskaite, J., Hill, H. A. O., Wilkins, P. C. & Dalton, H. Direct electrochemistry of the hydroxylase of soluble methane monooxygenase from Methylococcus capsulatus (Bath). Eur. J. Biochem. 241, 552–556 (1996).

    Article  CAS  PubMed  Google Scholar 

  157. Reipa, V., Mayhew, M. P. & Vilker, V. L. A direct electrode-driven P450 cycle for biocatalysis. Proc. Natl Acad. Sci. USA 94, 13554–13558 (1997). A bioreactor where the reducing equivalent to the cycle is supplied to P450cam through putidaredoxin with an antimony-doped tin oxide working electrode.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Mayhew, M. P., Reipa, V., Holden, M. J. & Vilker, V. L. Improving the cytochrome P450 enzyme system for electrode‐driven biocatalysis of styrene epoxidation. Biotechnol. Prog. 16, 610–616 (2000).

    Article  CAS  PubMed  Google Scholar 

  159. Zhang, W. & Hollmann, F. Nonconventional regeneration of redox enzymes-a practical approach for organic synthesis? Chem. Comm. 54, 7281–7289 (2018).

    Article  CAS  PubMed  Google Scholar 

  160. Sturm-Richter, K. 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. 186, 89–96 (2015).

    Article  CAS  PubMed  Google Scholar 

  161. Mayr, J. C. et al. Resting Escherichia coli as chassis for microbial electrosynthesis: production of chiral alcohols. ChemSusChem 12, 1631–1634 (2019). Demonstrated microbial electrosynthesis using resting E. coli as a biocatalytic chassis for a production platform towards fine chemicals through electric power.

    Article  CAS  PubMed  Google Scholar 

  162. Ruinatscha, R., Dusny, C., Buehler, K. & Schmid, A. Productive asymmetric styrene epoxidation based on a next generation electroenzymatic methodology. Adv. Synth. Catal. 351, 2505–2515 (2009).

    Article  CAS  Google Scholar 

  163. Dixon, M. & Kleppe, K. D-amino acid oxidase II. Specificity, competitive inhibition and reaction sequence. Biochim. Biophys. Acta 96, 368–382 (1965).

    Article  CAS  Google Scholar 

  164. Kawabata, S., Iwata, N. & Yoneyama, H. Asymmetric electrosynthesis of amino acid using an electrode modified with amino acid oxidase and electron mediator. Chem. Lett. 29, 110–111 (2000).

    Article  Google Scholar 

  165. Toogood, H. S., Knaus, T. & Scrutton, N. S. Alternative hydride sources for ene‐reductases: current trends. ChemCatChem 6, 951–954 (2014).

    Article  CAS  Google Scholar 

  166. Simon, H., Günther, H., Bader, J. & Tischer, W. Electro-enzymatic and electro-microbial stereospecific reductions. Angew. Chem. Int. Ed. 20, 861–863 (1981).

    Article  Google Scholar 

  167. Dembitsky, V. M. Oxidation, epoxidation and sulfoxidation reactions catalysed by haloperoxidases. Tetrahedron 26, 4701–4720 (2003).

    Article  CAS  Google Scholar 

  168. Kohlmann, C. & Lütz, S. Electroenzymatic synthesis of chiral sulfoxides. Eng. Life Sci. 6, 170–174 (2006).

    Article  CAS  Google Scholar 

  169. Park, J. B. & Clark, D. S. Deactivation mechanisms of chloroperoxidase during biotransformations. Biotechnol. Bioeng. 93, 1190–1195 (2006).

    Article  CAS  PubMed  Google Scholar 

  170. Harnisch, F. & Urban, C. Electrobiorefineries: unlocking the synergy of electrochemical and microbial conversions. Angew. Chem. Int. Ed. 57, 10016–10023 (2018).

    Article  CAS  Google Scholar 

  171. Kumar, A. et al. The ins and outs of microorganism–electrode electron transfer reactions. Nat. Rev. Chem. 1, 0024 (2017).

    Article  CAS  Google Scholar 

  172. Matthiesen, J. E. et al. Electrochemical conversion of biologically produced muconic acid: key considerations for scale-up and corresponding technoeconomic analysis. ACS Sustain. Chem. Eng. 4, 7098–7109 (2016).

    Article  CAS  Google Scholar 

  173. Suastegui, M. et al. Combining metabolic engineering and electrocatalysis: Application to the production of polyamides from sugar. Angew. Chem. Int. Ed. 55, 2368–2373 (2016). This study reported a route that combines bio- and electrocatalysis to convert glucose into bio-based unsaturated nylon-6,6.

    Article  CAS  Google Scholar 

  174. Holzhäuser, F. J. et al. Electrocatalytic upgrading of itaconic acid to methylsuccinic acid using fermentation broth as a substrate solution. Green. Chem. 19, 2390–2397 (2017).

    Article  Google Scholar 

  175. Urban, C. et al. Production of drop-in fuels from biomass at high selectivity by combined microbial and electrochemical conversion. Energy Environ. Sci. 10, 2231–2244 (2017).

    Article  CAS  Google Scholar 

  176. Qian, D.-J. et al. Electrochemical hydrogen evolution by use of a glass carbon electrode sandwiched with clay, poly (butylviologen) and hydrogenase. Mater. Lett. 57, 1130–1134 (2003).

    Article  CAS  Google Scholar 

  177. Tatsumi, H., Takagi, K., Fujita, M., Kano, K. & Ikeda, T. Electrochemical study of reversible hydrogenase reaction of Desulfovibrio vulgaris cells with methyl viologen as an electron carrier. Anal. Chem. 71, 1753–1759 (1999).

    Article  CAS  PubMed  Google Scholar 

  178. Rozendal, R. A., Jeremiasse, A. W., Hamelers, H. V. & Buisman, C. J. Hydrogen production with a microbial biocathode. Environ. Sci. Technol. 42, 629–634 (2007).

    Article  CAS  Google Scholar 

  179. Nichols, E. M. et al. Hybrid bioinorganic approach to solar-to-chemical conversion. Proc. Natl Acad. Sci. USA 112, 11461–11466 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  180. Rodrigues, R. M. et al. Perfluorocarbon nanoemulsion promotes the delivery of reducing equivalents for electricity-driven microbial CO2 reduction. Nat. Catal. 2, 407 (2019). The introduction of a biocompatible perfluorocarbon nanoemulsion as a H 2 carrier increases the throughput of CO 2 reduction in this study.

    Article  CAS  Google Scholar 

  181. Torella, J. P. et al. Efficient solar-to-fuels production from a hybrid microbial-water-splitting catalyst system. Proc. Natl Acad. Sci. USA 112, 2337–2342 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  182. Liu, C., Colón, B. C., Ziesack, M., Silver, P. A. & Nocera, D. G. Water splitting-biosynthetic system with CO2 reduction efficiencies exceeding photosynthesis. Science 352, 1210–1213 (2016).

    Article  CAS  PubMed  Google Scholar 

  183. Li, H. et al. Integrated electromicrobial conversion of CO2 to higher alcohols. Science 335, 1596–1596 (2012).

    Article  CAS  PubMed  Google Scholar 

  184. Jayathilake, B. S., Bhattacharya, S., Vaidehi, N. & Narayanan, S. Efficient and selective electrochemically driven enzyme-catalyzed reduction of carbon dioxide to formate using formate dehydrogenase and an artificial cofactor. Acc. Chem. Res. 52, 676–685 (2019).

    Article  CAS  PubMed  Google Scholar 

  185. Choe, H. et al. Efficient CO2-reducing activity of NAD-dependent formate dehydrogenase from Thiobacillus sp. KNK65MA for formate production from CO2 gas. PLoS ONE 9, e103111 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Srikanth, S., Maesen, M., Dominguez-Benetton, X., Vanbroekhoven, K. & Pant, D. Enzymatic electrosynthesis of formate through CO2 sequestration/reduction in a bioelectrochemical system (BES). Bioresour. Technol. 165, 350–354 (2014).

    Article  CAS  PubMed  Google Scholar 

  187. Reda, T., Plugge, C. M., Abram, N. J. & Hirst, J. Reversible interconversion of carbon dioxide and formate by an electroactive enzyme. Proc. Natl Acad. Sci. USA 105, 10654–10658 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  188. Batlle-Vilanova, P. et al. Microbial electrosynthesis of butyrate from carbon dioxide: production and extraction. Bioelectrochemistry 117, 57–64 (2017).

    Article  CAS  PubMed  Google Scholar 

  189. Nevin, K. P. et al. Electrosynthesis of organic compounds from carbon dioxide is catalyzed by a diversity of acetogenic microorganisms. Appl. Environ. Microbiol. 77, 2882–2886 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  190. Nevin, K. P., Woodard, T. L., Franks, A. E., Summers, Z. M. & Lovley, D. R. Microbial electrosynthesis: feeding microbes electricity to convert carbon dioxide and water to multicarbon extracellular organic compounds. mBio 1, e00103-10 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  191. Bajracharya, S. et al. Long-term operation of microbial electrosynthesis cell reducing CO2 to multi-carbon chemicals with a mixed culture avoiding methanogenesis. Bioelectrochemistry 113, 26–34 (2017).

    Article  CAS  PubMed  Google Scholar 

  192. Rabaey, K. & Rozendal, R. A. Microbial electrosynthesis — revisiting the electrical route for microbial production. Nat. Rev. Microbiol. 8, 706 (2010).

    Article  CAS  PubMed  Google Scholar 

  193. Ganigué, R., Puig, S., Batlle-Vilanova, P., Balaguer, M. D. & Colprim, J. Microbial electrosynthesis of butyrate from carbon dioxide. Chem. Commun. 51, 3235–3238 (2015).

    Article  CAS  Google Scholar 

  194. Hu, B. et al. Electrocatalytic CO2 reduction catalyzed by nitrogenase MoFe and FeFe proteins. Bioelectrochemistry 120, 104–109 (2018).

    Article  CAS  PubMed  Google Scholar 

  195. Sciarria, T. P. et al. Bio-electrorecycling of carbon dioxide into bioplastics. Green. Chem. 20, 4058–4066 (2018).

    Article  Google Scholar 

  196. Suriyamongkol, P., Weselake, R., Narine, S., Moloney, M. & Shah, S. Biotechnological approaches for the production of polyhydroxyalkanoates in microorganisms and plants-a review. Biotechnol. Adv. 25, 148–175 (2007).

    Article  CAS  PubMed  Google Scholar 

  197. Pleissner, D. et al. Fermentative polyhydroxybutyrate production from a novel feedstock derived from bakery waste. BioMed. Res. Int. 8, 819474 (2014).

    Google Scholar 

  198. Colombo, B. et al. Enhanced polyhydroxyalkanoate (PHA) production from the organic fraction of municipal solid waste by using mixed microbial culture. Biotechnol. Biofuels 10, 201 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  199. Khalil, A. S. & Collins, J. J. Synthetic biology: applications come of age. Nat. Rev. Genet. 11, 367 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  200. Shi, T., Han, P., You, C. & Zhang, Y.-H. P. J. An in vitro synthetic biology platform for emerging industrial biomanufacturing: Bottom-up pathway design. Syst. Synth. Biol. 3, 186–195 (2018).

    Google Scholar 

  201. Zhang, Y.-H. P. Production of biofuels and biochemicals by in vitro synthetic biosystems: opportunities and challenges. Biotechnol. Adv. 33, 1467–1483 (2015).

    Article  CAS  PubMed  Google Scholar 

  202. Zhang, Y.-H. P. Simpler is better: high-yield and potential low-cost biofuels production through cell-free synthetic pathway biotransformation (SyPaB). ACS Catal. 1, 998–1009 (2011).

    Article  CAS  Google Scholar 

  203. Atsumi, S., Hanai, T. & Liao, J. C. Non-fermentative pathways for synthesis of branched-chain higher alcohols as biofuels. Nature 451, 86 (2008).

    Article  CAS  PubMed  Google Scholar 

  204. Yang, Y. et al. Enhancing bidirectional electron transfer of Shewanella oneidensis by a synthetic flavin pathway. ACS Synth. Biol. 4, 815–823 (2015).

    Article  CAS  PubMed  Google Scholar 

  205. Chen, X., Li, S. & Liu, L. Engineering redox balance through cofactor systems. Trends Biotechnol. 32, 337–343 (2014).

    Article  CAS  PubMed  Google Scholar 

  206. Wang, L. et al. Synthetic cofactor-linked metabolic circuits for selective energy transfer. ACS Catal. 7, 1977–1983 (2017).

    Article  CAS  Google Scholar 

  207. Wagoner, E. R. & Peters, D. G. Electrocatalytic reduction of 1,1,2-trichloro-1,2,2-trifluoroethane (CFC-113) at silver cathodes in organic and organic-aqueous solvents. J. Electrochem. Soc. 160, G135–G141 (2013).

    Article  CAS  Google Scholar 

  208. Höllrigl, V., Otto, K. & Schmid, A. Electroenzymatic asymmetric reduction of rac-3-methylcyclohexanone to (1S, 3S)-3-methylcyclohexanol in organic/aqueous media catalyzed by a thermophilic alcohol dehydrogenase. Adv. Synth. Catal. 349, 1337–1340 (2007).

    Article  CAS  Google Scholar 

  209. Enzmann, F., Stöckl, M., Zeng, A. P. & Holtmann, D. Same but different-Scale up and numbering up in electrobiotechnology and photobiotechnology. Eng. Life Sci. 19, 121–132 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  210. Rosa, L. F., Hunger, S., Gimkiewicz, C., Zehnsdorf, A. & Harnisch, F. Paving the way for bioelectrotechnology: Integrating electrochemistry into bioreactors. Eng. Life Sci. 17, 77–85 (2017).

    Article  CAS  PubMed  Google Scholar 

  211. Krieg, T. et al. in Bioelectrosynthesis 231–271 (Springer, 2018).

  212. Enzmann, F. et al. Transferring bioelectrochemical processes from H-cells to a scalable bubble column reactor. Chem. Eng. Sci. 193, 133–143 (2019).

    Article  CAS  Google Scholar 

  213. Oliveira, V., Simões, M., Melo, L. & Pinto, A. Overview on the developments of microbial fuel cells. Biochem. Eng. J. 73, 53–64 (2013).

    Article  CAS  Google Scholar 

  214. Enzmann, F. & Holtmann, D. Rational scale-up of a methane producing bioelectrochemical reactor to 50 L pilot scale. Chem. Eng. Sci. 207, 1148–1158 (2019). A scalable bubble column reactor was developed and further scaled-up to a 50 l pilot.

    Article  CAS  Google Scholar 

  215. Kitching, M., Butler, R. & Marsili, E. Microbial bioelectrosynthesis of hydrogen: current challenges and scale-up. Enzym. Microb. Technol. 96, 1–13 (2017).

    Article  CAS  Google Scholar 

  216. Cheng, S. & Logan, B. E. Increasing power generation for scaling up single-chamber air cathode microbial fuel cells. Bioresour. Technol. 102, 4468–4473 (2011).

    Article  CAS  PubMed  Google Scholar 

  217. Cusick, R. D. et al. Performance of a pilot-scale continuous flow microbial electrolysis cell fed winery wastewater. Appl. Microbiol. Biotechnol. 89, 2053–2063 (2011).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the Army Research Office MURI grant (W911NF1410263) and the National Science Foundation Center for Synthetic Organic Electrosynthesis for funding (CHE-1740656).

Author information

Authors and Affiliations

  1. Department of Chemistry, University of Utah, Salt Lake City, UT, USA

    Hui Chen, Fangyuan Dong & Shelley D. Minteer

  2. Department of Materials Science and Engineering, University of Utah, Salt Lake City, UT, USA

    Hui Chen, Fangyuan Dong & Shelley D. Minteer

Authors
  1. Hui Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fangyuan Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shelley D. Minteer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shelley D. Minteer.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, H., Dong, F. & Minteer, S.D. The progress and outlook of bioelectrocatalysis for the production of chemicals, fuels and materials. Nat Catal 3, 225–244 (2020). https://doi.org/10.1038/s41929-019-0408-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41929-019-0408-2

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing