Skip to content
Licensed Unlicensed Requires Authentication Published online by De Gruyter July 4, 2023

Microbial electrotechnology – Intensification of bioprocesses through the combination of electrochemistry and biotechnology

  • Markus Stöckl ORCID logo EMAIL logo , André Gemünde ORCID logo and Dirk Holtmann ORCID logo
From the journal Physical Sciences Reviews


Both biotechnological and electrochemical processes have economic and environmental significance. In particular, biotechnological processes are very specific and stable, while electrochemical processes are generally very atom-and energy-efficient. A combination of these processes is therefore a potentially important approach to intensify biotechnological processes. In this paper, the relevant options for process integration are presented, key performance indicators for quantitative evaluation are given, and an evaluation based on performance indicators is carried out using the example of the electrochemical reduction of CO2 to formate and the subsequent biotechnological conversion to the biopolymer polyhydroxybutyrate.

Corresponding author: Markus Stöckl, Sustainable Electrochemistry, DECHEMA Research Institute, Theodor-Heuss-Allee 25, 60486 Frankfurt am Main, Germany, E-mail:

Funding source: Bundesministerium fuer Bildung und Forschung

Award Identifier / Grant number: 33RC031A

Award Identifier / Grant number: 33RC031B

Funding source: Deutsche Forschungsgemeinschaft

Award Identifier / Grant number: 422694804


The authors would like to thank the editor for their guidance and review of this article before its publication.

  1. Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: AG and DH thank the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) for funding the project “Bioelectrochemical and engineering fundamentals to establish electro-biotechnology for biosynthesis – Power to value-added products (eBiotech)”– project number 422694804 and Bundesministerium fuer Bildung und Forschung (33RC031A, 33RC031A).

  3. Conflict of interest statement: The authors declare no conflicts of interest regarding this article.


1. Scott, K. Process intensification: an electrochemical perspective. Renew Sustain Energy Rev 2018;81:1406–26. in Google Scholar

2. Krieg, T, Sydow, A, Schröder, U, Schrader, J, Holtmann, D. Reactor concepts for bioelectrochemical syntheses and energy conversion. Trends Biotechnol 2014;32:645–55. in Google Scholar PubMed

3. Harnisch, F, Urban, C. Electrobiorefineries: unlocking the synergy of electrochemical and microbial conversions. Angew Chem Int Ed 2018;57:10016–23. in Google Scholar PubMed

4. Fruehauf, HM, Enzmann, F, Harnisch, F, Ulber, R, Holtmann, D. Microbial electrosynthesis—an inventory on technology readiness level and performance of different process variants. Biotechnol J 2020;15:2000066. in Google Scholar PubMed

5. Stöckl, M, Claassens, N, Lindner, S, Klemm, E, Holtmann, D. Coupling electrochemical CO2 reduction to microbial product generation – identification of the gaps and opportunities. Curr Opin Biotechnol 2022;74:154–63. in Google Scholar PubMed

6. Gizewski, J, Sande, Lv.d., Holtmann, D. Contribution of electrobiotechnology to sustainable development goals. Trends Biotechnol 2023. in Google Scholar PubMed

7. Lovley, DR, Phillips, EJ. Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl Environ Microbiol 1988;54:1472–80. in Google Scholar PubMed PubMed Central

8. Lovley, DR, Giovannoni, SJ, White, DC, Champine, JE, Phillips, EJP, Gorby, YA, et al.. Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Arch Microbiol 1993;159:336–44. in Google Scholar

9. Hau, HH, Gilbert, A, Coursolle, D, Gralnick, JA. Mechanism and Consequences of anaerobic respiration of cobalt by Shewanella oneidensis strain MR-1. Appl Environ Microbiol 2008;74:6880–6. in Google Scholar

10. Sand, W, Rohde, K, Sobotke, B, Zenneck, C. Evaluation of Leptospirillum ferrooxidans for leaching. Appl Environ Microbiol 1992;58:85–92. in Google Scholar PubMed PubMed Central

11. Schippers, A, Jozsa, P, Sand, W. Sulfur chemistry in bacterial leaching of pyrite. Appl Environ Microbiol 1996;62:3424–31. in Google Scholar PubMed PubMed Central

12. Rohwerder, T, Gehrke, T, Kinzler, K, Sand, W. Bioleaching review part A: progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation. Appl Microbiol Biotechnol 2003;63:239–48. in Google Scholar PubMed

13. Carbajosa, S, Malki, M, Caillard, R, Lopez, MF, Palomares, FJ, Martín-Gago, JA, et al.. Electrochemical growth of Acidithiobacillus ferrooxidans on a graphite electrode for obtaining a biocathode for direct electrocatalytic reduction of oxygen. Biosens Bioelectron 2010;26:877–80. in Google Scholar PubMed

14. Tremblay, PL, Zhang, T. Electrifying microbes for the production of chemicals. Front Microbiol 2015;6:201. in Google Scholar PubMed PubMed Central

15. Logan, BE, Murano, C, Scott, K, Gray, ND, Head, IM. Electricity generation from cysteine in a microbial fuel cell. Water Res 2005;39:942–52. in Google Scholar PubMed

16. Marsili, E, Baron, DB, Shikhare, ID, Coursolle, D, Gralnick, JA, Bond, DR. Shewanella secretes flavins that mediate extracellular electron transfer. Proc Natl Acad Sci U S A 2008;105:3968–73. in Google Scholar PubMed PubMed Central

17. Bond, DR, Holmes, DE, Tender, LM, Lovley, DR. Electrode-reducing microorganisms that harvest energy from marine sediments. Science 2002;295:483–5. in Google Scholar PubMed

18. Lovley, DR. Powering microbes with electricity: direct electron transfer from electrodes to microbes. Environ Microbiol Rep 2011;3:27–35. in Google Scholar PubMed

19. Nevin, KP, Hensley, SA, Franks, AE, Summers, ZM, Ou, J, Woodard, TL, et al.. Electrosynthesis of organic compounds from carbon dioxide is catalyzed by a diversity of acetogenic microorganisms. Appl Environ Microbiol 2011;77:2882–6. in Google Scholar

20. Nevin, K, Woodard, T, Franks, A, Summers, Z, Lovley, D. Microbial electrosynthesis: feeding microbes electricity to convert carbon dioxide and water to multicarbon extracellular organic compounds. mBio 2010;1:1–4. in Google Scholar

21. Bird, LJ, Kundu, BB, Tschirhart, T, Corts, AD, Su, L, Gralnick, JA, et al.. Engineering wired life: synthetic biology for electroactive bacteria. ACS Synth Biol 2021;10:2808–23. in Google Scholar PubMed

22. Sydow, A, Krieg, T, Mayer, F, Schrader, J, Holtmann, D. Electroactive bacteria—molecular mechanisms and genetic tools. Appl Microbiol Biotechnol 2014;98:8481–95. in Google Scholar PubMed

23. Karthikeyan, R, Singh, R, Bose, A. Microbial electron uptake in microbial electrosynthesis: a mini-review. J Ind Microbiol Biotechnol 2019;46:1419–26. in Google Scholar PubMed

24. Strycharz, SM, Glaven, RH, Coppi, MV, Gannon, SM, Perpetua, LA, Liu, A, et al.. Gene expression and deletion analysis of mechanisms for electron transfer from electrodes to Geobacter sulfurreducens. Bioelectrochemistry 2011;80:142–50. in Google Scholar PubMed

25. Holmes, DE, Chaudhuri, SK, Nevin, KP, Mehta, T, Methe, BA, Liu, A, et al.. Microarray and genetic analysis of electron transfer to electrodes in Geobacter sulfurreducens. Environ Microbiol 2006;8:1805–15. in Google Scholar PubMed

26. Bond, DR, Lovley, DR. Electricity production by Geobacter sulfurreducens attached to electrodes. Appl Environ Microbiol 2003;69:1548–55. in Google Scholar PubMed PubMed Central

27. Stöckl, M, Teubner, NC, Holtmann, D, Mangold, KM, Sand, W. Extracellular polymeric substances from geobacter sulfurreducens biofilms in microbial fuel cells. ACS Appl Mater Interfaces 2019;11:8961–8. in Google Scholar PubMed

28. Frühauf, HM, Holtmann, D, Stöckl, M. Influence of electrode surface charge on current production by Geobacter sulfurreducens microbial anodes. Bioelectrochemistry 2022;147:108213. in Google Scholar PubMed

29. Engel, M, Gemünde, A, Holtmann, D, Müller-Renno, C, Ziegler, C, Tippkötter, N, et al.. Clostridium acetobutylicum’s connecting world: cell appendage formation in bioelectrochemical systems. Chemelectrochem 2020;7:414–20. in Google Scholar

30. Carmona-Martinez, AA, Harnisch, F, Fitzgerald, LA, Biffinger, JC, Ringeisen, BR, Schröder, U. Cyclic voltammetric analysis of the electron transfer of Shewanella oneidensis MR-1 and nanofilament and cytochrome knock-out mutants. Bioelectrochemistry 2011;81:74–80. in Google Scholar PubMed

31. Krieg, T, Phan, LMP, Wood, JA, Sydow, A, Vassilev, I, Krömer, JO, et al.. Characterization of a membrane-separated and a membrane-less electrobioreactor for bioelectrochemical syntheses. Biotechnol Bioeng 2018;115:1705–16. in Google Scholar PubMed

32. Stöckl, M, Schlegel, C, Sydow, A, Holtmann, D, Ulber, R, Mangold, KM. Membrane separated flow cell for parallelized electrochemical impedance spectroscopy and confocal laser scanning microscopy to characterize electro-active microorganisms. Electrochim Acta 2016;220:444–52. in Google Scholar

33. Arinda, T, Philipp, LA, Rehnlund, D, Edel, M, Chodorski, J, Stöckl, M, et al.. Addition of riboflavin-coupled magnetic beads increases current production in bioelectrochemical systems via the increased formation of anode-biofilms. Front Microbiol 2019;10:1–8. in Google Scholar PubMed PubMed Central

34. Rabaey, K, Boon, N, Siciliano, SD, Verhaege, M, Verstraete, W. Biofuel cells select for microbial consortia that self-mediate electron transfer. Appl Environ Microbiol 2004;70:5373–82. in Google Scholar PubMed PubMed Central

35. Saunders, SH, Tse, EC, Yates, MD, Otero, FJ, Trammell, SA, Stemp, ED, et al.. Extracellular DNA promotes efficient extracellular electron transfer by pyocyanin in Pseudomonas aeruginosa biofilms. Cell 2020;182:919–32.e19. in Google Scholar PubMed PubMed Central

36. Bosire, EM, Rosenbaum, MA. Electrochemical potential influences phenazine production, electron transfer and consequently electric current generation by Pseudomonas aeruginosa. Front Microbiol 2017;8:1–11. in Google Scholar PubMed PubMed Central

37. Schmitz, S, Nies, S, Wierckx, N, Blank, LM, Rosenbaum, MA. Engineering mediator-based electroactivity in the obligate aerobic bacterium Pseudomonas putida KT2440. Front Microbiol 2015;6:1–13. in Google Scholar PubMed PubMed Central

38. Hintermayer, S, Yu, S, Krömer, JO, Weuster-Botz, D. Anodic respiration of Pseudomonas putida KT2440 in a stirred-tank bioreactor. Biochem Eng J 2016;115:1–13. in Google Scholar

39. Lai, B, Yu, S, Bernhardt, PV, Rabaey, K, Virdis, B, Krömer, JO. Anoxic metabolism and biochemical production in Pseudomonas putida F1 driven by a bioelectrochemical system. Biotechnol Biofuels 2016;9:39. in Google Scholar PubMed PubMed Central

40. Vassilev, I, Gießelmann, G, Schwechheimer, SK, Wittmann, C, Virdis, B, Krömer, JO. Anodic electro-fermentation: anaerobic production of L-Lysine by recombinant Corynebacterium glutamicum. Biotechnol Bioeng 2018;115:1499–508. in Google Scholar PubMed

41. Gemünde, A, Gail, J, Holtmann, D. Anodic respiration of Vibrio natriegens in a bioelectrochemical system. ChemSusChem 2023:e202300181. in Google Scholar PubMed

42. Stöckl, M, Harms, S, Dinges, I, Dimitrova, S, Holtmann, D. From CO2 to bioplastic – coupling the electrochemical CO2 reduction with a microbial product generation by drop-in electrolysis. ChemSusChem 2020;13:4086–93. in Google Scholar PubMed PubMed Central

43. Krieg, T, Sydow, A, Faust, S, Huth, I, Holtmann, D. CO2 to terpenes: autotrophic and electroautotrophic α-humulene production with Cupriavidus necator. Angew Chem Int Ed 2018;57:1879–82. in Google Scholar PubMed

44. Li, H, Opgenorth, PH, Wernick, DG, Rogers, S, Wu, TY, Higashide, W, et al.. Integrated electromicrobial conversion of CO2 to higher alcohols. Science 2012;335:1596. in Google Scholar PubMed

45. Teetz, N, Holtmann, D, Harnisch, F, Stöckl, M. Upgrading Kolbe electrolysis—highly efficient production of green fuels and solvents by coupling biosynthesis and electrosynthesis. Angew Chem Int Ed 2022;61:e202210596. in Google Scholar

46. Hegner, R, Neubert, K, Kroner, C, Holtmann, D, Harnisch, F. Coupled electrochemical and microbial catalysis for the production of polymer bricks. ChemSusChem 2020;13:5295–300. in Google Scholar PubMed PubMed Central

47. Im, C, Valgepea, K, Modin, O, Nygård, Y. Clostridium ljungdahlii as a biocatalyst in microbial electrosynthesis – effect of culture conditions on product formation. Bioresour Technol Rep 2022;19:101156. in Google Scholar

48. Ueki, T. Cytochromes in extracellular electron transfer in geobacter. Appl Environ Microbiol 2021;87:1–16. in Google Scholar

49. Madjarov, J, Soares, R, Paquete, CM, Louro, RO. Sporomusa ovata as catalyst for bioelectrochemical carbon dioxide reduction: a review across disciplines from microbiology to process engineering. Front Microbiol 2022;13:913311. in Google Scholar PubMed PubMed Central

50. Gemünde, A, Lai, B, Pause, L, Krömer, J, Holtmann, D. Redox mediators in microbial electrochemical systems. Chemelectrochem 2022;9:e202200216. in Google Scholar

51. Vassilev, I, Averesch, NJ, Ledezma, P, Kokko, M. Anodic electro-fermentation: empowering anaerobic production processes via anodic respiration. Biotechnol Adv 2021;48:107728. in Google Scholar PubMed

52. Stöckl, M, Lange, T, Izadi, P, Bolat, S, Teetz, N, Harnisch, F, et al.. Application of gas diffusion electrodes in bioeconomy: an update. Biotechnol Bioeng 2023;120:1465–77. in Google Scholar PubMed

53. Potter, MC. Electrical effects accompanying the decomposition of organic compounds. Proc R Soc Lond – Ser B Contain Pap a Biol Character 1911;84:260–76.10.1098/rspb.1911.0073Search in Google Scholar

54. Hiegemann, H, Herzer, D, Nettmann, E, Lübken, M, Schulte, P, Schmelz, KG, et al.. An integrated 45L pilot microbial fuel cell system at a full-scale wastewater treatment plant. Bioresour Technol 2016;218:115–22. in Google Scholar PubMed

55. Hiegemann, H, Littfinski, T, Krimmler, S, Lübken, M, Klein, D, Schmelz, KG, et al.. Performance and inorganic fouling of a submergible 255 L prototype microbial fuel cell module during continuous long-term operation with real municipal wastewater under practical conditions. Bioresour Technol 2019;294:122227. in Google Scholar PubMed

56. Krieg, T, Mayer, F, Sell, D, Holtmann, D. Insights into the applicability of microbial fuel cells in wastewater treatment plants for a sustainable generation of electricity. Environ Technol 2019;40:1101–9. in Google Scholar PubMed

57. Kim, TS, Kim, BH. Electron flow shift in Clostridium acetobutylicum fermentation by electrochemically introduced reducing equivalent. Biotechnol Lett 1988;10:123–8. in Google Scholar

58. Emde, R, Schink, B. Enhanced propionate formation by Propionibacterium freudenreichii subsp. freudenreichii in a three-electrode amperometric culture system. Appl Environ Microbiol 1990;56:2771–6. in Google Scholar PubMed PubMed Central

59. Cheng, S, Xing, D, Call, DF, Logan, BE. Direct biological conversion of electric current into methane by electromethanogenesis. Environ Sci Technol 2009;43:3953–8. in Google Scholar PubMed

60. Villano, M, Aulenta, F, Ciucci, C, Ferri, T, Giuliano, A, Majone, M. Bioelectrochemical reduction of CO2 to CH4 via direct and indirect extracellular electron transfer by a hydrogenophilic methanogenic culture. Bioresour Technol 2010;101:3085–90. in Google Scholar PubMed

61. Beese-Vasbender, PF, Grote, JP, Garrelfs, J, Stratmann, M, Mayrhofer, KJ. Selective microbial electrosynthesis of methane by a pure culture of a marine lithoautotrophic archaeon. Bioelectrochemistry 2015;102:50–5. in Google Scholar PubMed

62. Schievano, A, Pepé Sciarria, T, Vanbroekhoven, K, De Wever, H, Puig, S, Andersen, SJ, et al.. Electro-fermentation – merging electrochemistry with fermentation in industrial applications. Trends Biotechnol 2016;34:866–78. in Google Scholar PubMed

63. Moscoviz, R, Toledo-Alarcón, J, Trably, E, Bernet, N. Electro-fermentation: how to drive fermentation using electrochemical systems. Trends Biotechnol 2016;34:856–65. in Google Scholar PubMed

64. Yamada, S, Takamatsu, Y, Ikeda, S, Kouzuma, A, Watanabe, K. Towards application of electro-fermentation for the production of value-added chemicals from biomass feedstocks. Front Chem 2021;9:805597. in Google Scholar PubMed PubMed Central

65. Rousseau, R, Etcheverry, L, Roubaud, E, Basséguy, R, Délia, ML, Bergel, A. Microbial electrolysis cell (MEC): strengths, weaknesses and research needs from electrochemical engineering standpoint. Appl Energy 2020;257:113938. in Google Scholar

66. Saravanan, A, Karishma, S, Senthil Kumar, P, Yaashikaa, P, Jeevantantham, S, Gayathri, B. Microbial electrolysis cells and microbial fuel cells for biohydrogen production: current advances and emerging challenges. Biomass Conv Bioref 2020;1–21. in Google Scholar

67. Haas, T, Krause, R, Weber, R, Demler, M, Schmid, G. Technical photosynthesis involving CO2 electrolysis and fermentation. Nat Catal 2018;1:32–9. in Google Scholar

68. Enzmann, F, Stöckl, M, Pfitzer, M, Holtmann, D. Empower C1: combination of electrochemistry and biology to convert C1 compounds. In: Zeng, AP, Claassens, NJ, editors. One-carbon feedstocks for sustainable bioproduction. Cham: Springer International Publishing; 2022:213–41 pp.10.1007/10_2021_171Search in Google Scholar PubMed

69. Enzmann, F, Stöckl, M, Zeng, AP, Holtmann, D. Same but different-Scale up and numbering up in electrobiotechnology and photobiotechnology. Eng Life Sci 2019;19:121–32. in Google Scholar PubMed PubMed Central

70. Urban, C, Xu, J, Sträuber, H, dos Santos Dantas, TR, Mühlenberg, J, Härtig, C, et al.. Production of drop-in fuels from biomass at high selectivity by combined microbial and electrochemical conversion. Energy Environ Sci 2017;10:2231–44. in Google Scholar

71. Suastegui, M, Matthiesen, JE, Carraher, JM, Hernandez, N, Rodriguez Quiroz, N, Okerlund, A, et al.. Combining metabolic engineering and electrocatalysis: application to the production of polyamides from sugar. Angew Chem Int Ed 2016;55:2368–73. in Google Scholar PubMed

72. Holzhäuser, FJ, Artz, J, Palkovits, S, Kreyenschulte, D, Büchs, J, Palkovits, R. Electrocatalytic upgrading of itaconic acid to methylsuccinic acid using fermentation broth as a substrate solution. Green Chem 2017;19:2390–7. in Google Scholar

73. He, L, Du, P, Chen, Y, Lu, H, Cheng, X, Chang, B, et al.. Advances in microbial fuel cells for wastewater treatment. Renew Sustain Energy Rev 2017;71:388–403. in Google Scholar

74. Krieg, T, Madjarov, J, Rosa, L, Enzmann, F, Harnisch, F, Holtmann, D, et al.. Reactors for microbial electrobiotechnology. In: Harnisch, F, Holtmann, D, editors. Bioelectrosynthesis. Cham: Springer International Publishing; 2019:231–71 pp.10.1007/10_2017_40Search in Google Scholar PubMed

75. Enzmann, F, Gronemeier, D, Holtmann, D. Evaluation of bioelectromethanogenesis part I: energy calculations. Chem Ing Tech 2020;92:137–43. in Google Scholar

76. Logan, BE, Hamelers, B, Rozendal, R, Schröder, U, Keller, J, Freguia, S, et al.. Microbial fuel cells: methodology and technology. Environ Sci Technol 2006;40:5181–92. in Google Scholar PubMed

77. Jeremiasse, AW, Hamelers, HV, Croese, E, Buisman, CJ. Acetate enhances startup of a H2-producing microbial biocathode. Biotechnol Bioeng 2012;109:657–64. in Google Scholar PubMed

78. Seelajaroen, H, Spiess, S, Haberbauer, M, Hassel, MM, Aljabour, A, Thallner, S, et al.. Enhanced methane producing microbial electrolysis cells for wastewater treatment using poly(neutral red) and chitosan modified electrodes. Sustain Energy Fuels 2020;4:4238–48. in Google Scholar

79. Okamoto, A, Hashimoto, K, Nealson, KH, Nakamura, R. Rate enhancement of bacterial extracellular electron transport involves bound flavin semiquinones. Proc Natl Acad Sci U S A 2013;110:7856–61. in Google Scholar PubMed PubMed Central

80. Modin, O, Gustavsson, DJ. Opportunities for microbial electrochemistry in municipal wastewater treatment-an overview. Water Sci Technol 2014;69:1359–72. in Google Scholar PubMed

81. Vlaeminck, E, Quataert, K, Uitterhaegen, E, De Winter, K, Soetaert, WK. Advanced PHB fermentation strategies with CO2-derived organic acids. J Biotechnol 2022;343:102–9. in Google Scholar PubMed

82. Claassens, NJ, Bordanaba-Florit, G, Cotton, CA, De Maria, A, Finger-Bou, M, Friedeheim, L, et al.. Replacing the Calvin cycle with the reductive glycine pathway in Cupriavidus necator. Metab Eng 2020;62:30–41. in Google Scholar PubMed

Received: 2023-06-12
Accepted: 2023-06-15
Published Online: 2023-07-04

© 2023 Walter de Gruyter GmbH, Berlin/Boston

Downloaded on 2.12.2023 from
Scroll to top button