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:

Electroactive microorganisms in bioelectrochemical systems

Nature Reviews Microbiology volume 17, pages 307–319 (2019)Cite this article

Subjects

Abstract

A vast array of microorganisms from all three domains of life can produce electrical current and transfer electrons to the anodes of different types of bioelectrochemical systems. These exoelectrogens are typically iron-reducing bacteria, such as Geobacter sulfurreducens, that produce high power densities at moderate temperatures. With the right media and growth conditions, many other microorganisms ranging from common yeasts to extremophiles such as hyperthermophilic archaea can also generate high current densities. Electrotrophic microorganisms that grow by using electrons derived from the cathode are less diverse and have no common or prototypical traits, and current densities are usually well below those reported for model exoelectrogens. However, electrotrophic microorganisms can use diverse terminal electron acceptors for cell respiration, including carbon dioxide, enabling a variety of novel cathode-driven reactions. The impressive diversity of electroactive microorganisms and the conditions in which they function provide new opportunities for electrochemical devices, such as microbial fuel cells that generate electricity or microbial electrolysis cells that produce hydrogen or methane.

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: Components of microbial fuel cells and other bioelectrochemical systems.
Fig. 2: Diversity of exoelectrogenic and electrotrophic microorganisms.
Fig. 3: Current production by exoelectrogenic microorganisms.
Fig. 4: Current consumption by electrotrophic microorganisms.
Fig. 5: Direct interspecies electron transfer between microorganisms.

Similar content being viewed by others

References

  1. Potter, M. C. Electrical effects accompanying the decomposition of organic compounds. Proc. R. Soc. Lond. B Biol. Sci. 84, 260–276 (1911).

    Google Scholar 

  2. Logan, B. E. Microbial Fuel Cells (John Wiley & Sons, Inc., 2008).

  3. Logan, B. E. & Rabaey, K. Conversion of wastes into bioelectricity and chemicals using microbial electrochemical technologies. Science 337, 686–690 (2012).

    CAS  PubMed  Google Scholar 

  4. Myers, J. M. & Myers, C. R. Role for outer membrane cytochromes OmcA and OmcB of Shewanella putrefaciens MR-1 in reduction of manganese dioxide. Appl. Environ. Microbiol. 67, 260–269 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  5. El-Naggar, M. Y. et al. Electrical transport along bacterial nanowires from Shewanella oneidensis MR-1. Proc. Nat. Acad. Sci. USA 107, 18127–18131 (2010).

    CAS  PubMed  Google Scholar 

  6. Pirbadian, S. et al. Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components. Proc. Nat. Acad. Sci. 111, 12883–12888 (2014).

    CAS  PubMed  Google Scholar 

  7. von Canstein, H., Ogawa, J., Shimizu, S. & Lloyd, J. R. Secretion of flavins by Shewanella species and their role in extracellular electron transfer. Appl. Environ. Microbiol. 74, 615–623 (2008).

    Google Scholar 

  8. Xu, S., Jangir, Y. & El-Naggar, M. Y. Disentangling the roles of free and cytochrome-bound flavins in extracellular electron transport from Shewanella oneidensis MR-1. Electrochim. Acta 198, 49–55 (2016).

    CAS  Google Scholar 

  9. Lovley, D. R. Syntrophy goes electric: direct interspecies electron transfer. Annu. Rev. Microbiol. 71, 643–664 (2017).

    CAS  Google Scholar 

  10. Lovley, D. R. Happy together: microbial communities that hook up to swap electrons. ISME J. 11, 327–336 (2017).

    CAS  PubMed  Google Scholar 

  11. Light, S. H. et al. A flavin-based extracellular electron transfer mechanism in diverse Gram-positive bacteria. Nature 562, 140–144 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Reguera, G. Harnessing the power of microbial nanowires. Microb. Biotechnol. 11, 979–994 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Wang, Z., Cao, C., Zheng, Y., Chen, S. & Zhao, F. Abiotic oxygen reduction reaction catalysts used in microbial fuel cells. ChemElectroChem 1, 1813–1821 (2014).

    CAS  Google Scholar 

  14. Bond, D. R. & Lovley, D. R. Electricity production by Geobacter sulfurreducens attached to electrodes. Appl. Environ. Microbiol. 69, 1548–1555 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Bretschger, O. et al. Current production and metal oxide reduction by Shewanella oneidensis MR-1 wild type and mutants. Appl. Environ. Microbiol. 73, 7003–7012 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Koch, C. & Harnisch, F. Is there a specific ecological niche for electroactive microorganisms? ChemElectroChem 3, 1282–1295 (2016).

    CAS  Google Scholar 

  17. Yang, W., Kim, K.-Y., Saikaly, P. E. & Logan, B. E. The impact of new cathode materials relative to baseline performance of microbial fuel cells all with the same architecture and solution chemistry. Energy Environ. Sci. 10, 1025–1033 (2017).

    CAS  Google Scholar 

  18. Qu, Y., Feng, Y., Wang, X. & Logan, B. E. Use of a coculture to enable current production by Geobacter sulfurreducens. Appl. Environ. Microbiol. 78, 3484–3487 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Oh, S. & Logan, B. E. Proton exchange membrane and electrode surface areas as factors that affect power generation in microbial fuel cells. Appl. Microbiol. Biotechnol. 70, 162–169 (2006). This paper addresses how power densities can vary depending on relative electrode sizes and the membrane cross-sectional area in two-chamber MFCs.

    CAS  PubMed  Google Scholar 

  20. Yang, W. & Logan, B. E. Immobilization of a metal–nitrogen–carbon catalyst on activated carbon with enhanced cathode performance in microbial fuel cells. ChemSusChem 9, 2226–2232 (2016). This paper demonstrates high power densities using activated carbon air cathodes.

    CAS  PubMed  Google Scholar 

  21. Oliot, M. et al. Separator electrode assembly (SEA) with 3-dimensional bioanode and removable air-cathode boosts microbial fuel cell performance. J. Power Sources 356, 389–399 (2017). This paper demonstrates the highest power density for electrodes with equal projected surface area.

    CAS  Google Scholar 

  22. Liang, P., Huang, X., Fan, M.-Z., Cao, X.-X. & Wang, C. Composition and distribution of internal resistance in three types of microbial fuel cells. Appl. Microbiol. Biotechnol. 77, 551–558 (2007).

    CAS  PubMed  Google Scholar 

  23. Holmes, D. E. et al. Microbial communities associated with electrodes harvesting electricity from a variety of aquatic sediments. Microb. Ecol. 48, 178–190 (2004). This is an analysis of the communities in a variety of sediments from natural system.

    CAS  PubMed  Google Scholar 

  24. Kiely, P. D., Regan, J. M. & Logan, B. E. The electric picnic: synergistic requirements for exoelectrogenic microbial communities. Curr. Opin. Biotechnol. 22, 378–385 (2011).

    CAS  PubMed  Google Scholar 

  25. Lovley, D. R. Bug juice: harvesting electricity with microorganisms. Nat. Rev. Microbiol. 4, 497–508 (2006).

    CAS  PubMed  Google Scholar 

  26. Kiely, P. D., Rader, G., Regan, J. M. & Logan, B. E. Long-term cathode performance and the microbial communities that develop in microbial fuel cells fed different fermentation endproducts. Bioresour. Technol. 102, 361–366 (2011).

    CAS  PubMed  Google Scholar 

  27. Kiely, P. D. et al. Anode microbial communities produced by changing from microbial fuel cell to microbial electrolysis cell operation using two different wastewaters. Bioresour. Technol. 102, 388–394 (2011).

    CAS  PubMed  Google Scholar 

  28. Yi, H. et al. Selection of a variant of Geobacter sulfurreducens with enhanced capacity for current production in microbial fuel cells. Biosens. Bioelectron. 24, 3498–3503 (2009).

    CAS  PubMed  Google Scholar 

  29. Ringeisen, B. R. et al. High power density from a miniature microbial fuel cell using Shewanella oneidensis DSP10. Environ. Sci. Technol. 40, 2629–2634 (2006).

    CAS  PubMed  Google Scholar 

  30. Rosenbaum, M., Cotta, M. A. & Angenent, L. T. Aerated Shewanella oneidensis in continuously fed bioelectrochemical systems for power and hydrogen production. Biotechnol. Bioeng. 105, 880–888 (2009).

    Google Scholar 

  31. Watson, V. J. & Logan, B. E. Power production in MFCs inoculated with Shewanella oneidensis MR-1 or mixed cultures. Biotechnol. Bioeng. 105, 489–498 (2010).

    CAS  PubMed  Google Scholar 

  32. Gorby, Y. A. et al. Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. Proc. Natl Acad. Sci. USA 103, 11358–11363 (2006). This is the first published report on conductive appendages of the Shewanella genus.

    CAS  PubMed  Google Scholar 

  33. Subramanian, P., Pirbadian, S., El-Naggar, M. Y. & Jensen, G. J. Ultrastructure of Shewanella oneidensis MR-1 nanowires revealed by electron cryotomography. Proc. Natl Acad. Sci. USA 115, E3246–E3255 (2018). This paper provides a clear description of the appendages produced by Shewanella oneidensis MR-1.

    CAS  PubMed  Google Scholar 

  34. Reguera, G. et al. Extracellular electron transfer via microbial nanowires. Nature 435, 1098–1101 (2005). This is the first description of conductive pili produced by Geobacter sp.

    CAS  PubMed  Google Scholar 

  35. Myers, C. R. & Myers, J. M. Localization of cytochromes to the outer membrane of anaerobically grown Shewanella putrefaciens MR-1. J. Bacteriol. 174, 3429–3438 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Marsili, E. et al. Shewanella secretes flavins that mediate extracellular electron transfer. Proc. Natl Acad. Sci. USA 105, 3968–3973 (2008).

    CAS  PubMed  Google Scholar 

  37. Call, D. F. & Logan, B. E. Lactate oxidation coupled to iron or electrode reduction by Geobacter sulfurreducens PCA. Appl. Environ. Microbiol. 77, 8791–8794 (2011). This paper provides a direct comparison of current production of G. sulfurreducens and S. oneidensis using the same substrate.

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Hunt, K. A., Flynn, J. M., Naranjo, B. n., Shikhare, I. D. & Gralnick, J. A. Substrate-Level phosphorylation is the primary source of energy conservation during anaerobic respiration of Shewanella oneidensis strain MR-1. J. Bacteriol. 192, 3345–3351 (2010). This paper provides a clear explanation of the basis for current generation by a Shewanella species.

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Yang, L. et al. Boosting current generation in microbial fuel cells by an order of magnitude by coating an ionic liquid polymer on carbon anodes. Biosens. Bioelectron. 91, 644–649 (2017).

    CAS  PubMed  Google Scholar 

  40. Monteverde, D. R. et al. Distribution of extracellular flavins in a coastal marine basin and their relationship to redox gradients and microbial community members. Environ. Sci. Technol. 52, 12265–12274 (2018).

    CAS  Google Scholar 

  41. Cao, X., Huang, X., Zhang, X., Liang, P. & Fan, M. A mini-microbial fuel cell for voltage testing of exoelectrogenic bacteria. Front. Environ. Sci. Eng. 3, 307–312 (2009).

    CAS  Google Scholar 

  42. Li, H. et al. Power output of microbial fuel cell emphasizing interaction of anodic binder with bacteria. J. Power Sources 379, 115–122 (2018).

    CAS  Google Scholar 

  43. Doyle, L. E. & Marsili, E. Weak electricigens: a new avenue for bioelectrochemical research. Bioresour. Technol. 258, 354–364 (2018).

    CAS  PubMed  Google Scholar 

  44. Rabaey, K., Lissens, G., Siciliano, S. D. & Verstraete, W. A microbial fuel cell capable of converting glucose to electricity at high rate and efficiency. Biotechnol. Lett. 25, 1531–1535 (2003).

    CAS  PubMed  Google Scholar 

  45. Rabaey, K., Boon, N., Siciliano, S. D., Verhaege, M. & Verstraete, W. Biofuel cells select for microbial consortia that self-mediate electron transfer. Appl. Environ. Microbiol. 70, 5373–5382 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Rabaey, K., Boon, N., Hofte, M. & Verstraete, W. Microbial phenazine production enhances electron transfer in biofuel cells. Environ. Sci. Technol. 39, 3401–3408 (2005). This paper demonstrates the role of phenazines for mediating electron transfer.

    CAS  PubMed  Google Scholar 

  47. Pham, T. H. et al. Metabolites produced by Pseudomonas sp. enable a Gram positive bacterium to achieve extracellular electron transfer. Appl. Microbiol. Biotechnol. 77, 1119–1129 (2008).

    CAS  PubMed  Google Scholar 

  48. Kiely, P. D., Call, D. F., Yates, M. D., Regan, J. R. & Logan, B. E. Anodic biofilms in microbial fuel cells harbor low numbers of higher-power producing bacteria than abundant genera. Appl. Microbiol. Biotechnol. 88, 371–380 (2010).

    CAS  PubMed  Google Scholar 

  49. Zhang, T. et al. A novel mediatorless microbial fuel cell based on biocatalysis of Escherichia coli. Chem. Commun. (Camb.) 21, 2257–2259 (2006).

    Google Scholar 

  50. Sayed, E. T., Saito, Y., Tsujiguchi, T. & Nakagawa, N. Catalytic activity of yeast extract in biofuel cell. J. Biosci. Bioeng. 114, 521–525 (2012).

    CAS  PubMed  Google Scholar 

  51. Holmes, D. E., Nicoll, J. S., Bond, D. R. & Lovley, D. R. Potential role of a novel psychrotolerant member of the family Geobacteraceae, Geopsychrobacter electrodiphilus gen. nov., sp. nov., in electricity production by a marine sediment fuel cell. Appl. Environ. Microbiol. 70, 6023–6030 (2004); erratum 75, 885 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Logan, B. E. Exoelectrogenic bacteria that power microbial fuel cells. Nat. Rev. Microbiol 7, 375–381 (2009).

    CAS  PubMed  Google Scholar 

  53. Samrot, A. V. et al. Electricity generation by Enterobacter cloacae SU-1 in mediator less microbial fuel cell. Int. J. Hydrogen Energy 35, 7723–7729 (2010).

    CAS  Google Scholar 

  54. Angenent, L. et al. Comments on “Electricity generation by Enterobacter cloacae SU-1 in mediator less microbial fuel cell” by Samrot et al., Int. J. Hydrogen Energy, 35 (15) 2010, 7723–7729. Int. J. Hydrogen Energy 36, 9396–9397 (2011).

    CAS  Google Scholar 

  55. Samrot, A. V. et al. Retraction notice to: Electricity generation by Enterobacter cloacae SU-1 in mediator less microbial fuel cell [Int J Hydrogen Energy (2010) 33:7723–7729]. Int. J. Hydrogen Energy 37, 728 (2012).

    CAS  Google Scholar 

  56. Kargi, F. & Eker, S. High power generation with simultaneous COD removal using a circulating column microbial fuel cell. J. Chem. Technol. Biotechnol. 84, 961–965 (2009).

    CAS  Google Scholar 

  57. Zhu, X. & Logan, B. E. Copper anode corrosion affects power generation in microbial fuel cells. J. Chem. Technol. Biotechnol. 89, 471–474 (2014).

    CAS  Google Scholar 

  58. Baudler, A., Schmidt, I., Langner, M., Greiner, A. & Schroder, U. Does it have to be carbon? Metal anodes in microbial fuel cells and related bioelectrochemical systems. Energy Environ. Sci. 8, 2048–2055 (2015).

    CAS  Google Scholar 

  59. Sekar, N., Wu, C.-H., Adams, M. W. W. & Ramasamy, R. P. Electricity generation by Pyrococcus furiosus in microbial fuel cells operated at 90 °C. Biotechnol. Bioeng. 114, 1419–1427 (2017).

    CAS  PubMed  Google Scholar 

  60. Yilmazel, Y. D., Zhu, X., Kim, K.-Y., Holmes, D. E. & Logan, B. E. Electrical current generation in microbial electrolysis cells by hyperthermophilic archaea Ferroglobus placidus and Geoglobus ahangari. Bioelectrochemistry 119, 142–149 (2016). This paper demonstrates electricity production at very high temperatures by iron-reducing hyperthermophiles.

    Google Scholar 

  61. Chen, S. & Smith, A. L. Methane-driven microbial fuel cells recover energy and mitigate dissolved methane emissions from anaerobic effluents. Environ. Sci. (Camb.) 4, 67–79 (2018).

    CAS  Google Scholar 

  62. Myung, J., Saikaly, P. E. & Logan, B. E. A two-staged system to generate electricity in microbial fuel cells using methane. Chem. Eng. J. 352, 262–267 (2018). This paper uses methane to produce electricity in a two-stage process.

    CAS  Google Scholar 

  63. McAnulty, M. J. et al. Electricity from methane by reversing methanogenesis. Nat. Commun. 8, 15419 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Hubenova, Y. & Mitov, M. Extracellular electron transfer in yeast-based biofuel cells: a review. Bioelectrochemistry 106 (Pt A), 177–185 (2015).

    Google Scholar 

  65. Raghavulu, S. V., Goud, R. K., Sarma, P. N. & Mohan, S. V. Saccharomyces cerevisiae as anodic biocatalyst for power generation in biofuel cell: Influence of redox condition and substrate load. Bioresour. Technol. 102, 2751–2757 (2011).

    CAS  PubMed  Google Scholar 

  66. Hubenova, Y. & Mitov, M. Mitochondrial origin of extracelullar transferred electrons in yeast-based biofuel cells. Bioelectrochemistry 106 (Pt A), 232–239 (2015).

    Google Scholar 

  67. Hubenova, Y. V. et al. Improvement of yeast−biofuel cell output by electrode modifications. Ind. Engin. Chem. Res. 50, 557–564 (2011).

    CAS  Google Scholar 

  68. Sayed, E. T., Tsujiguchi, T. & Nakagawa, N. Catalytic activity of baker’s yeast in a mediatorless microbial fuel cell. Bioelectrochemistry 86, 97–101 (2012).

    CAS  PubMed  Google Scholar 

  69. Wu, S. et al. Extracellular electron transfer mediated by flavins in gram-positive Bacillus sp. WS-XY1 and yeast Pichia stipitis. Electrochim. Acta 146, 564–567 (2014).

    CAS  Google Scholar 

  70. Dexter, S. C. & Gao, G. Y. Effect of seawater biofilms on corrosion potential and oxygen reduction of stainless steel. Corros. Sci. 44, 717–723 (1988).

    CAS  Google Scholar 

  71. Hasvold, Ø. et al. Sea-water battery for subsea control systems. J. Power Sources 65, 253–261 (1997). This paper provides evidence that bacteria on cathodes can improve oxygen reduction by the electrode.

    CAS  Google Scholar 

  72. Gregory, K. B., Bond, D. R. & Lovley, D. R. Graphite electrodes as electron donors for anaerobic repiration. Environ. Microbiol. 6, 596–604 (2004).

    CAS  PubMed  Google Scholar 

  73. Clauwaert, P. et al. Biological denitrification in microbial fuel cells. Environ. Sci. Technol. 41, 3354–3360 (2007). This paper demonstrates the complete denitrification in an MFC.

    CAS  PubMed  Google Scholar 

  74. Puig, S. et al. Autotrophic denitrification in microbial fuel cells treating low ionic strength waters. Environ. Sci. Technol. 46, 2309–2315 (2012).

    CAS  PubMed  Google Scholar 

  75. Jiang, X. et al. Electrochemical study of enhanced nitrate removal in wastewater treatment using biofilm electrode. Bioresour. Technol. 252, 134–142 (2018).

    PubMed  Google Scholar 

  76. Beese-Vasbender, P. F., Nayak, S., Erbe, A., Stratmann, M. & Mayrhofer, K. J. J. Electrochemical characterization of direct electron uptake in electrical microbially influenced corrosion of iron by the lithoautotrophic SRB Desulfopila corrodens strain IS4. Electrochim. Acta 167, 321–329 (2015).

    CAS  Google Scholar 

  77. Cordas, C. M., Guerra, L. T., Xavier, C. & Moura, J. J. G. Electroactive biofilms of sulphate reducing bacteria. Electrochim. Acta 54, 29–34 (2008).

    CAS  Google Scholar 

  78. Aulenta, F., Catapano, L., Snip, L., Villano, M. & Majone, M. Linking bacterial metabolism to graphite cathodes: electrochemical insights into the H2-producing capability of Desulfovibrio sp. ChemSusChem 5, 1080–1085 (2012).

    CAS  PubMed  Google Scholar 

  79. Rhoads, A., Beyenal, H. & Lewandowski, Z. Microbial fuel cell using anaerobic respiration as an anodic reaction and biomineralied manganese as a cathodic reactant. Environ. Sci. Technol. 39, 4666–4671 (2005).

    CAS  PubMed  Google Scholar 

  80. Bergel, A., Feron, D. & Mollica, A. Catalysis of oxygen reduction in PEM fuel cell by seawater biofilm. Electrochem. Commun. 7, 900–904 (2005).

    CAS  Google Scholar 

  81. Erable, B. et al. Marine aerobic biofilm as biocathode catalyst. Bioelectrochemistry 78, 51–56 (2010).

    CAS  PubMed  Google Scholar 

  82. Debuy, S., Pecastaings, S., Bergel, A. & Erable, B. Oxygen-reducing biocathodes designed with pure cultures of microbial strains isolated from seawater biofilms. Int. Biodeterior. Biodegradation 103, 16–22 (2015).

    CAS  Google Scholar 

  83. Malanoski, A. P. et al. Relative abundance of ‘Candidatus Tenderia electrophaga’ is linked to cathodic current in an aerobic biocathode community. Microb. Biotechnol. 11, 98–111 (2018).

    CAS  PubMed  Google Scholar 

  84. Lu, Z. et al. Behavior of metal ions in bioelectrochemical systems: a review. J. Power Sources 275, 243–260 (2015).

    CAS  Google Scholar 

  85. Yates, M. D., Cusick, R. D. & Logan, B. E. Extracellular palladium nanoparticle production using Geobacter sulfurreducens. ACS Sustain. Chem. Eng. 1, 1165–1171 (2013).

    CAS  Google Scholar 

  86. Ishii, T., Kawaichi, S., Nakagawa, H., Hashimoto, K. & Nakamura, R. From chemolithoautotrophs to electrolithoautotrophs: CO2 fixation by Fe(II)-oxidizing bacteria coupled with direct uptake of electrons from solid electron sources. Front. Microbiol. 6, 994 (2015).

    PubMed  PubMed Central  Google Scholar 

  87. Rozendal, R. A., Jeremiasse, A. W., Hamelers, H. V. M. & Buisman, C. J. N. Hydrogen production with a microbial biocathode. Environ. Sci. Technol. 42, 629–634 (2008).

    CAS  PubMed  Google Scholar 

  88. Geelhoed, J. S. & Stams, A. J. M. Electricity-assisted biological hydrogen production from acetate by Geobacter sulfurreducens. Environ. Sci. Technol. 45, 815–820 (2011).

    CAS  PubMed  Google Scholar 

  89. Bajracharya, S. et al. Biotransformation of carbon dioxide in bioelectrochemical systems: state of the art and future prospects. J. Power Sources 356, 256–273 (2017).

    CAS  Google Scholar 

  90. Jiang, Y. et al. Carbon dioxide and organic waste valorization by microbial electrosynthesis and electro-fermentation. Water Res. 149, 42–55 (2019).

    CAS  PubMed  Google Scholar 

  91. Nevin, K. P., Woodard, T. L., Franks, A. E., Summers, A. 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). This paper is one of the first studies showing chemical production from a biocathode.

    PubMed  PubMed Central  Google Scholar 

  92. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Bajracharya, S. et al. Carbon dioxide reduction by mixed and pure cultures in microbial electrosynthesis using an assembly of graphite felt and stainless steel as a cathode. Bioresour. Technol. 195, 14–24 (2015).

    CAS  PubMed  Google Scholar 

  94. Aryal, N., Tremblay, P.-L., Lizak, D. M. & Zhang, T. Performance of different Sporomusa species for the microbial electrosynthesis of acetate from carbon dioxide. Bioresour. Technol. 233, 184–190 (2017).

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  96. Gildemyn, S., Rozendal, R. A. & Rabaey, K. A. Gibbs free energy-based assessment of microbial electrocatalysis. Trends Biotechnol. 35, 393–406 (2017).

    CAS  PubMed  Google Scholar 

  97. Clauwaert, P. & Verstraete, W. Methanogenesis in membraneless microbial electrolysis cells. Appl. Microbiol. Biotechnol. 82, 829–836 (2008).

    PubMed  Google Scholar 

  98. Sato, K., Kawaguchi, H. & Kobayashi, H. Bio-electrochemical conversion of carbon dioxide to methane in geological storage reservoirs. Energy Convers. Manag. 66, 343–350 (2013).

    CAS  Google Scholar 

  99. Jiang, Y. et al. Bioelectrochemical systems for simultaneously production of methane and acetate from carbon dioxide at relatively high rate. Int. J. Hydrogen Energy 38, 3497–3502 (2013).

    CAS  Google Scholar 

  100. Cheng, S., Xing, D., Call, D. F. & Logan, B. E. Direct biological conversion of electrons into methane by electromethanogenesis. Environ. Sci. Technol. 43, 3953–3958 (2009). This paper provides the first reported evidence that methanogens could be using electrons directly from the cathode to produce methane.

    CAS  PubMed  Google Scholar 

  101. Deutzmann, J. S., Sahin, M. & Spormann, A. M. Extracellular enzymes facilitate electron uptake in biocorrosion and bioelectrosynthesis. mBio 6, e00496–15 (2015). This paper provides clear evidence that M. maripaludis releases enzymes that facilitate electron transfer from the cathode.

    PubMed  PubMed Central  Google Scholar 

  102. Van Eerten-Jansen, M. C. A. A. et al. Microbial community analysis of a methane-producing biocathode in a bioelectrochemical system. Archaea 2013, 12 (2013).

    Google Scholar 

  103. Siegert, M., Yates, M. D., Spormann, A. M. & Logan, B. E. Methanobacterium dominates biocathodic Archaeal communities in methanogenic microbial electrolysis cells. ACS Sustain. Chem. Eng. 3, 1668–1676 (2015). This paper shows that Methanobacterium spp. predominate on cathodes that poorly catalyse hydrogen production, but they do not predominate on platinum-catalysed cathodes.

    CAS  Google Scholar 

  104. Summers, Z. M. et al. Direct exchange of electrons within aggregates of an evolved syntrophic coculture of anaerobic bacteria. Science 330, 1413–1415 (2010).

    CAS  PubMed  Google Scholar 

  105. Rotaru, A.-E. et al. Direct interspecies electron transfer between Geobacter metallireducens and Methanosarcina barkeri. Appl. Environ. Microbiol. 80, 4599–4605 (2014).

    PubMed  PubMed Central  Google Scholar 

  106. Rotaru, A.-E. et al. A new model for electron flow during anaerobic digestion: direct interspecies electron transfer to Methanosaeta for the reduction of carbon dioxide to methane. Energy Environ. Sci. 7, 408–415 (2014).

    CAS  Google Scholar 

  107. Kato, S., Hashimoto, K. & Watanabe, K. Methanogenesis facilitated by electric syntrophy via (semi)conductive iron-oxide minerals. Environ. Microbiol. 14, 1646–1654 (2012).

    CAS  PubMed  Google Scholar 

  108. 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).

    CAS  PubMed  Google Scholar 

  109. Martins, G., Salvador, A. F., Pereira, L. & Alves, M. M. Methane production and conductive materials: a critical review. Environ. Sci. Technol. 52, 10241–10253 (2018). This is a good critical review of the complicating factors involved in understanding how conductive materials can influence methane production in bioreactors.

    CAS  PubMed  Google Scholar 

  110. Bourdakos, N., Marsili, E. & Mahadevan, R. A defined co-culture of Geobacter sulfurreducens and Escherichia coli in a membrane-less microbial fuel cell. Biotechnol. Bioeng. 111, 709–718 (2014).

    CAS  PubMed  Google Scholar 

  111. Karthikeyan, R. Sathish kumar, K., Murugesan, M., Berchmans, S. & Yegnaraman, V. Bioelectrocatalysis of Acetobacter aceti and Gluconobacter roseus for current generation. Environ. Sci. Technol. 43, 8684–8689 (2009).

    CAS  PubMed  Google Scholar 

  112. Ren, Z., Ward, T. E. & Regan, J. M. Electricity production from cellulose in a microbial fuel cell using a defined binary culture and an undefined mixed culture. Environ. Sci. Technol. 41, 4781–4786 (2007).

    CAS  PubMed  Google Scholar 

  113. Venkataraman, A., Rosenbaum, M. A., Perkins, S. D., Werner, J. J. & Angenent, L. T. Metabolite-based mutualism between Pseudomonas aeruginosa PA14 and Enterobacter aerogenes enhances current generation in bioelectrochemical systems. Energy Environ. Sci. 4, 4550–4559 (2011).

    CAS  Google Scholar 

  114. Malvankar, N. S. et al. Electrical conductivity in a mixed-species biofilm. Appl. Environ. Microbiol. 78, 5967–5971 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  115. Lovley, D. R. Electromicrobiology. Annu. Rev. Microbiol. 66, 391–409 (2012).

    CAS  Google Scholar 

  116. Walker, D. J. F. et al. Electrically conductive pili from pilin genes of phylogenetically diverse microorganisms. ISME J. 12, 48 (2017).

    PubMed  PubMed Central  Google Scholar 

  117. Li, F. et al. Engineering Shewanella oneidensis enables xylose-fed microbial fuel cell. Biotechnol. Biofuels 10, 196 (2017).

    PubMed  PubMed Central  Google Scholar 

  118. Choi, D. et al. Metabolically engineered glucose-utilizing Shewanella strains under anaerobic conditions. Bioresour. Technol. 154, 59–66 (2014).

    CAS  PubMed  Google Scholar 

  119. Flynn, J. M., Ross, D. E., Hunt, K. A., Bond, D. R. & Gralnick, J. A. Enabling unbalanced fermentations by using engineered electrode-interfaced bacteria. mBio 1, e00190–10 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  120. Johnson, E. T. et al. Enhancement of survival and electricity production in an engineered bacterium by light-driven proton pumping. Appl. Environ. Microbiol. 76, 4123–4129 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  121. Leang, C., Malvankar, N. S., Franks, A. E., Nevin, K. P. & Lovley, D. R. Engineering Geobacter sulfurreducens to produce a highly cohesive conductive matrix with enhanced capacity for current production. Energy Environ. Sci. 6, 1901–1908 (2013).

    CAS  Google Scholar 

  122. Kouzuma, A., Oba, H., Tajima, N., Hashimoto, K. & Watanabe, K. Electrochemical selection and characterization of a high current-generating Shewanella oneidensis mutant with altered cell-surface morphology and biofilm-related gene expression. BMC Microbiol. 14, 190–190 (2014).

    PubMed  PubMed Central  Google Scholar 

  123. Liu, T. et al. Enhanced Shewanella biofilm promotes bioelectricity generation. Biotechnol. Bioeng. 112, 2051–2059 (2015).

    CAS  PubMed  Google Scholar 

  124. Ueki, T. et al. Construction of a Geobacter strain with exceptional growth on cathodes. Front. Microbiol. 9, 1512 (2018).

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  126. Cao, Y., Li, X., Li, F. & Song, H. CRISPRi–sRNA: transcriptional–translational regulation of extracellular electron transfer in Shewanella oneidensis. ACS Synth. Biol. 6, 1679–1690 (2017).

    CAS  PubMed  Google Scholar 

  127. TerAvest, M. A., Zajdel, T. J. & Ajo-Franklin, C. M. The mtr pathway of Shewanella oneidensis MR-1 couples substrate utilization to current production in Escherichia coli. ChemElectroChem 1, 1874–1879 (2014).

    CAS  Google Scholar 

  128. Feng, J. et al. Enhancing the performance of Escherichia coli-inoculated microbial fuel cells by introduction of the phenazine-1-carboxylic acid pathway. J. Biotechnol. 275, 1–6 (2018).

    CAS  PubMed  Google Scholar 

  129. Liu, T., Yu, Y.-Y., Chen, T. & Chen, W. N. A synthetic microbial consortium of Shewanella and Bacillus for enhanced generation of bioelectricity. Biotechnol. Bioeng. 114, 526–532 (2017).

    CAS  PubMed  Google Scholar 

  130. Liu, Y. et al. A three-species microbial consortium for power generation. Energy Environ. Sci. 10, 1600–1609 (2017). This paper reports on a consortium of microorganisms developed to produce current from a specific substrate.

    CAS  Google Scholar 

  131. Kim, T., Logan, B. E. & Gorski, C. A. A. pH-gradient flow cell for converting waste CO2 into electricity. Environ. Sci. Technol. Lett. 4, 49–53 (2017). This paper demonstrates that only concentration differences are needed to produce current.

    CAS  Google Scholar 

  132. Park, D. H. & Zeikus, J. G. Electricity generation in microbial fuel cells using neutral red as an electronophore. Appl. Environ. Microbiol. 66, 1292–1297 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  133. Katz, E., Shipway, A. N. & Willner, I. in Handbook of Fuel Cells – Fundamentals, Technology and Applications Vol. 1 (eds Vielstich, W., Gasteiger, H. A. & Lamm, A.) 1–27 (John Wiley & Sons, Ltd, 2003).

  134. Kim, B.-H. et al. Electrochemical activity of an Fe(III)-reducing bacterium, Shewanella putrefaciens IR-1, in the presence of alternative electron acceptors. Biotechnol. Tech. 13, 475–478 (1999).

    CAS  Google Scholar 

  135. Kim, H.-J., Hyun, M.-S., Chang, I. S. & Kim, B.-H. A microbial fuel cell type lactate biosensor using a metal-reducing bacterium, Shewanella putrefaciens. J. Microbiol. Biotechnol. 9, 365–367 (1999).

    CAS  Google Scholar 

  136. Kim, B. H., Park, D. H., Shin, P. K., Chang, I. S. & Kim, H. J. Mediator-less biofuel cell. US Patent 5976719 (1999). This is the beginning of MFCs without mediators.

  137. Kim, B. H., Kim, H.-J., Hyun, M.-S. & Park, D.-H. Direct electrode reaction of Fe(III)-reducing bacterium, Shewanella putrefaciens. J. Microbiol. Biotechnol. 9, 127–131 (1999).

    Google Scholar 

  138. Reimers, C. E., Tender, L. M., Fertig, S. & Wang, W. Harvesting energy from the marine sediment-water interface. Environ. Sci. Technol. 35, 192–195 (2001). This is the first demonstration of how bacteria in sediments can be used to produce electrical power.

    CAS  PubMed  Google Scholar 

  139. Tender, L. M. et al. Harnessing microbially generated power on the seafloor. Nat. Biotechnol. 20, 821–825 (2002).

    CAS  PubMed  Google Scholar 

  140. Bond, D. R., Holmes, D. E., Tender, L. M. & Lovley, D. R. Electrode-reducing microorganisms that harvest energy from marine sediments. Science 295, 483–485 (2002).

    CAS  PubMed  Google Scholar 

  141. Liu, H., Ramnarayanan, R. & Logan, B. E. Production of electricity during wastewater treatment using a single chamber microbial fuel cell. Environ. Sci. Technol. 38, 2281–2285 (2004). This paper introduces the concept of using MFCs for waste water treatment.

    CAS  PubMed  Google Scholar 

  142. He, Z., Minteer, S. D. & Angenent, L. T. Electricity generation from artificial wastewater using an upflow microbial fuel cell. Environ. Sci. Technol. 39, 5262–5267 (2005).

    CAS  PubMed  Google Scholar 

  143. Fu, Q. et al. A thermophilic Gram-negative nitrate-reducing bacterium, Calditerrivibrio nitroreducens, exhibiting electricity generation capability. Environ. Sci. Technol. 47, 12583–12590 (2013).

    CAS  PubMed  Google Scholar 

  144. Parameswaran, P. et al. Kinetic, electrochemical, and microscopic characterization of the thermophilic, anode-respiring bacterium Thermincola ferriacetica. Environ. Sci. Technol. 47, 4934–4940 (2013).

    CAS  PubMed  Google Scholar 

  145. Malki, M., Lacey, A. L. D., Rodríguez, N., Amils, R. & Fernandez, V. M. Preferential use of an anode as an electron acceptor by an acidophilic bacterium in the presence of oxygen. Appl. Environ. Microbiol. 74, 4472–4476 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  146. Badalamenti, J. P., Krajmalnik-Brown, R. & Torres, C. I. Generation of high current densities by pure cultures of anode-respiring Geoalkalibacter spp. under alkaline and saline conditions in microbial electrochemical cells. mBio 4, e00144–13 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  147. Kashefi, K. et al. Geoglobus ahangari gen. nov., sp. nov., a novel hyperthermophilic archaeon capable of oxidizing organic acids and growing autotrophically on hydrogen with Fe(III) serving as the sole electron acceptor. Int. J. Syst. Evol. Microbiol. 52, 719–728 (2002).

    CAS  PubMed  Google Scholar 

  148. Nielsen, L. P. & Risgaard-Petersen, N. Rethinking sediment biogeochemistry after the discovery of electric currents. Ann. Rev. Mar. Sci. 7, 425–442 (2015). This is a thoughtful review of how cable bacteria could be greatly impacting the biogeochemical processes in marine sediments.

    PubMed  Google Scholar 

  149. Trojan, D. et al. A taxonomic framework for cable bacteria and proposal of the candidate genera Electrothrix and Electronema. Syst. Appl. Microbiol. 39, 297–306 (2016).

    PubMed  PubMed Central  Google Scholar 

  150. Reimers, C. E., Li, C., Graw, M. F., Schrader, P. S. & Wolf, M. The identification of cable bacteria attached to the anode of a benthic microbial fuel cell: evidence of long distance extracellular electron transport to electrodes. Front. Microbiol. 8, 2055 (2017).

    PubMed  PubMed Central  Google Scholar 

  151. Vilajeliu-Pons, A. et al. Microbial electricity driven anoxic ammonium removal. Water Res. 130, 168–175 (2018).

    CAS  PubMed  Google Scholar 

  152. Di Domenico, E. G. et al. Development of electroactive and anaerobic ammonium-oxidizing (anammox) biofilms from digestate in microbial fuel cells. Biomed. Res. Int. 2015, 351014 (2015).

    PubMed  PubMed Central  Google Scholar 

  153. Yin, X., Qiao, S., Zhou, J. & Quan, X. Using three-bio-electrode reactor to enhance the activity of anammox biomass. Bioresour. Technol. 196, 376–382 (2015).

    CAS  PubMed  Google Scholar 

  154. Shaw, D. R., Ali, M., Katuri, K. P. & Saikaly, P. E. in ISMET 6 - General Meeting of the International Society for Microbial Electrochemistry and Technology (ISMET, Lisbon 2017).

  155. Ruiz-Urigüen, M., Shuai, W. & Jaffé, P. R. Feammox Acidimicrobiaceae sp. A6, a lithoautotrophic electrode-colonizing bacterium. Appl. Environ. Microbiol. https://doi.org/10.1128/AEM.02029-18 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  156. Qu, B., Fan, B., Zhu, S. & Zheng, Y. Anaerobic ammonium oxidation with an anode as the electron acceptor. Env. Microbiol. Rep. 6, 100–105 (2014).

    CAS  Google Scholar 

  157. Ishii, S. i. et al. Functionally stable and phylogenetically diverse microbial enrichments from microbial fuel cells during wastewater treatment. PLOS ONE 7, e30495 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  158. Finster, K. & Bak, F. & Pfennig, N. Desulfuromonas acetexigens sp. nov., a dissimilatory sulfur-reducing eubacterium from anoxic freshwater sediments. Arch. Microbiol. 161, 328–332 (1994).

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  160. Katuri, K. P., Albertsen, M. & Saikaly, P. E. Draft genome sequence of Desulfuromonas acetexigens strain 2873, a novel anode-respiring bacterium. Genome Announc. 5, e01522–01516 (2017).

    PubMed  PubMed Central  Google Scholar 

  161. Lovley, D. R. Live wires: direct extracellular electron exchange for bioenergy and the bioremediation of energy-related contamination. Energy Environ. Sci. 4, 4896–4906 (2011).

    CAS  Google Scholar 

  162. Li, Z., Jinlian, M., Zhen, Y., Yueqiang, W. & Jia, T. Magnetite accelerates syntrophic acetate oxidation in methanogenic systems with high ammonia concentrations. Microb. Biotechnol. 11, 710–720 (2018).

    Google Scholar 

  163. Liu, F. et al. Promoting direct interspecies electron transfer with activated carbon. Energy Environ. Sci. 5, 8982–8989 (2012).

    CAS  Google Scholar 

Download references

Acknowledgements

The authors acknowledge funding by the US Department of Energy (DOE) Energy Efficiency and Renewable Energy (EERE) Fuel Cell Technologies Office through a contract from the National Renewable Energy Laboratory (NREL), Project #21263, and by the Environmental Security Technology Certification Program via cooperative research agreement W9132T-16-2-0014 through the US Army Engineer Research and Development Center.

Author information

Authors and Affiliations

  1. Department of Civil and Environmental Engineering, The Pennsylvania State University, University Park, PA, USA

    Bruce E. Logan & Ruggero Rossi

  2. Biological and Environmental Sciences and Engineering Division, Water Desalination and Reuse Research Center, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia

    Ala’a Ragab & Pascal E. Saikaly

Authors
  1. Bruce E. Logan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ruggero Rossi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ala’a Ragab
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pascal E. Saikaly
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors researched data, wrote the article and reviewed and edited the manuscript before submission. B.E.L. and R.R. prepared drafts for figures 1 and 3–5, and P.E.S. and A.R. prepared figure 2.

Corresponding authors

Correspondence to Bruce E. Logan or Pascal E. Saikaly.

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.

Supplementary information

Glossary

Bioelectrochemical systems

Devices that contain microorganisms that donate to or accept electrons from an electrode.

Microbial electrochemical technologies

(METs). Bioelectrochemical systems that are used for a specific purpose, for example, microbial fuel cells used to produce electricity.

Catholyte

An electrolyte that surrounds the cathode when a bioelectrochemical system is divided into two chambers; if there is only one chamber, the cathode is exposed to the anolyte.

Exoelectrogenic

The ability of microorganisms to transfer electrons outside the cell.

Electrotrophic

The ability of microorganisms to accept electrons into the cell from external sources.

Single-chamber

A single-chamber microbial fuel cell (MFC) is an MFC with an air cathode that is exposed to air on one side and water on the other side. By contrast, two-chamber systems are reactors with a membrane that separates the anode and cathode chambers.

Anolyte

The electrolyte that surrounds the anode in a bioelectrochemical system. In one-chamber systems, the cathode is exposed to the same electrolyte.

Biocathodes

Cathodes that transfer electrons to microorganisms on the electrode surface.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Logan, B.E., Rossi, R., Ragab, A. et al. Electroactive microorganisms in bioelectrochemical systems. Nat Rev Microbiol 17, 307–319 (2019). https://doi.org/10.1038/s41579-019-0173-x

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41579-019-0173-x

This article is cited by

Search

Advanced search

Quick links

Nature Briefing: Translational Research

Sign up for the Nature Briefing: Translational Research newsletter — top stories in biotechnology, drug discovery and pharma.

Get what matters in translational research, free to your inbox weekly. Sign up for Nature Briefing: Translational Research