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:

Electromicrobiology: the ecophysiology of phylogenetically diverse electroactive microorganisms

Nature Reviews Microbiology volume 20, pages 5–19 (2022)Cite this article

Subjects

Abstract

Electroactive microorganisms markedly affect many environments in which they establish outer-surface electrical contacts with other cells and minerals or reduce soluble extracellular redox-active molecules such as flavins and humic substances. A growing body of research emphasizes their broad phylogenetic diversity and shows that these microorganisms have key roles in multiple biogeochemical cycles, as well as the microbiome of the gut, anaerobic waste digesters and metal corrosion. Diverse bacteria and archaea have independently evolved cytochrome-based strategies for electron exchange between the outer cell surface and the cell interior, but cytochrome-free mechanisms are also prevalent. Electrically conductive protein filaments, soluble electron shuttles and non-biological conductive materials can substantially extend the electronic reach of microorganisms beyond the surface of the cell. The growing appreciation of the diversity of electroactive microorganisms and their unique electronic capabilities is leading to a broad range of applications.

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: Phylogenetic diversity of electroactive microorganisms.
Fig. 2: Functional roles of electroactive microorganisms.
Fig. 3: Mechanisms for electron transport across the outer surface.
Fig. 4: Mechanisms to enhance extracellular electron transport to solid-phase electron acceptors and long-range electron transport.
Fig. 5: Applications emerging from the study of electroactive microorganisms.

Similar content being viewed by others

References

  1. Lovley, D. R. Electromicrobiology. Ann. Rev. Microbol. 66, 391–409 (2012).

    CAS  Google Scholar 

  2. Logan, B. E., Rossi, R., Ragab, A. & Saikaly, P. E. Electroactive microorganisms in bioelectrochemical systems. Nat. Rev. Microbiol. 17, 307–319 (2019).

    CAS  PubMed  Google Scholar 

  3. Chen, H. et al. Fundamentals, applications, and future directions of bioelectrocatalysis. Chem. Rev. 120, 12903–12993 (2020). This article presents an excellent overview of the diversity of proposed bioelectrochemical technologies and hurdles to overcome to enable scalable, practical application.

    CAS  PubMed  Google Scholar 

  4. Lovley, D. R. in Origins, Evolution and Biodiversity of Microbial Life (ed. Seckbach, J.) 301–313 (Kluwer, 2004).

  5. Lovley, D. R. & Yao, J. Intrinsically conductive microbial nanowires for ‘green’ electronics with novel functions. Trends Biotechnol. https://doi.org/10.1016/j.tibtech.2020.12.005 (2021).

    Article  PubMed  Google Scholar 

  6. Koch, C. & Harnisch, F. Is there a specific ecological niche for electroactive microorganisms? ChemElectroChem 3, 1282–1295 (2016). This article presents a comprehensive compilation of known electroactive microorganisms.

    CAS  Google Scholar 

  7. Lovley, D. R., Holmes, D. E. & Nevin, K. P. Dissimilatory Fe(III) and Mn(IV) reduction. Adv. Microb. Phys. 49, 219–286 (2004).

    CAS  Google Scholar 

  8. Lovley, D. R. Organic matter mineralization with the reduction of ferric iron: a review. Geomicrobiol. J. 5, 375–399 (1987).

    CAS  Google Scholar 

  9. Lovley, D. R., Stolz, J. F., Nord, G. L. & Phillips, E. J. P. Anaerobic production of magnetite by a dissimilatory iron-reducing microorganism. Nature 330, 252–254 (1987).

    CAS  Google Scholar 

  10. Lovley, D. R. & Phillips, E. J. P. Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl. Environ. Microbiol. 54, 1472–1480 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  Google Scholar 

  12. Tang, H.-Y. et al. Direct metal–microbe electron transfer is required for microbial corrosion of stainless steel. ISME J. https://doi.org/10.1038/s41396-41021-00990-41392 (2021).

    Article  PubMed  Google Scholar 

  13. Zheng, S., Liu, F., Wang, B., Zhang, Y. & Lovley, D. R. A Methanobacterium capable of direct interspecies electron transfer. Environ. Sci. Technol. 54, 15347–15354 (2020).

    CAS  PubMed  Google Scholar 

  14. Hubenova, Y., Hubenova, E. & Mitov, M. Electroactivity of the Gram-positive bacterium Paenibacillus dendritiformis MA-72. Bioelectrochemistry 136, 107632 (2020).

    CAS  PubMed  Google Scholar 

  15. Huang, S. & Jaffé, P. R. Isolation and characterization of an ammonium-oxidizing iron reducer: Acidimicrobiaceae sp. A6. PLoS ONE 13, e0194007 (2018).

    PubMed  PubMed Central  Google Scholar 

  16. Shaw, D. R. et al. Extracellular electron transfer-dependent anaerobic oxidation of ammonium by anammox bacteria. Nat. Commun. 11, 2058 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Cai, C. et al. A methanotrophic archaeon couples anaerobic oxidation of methane to Fe(III) reduction. ISME J. 12, 1929–1939 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Leu, A. O. et al. Anaerobic methane oxidation coupled to manganese reduction by members of the Methanoperedenaceae. ISME J. 14, 1030–1041 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Walker, D. J. F. et al. Syntrophus conductive pili demonstrate that common hydrogen-donating syntrophs can have a direct electron transfer option. ISME J. 14, 837–846 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Holmes, D. E. et al. A membrane-bound cytochrome enables Methanosarcina acetivorans to conserve energy from extracellular electron transfer. mBio 10, e00789-19 (2019).

    PubMed  PubMed Central  Google Scholar 

  21. Prakash, D., Chauhan, S. S. & Ferry, J. G. Life on the thermodynamic edge: respiratory growth of an acetotrophic methanogen. Sci. Adv. 5, eaaw9059 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Conley, B. E., Weinstock, M. T., Bond, D. R. & Gralnick, J. A. A hybrid extracellular electron transfer pathway enhances the survival of Vibrio natriegens. Appl. Environ. Microbiol. 86, e01253-20 (2020).

    PubMed  PubMed Central  Google Scholar 

  23. Light, S. H. et al. A flavin-based extracellular electron transfer mechanism in diverse Gram-positive bacteria. Nature 562, 140–144 (2018). This article reports the important discovery of a mechanism for EET that is found in many Gram-positive microorganisms.

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Naradasu, D., Guionet, A., Okinaga, T., Nishihara, T. & Okamoto, A. Electrochemical characterization of current-producing human oral pathogens by whole-cell electrochemistry. ChemElectroChem 7, 2012–2019 (2020).

    CAS  Google Scholar 

  25. Zhang, S., Miran, W., Naradasu, D., Guo, S. & Okamoto, A. A human pathogen Capnocytophaga ochracea exhibits current producing capability. Electrochemistry 88, 224–229 (2020).

    CAS  Google Scholar 

  26. Hernsdorf, A. W. et al. Potential for microbial H2 and metal transformations associated with novel bacteria and archaea in deep terrestrial subsurface sediments. ISME J. 11, 1915–1929 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Holmes, D. E. et al. Metatranscriptomic evidence for direct interspecies electron transfer between Geobacter and Methanothrix species in rice paddy soils. Appl. Env. Microbiol. 83, e00223-17 (2017).

    Google Scholar 

  28. Bray, M. S. et al. Phylogenetic and structural diversity of aromatically dense pili from environmental metagenomes. Environ. Microbiol. Rep. 12, 49–57 (2020).

    CAS  PubMed  Google Scholar 

  29. Walker, D. J. F. et al. Electrically conductive pili from genes of phylogenetically diverse microorganisms. ISME J. 12, 48–58 (2018).

    CAS  PubMed  Google Scholar 

  30. Walker, D. J. F. et al. The archaellum of Methanospirillum hungatei is electrically conductive. mBio 10, e00579-19 (2019).

    PubMed  PubMed Central  Google Scholar 

  31. Arbour, T. J., Gilbert, N. & Banfield, J. F. Diverse microorganisms in sediment and groundwater are implicated in extracellular redox processes based on genomic analysis of bioanode communities. Front. Microbiol. 11, 1694 (2020).

    PubMed  PubMed Central  Google Scholar 

  32. Zhao, Z., Li, Y., Zhang, Y. & Lovley, D. R. Sparking anaerobic digestion: promoting direct interspecies electron transfer to enhance methane production. iScience 23, 101794 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Shi, L., Fredrickson, J. K. & Zachara, J. M. Genomic analyses of bacterial porin–cytochrome gene clusters. Front. Microbiol. 5, 657 (2014). This article describes the diversity and distribution of porin–cytochrome systems in the microbial world.

    PubMed  PubMed Central  Google Scholar 

  34. Holmes, D. E., Dang, Y., Walker, D. J. F. & Lovley, D. R. The electrically conductive pili of Geobacter species are a recently evolved feature for extracellular electron transfer. Microb. Genomics 2, e000072 (2016).

    Google Scholar 

  35. Lovley, D. R. Dissimilatory Fe(III) and Mn(IV) reduction. Microbiol. Rev. 55, 259–287 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Lovley, D. R. Dissimilatory metal reduction. Ann. Rev. Microbiol. 47, 263–290 (1993).

    CAS  Google Scholar 

  37. Lovley, D. R. Microbial reduction of iron, manganese, and other metals. Adv. Agron. 54, 175–231 (1995).

    CAS  Google Scholar 

  38. Gnanaprakasam, E. T. et al. Microbial community structure and arsenic biogeochemistry in two arsenic-impacted aquifers in Bangladesh. mBio 8, e01326-17 (2017).

    PubMed  PubMed Central  Google Scholar 

  39. Chaudhuri, S. K. & Lovley, D. R. Electricity generation by direct oxidation of glucose in mediatorless microbial fuel cells. Nat. Biotechnol. 21, 1229–1232 (2003).

    CAS  PubMed  Google Scholar 

  40. Caccavo, F. Jr et al. Geovibrio ferrireducens, a phylogenetically distinct dissimilatory Fe(III)-reducing bacterium. Arch. Microbiol. 165, 370–376 (1996).

    CAS  PubMed  Google Scholar 

  41. Lovley, D. R. & Phillips, E. J. P. Requirement for a microbial consortium to completely oxidize glucose in Fe(III)-reducing sediments. Appl. Environ. Microbiol. 55, 3234–3236 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Lovley, D. R. 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. 159, 336–344 (1993).

    CAS  PubMed  Google Scholar 

  43. Roden, E. E. & Lovley, D. R. Dissimilatory Fe(III) reduction by the marine microorganism, Desulfuromonas acetoxidans. Appl. Environ. Microbiol. 59, 734–742 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Xu, Z. et al. Geomonas oryzae gen. nov., sp. nov., Geomonas edaphica sp. nov., Geomonas ferrireducens sp. nov., Geomonas terrae sp. nov., four ferric-reducing bacteria isolated from paddy soil, and reclassification of three species of the genus Geobacter as members of the genus Geomonas gen. nov. Front. Microbiol. 10, 2201 (2019).

    PubMed  PubMed Central  Google Scholar 

  45. Coates, J. D., Ellis, D. J. & Lovley, D. R. Geothrix fermentans gen. nov. sp. nov., an acetate-oxidizing Fe(III) reducer capable of growth via fermentation. Internat. J. Sys. Bacteriol. 49, 1615–1622 (1999).

    CAS  Google Scholar 

  46. Lovley, D. R. et al. Oxidation of aromatic contaminants coupled to microbial iron reduction. Nature 339, 297–299 (1989).

    CAS  Google Scholar 

  47. Rooney-Varga, J. N., Anderson, R. T., Fraga, J. L., Ringelberg, D. & Lovley, D. R. Microbial communities associated with anaerobic benzene degradation in a petroleum-contaminated aquifer. Appl. Env. Microbiol. 65, 3056–3064 (1999).

    CAS  Google Scholar 

  48. Zhang, T., Bain, T. S., Nevin, K. P., Barlett, M. A. & Lovley, D. R. Anaerobic benzene oxidation by Geobacter species. Appl. Env. Microbiol. 78, 8304–8310 (2012).

    CAS  Google Scholar 

  49. Ettwig, K. F. et al. Archaea catalyze iron-dependent anaerobic oxidation of methane. Proc. Natl Acad. Sci. USA 113, 12792–12796 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Lovley, D. R., Roden, E. E., Phillips, E. J. P. & Woodward, J. C. Enzymatic iron and uranium reduction by sulfate-reducing bacteria. Mar. Geol. 113, 41–53 (1993).

    CAS  Google Scholar 

  51. Tebo, B. M. & Obraztsova, A. Y. Sulfate-reducing bacterium grows with Cr(VI), U(VI), Mn(IV), and Fe(III) as electron acceptors. FEMS Microbiol. Lett. 162, 193–198 (1998).

    CAS  Google Scholar 

  52. Holmes, D. E., Bond, D. R. & Lovley, D. R. Electron transfer by Desulfobulbus propionicus to Fe(III) and graphite electrodes. Appl. Environ. Microbiol. 70, 1234–1237 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Bond, D. R. & Lovley, D. R. Reduction of Fe(III) oxide by methanogens in the presence and absence of extracellular quinones. Environ. Microbiol. 4, 115–124 (2002).

    CAS  PubMed  Google Scholar 

  54. Tor, J. M., Lovley, D. R., Kashefi, K. & Holmes, D. E. Potential importance of dissimilatory Fe(III)-reducing microorganisms in hot sedimentary environments. Geophys. Monogr. Ser. 114, 199–211 (2004).

    Google Scholar 

  55. Kashefi, K. & Lovley, D. R. Extending the upper temperature limit for life. Science 301, 934 (2003).

    CAS  PubMed  Google Scholar 

  56. Vargas, M., Kashefi, K., Blunt-Harris, E. L. & Lovley, D. R. Microbiological evidence for Fe(III) reduction on early Earth. Nature 395, 65–67 (1998).

    CAS  PubMed  Google Scholar 

  57. Holmes, D. E., Risso, C., Smith, J. A. & Lovley, D. R. Anaerobic oxidation of benzene by the hyperthermophlic archaeon Ferroglobus placidus. Appl. Env. Microbiol. 77, 5926–5933 (2011).

    CAS  Google Scholar 

  58. Tor, J. M., Kashefi, K. & Lovley, D. R. Acetate oxidation coupled to Fe(III) reduction in hyperthermophilic microorganisms. Appl. Environ. Microbiol. 67, 1363–1365 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Tor, J. M. & Lovley, D. R. Anaerobic oxidation of aromatic compounds coupled to Fe(III) reduction by Ferroglobus placidus. Environ. Microbiol. 3, 281–287 (2001).

    CAS  PubMed  Google Scholar 

  60. Pfeffer, C. et al. Filamentous bacteria transport electrons over centimetre distances. Nature 491, 218–221 (2012). This article is the first description of cable bacteria.

    CAS  PubMed  Google Scholar 

  61. Bjerg, J. T. et al. Long-distance electron transport in individual, living cable bacteria. Proc. Natl Acad. Sci. USA 115, 5786–5791 (2018). This article presents direct experimental evidence for electron transport along the filaments of cable bacteria.

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Meysman, F. J. R. Cable bacteria take a new breath using long-distance electricity. Trends Microbiol. 26, 411–422 (2018).

    CAS  PubMed  Google Scholar 

  63. Rao, A. M. F., Malkin, S. Y., Hidalgo-Martinez, S. & Meysman, F. J. R. The impact of electrogenic sulfide oxidation on elemental cycling and solute fluxes in coastal sediment. Geochem. Cosmochim. Acta 172, 265–286 (2016).

    CAS  Google Scholar 

  64. van de Velde, S., Callebaut, I., Gao, Y. & Meysman, F. J. R. Impact of electrogenic sulfur oxidation on trace metal cycling in a coastal sediment. Chem. Geol. 452, 9–23 (2017).

    Google Scholar 

  65. 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 

  66. Yee, M. O. & Rotaru, A.-E. Extracellular electron uptake in Methanosarcinales is independent of multiheme c-type cytochromes. Sci. Rep. 10, 372 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  67. 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 

  68. McGlynn, S. E., Chadwick, G. L., Kempes, C. P. & Orphan, V. J. Single cell activity reveals direct electron transfer in methanotrophic consortia. Nature 526, 531–535 (2015).

    CAS  PubMed  Google Scholar 

  69. Wegener, G., Krukenberg, V., Riedel, D., Tegetmeyer, H. E. & Boetius, A. Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria. Nature 526, 587–590 (2015).

    CAS  PubMed  Google Scholar 

  70. Ha, P. T. et al. Syntrophic anaerobic photosynthesis via direct interspecies electron transfer. Nat. Commun. 7, 13924 (2017).

    Google Scholar 

  71. Gupta, D., Guzman, M. S. & Bose, A. Extracellular electron uptake by autotrophic microbes: physiological, ecological, and evolutionary implications. J. Ind. Microbiol. Biotechnol. 47, 863–876 (2020). This article presents an excellent overview of known mechanisms for direct electron uptake in electrotrophs.

    CAS  PubMed  Google Scholar 

  72. Kappler, A. & Brune, A. Dynamics of redox potential and changes in redox state of iron and humic acids during gut passage in soil-feeding termites (Cubitermes spp.). Soil. Biol. Biochem. 34, 221–227 (2002).

    CAS  Google Scholar 

  73. Vu, A., Nguyen, N. C. & Leadbetter, J. R. Iron reduction in the metal-rich guts of wood-feeding termites. Geobiol. J. 2, 239–247 (2004).

    CAS  Google Scholar 

  74. Hobbie, S. N., Li, X., Basen, M., Stingi, U. & Brune, A. Humic substance-mediated Fe(III) reduction by a fermenting Bacillus strain from the alkaline gut of a humus-feeding scarab beetle larva. Syst. Appl. Microbiol. 35, 226–232 (2012).

    CAS  PubMed  Google Scholar 

  75. Zhou, G.-W. et al. Mobile incubator for iron(III) reduction in the gut of the soil-feeding earthworm Pheretima guillelmi and interaction with denitrification. Environ. Sci. Technol. 53, 4215–4223 (2019).

    CAS  PubMed  Google Scholar 

  76. Wang, W. et al. Bacterial extracellular elecron transfer occurs in the mammalian gut. Anal. Chem. 91, 12138–12141 (2019). This article demonstrates abundant electroactivity in the gut microbiome.

    CAS  PubMed  Google Scholar 

  77. Naradasu, D., Miran, W., Sakamoto, M. & Okamoto, A. Isolation and characterization of human gut bacteria capable of extracellular electron transport by electrochemical techniques. Front. Microbiol. 9, 3267 (2019).

    PubMed  PubMed Central  Google Scholar 

  78. Light, S. H. et al. Extracellular electron transfer powers flavinylated extracellular reductases in Gram-positive bacteria. Proc. Natl Acad. Sci. USA 116, 26892–26899 (2019).

    CAS  PubMed Central  Google Scholar 

  79. Rago, L., Popp, D., Heiker, J. T. & Harnisch, F. Electroactive microorganisms in mouse feces. Electrochm. Acta 365, 137326 (2021).

    CAS  Google Scholar 

  80. Tahernia, M. et al. Characterization of electrogenic gut bacteria. ACS Omega 5, 29439–29446 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Yang, J. J., Rahim, A. R., Yang, A. J., Chuang, T.-H. & Huang, C.-M. Production of electricity and reduction of high-fat diet-induced IL-6 by glucose fermentation of Leuconostoc mesenteroides. Biochem. Biophys. Res. Commun. 533, 651–656 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Hederstedt, L., Gorton, L. & Pankratova, G. Two routes for extracellular electron transfer in Enterococcus faecalis. J. Bacteriol. 202, e00725-19 (2020). This article further demonstrates the diversity of potential routes for EET in Gram-positive microorganisms.

    PubMed  PubMed Central  Google Scholar 

  83. Schwab, L., Rago, L., Koch, C. & Harnisch, F. Identification of Clostridium cochlearium as an electroactive microorganism from the mouse gut microbiome. Bioelectrochemistry 130, 107334 (2019).

    CAS  PubMed  Google Scholar 

  84. Khan, M. T. et al. The gut anaerobe Faecalibacterium prausnitzii uses an extracellular electron shuttle to grow at oxic–anoxic interphases. ISME J. 6, 1578–1585 (2012). This article is an important early paper on the prevalence and role of EET in the gut.

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Sadabad, M. S. et al. A simple coculture system shows mutualism between anaerobic faecalibacteria and epithelial Caco-2 cells. Sci. Rep. 5, 17906 (2015).

    Google Scholar 

  86. Ericsson, A. C., Davis, D. J., Franklin, C. L. & Hagan, C. E. Exoelectrogenic capacity of host microbiota predicts lymphocyte recruitment to the gut. Physiol. Genomics 47, 243–252 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Lekbach, Y. et al. Microbial corrosion of metals — the corrosion microbiome. Adv. Microb. Physiol. 78, 317–390 (2021).

    PubMed  Google Scholar 

  88. 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).

    PubMed  PubMed Central  Google Scholar 

  89. Shi, L. et al. Extracellular electron transfer mechanisms between microorganisms and minerals. Nat. Rev. Microbiol. 14, 651–662 (2016).

    CAS  PubMed  Google Scholar 

  90. White, G. F. et al. Mechanisms of bacterial extracellular electron exchange. Adv. Microb. Phys. 68, 87–138 (2016).

    CAS  Google Scholar 

  91. Beblawy, S. et al. Extracellular reduction of solid electron acceptors by Shewanella oneidensis. Mol. Microbiol. 109, 571–583 (2018). This article presents a detailed review of electron transport mechanisms in S. oneidensis, an important model microorganism for the elucidation of extracellular electron transport mechanisms.

    CAS  PubMed  Google Scholar 

  92. 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). This study discovers the porin–cytochrome mechanisms for EET.

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Orellana, R. et al. U(VI) reduction by a diversity of c-type cytochromes of Geobacter sulfurreducens. Appl. Env. Microbiol. 79, 6369–6374 (2013).

    CAS  Google Scholar 

  94. Edwards, M. J. et al. Structural modeling of an outer membrane electron conduit from a metal-reducing bacterium suggests electron transfer via periplasmic redox partners. J. Biol. Chem. 293, 8103–8112 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Lovley, D. R. et al. Geobacter: the microbe electric’s physiology, ecology, and practical applications. Adv. Microb. Physiol. 59, 1–100 (2011).

    CAS  PubMed  Google Scholar 

  96. Carlson, H. K. et al. Surface multiheme c-type cytochromes from Thermincola potens and implications for respiratory metal reduction by Gram-positive bacteria. Proc. Natl Acad. Sci. USA 109, 1702–1707 (2012). This article is the first description of the potential for cytochrome conduits through the Gram-positive cell wall.

    CAS  PubMed  PubMed Central  Google Scholar 

  97. Costa, N. L. et al. How thermophilic Gram-positive organisms perform extracellular electron transfer: characterization of the cell surface terminal reductase OcwA. mBio 10, e01210-19 (2019).

    PubMed  PubMed Central  Google Scholar 

  98. Gavrilov, S. N., Slobodkin, A. I., Robb, F. T. & deVries, S. Characterization of membrane-bound Fe(III)–EDTA reductase activities of the thermophilic Gram-positive dissimilatory iron-reducing bacterium Thermoterrabacterium ferrireducens. Microbiology 76, 139–146 (2009).

    Google Scholar 

  99. Gavrilov, S. N., Lloyd, J. R., Kostrikina, N. A. & Slobodkin, A. I. Fe(III) oxide reduction by a Gram-positive thermophile: physiological mechanisms for dissimilatory reduction of poorly crystalline Fe(III) oxide by a thermophilic Gram-positive bacterium Carboxydothermus ferrireducens. Geomicrobiol. J. 29, 804–819 (2012).

    CAS  Google Scholar 

  100. Smith, J. A. et al. Mechanisms involved in Fe(III) respiration by the hyperthermophilic archaeon Ferroglobus placidus. Appl. Environ. Microbiol. 81, 2735–2744 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Manzella, M. P., Reguera, G. & Kashefi, K. Extracellular electron transfer to Fe(III) oxides by the hyperthermophilic archaeon Geoglobus ahangari via a direct contact mechanism. Appl. Env. Microbiol. 79, 4694–4700 (2013).

    CAS  Google Scholar 

  102. Leu, A. O. et al. Lateral gene transfer drives metabolic flexibility in the anaerobic methane-oxidizing archaeal family Methanoperedenaceae. mBio 11, e01325-20 (2020).

    PubMed  PubMed Central  Google Scholar 

  103. Zhou, J., Holmes, D. E., Tang, H.-Y. & Lovley, D. R. Correlation of key physiological properties of Methanosarcina isolates with their environment of origin. Appl. Env. Microbiol. 87, e00731-21 (2021).

    Google Scholar 

  104. Lam, L. N. et al. Sortase-assembled pili promote extracellular electron transfer and iron acquisition in Enterococcus faecalis biofilm. Preprint at bioRxiv https://doi.org/10.1101/601666 (2019).

    Article  Google Scholar 

  105. Coppi, M. V. et al. Involvement of Geobacter sulfurreducens SfrAB in acetate metabolism rather than intracellular Fe(III) reduction. Microbiology 153, 3572–3585 (2007).

    CAS  PubMed  Google Scholar 

  106. Lovley, D. R., Coates, J. D., Blunt-Harris, E. L., Phillips, E. J. P. & Woodward, J. C. Humic substances as electron acceptors for microbial respiration. Nature 382, 445–448 (1996).

    CAS  Google Scholar 

  107. Lovley, D. R. et al. Humic substances as a mediator for microbially catalyzed metal reduction. Acta Hydrochim. Hydrobiol. 26, 152–157 (1998).

    CAS  Google Scholar 

  108. Nevin, K. P. & Lovley, D. R. Mechanisms for Fe(III) oxide reduction in sedimentary environments. Geomicrobiol. J. 19, 141–159 (2002).

    CAS  Google Scholar 

  109. 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  PubMed  Google Scholar 

  110. Nevin, K. P. & Lovley, D. R. Novel mechanisms for accessing insoluble Fe(III) oxide during dissimilatory Fe(III) reduction by Geothrix fermentans. Appl. Environ. Microbiol. 68, 2294–2299 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  112. Mehta-Kolte, M. G. & Bond, D. R. Geothrix fermentans secretes two different redox-active compounds to utilize electron acceptors across a wide range of redox potentials. Appl. Env. Microbiol. 78, 6987–6995 (2012).

    CAS  Google Scholar 

  113. Glasser, N. R., Saunders, S. H. & Newman, D. K. The colorful world of extracellular electron shuttles. Annu. Rev. Microbiol. 71, 731–751 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  114. Kotloski, N. J. & Gralnick, J. A. Flavin electron shuttles dominate extracellular electron transfer by Shewanella oneidensis. mBio 4, e00553-12 (2013). This article presents experimental evidence for the importance of a self-produced electron shuttle.

    PubMed  PubMed Central  Google Scholar 

  115. 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 

  116. Smith, J. A. et al. Going wireless: Fe(III) oxide reduction without pili by Geobacter sulfurreducens strain JS-1. Appl. Env. Microbiol. 80, 4331–4340 (2014).

    Google Scholar 

  117. Snoeyenbos-West, O. L., Nevin, K. P., Anderson, R. T. & Lovley, D. R. Enrichment of Geobacter species in responce to stimulation of Fe(III) reduction in sandy aquifer sediments. Microb. Ecol. 39, 153–167 (2000).

    CAS  PubMed  Google Scholar 

  118. Mouser, P. J. et al. Influence of heterogenous ammonium availability on bacterial community structure and the expression of nitrogen fixation and ammonium transporter genes during in situ bioremediation of urnaium-contaminated groundwater. Environ. Sci. Technol. 43, 4386–4392 (2009).

    CAS  PubMed  Google Scholar 

  119. Saunders, S. H. et al. Extracellular DNA promotes efficient extracellular electron transfer by pyocyanin in Pseudomonas aeruginosa biofilms. Cell 182, 919–932 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  120. Taillerfert, M. et al. Shewanella putrefaciens produces an Fe(III)-solubilizing organic ligand during anaerobic respiration on insoluble Fe(III) oxides. J. Inorg. Biochem. 101, 1760–1767 (2007).

    Google Scholar 

  121. Childers, S. E., Ciufo, S. & Lovley, D. R. Geobacter metallireducens accesses insoluble Fe(III) oxide by chemotaxis. Nature 416, 767–769 (2002).

    CAS  PubMed  Google Scholar 

  122. Tremblay, P.-L., Aklujkar, M., Leang, C. & Lovley, D. R. A genetic system for Geobacter metallireducens: role of flagella and pili in extracellular electron transfer. Enivr. Microbiol. Rep. 4, 82–88 (2012).

    CAS  Google Scholar 

  123. Ueki, T., Leang, C., Inoue, K. & Lovley, D. R. Identification of multicomponent histidine-aspartate phosphorelay system controlling flagellar and motility gene expression in Geobacter species. J. Biol. Chem. 287, 10958–10966 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  125. Lovley, D. R. & Holmes, D. E. Protein nanowires: the electrification of the microbial world and maybe our own. J. Bacteriol. 202, e00331-20 (2020).

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  127. Liu, X. et al. Biological synthesis of high-conductive pili in aerobic bacterium Pseudomonas aeruginosa. Appl. Microbiol. Biotechnol. 103, 1535–1544 (2019).

    CAS  PubMed  Google Scholar 

  128. Ueki, T. et al. An Escherichia coli chassis for production of electrically conductive protein nanowires. ACS Synth. Biol. 9, 647–654 (2020).

    CAS  PubMed  Google Scholar 

  129. 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).

    PubMed  PubMed Central  Google Scholar 

  130. Liu, X. et al. A Geobacter sulfurreducens strain expressing Pseudomonas aeruginosa type IV pili localizes OmcS on pili but is deficient in Fe(III) oxide reduction and current production. Appl. Env. Microbiol. 80, 1219–1224 (2014).

    Google Scholar 

  131. Adhikari, R. Y., Malvankar, N. S., Tuominen, M. T. & Lovley, D. R. Conductivity of individual Geobacter pili. RSC Adv. 6, 8354–8357 (2016).

    CAS  Google Scholar 

  132. Ueki, T. et al. Geobacter strains expressing poorly conductive pili reveal constraints on direct interspecies electron transfer mechanisms. mBio 9, e01273-18 (2018).

    PubMed  PubMed Central  Google Scholar 

  133. Tan, Y. et al. Expressing the Geobacter metallireducens PilA in Geobacter sulfurreducens yields pili with exceptional conductivity. mBio 8, e02203-16 (2017).

    PubMed  PubMed Central  Google Scholar 

  134. Filman, D. J. et al. Cryo-EM reveals the structural basis of long-range electron transport in a cytochrome-based bacterial nanowire. Commun. Biol. 2, 219 (2019).

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  136. Yalcin, S. E. et al. Electric field stimulates production of highly conductive microbial OmcZ nanowires. Nat. Chem. Biol. 16, 1136–1142 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  137. Inoue, K. et al. Specific localization of the c-type cytochrome OmcZ at the anode surface in current-producing biofilms of Geobacter sulfurreducens. Environ. Microbiol. Rep. 3, 211–217 (2010).

    PubMed  Google Scholar 

  138. Nevin, K. P. et al. Anode biofilm transcriptomics reveals outer surface components essential for high current power production in Geobacter sulfurreducens fuel cells. PLoS ONE 4, e5628 (2009).

    PubMed  PubMed Central  Google Scholar 

  139. Mehta, T., Coppi, M. V., Childers, S. E. & Lovley, D. R. Outer membrane c-type cytochromes required for Fe(III) and Mn(IV) oxide reduction in Geobacter sulfurreducens. Appl. Environ. Microbiol. 71, 8634–8641 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  140. Walker, D. J. F. et al. Cytochrome OmcS is not essential for long-range electron transport in Geobacter sulfurreducens strain KN400. Preprint at bioRxiv https://doi.org/10.1101/2020.07.22.214791 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  142. Liu, X., Ye, Y., Xiao, K., Rensing, C. & Zhou, S. Molecular evidence for the adaptive evolution of Geobacter sulfurreducens to perform dissimilatory iron reduction in natural environments. Mol. Microbiol. 113, 783–793 (2020).

    CAS  PubMed  Google Scholar 

  143. Meysman, F. J. R. et al. A highly conductive fibre network enables centimetre-scale electron transport in multicellular cable bacteria. Nat. Commun. 10, 4120 (2019). This article quantifies the conductivity of the intracellular fibre network of cable bacteria.

    PubMed  PubMed Central  Google Scholar 

  144. Eachambadi, R. T. et al. An ordered and fail-safe electrical network in cable bacteria. Adv. Biosyst. 4, 2000006 (2020).

    Google Scholar 

  145. Kjeldsen, K. U. et al. On the evolution and physiology of cable bacteria. Proc. Natl Acad. Sci. USA 116, 19116–19125 (2019). This article presents important insights into cable bacteria derived from whole-genome sequencing.

    CAS  PubMed  PubMed Central  Google Scholar 

  146. Kato, S., Nakamura, R., Kai, F., Wantanabe, K. & Hashimoto, K. Respiratory interactions of soil bacteria with (semi)conductive iron-oxide minerals. Environ. Microbio 12, 3114–3123 (2010).

    CAS  Google Scholar 

  147. 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 

  148. Roden, E. R. et al. Extracellular electron transfer through microbial reduction of solid-phase humic substances. Nat. Geosci. 3, 417–421 (2010).

    CAS  Google Scholar 

  149. Chen, S. et al. Promoting interspecies electron transfer with biochar. Sci. Rep. 4, 5019 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  Google Scholar 

  151. Chen, S. et al. Carbon cloth stimulates direct interspecies electron transfer in syntrophic co-cultures. Bioresour. Tech. 173, 82–86 (2014).

    CAS  Google Scholar 

  152. Lu, Y. & Zhang, W. Biogeochemistry of methanogenesis with a specific emphasis on the mineral-facilitating effects. Acta Geochim. 36, 379–384 (2017).

    CAS  Google Scholar 

  153. Lovley, D. R., Woodward, J. C. & Chapelle, F. H. Stimulated anoxic biodegradation of aromatic hydrocarbons using Fe(III) ligands. Nature 370, 128–131 (1994).

    CAS  PubMed  Google Scholar 

  154. Lovley, D. R., Woodward, J. C. & Chapelle, F. H. Rapid anaerobic benzene oxidation with a variety of chelated Fe(III) forms. Appl. Env. Microbiol. 62, 288–291 (1996).

    CAS  Google Scholar 

  155. Bonaglia, S. et al. Activated carbon stimulates microbial diversity and PAH biodegradation under anaerobic conditions in oil-polluted sediments. Chemosphere 248, 126023 (2020).

    CAS  PubMed  Google Scholar 

  156. Lovley, D. R., Phillips, E. J. P., Gorby, Y. A. & Landa, E. R. Microbial reduction of uranium. Nature 350, 413–416 (1991).

    CAS  Google Scholar 

  157. Williams, K. H., Bargar, J. R., Lloyd, J. R. & Lovley, D. R. Bioremediation of uranium-contaminated groundwater: a systems approach to subsurface biogeochemistry. Curr. Opin. Biotechnol. 24, 489–497 (2013).

    CAS  PubMed  Google Scholar 

  158. 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 article presents an excellent review of the understanding of the strategy of promoting methane production with conductive materials.

    CAS  PubMed  Google Scholar 

  159. Guo, N. et al. Marine bacteria inhibit corrosion of steel via synergistic biomineralization. J. Mater. Sci. Technol. 66, 82–90 (2021).

    Google Scholar 

  160. Sun, Y.-L. et al. Conductive composite materials fabricated with microbially produced protein nanowires. Small 14, 1802624 (2018).

    Google Scholar 

  161. Sun, Y.-L. et al. Solvent-induced assembly of microbial protein nanowires into superstructured bundles. Biomacromolecules 22, 1305–1311 (2021).

    CAS  PubMed  Google Scholar 

  162. Liu, X. et al. Power generation from ambient humidity using protein nanowires. Nature 578, 550–554 (2020).

    CAS  PubMed  Google Scholar 

  163. Fu, T. et al. Bioinspired bio-voltage memristors. Nat. Commun. 11, 1861 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  164. Smith, A. F. et al. Bioelectronic protein nanowire sensors for ammonia detection. Nano Res. 13, 1479–1484 (2020).

    CAS  Google Scholar 

  165. Liu, X. et al. Multifunctional protein nanowire humidity sensors for green wearable electronics. Adv. Electron. Mater. 6, 2000721 (2020).

    CAS  Google Scholar 

  166. Gan, C. et al. Visualizing and isolating iron-reducing microorganisms at single cell level. Appl. Environ. Microbiol. 87, e02192-20 (2021).

    PubMed  PubMed Central  Google Scholar 

  167. Ueoka, N. & Watanabe, K. K. Electrode plate-culture methods for colony isolation of exoelectrogens from anode microbiomes. Bioelectrochemistry 124, 1–6 (2018). This article presents an innovative strategy for recovering electroactive microorganisms in culture.

    CAS  PubMed  Google Scholar 

  168. Yee, M. O., Deutzmann, J. S., Spormann, A. M. & Rotaru, A.-E. Cultivating electroactive microbes — from field to bench. Nanotechnology 31, 174003 (2020).

    CAS  PubMed  Google Scholar 

  169. Eren, A. M. et al. Anvi’o: an advanced analysis and visualization platform for ‘omics data. Peer J. 3, e1319 (2015).

    PubMed  PubMed Central  Google Scholar 

  170. Kumar, S., Stecher, G. & Tamura, K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  171. Adeney, W. E. On the reduction of manganese peroxide in sewage. Sci. Proc. R. Dublin Soc. 8, 247–251 (1894).

    Google Scholar 

  172. Potter, M. C. On the difference of potential due to the vital activity of microorganisms. Proc. Univ. Durh. Phil. Soc. 3, 245–249 (1910).

    Google Scholar 

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

    Google Scholar 

  174. Balashova, V. V. & Zavarzin, G. A. Anaerobic reduction of ferric iron by hydrogen bacteria. Microbiology 48, 635–639 (1980).

    Google Scholar 

  175. Semple, K. M. & Westlake, D. W. S. Characterization of iron-reducing Alteromonas putrefaciens strains from oil field fluids. Can. J. Microbiol. 33, 366–371 (1987).

    CAS  Google Scholar 

  176. Myers, C. R. & Nealson, K. H. Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science 240, 1319–1321 (1988).

    CAS  PubMed  Google Scholar 

  177. Lovley, D. R., Phillips, E. J. P. & Lonergan, D. J. Hydrogen and formate oxidation coupled to dissimilatory reduction of iron or manganese by Alteromonas putrefaciens. Appl. Environ. Microbiol. 55, 700–706 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  178. Hunt, K. A., Flynn, J. M., Naranjo, B., 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 article presents important clarification that S. oneidensis does not function as a respiratory electrotroph.

    CAS  PubMed  PubMed Central  Google Scholar 

  179. Kim, H. J. et al. A mediator-less microbial fuel cell using a metal reducing bacterium, Shewenella putrefaciens. Enzyme Microb. Technol. 30, 145–152 (2002).

    CAS  Google Scholar 

  180. 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 

  181. 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 

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

    CAS  PubMed  Google Scholar 

  183. Morita, M. et al. Potential for direct interspecies electron transfer in methanogenic wastewater digester aggregates. mBio 2, e00159-11 (2011).

    PubMed  PubMed Central  Google Scholar 

  184. Schicklberger, M., Sturm, G. & Gescher, J. Genomic plasticity enables a secondary electron transport pathway in Shewanella oneidensis. Appl. Env. Microbiol. 79, 1150–1159 (2013).

    CAS  Google Scholar 

  185. Jensen, H. M. et al. Engineering of a synthetic electron conduit in living cells. Proc. Natl Acad. Sci. USA 107, 19213–19218 (2010). This article presents an important early demonstration of the potential for bottom-up engineering of electroactive E. coli.

    CAS  PubMed  PubMed Central  Google Scholar 

  186. TerAvest, M. A. & Ajo-Franklin, C. M. Transforming exoelectrogens for biotechnology using synthetic biology. Biotechnol. Bioeng. 113, 687–697 (2016).

    CAS  PubMed  Google Scholar 

  187. Su, L. et al. Modifying cytochrome c maturation can increase the bioelectronic performance of engineered Escherichia coli. ACS Synth. Biol. 9, 115–124 (2020).

    CAS  PubMed  Google Scholar 

  188. Su, L., Fukushima, T. & Ajo-Franklin, C. M. A hybrid cyt c maturation system enhances the bioelectrical performance of engineered Escherichia coli by improving the rate-limiting step. Biosens. Bioelectron. 165, 112312 (2020).

    CAS  PubMed  Google Scholar 

  189. Thirumurthy, M. A. & Jones, A. K. Geobacter cytochrome OmcZs binds riboflavin: implications for extracellular electron transfer. Nanotechnology 31, 124001 (2020).

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank their former laboratory colleagues at the US Geological Survey and the University of Massachusetts, as well as collaborators too numerous to list, who have contributed to the study of electroactive microorganisms for more than 35 years. They apologize to all investigators whose excellent work could not be cited due to space constraints.

Author information

Authors and Affiliations

  1. Electrobiomaterials Institute, Key Laboratory for Anisotropy and Texture of Materials (Ministry of Education), Northeastern University, Shenyang, China

    Derek R. Lovley

  2. Department of Microbiology, University of Massachusetts, Amherst, MA, USA

    Derek R. Lovley & Dawn E. Holmes

  3. Institute for Applied Life Sciences (IALS), University of Massachusetts, Amherst, MA, USA

    Derek R. Lovley & Dawn E. Holmes

  4. Department of Physical and Biological Sciences, Western New England University, Springfield, MA, USA

    Dawn E. Holmes

Authors
  1. Derek R. Lovley
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dawn E. Holmes
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

D.E.H. performed the phylogenetic analysis displayed in Fig. 1. D.R.L. reviewed the literature and assembled additional figures. Both authors edited and approved the final text.

Corresponding author

Correspondence to Derek R. Lovley.

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.

Glossary

Microbial electrochemical technologies

Applications that rely on microorganism–electrode electron exchange, such as microbial fuel cells.

Electroactive microorganisms

Microorganisms that can exchange electrons with their extracellular environment.

Electromicrobiomes

Environments in which microorganisms electrically interact with each other and/or their extracellular environment.

Extracellular electron transfer

(EET). Electron transfer to or from another cell, electron acceptors not in solution or dissolved compounds that do not enter the cell.

Electrogens

Microorganisms that generate electricity in a bioelectrochemical system or donate electrons to natural extracellular electron acceptors.

Electrotrophs

Microorganisms that consume electricity in a bioelectrochemical system or accept electrons from natural extracellular electron donors.

Fe(III) oxides

Collectively, the diverse, poorly soluble Fe(III) minerals of various degrees of crystallinity that are abundant in most soils and sediments.

Anammox bacteria

Bacteria that combine ammonium with nitrite or nitrate to form nitrogen gas.

Cable bacteria

Bacteria that form filaments comprising thousands of cells to conduct electrons from anaerobic to aerobic zones of soils and sediments.

Direct interspecies electron transfer

(DIET). Electron exchange between two microbial species via electrical connections rather than a diffusible electron carrier such as H2.

Electron shuttles

Redox active molecules that can be reversibly oxidized and reduced that, at catalytic quantities, serve as an intermediary for extracellular electron transfer between cells and extracellular electron acceptors or donors.

Chelators

In the context of electromicrobiology, an organic compound that tightly binds and solubilizes metal ions, notably Fe(III).

Pilin

A monomer protein that bacteria assemble into pili.

Biofilms

A collective of one or more species of microorganisms adhered to a surface.

Archaella

Filaments produced by archaea for motility or attachment, which in some instances may be electrically conductive.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lovley, D.R., Holmes, D.E. Electromicrobiology: the ecophysiology of phylogenetically diverse electroactive microorganisms. Nat Rev Microbiol 20, 5–19 (2022). https://doi.org/10.1038/s41579-021-00597-6

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41579-021-00597-6

This article is cited by

Search

Advanced search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

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