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Microbial nanowires for sustainable electronics

  • Review Article
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From Nature Reviews Bioengineering

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Abstract

Microbial protein nanowires are emerging as an alternative to abiotic nanowires for electronics applications. Microbial nanowires are sustainably produced, robust, non-toxic, biodegradable and uniquely malleable to precision genetic tailoring, which can confer specific functionalities. At present, the microbial nanowires that seem most adaptable to electronics applications are curli fibres, electrically conductive pili (e-pili) and c-type cytochrome filaments. These nanowires are all highly resistant to conditions that denature most proteins. Editing of the genes encoding curli fibre and e-pili monomers has yielded nanowires with enhanced functions, including increased conductivity, improved sensor selectivity and sensitivity, metal-binding properties, increased surface attachment, and improved nanowire alignment. Such microbial nanowires are highly processable in the organic solvents required for some device fabrication methods and readily incorporated into polymers without loss of function. This Review describes promising electronic devices for sensing, electricity generation and neuromorphic memory that depend on microbial nanowire components and discusses preliminary evidence of the feasibility of other microbial nanowire applications such as transistors, optoelectronics and supercapacitors. Factors that affect the commercialization of microbial nanowire-based electronics are also considered.

Key points

  • Microbial nanowires offer advantages over comparable abiotic materials, such as silicon nanowires and carbon nanotubes, because microbial products can be produced from renewable feedstocks without requiring high energy inputs or toxic reagents.

  • Microbial nanowires can be precision genetically tailored to have specific conductivities and functionalities. Tailoring can be accomplished simply by modifying the amino acid content of nanowire monomers and/or altering their encoding genes.

  • Functional re-engineering and incorporation into novel electronic devices have already been demonstrated for curli fibres and electrically conductive pili. Cytochrome nanowires also have unique properties with potential applications in electronics.

  • Sensors with high specificity and selectivity as well as novel memory and electricity-generating devices have been fabricated with microbial nanowires. Other envisioned applications include supercapacitors and transistors.

  • Escherichia coli is an effective chassis for large-scale production of curli fibres and electrically conductive pili, but substantial optimization of microbial nanowire production and harvesting is required for commercial-scale filament production.

  • Continued prospection of the microbial world to identify new types of microbial nanowires is warranted to expand the potential functionality options for the fabrication of novel nanowire-based materials and devices.

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Fig. 1: Microbial nanowires with potential applications in electronic devices.
Fig. 2: Tuning and modification of curli fibres and e-pili characteristics.
Fig. 3: Strategies for assembly of microbial nanowires into large structures.
Fig. 4: Strategies for improving the mass production of microbial nanowires.
Fig. 5: Electronic devices fabricated with microbial nanowires.

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References

  1. Lovley, D. R. e-Biologics: fabrication of sustainable electronics with ‘green’ biological materials. mBio 8, e00695-17 (2017).

    Article  Google Scholar 

  2. Lovley, D. R. & Yao, J. Intrinsically conductive microbial nanowires for ‘green’ electronics with novel functions. Trends Biotechnol. 39, 940–952 (2021).

    Article  Google Scholar 

  3. Atkinson, J. T., Chavez, M. S., Ninman, C. M. & El-Naggar, M. Y. Living electronics: a catalogue of engineered living electronic components. Microb. Biotechnol. 16, 507–533 (2023).

    Article  Google Scholar 

  4. Tao, K., Makam, P., Aizen, R. & Gazit, E. Self-assembling peptide semiconductors. Science 358, eaam9756 (2017).

    Article  Google Scholar 

  5. Fuller, C. W. et al. Molecular electronics sensors on a scalable semiconductor chip: a platform for single-molecule measurement of binding kinetics and enzyme activity. Proc. Natl Acad. Sci. USA 119, e2112812119 (2022).

    Article  Google Scholar 

  6. Jiang, T., Zeng, B.-F., Zhang, B. & Tang, L. Single-molecular protein-based bioelectronics via electronic transport: fundamentals, devices and applications. Chem. Soc. Rev. 52, 5968–6002 (2023).

    Article  Google Scholar 

  7. Chellamuthu, P. et al. Engineering bacteria for biogenic synthesis of chalcogenide nanomaterials. Microb. Biotechnol. 12, 161–172 (2018).

    Article  Google Scholar 

  8. Roy, S., Xie, O. & Dorval Courchesne, N.-M. Challenges in engineering conductive protein fibres: disentangling the knowledge. Can. J. Chem. Engin. 98, 2081–2095 (2020).

    Article  Google Scholar 

  9. Gutermann, T. & Gazit, E. Toward peptide-based bioelectronics: reductionist design of conductive pili mimetics. Bioelctron Med. 1, 131–137 (2018).

    Article  Google Scholar 

  10. Creasey, R. C. G. et al. Microbial nanowires — electron transport and the role of synthetic analogues. Acta Biomater. 69, 1–30 (2018).

    Article  MathSciNet  Google Scholar 

  11. Hsu, L., Deng, P., Zhang, Y. & JIang, X. Core/shell bacterial cables: a one-dimensional platform for probing microbial electron transfer. Nano Lett. 18, 4606–4610 (2018).

    Article  Google Scholar 

  12. Liu, X. et al. Microbial biofilms for electricity generation from water evaporation and power to wearables. Nat. Commun. 13, 4369 (2022).

    Article  Google Scholar 

  13. Bird, L. J. et al. Engineering wired life: synthetic biology for electroactive bacteria. ACS Synth. Biol. 10, 2808–2823 (2021).

    Article  Google Scholar 

  14. Lekbach, Y. et al. Microbial nanowires with genetically modified peptide ligands to sustainably fabricate electronic sensing devices. Biosens. Bioelectron. 226, 115147 (2023). This study demonstrated that genetically tailoring of a nanowire amino acid sequence led to increased sensitivity and selectivity in electronic sensing applications.

    Article  Google Scholar 

  15. Londer, Y. Y., Pokkuluir, P. R., Orshonsky, V., Orshonsky, L. & Schiffer, M. Heterologous expression of dodecaheme “nanowire” cytochromes c from Geobacter sulfurreducens. Protein Expr. Purif. 47, 241–248 (2006).

    Article  Google Scholar 

  16. Clarke, T. A. Plugging into bacterial nanowires: a comparison of model electrogenic organisms. Curr. Opin. Microbiol. 66, 56–62 (2022).

    Article  Google Scholar 

  17. Balistreri, A., Goetzler, E. & Chapman, M. Functional amyloids are the rule rather than the exception in cellular biology. Microorganisms 8, 1951 (2020).

    Article  Google Scholar 

  18. Barnhart, M. M. & Chapman, M. R. Curli biogenesis and function. Annu. Rev. Microbiol. 60, 131–147 (2006).

    Article  Google Scholar 

  19. Evans, M. L. & Chapman, M. R. Curli biogenesis: order out of disorder. Biochim. Biophys. Acta 1843, 1551–1558 (2014). This review provides an excellent overview of the curli secretion pathway and assembly into nanowire-like extracellular appendages.

    Article  Google Scholar 

  20. Chapman, M. R. et al. Role of Escherichia coli curli operons in directing amyloid fiber formation. Science 295, 851–855 (2002).

    Article  Google Scholar 

  21. Nenninger, A. A. et al. CsgE is a curli secretion specificity factor that prevents amyloid fibre aggregation. Mol. Microbiol. 81, 486–499 (2011).

    Article  Google Scholar 

  22. Wang, X., Hammer, N. D. & Chapman, M. R. The molecular basis of functional bacterial amyloid polymerization and nucleation. J. Biol. Chem. 283, 21530–21539 (2008).

    Article  Google Scholar 

  23. Wang, X., Zhou, Y., Ren, J. J., Hammer, N. D. & Chapman, M. R. Gatekeeper residues in the major curlin subunit modulate bacterial amyloid fiber biogenesis. Proc. Natl Acad. Sci. USA 107, 163–168 (2010).

    Article  Google Scholar 

  24. Shewmaker, F. et al. The functional curli amyloid is not based on in-register parallel β-sheet structure. J. Biol. Chem. 284, 25065–25076 (2009).

    Article  Google Scholar 

  25. Dueholm, M. S. et al. Fibrillation of the major curli subunit CsgA under a wide range of conditions implies a robust design of aggregation. Biochemistry 50, 8281–8290 (2011).

    Article  Google Scholar 

  26. Dorval Courchesne, N. M. et al. Biomimetic engineering of conductive curli protein films. Nanotechnology 29, 454002 (2018). This study demonstrated that increasing the aromatic amino acid content in CsgA subunits yields curli fibre thin films with enhanced conductivity.

    Article  Google Scholar 

  27. Schleeger, M. et al. Amyloids: from molecular structure to mechanical properties. Polymer 54, 2473–2488 (2013).

    Article  Google Scholar 

  28. Lamour, G. et al. Mapping the broad structural and mechanical properties of amyloid fibrils. Biophys. J. 112, 584–594 (2017).

    Article  Google Scholar 

  29. Duraj-Thatte, A. M. et al. Genetically programmable self-regenerating bacterial hydrogels. Adv. Mater. 31, e1901826 (2019).

    Article  Google Scholar 

  30. Dorval Courchesne, N. M., Duraj-Thatte, A., Tay, P. K. R., Nguyen, P. Q. & Joshi, N. S. Scalable production of genetically engineered nanofibrous macroscopic materials via filtration. ACS Biomater. Sci. Eng. 3, 733–741 (2017). Early description of a scalable process for isolating curli fibres, without the need for affinity tags, using size-based separation.

    Article  Google Scholar 

  31. Duraj-Thatte, A. M. et al. Water-processable, biodegradable and coatable aquaplastic from engineered biofilms. Nat. Chem. Biol. 17, 732–738 (2021).

    Article  Google Scholar 

  32. Abdali, Z. et al. Curli-mediated self-assembly of a fibrous protein scaffold for hydroxyapatite mineralization. ACS Synth. Biol. 9, 3334–3343 (2020).

    Article  Google Scholar 

  33. Praveschotinunt, P. et al. Tracking of engineered bacteria in vivo using nonstandard amino acid incorporation. ACS Synth. Biol. 7, 1640–1650 (2018).

    Article  Google Scholar 

  34. Tay, P. K. R., Nguyen, P. Q. & Joshi, N. S. A synthetic circuit for mercury bioremediation using self-assembling functional amyloids. ACS Synth. Biol. 6, 1841–1850 (2017).

    Article  Google Scholar 

  35. Nussbaumer, M. G. et al. Bootstrapped biocatalysis: biofilm-derived materials as reversibly functionalizable multienzyme surfaces. ChemCatChem 9, 4328–4333 (2017).

    Article  Google Scholar 

  36. Praveschotinunt, P. et al. Engineered E. coli Nissle 1917 for the delivery of matrix-tethered therapeutic domains to the gut. Nat. Commun. 10, 5580 (2019).

    Article  Google Scholar 

  37. Saldanha, D. J., Abdali, Z., Modafferi, D., Janfeshan, B. & Dorval Courchesne, N.-M. Fabrication of fluorescent pH-responsive protein–textile composites. Sci. Rep. 10, 13052 (2020).

    Article  Google Scholar 

  38. Huyer, C. et al. Fabrication of curli fiber-PEDOT:PSS biomaterials with tunable self-healing, mechanical, and electrical properties. ACS Biomater. Sci. Eng. 9, 2156–2169 (2023).

    Article  Google Scholar 

  39. Cai, A., Abdali, Z., Saldanha, D. J., Aminzare, M. & Dorval Courchesne, N.-M. Endowing textiles with self-repairing ability through the fabrication of composites with a bacterial biofilm. Sci. Rep. 13, 11389 (2023).

    Article  Google Scholar 

  40. Duraj-Thatte, A. M. et al. Programmable microbial ink for 3D printing of living materials produced from genetically engineered protein nanofibers. Nat. Commun. 12, 6600 (2021).

    Article  Google Scholar 

  41. Axpe, E. et al. Fabrication of amyloid curli fibers–alginate nanocomposite hydrogels with enhanced stiffness. ACS Biomater. Sci. Eng. 4, 2100–2105 (2018).

    Article  Google Scholar 

  42. Reguera, G. et al. Extracellular electron transfer via microbial nanowires. Nature 435, 1098–1101 (2005). This paper demonstrated microbial expression of electrically conductive protein nanowires and their physiological role in extracellular electron transfer.

    Article  Google Scholar 

  43. Lovley, D. R. & Holmes, D. E. Electromicrobiology: the ecophysiology of phylogenetically diverse electroactive microorganisms. Nat. Rev. Microbiol. 20, 5–19 (2022).

    Article  Google Scholar 

  44. Wang, F. et al. Structure of microbial nanowires reveals stacked hemes that transport electrons over micrometers. Cell 177, 361–369 (2019). This paper included a description of a cytochrome nanowire structure and measurements of cytochrome nanowire conductivity.

    Article  Google Scholar 

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

    Article  Google Scholar 

  46. Gu, Y. et al. Structure of Geobacter pili reveals secretory rather than nanowire behaviour. Nature 597, 430–434 (2021).

    Article  Google Scholar 

  47. Gu, Y. et al. Structure of Geobacter cytochrome OmcZ identifies mechanism of nanowire assembly and conductivity. Nat. Microbiol. 8, 284–298 (2023).

    Article  Google Scholar 

  48. Wang, F. et al. Structure of Geobacter OmcZ filaments suggests extracellular cytochrome polymers evolved independently multiple times. eLife 11, e8155 (2022). This report describes the only known structurally branched cytochrome nanowire.

    Article  Google Scholar 

  49. Wang, F. et al. Cryo-EM structure of an extracellular Geobacter OmcE cytochrome filament reveals tetrahaem packing. Nat. Microbiol. 7, 1291–1300 (2022).

    Article  Google Scholar 

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

    Article  Google Scholar 

  51. Lovley, D. R. On the existence of pilin-based microbial nanowires. Front. Microbiol. 13, 872610 (2022).

    Article  Google Scholar 

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

    Article  Google Scholar 

  53. Ueki, T. et al. An Escherichia coli chassis for production of electrically conductive protein nanowires. ACS Synth. Biol. 9, 647–654 (2020). This paper describes the construction of a bacterial strain optimized for mass production of pilin-based conductive nanowires.

    Article  Google Scholar 

  54. Szmuc, E. et al. Engineering Geobacter pili to produce metal:organic filaments. Biosens. Bioelectron. 222, 114993 (2023).

    Article  Google Scholar 

  55. Liu, X., Walker, D. J. F., Nonnenmann, S., Sun, D. & Lovley, D. R. Direct observation of electrically conductive pili emanating from Geobacter sulfurreducens. mBio 12, e02209-21 (2021).

    Article  Google Scholar 

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

    Article  Google Scholar 

  57. Sonawane, J. M. et al. Incorporating microbial pilin-based nanowires in a water-stable electronic polymer composite. Preprint at bioRxiv https://doi.org/10.1101/2024.1106.1111.598525 (2024).

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

    Article  Google Scholar 

  59. 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).

    Article  Google Scholar 

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

    Article  Google Scholar 

  61. Steidl, R. J., Lampa-Pastirk, S. & Reguera, G. Mechanistic stratification in electroactive biofilms of Geobacter sulfurreducens mediated by pilus nanowires. Nat. Commun. 7, 12217 (2016).

    Article  Google Scholar 

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

    Article  Google Scholar 

  63. Liu, X. et al. Cytochrome OmcS is not essential for extracellular electron transport via conductive pili in Geobacter sulfurreducens strain KN400. Appl. Env. Microbiol. 88, e0162221 (2022).

    Article  Google Scholar 

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

    Article  Google Scholar 

  65. Guberman-Pfeffer, M. J. To be or not to be a cytochrome: electrical characterizations are inconsistent with Geobacter cytochrome ‘nanowires’. Front. Microbiol. 15, 1397124 (2024).

    Article  Google Scholar 

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

    Article  Google Scholar 

  67. 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).

    Article  Google Scholar 

  68. Walker, D. J. F. et al. The archaellum of Methanospirillum hungatei is electrically conductive. mBio 10, e00579-19 (2019). This study demonstrated that archaea can express electrically conductive protein nanowires.

    Article  Google Scholar 

  69. Myers, B. et al. Engineering nanowires in bacteria to elucidate electron transport structural–functional relationships. Sci. Rep. 13, 8843 (2023).

    Article  Google Scholar 

  70. 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. Genom. 2, e000072 (2016).

    Google Scholar 

  71. Sun, Y.-L. et al. Conductive composite materials fabricated with microbially produced protein nanowires. Small 14, 1802624 (2018). This report demonstrated the fabrication of electrically conductive composites composed of microbial nanowires and a polymer.

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  74. Liu, X. et al. Power generation from ambient humidity using protein nanowires. Nature 578, 550–554 (2020). This study describes the generation of electricity from atmospheric humidity using thin films of microbial nanowires.

    Article  Google Scholar 

  75. Liu, X., Gao, H., Sun, L. & Yao, J. Generic Air-Gen effect in nanoporous materials for sustainable energy harvesting from air humidity. Adv. Mater. 2023, 2300748 (2023).

    Google Scholar 

  76. Lampa-Pastirk, S. et al. Thermally activated charge transport in microbial protein nanowires. Sci. Rep. 6, 23517 (2016).

    Article  Google Scholar 

  77. Poweleit, N. et al. CryoEM structure of the Methanospirillum hungatei archaellum reveals structural features distinct from the bacterial flagellum and type IV pilus. Nat. Microbiol. 2, 16222 (2016).

    Article  Google Scholar 

  78. Tran, H. T. Investigation of chemotaxis genes and their functions in Geobacter species. PhD thesis, University of Massachusetts Amherst (2009).

  79. 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).

    Article  Google Scholar 

  80. Baquero, D. P. et al. Extracellular cytochrome nanowires appear to be ubiquitous in prokaryotes. Cell 186, 2853–2864 (2023).

    Article  Google Scholar 

  81. 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).

    Article  Google Scholar 

  82. Schwarz, I. A. et al. Lack of physiological evidence for cytochrome filaments functioning as conduits for extracellular electron transfer. mBio 15, e00690-24 (2024).

    Article  Google Scholar 

  83. Dahl, P. J. et al. A 300-fold conductivity increase in microbial cytochrome nanowires due to temperature-induced restructuring of hydrogen bonding networks. Sci. Adv. 8, eabm7193 (2022).

    Article  Google Scholar 

  84. Guberman-Pfeffer, M. J. Structural determinants of redox conduction favor robustness over tunability in microbial cytochrome nanowires. J. Phys. Chem. B 127, 7148–7161 (2023). This report presents a theoretical analysis of electrical conductivity in archetypal cytochrome nanowire structures.

    Article  Google Scholar 

  85. Gubermann-Pfeffer, M. J. Assessing thermal response of redox conduction for anti-Arrhenius kinetics in a microbial cytochrome nanowire. J. Phys. Chem. B 126, 10083–10097 (2022).

    Article  Google Scholar 

  86. Jiang, X. et al. Probing single-to multi-cell level charge transport in Geobacter sulfurreducens DL-1. Nat. Commun. 4, 2751 (2013).

    Article  Google Scholar 

  87. Karamash, M. et al. Reduction kinetic of water soluble metal salts by Geobacter sulfurreducens: Fe2+/hemes stabilize and regulate electron flux rates. Front. Microbiol. 13, 909109 (2022).

    Article  Google Scholar 

  88. Blumberger, J. Electron transfer and transport through multi-heme proteins: recent progress and future directions. Curr. Opin. Chem. Biol. 47, 24–31 (2018).

    Article  Google Scholar 

  89. Futera, Z. et al. Coherent electron transport across a 3 nm bioelectronic junction made of multi-heme proteins. J. Phys. Chem. Lett. 11, 9766–9774 (2020).

    Article  Google Scholar 

  90. Bostick, C. D. et al. Protein bioelectronics: a review of what we do and do not know. Rep. Progr Phys. 81, 026601 (2018).

    Article  Google Scholar 

  91. Jiang, X. et al. Which multi-heme protein complex transfers electrons more efficiently? Comparing MtrCAB from Shewanella with OmcS from Geobacter. J. Phys. Chem. Lett. 11, 9421–9425 (2020).

    Article  Google Scholar 

  92. van Wonderen, J. H. et al. Ultrafast light-driven electron transfer in a Ru(II)tris(bipyridine)-labeled multiheme cytochrome. J. Am. Chem. Soc. 141, 15190–15200 (2019).

    Article  Google Scholar 

  93. van Wonderen, J. H. et al. Nanosecond heme-to-heme electron transfer rates in a multiheme cytochrome nanowire reported by a spectrally unique His/Met-ligated heme. Proc. Natl Acad. Sci. USA 118, e2107939118 (2021).

    Article  Google Scholar 

  94. Moser, C. C., Page, C. C., Chen, X. & Dutton, P. L. In: Enzyme-Catalyzed Electron and Radical Transfer. Book series: Subcellular Biochemistry (eds Holzenburg, A. & Scrutton, N.S.) vol. 35, 1–28 (2000).

  95. Guberman-Pfeffer, M. J. From hot water to dry dirt: microbes use cytochrome ‘nanowires’ of similar conductivity but different structure. Preprint at bioRxiv https://doi.org/10.1101/2023.06.12.544705 (2023).

  96. Hutchins, G. H. et al. An expandable, modular de novo protein platform for precision redox engineering. Proc. Natl Acad. Sci. USA 120, e2306046120 (2023).

    Article  Google Scholar 

  97. Travaglini, L. et al. Fabrication of electronically conductive protein–heme nanowires for power harvesting. Small https://doi.org/10.1002/smll.202311661 (2024).

    Article  Google Scholar 

  98. Pfeffer, C. et al. Filamentous bacteria transport electrons over centimetre distances. Nature 491, 218–221 (2012). This study reports the discovery of cable bacteria and their remarkable long-range electron transport.

    Article  Google Scholar 

  99. Bjerg, J. T. et al. Long-distance electron transport in individual, living cable bacteria. Proc. Natl Acad. Sci. USA 115, 5786–5791 (2018).

    Article  Google Scholar 

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

    Article  Google Scholar 

  101. Jiang, Z. et al. In vitro single-cell dissection revealing the interior structure of cable bacteria. Proc. Natl Acad. Sci. USA 115, 8517–8522 (2018).

    Article  Google Scholar 

  102. 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 paper provides important data on the conductivity of cable bacteria filaments.

    Article  Google Scholar 

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

    Article  Google Scholar 

  104. Bonné, R. et al. Intrinsic electrical properties of cable bacteria reveal an Arrhenius temperature dependence. Sci. Rep. 10, 19798 (2020).

    Article  Google Scholar 

  105. Boschker, H. T. S. et al. Efficient long-range conduction in cable bacteria through nickel protein wires. Nat. Commun. 12, 3996 (2021).

    Article  Google Scholar 

  106. Yang, T., Chavez, M. S., Niman, C. M., Xu, S. & El-Naggar, M. Y. Long-distance electron transport in multicellular freshwater cable bacteria. eLife https://doi.org/10.7554/eLife.91097.1.sa2 (2023).

  107. Nielsen, L. P. & Risgaard-Petersen, N. Rethinking sediment biogeochemistry after the discovery of electric currents. Ann. Rev. Mar. Sci. 7, 424–442 (2015).

    Article  Google Scholar 

  108. van der Veen, J. R., Valianti, S., van der Zant, H. S. J., Blanter, Y. M. & Meysman, F. J. R. A model analysis of centimeter-long electron transport in cable bacteria. Phys. Chem. Chem. Phys. 26, 3139–3151 (2024).

    Article  Google Scholar 

  109. Bonné, R., Wouters, K., Lustermans, J. J. M. & Manca, J. V. Biomaterials and electroactive bacteria for biodegradable electronics. Front. Microbiol. 13, 906363 (2022).

    Article  Google Scholar 

  110. Dohnalkova, A. C. et al. Imaging hydrated microbial extracellular polymers: comparative analysis by electron microscopy. Appl. Env. Microbiol. 77, 1254–1262 (2011).

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  113. Subramanian, P., Pribadian, S., El-Naggar, M. Y. & Jensen, G. J. The ultrastructure of Shewanella oneidensis MR-1 nanowires revealed by electron cryo-tomography. Proc. Natl Acad. Sci. USA 115, E3246–E3255 (2018).

    Article  Google Scholar 

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

    Article  Google Scholar 

  115. Bid, A., Bora, A. & Raychaudhuri, A. K. Temperature dependence of the resistance of metallic nanowires of diameter ≥15 nm: applicability of Bloch-Grüneisen theorem. Phys. Rev. B 74, 035426 (2006).

    Article  Google Scholar 

  116. Tan, Y. et al. Synthetic biological protein nanowires with high conductivity. Small 12, 4481–4485 (2016).

    Article  Google Scholar 

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

    Article  Google Scholar 

  118. Shapiro, D. M. et al. Protein nanowires with tunable functionality and programmable self-assembly using sequence-controlled synthesis. Nat. Commun. 13, 829 (2022).

    Article  Google Scholar 

  119. Ru, X., Zhang, P. & Beratan, D. N. Assessing possible mechanisms of micrometer scale electron transfer in heme free Geobacter sulfurreducens pili. J. Phys. Chem. B 123, 5035–5047 (2019).

    Article  Google Scholar 

  120. Krishnan, S., Aksimentiev, A., Lindsay, S. & Matyushov, D. Long-range conductivity in proteins mediated by aromatic residues. ACS Phys. Chem. Au 3, 444–455 (2023).

    Article  Google Scholar 

  121. Kalyoncu, E., Ahan, R. E., Olmez, T. T. & Safak Seker, U. O. Genetically encoded conductive protein nanofibers secreted by engineered cells. RSC Adv. 7, 32543–32551 (2017). This study combined inspiration from the Geobacter pilin protein and a CsgA scaffold to produce conductive E. coli biofilms.

    Article  Google Scholar 

  122. Chen, A. Y. et al. Synthesis and patterning of tunable multiscale materials with engineered cells. Nat. Mater. 13, 515–523 (2014). This study developed genetic engineering strategies to pattern functional curli fibres, including conductive fibres, by interfacing with inorganic nanoparticles.

    Article  Google Scholar 

  123. Seker, U. O. S., Chen, A. Y., Citorik, R. J. & Lu, T. K. Synthetic biogenesis of bacterial amyloid nanomaterials with tunable inorganic–organic interfaces and electrical conductivity. ACS Synth. Biol. 6, 266–275 (2017).

    Article  Google Scholar 

  124. Kim, J. et al. Peptide-mediated shape- and size-tunable synthesis of gold nanostructures. Acta Biomater. 6, 2681–2689 (2010).

    Article  Google Scholar 

  125. Nam, K. T. et al. Virus-enabled synthesis and assembly of nanowires for lithium ion battery electrodes. Science 312, 885–888 (2006).

    Article  Google Scholar 

  126. Slocik, J. M., Stone, M. O. & Naik, R. R. Synthesis of gold nanoparticles using multifunctional peptides. Small 1, 1048–1052 (2005).

    Article  Google Scholar 

  127. Nguyen, P. Q., Botyanszki, Z., Tay, P. K. R. & Joshi, N. S. Programmable biofilm-based materials from engineered curli nanofibres. Nat. Commun. 5, 4945 (2014). This study demonstrates how curli fibres can serve as a platform to display functional peptides on the surface of the filaments.

    Article  Google Scholar 

  128. Wang, X. et al. Photocatalyst-mineralized biofilms as living bio-abiotic interfaces for single enzyme to whole-cell photocatalytic applications. Sci. Adv. 8, eabm7665 (2022).

    Article  Google Scholar 

  129. Hidalgo, G., Chen, X., Hay, A. G. & Lion, L. W. Curli produced by Escherichia coli PHL628 provide protection from Hg(II). Appl. Env. Microbiol. 76, 6939–6941 (2010).

    Article  Google Scholar 

  130. Sarlet, A., Ruffine, V., Blank, K. G. & Bidan, C. M. Influence of metal cations on the viscoelastic properties of Escherichia coli biofilms. ACS Omega 8, 4667–4676 (2023).

    Article  Google Scholar 

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

    Article  Google Scholar 

  132. Giltner, C. L. et al. The Pseudomonas aeruginosa type IV pilin receptor binding domain functions as an adhesin for both biotic and abiotic surfaces. Mol. Microbiol. 59, 1083–1096 (2006).

    Article  Google Scholar 

  133. Brown, S. Metal-recognition by repeating polypeptides. Nat. Biotechnol. 15, 269–272 (1997).

    Article  Google Scholar 

  134. Seker, U. O., Wilson, B., Sahin, D., Tamerler, C. & Sarikaya, M. Quantitative affinity of genetically engineered repeating polypeptides to inorganic surfaces. Biomacromolecules 10, 250–257 (2009).

    Article  Google Scholar 

  135. Sanghvi, A. B., Miller, K. P., Belcher, A. M. & Schmidt, C. E. Biomaterials functionalization using a novel peptide that selectively binds to a conducting polymer. Nat. Mater. 4, 496–502 (2005).

    Article  Google Scholar 

  136. Naik, R. R., Brott, L. L., Clarson, S. J. & Stone, M. O. Silica-precipitating peptides isolated from a combinatorial phage display peptide library. J. Nanosci. Nanotechnol. 2, 95–100 (2002).

    Article  Google Scholar 

  137. DeBenedictis, E. P., Ma, D. & Keten, S. Structural predictions for curli amyloid fibril subunits CsgA and CsgB. RSC Adv. 7, 48102 (2017).

    Article  Google Scholar 

  138. Zhong, C. et al. Strong underwater adhesives made by self-assembling multi-protein nanofibres. Nat. Nanotechnol. 9, 858–866 (2014).

    Article  Google Scholar 

  139. Li, L. & Zeng, H. Marine mussel adhesion and bio-inspired wet adhesives. Biotribology 5, 44–51 (2016).

    Article  Google Scholar 

  140. Kim, S., Sung, B. H., Kim, S. C. & Lee, H. S. Genetic incorporation of L-dihydroxyphenylalanine (DOPA) biosynthesized by a tyrosine phenol-lyase. Chem. Commun. 54, 3002–3005 (2018).

    Article  Google Scholar 

  141. Moser, F., Tham, E., González, L. M., Lu, T. K. & Voigt, C. A. Light-controlled, high-resolution patterning of living engineered bacteria onto textiles, ceramics, and plastic. Adv. Funct. Mater. 29, 1901788 (2019).

    Article  Google Scholar 

  142. 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).

    Article  Google Scholar 

  143. Malvankar, N. S., Mester, T., Tuominen, M. T. & Lovley, D. R. Supercapacitors based on c-type cytochromes using conductive nanostructured networks of living bacteria. ChemPhysChem 13, 463–468 (2012).

    Article  Google Scholar 

  144. Neu, J. et al. Microbial biofilms as living photoconductors due to ultrafast electron transfer in cytochrome OmcS nanowires. Nat. Commun. 13, 5150 (2022).

    Article  Google Scholar 

  145. Swasthi, H. M., Bhasne, K., Mahapatra, S. & Mukhopadhyay, S. Human fibrinogen inhibits amyloid assembly of biofilm-forming CsgA. Biochemistry 57, 6270–6273 (2018).

    Article  Google Scholar 

  146. Jain, N. et al. Inhibition of curli assembly and Escherichia coli biofilm formation by the human systemic amyloid precursor transthyretin. Proc. Natl Acad. Sci. USA 114, 12184–12189 (2017).

    Article  Google Scholar 

  147. Ueki, T. et al. Generation of high current densities in Geobacter sulfurreducens lacking the putative gene for the PilB pilus assembly motor. Microbiol. Spectr. 9, e0087721 (2021).

    Article  Google Scholar 

  148. Lin, T. et al. Expression of filaments of the Geobacter extracellular cytochrome OmcS in Shewanella oneidensis. Biotechnol. Bioeng. 121, 2002–2012 (2024). This report describes heterologous expression of cytochrome-based nanowires in a host amenable to large-scale culture under aerobic conditions.

    Article  Google Scholar 

  149. Hospenthal, M. K., Costa, T. R. D. & Waksman, G. A comprehensive guide to pilus biogenesis in Gram-negative bacteria. Nat. Rev. Microbiol. 15, 365–379 (2017).

    Article  Google Scholar 

  150. Mondino, S., San Martin, F. & Buschiazzo, A. 3D cryo-EM imaging of bacterial flagella: novel structural and mechanistic insights into cell motility. J. Biol. Chem. 298, 102105 (2022).

    Article  Google Scholar 

  151. Diaz Ricci, J. C. & Hernandez, M. E. Plasmid effects on Escherichia coli metabolism. Crit. Rev. Biotechnol. 20, 79–108 (2000).

    Article  Google Scholar 

  152. Silva, F., Queiroz, J. A. & Domingues, F. C. Evaluating metabolic stress and plasmid stability in plasmid DNA production by Escherichia coli. Biotechnol. Adv. 30, 691–708 (2012).

    Article  Google Scholar 

  153. Luna Rico, A., Zheng, W., Petiot, N., Egelman, E. H. & Francetic, O. Functional reconstitution of the type IVa pilus assembly system from enterohaemorrhagic Escherichia coli. Mol. Microbiol. 111, 732–749 (2019).

    Article  Google Scholar 

  154. Kouzuma, A. Molecular mechanisms regulating the catabolic and electrochemical activities of Shewanella oneidensis MR-1. Biosci. Biotechnol. Biochem. 85, 1572–1581 (2021).

    Article  Google Scholar 

  155. Gralnick, J. A. & Bond, D. R. Electron transfer beyond the outer membrane: putting electrons to rest. Annu. Rev. Microbiol. 77, 517–539 (2023).

    Article  Google Scholar 

  156. Shi, L. et al. Direct involvement of type II secretion system in extracellular translocation of Shewanella oneidensis outer membrane cytochromes MtrC and OmcA. J. Bacteriol. 190, 5512–5516 (2008).

    Article  Google Scholar 

  157. Jensen, H. M. et al. Engineering of a synthetic electron conduit in living cells. Proc. Natl Acad. Sci. USA 107, 19213–19218 (2010).

    Article  Google Scholar 

  158. Goldbeck, C. P. et al. Tuning promoter strengths for improved synthesis and function of electron conduits in Escherichia coli. ACS Synth. Biol. 2, 150–159 (2013).

    Article  Google Scholar 

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

    Article  Google Scholar 

  160. Tran, D. P., Pham, T. T. T., Wolfrum, B., Offenhausser, A. & Thierry, B. CMOS-compatible silicon nanowire field-effect transistor biosensor: technology development toward commercialization. Materials 11, 785 (2018).

    Article  Google Scholar 

  161. Ahmad, R., Mahmoudi, T., Ahn, M.-S. & Hahn, T.-B. Recent advances in nanowires-based field-effect transistors for biological sensor applications. Biosens. Bioelectron. 100, 312–325 (2018).

    Article  Google Scholar 

  162. Baraban, L., Ibarlucea, B., Baek, E. & Cuniberti, G. Hybrid silicon nanowire devices and their functional diversity. Adv. Sci. 6, 1900522 (2019).

    Article  Google Scholar 

  163. Smith, R., Geary, S. M. & Salem, A. K. Silicon nanowires and their impact on cancer detection and monitoring. ACS Appl. Nano Mater. 3, 8552–8536 (2020).

    Article  Google Scholar 

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

    Article  Google Scholar 

  165. Wu, T.-Z., Lo, Y.-R. & Chan, E.-C. Exploring the recognized bio-mimicry materials for gas sensing. Biosens. Bioelectron. 16, 945–953 (2001).

    Article  Google Scholar 

  166. Sfragano, P. S., Moro, G., Polo, F. & Palchetti, I. The role of peptides in the design of electrochemical biosensors for clinical diagnostics. Biosensors 11, 246 (2021).

    Article  Google Scholar 

  167. Pardoux, É., Boturyn, D. & Roupioz, Y. Antimicrobial peptides as probes in biosensors detecting whole bacteria: a review. Molecules 25, 1998 (2020).

    Article  Google Scholar 

  168. Vanova, V. et al. Peptide-based electrochemical biosensors utilized for protein detection. Biosens. Bioelectron. 180, 113087 (2021).

    Article  Google Scholar 

  169. Fu, M.-Q. et al. Supramolecular fluorogenic peptide sensor array based on graphene oxide for the differential sensing of ebola virus. Chem. Commun. 56, 5735–5738 (2020).

    Article  Google Scholar 

  170. Pardoux, É., Roux, A., Mathey, R., Boturyn, D. & Roupioz, Y. Antimicrobial peptide arrays for wide spectrum sensing of pathogenic bacteria. Talanta 203, 322–327 (2019).

    Article  Google Scholar 

  171. Bruce, J. A. & Clapper, J. C. Conjugation of carboxylated graphene quantum dots with cecropin P1 for bacterial biosensing applications. ACS Omega 5, 26583–26591 (2020).

    Article  Google Scholar 

  172. Ramezanpour, S. et al. Highly selective fluorescent peptide-based chemosensors for aluminium ions in aqueous solution. Anal. Bioanal. Chem. 413, 3881–3891 (2021).

    Article  Google Scholar 

  173. Liu, Q., Wang, J. & Boyd, B. J. Peptide-based biosensors. Talanta 136, 114–127 (2015).

    Article  Google Scholar 

  174. Akbari-Saatlu, M. et al. Silicon nanowires for gas sensing: a review. Nanomaterials 10, 2215 (2020).

    Article  Google Scholar 

  175. Ren, G. et al. A facile and sustainable hygroelectric generator using whole-cell Geobacter sulfurreducens. Nano Energy 89, 106361 (2021).

    Article  Google Scholar 

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

    Article  Google Scholar 

  177. Ueki, T., Nevin, K. P., Woodard, T. L. & Lovley, D. R. Genetic switches and related tools for controlling gene expression and electrical outputs of Geobacter sulfurreducens. J. Ind. Microbiol. Biotechnol. 43, 1561–1575 (2016).

    Article  Google Scholar 

  178. Wang, Z. et al. Resistive switching materials for information processing. Nat. Rev. Mater. 5, 173–195 (2020).

    Article  Google Scholar 

  179. Wang, Z. et al. Threshold switching of Ag or Cu in dielectrics: materials, mechanism, and applications. Adv. Funct. Mater. 28, 1704862 (2018).

    Article  Google Scholar 

  180. Fu, T. et al. Self-sustained green neuromorphic interfaces. Nat. Commun. 12, 3351 (2021).

    Article  Google Scholar 

  181. Leung, K. M. et al. Shewanella oneidensis MR‐1 bacterial nanowires exhibit p‐type, tunable electronic behavior. Nano Lett. 13, 2407–2411 (2013).

    Article  Google Scholar 

  182. Malvankar, N. S. et al. Tunable metallic-like conductivity in nanostructured biofilms comprised of microbial nanowires. Nat. Nanotechnol. 6, 573–579 (2011).

    Article  Google Scholar 

  183. Adhikari, R. Study of Charge Transport Mechanism in Microbial Nanowires. PhD thesis, University of Massachusetts Amherst (2016).

  184. Liu, J. et al. Metalloproteins containing cytochrome, iron-sulfur, or copper redox centers. Chem. Rev. 114, 4366–4469 (2014).

    Article  Google Scholar 

  185. Livernois, W. & Anantram, M. P. Quantum transport in conductive bacterial nanowires. In 2021 IEEE 16th Nanotechnology Materials and Devices Conference 1–5 https://ieeexplore.ieee.org/document/9677490 (IEEE, 2021).

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

    Article  Google Scholar 

  187. Reardon, P. N. & Mueller, K. T. Structure of the type IVa major pilin from the electrically conductive bacterial nanowires of Geobacter sulfurreducens. J. Biol. Chem. 288, 29260–29266 (2013).

    Article  Google Scholar 

  188. Cui, Y., Wei, Q., Park, H. & Lieber, C. M. Nanowire nanosensors for highly sensitive and selective detection of biological and chemical species. Science 293, 1289–1292 (2001).

    Article  Google Scholar 

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The authors contributed equally to all aspects of the article.

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Correspondence to Derek R. Lovley.

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N.-M.D.C. declares that she is an inventor on US Patent No.11,643,443, which is related to microbial nanowires. D.R.L. declares that he is an inventor on US Patent Nos. 7,498,155, 11,066,449, 11,631,824, 11,823,808 and 11,982,637, which are related to microbial nanowires. M.J.G-P. declares no competing interests.

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Guberman-Pfeffer, M.J., Dorval Courchesne, NM. & Lovley, D.R. Microbial nanowires for sustainable electronics. Nat Rev Bioeng (2024). https://doi.org/10.1038/s44222-024-00204-2

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