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f Microbial nanowires: an electrifying tale

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Microbial nanowires: an electrifying tale, Page 1 of 1

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  • Electromicrobiology has gained momentum in the last 10 years with advances in microbial fuel cells and the discovery of microbial nanowires (MNWs). The list of MNW-producing micro-organisms is growing and providing intriguing insights into the presence of such micro-organisms in diverse environments and the potential roles MNWs can perform. This review discusses the MNWs produced by different micro-organisms, including their structure, composition and mechanism of electron transfer through MNWs. Two hypotheses, metallic-like conductivity and an electron hopping model, have been proposed for electron transfer and we present a current understanding of both these hypotheses. MNWs not only are poised to change the way we see micro-organisms but also may impact the fields of bioenergy, biogeochemistry and bioremediation; hence, their potential applications in these fields are highlighted here.

  • Abbreviations:
    AFM atomic force microscopy
    BRONJ bisphosphonate-related osteonecrosis of the jaw
    MNW microbial nanowire
    PLS pili-like structure
    STM scanning tunneling microscopy
    TEM transmission electron microscopy
    TFP type IV pili

© 2016 The Authors

  • Amdursky N., Marchak D., Sepunaru L., Pecht I., Sheves M., Cahen D..( 2014;). Electronic transport via proteins. . Adv Mater 26: 7142––7161. [CrossRef] [PubMed]
    [Google Scholar]
  • Angenent L. T., Karim K., Al-Dahhan M. H., Wrenn B. A., Domíguez-Espinosa R..( 2004;). Production of bioenergy and biochemicals from industrial and agricultural wastewater. . Trends Biotechnol 22: 477––485. [CrossRef] [PubMed]
    [Google Scholar]
  • Boesen T., Nielsen L. P..( 2013;). Molecular dissection of bacterial nanowires. . MBio 4: e00270-13. [CrossRef] [PubMed]
    [Google Scholar]
  • Bouhenni R. A., Vora G. J., Biffinger J. C., Shirodkar S., Brockman K., Ray R., Wu P., Johnson B. J., Biddle E. M. et al.( 2010;). The role of Shewanella oneidensis MR-1 outer surface structures in extracellular electron transfer. . Electroanalysis 22: 856––864. [CrossRef]
    [Google Scholar]
  • Castro L., Vera M., Muñoz J. Á., Blázquez M. L., González F., Sand W., Ballester A..( 2014;). Aeromonas hydrophila produces conductive nanowires. . Res Microbiol 165: 794––802. [CrossRef] [PubMed]
    [Google Scholar]
  • Chalmeau J., Dagkessamanskaia A., Le Grimellec C., Francois J. M., Sternick J., Vieu C..( 2009;). Contribution to the elucidation of the structure of the bacterial flagellum nano-motor through AFM imaging of the M-Ring. . Ultramicroscopy 109: 845––853. [CrossRef] [PubMed]
    [Google Scholar]
  • Cologgi D. L., Lampa-Pastirk S., Speers A. M., Kelly S. D., Reguera G..( 2011;). Extracellular reduction of uranium via Geobacter conductive pili as a protective cellular mechanism. . Proc Natl Acad Sci U S A 108: 15248––15252. [CrossRef] [PubMed]
    [Google Scholar]
  • Costerton J. W., Ellis B., Lam K., Johnson F., Khoury A. E..( 1994;). Mechanism of electrical enhancement of efficacy of antibiotics in killing biofilm bacteria. . Antimicrob Agents Chemother 38: 2803––2809. [CrossRef] [PubMed]
    [Google Scholar]
  • Creasey R. C. G., Shingaya Y., Nakayama T..( 2015;). Improved electrical conductance through self-assembly of bioinspired peptides into nanoscale fibers. . Mater Chem Phys 158: 52––59. [CrossRef]
    [Google Scholar]
  • De Mes T., Stams A., Reith J., Zeeman G..( 2003;). Methane production by anaerobic digestion of wastewater and solid wastes. . In Bio-Methane & Bio-Hydrogen . Netherlands:: Dutch Biological Hydrogen Foundation;.
     [Google Scholar]
  • Duggan P. S., Gottardello P., Adams D. G..( 2007;). Molecular analysis of genes in Nostoc punctiforme involved in pilus biogenesis and plant infection. . J Bacteriol 189: 4547––4551. [CrossRef] [PubMed]
    [Google Scholar]
  • Durand E., Bernadac A., Ball G., Lazdunski A., Sturgis J. N., Filloux A..( 2003;). Type II protein secretion in Pseudomonas aeruginosa: the pseudopilus is a multifibrillar and adhesive structure. . J Bacteriol 185: 2749––2758. [CrossRef] [PubMed]
    [Google Scholar]
  • Eaktasang N., Kang C. S., Lim H., Kwean O. S., Cho S., Kim Y., Kim H. S..( 2016;). Production of electrically-conductive nanoscale filaments by sulfate-reducing bacteria in the microbial fuel cell. . Bioresour Technol 210: 61––67. [CrossRef] [PubMed]
    [Google Scholar]
  • El-Naggar M. Y., Gorby Y. A., Xia W., Nealson K. H..( 2008;). The molecular density of states in bacterial nanowires. . Biophys J 95: L10––L12. [CrossRef] [PubMed]
    [Google Scholar]
  • El-Naggar M. Y., Wanger G., Leung K. M., Yuzvinsky T. D., Southam G., Yang J., Lau W. M., Nealson K. H., Gorby Y. A..( 2010;). Electrical transport along bacterial nanowires from Shewanella oneidensis MR-1. . Proc Natl Acad Sci U S A 107: 18127––18131. [CrossRef] [PubMed]
    [Google Scholar]
  • Ericsson A. C., Davis D. J., Franklin C. L., Hagan C. E..( 2015;). Exoelectrogenic capacity of host microbiota predicts lymphocyte recruitment to the gut. . Physiol Genomics 47: 243––252. [CrossRef] [PubMed]
    [Google Scholar]
  • Feliciano G. T., da Silva A. J., Reguera G., Artacho E..( 2012;). Molecular and electronic structure of the peptide subunit of Geobacter sulfurreducens conductive pili from first principles. . J Phys Chem A 116: 8023––8030. [CrossRef] [PubMed]
    [Google Scholar]
  • Feliciano G. T., Steidl R. J., Reguera G..( 2015;). Structural and functional insights into the conductive pili of Geobacter sulfurreducens revealed in molecular dynamics simulations. . Phys Chem Chem Phys 17: 22217––22226. [CrossRef] [PubMed]
    [Google Scholar]
  • Fitzgerald L. A., Petersen E. R., Ray R. I., Little B. J., Cooper C. J., Howard E. C., Ringeisen B. R., Biffinger J. C..( 2012;). Shewanella oneidensis MR-1 Msh pilin proteins are involved in extracellular electron transfer in microbial fuel cells. . Process Biochem 47: 170––174. [CrossRef]
    [Google Scholar]
  • Gorby Y. A., Yanina S., McLean J. S., Rosso K. M., Moyles D., Dohnalkova A., Beveridge T. J., Chang I. S., Kim B. H. et al.( 2006;). Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. . Proc Natl Acad Sci U S A 103: 11358––11363. [CrossRef] [PubMed]
    [Google Scholar]
  • Gralnick J. A., Newman D. K..( 2007;). Extracellular respiration. . Mol Microbiol 65: 1––11. [CrossRef] [PubMed]
    [Google Scholar]
  • Heckels J. E..( 1989;). Structure and function of pili of pathogenic Neisseria species. . Clin Microbiol Rev 2: S66––S73. [CrossRef] [PubMed]
    [Google Scholar]
  • Kulp T. R., Hoeft S. E., Asao M., Madigan M. T., Hollibaugh J. T., Fisher J. C., Stolz J. F., Culbertson C. W., Miller L. G. et al.( 2008;). Arsenic(III) fuels anoxygenic photosynthesis in hot spring biofilms from Mono Lake, California. . Science 321: 967––970. [CrossRef] [PubMed]
    [Google Scholar]
  • Lampa-Pastirk S., Veazey J. P., Walsh K. A., Feliciano G. T., Steidl R. J., Tessmer S. H., Reguera G..( 2016;). Thermally activated charge transport in microbial protein nanowires. . Sci Rep 6:. [CrossRef] [PubMed]
    [Google Scholar]
  • Lea-Smith D. J., Bombelli P., Vasudevan R., Howe C. J..( 2016;). Photosynthetic, respiratory and extracellular electron transport pathways in cyanobacteria. . Biochim Biophys Acta 1857: 247––255. [CrossRef] [PubMed]
    [Google Scholar]
  • Leang C., Qian X., Mester T., Lovley D. R..( 2010;). Alignment of the c-type cytochrome OmcS along pili of Geobacter sulfurreducens. . Appl Environ Microbiol 76: 4080––4084. [CrossRef] [PubMed]
    [Google Scholar]
  • Lebedev N., Mahmud S., Griva I., Blom A., Tender L. M..( 2015;). On the electron transfer through Geobacter sulfurreducens PilA protein. . J Polym Sci B: Polym Phys 53: 1706––1717. [CrossRef]
    [Google Scholar]
  • Leung K. M., Wanger G., Guo Q., Gorby Y., Southam G., Lau W. M., Yang J..( 2011;). Bacterial nanowires: conductive as silicon, soft as polymer. . Soft Matter 7: 6617––6621. [CrossRef]
    [Google Scholar]
  • Leung K. M., Wanger G., El-Naggar M. Y., Gorby Y., Southam G., Lau W. M., Yang J..( 2013;). Shewanella oneidensis MR-1 bacterial nanowires exhibit p-type, tunable electronic behavior. . Nano Lett 13: 2407––2411. [CrossRef] [PubMed]
    [Google Scholar]
  • Li Y., Li H..( 2014;). Type IV pili of Acidithiobacillus ferrooxidans can transfer electrons from extracellular electron donors. . J Basic Microbiol 54: 226––231. [CrossRef] [PubMed]
    [Google Scholar]
  • Liu X., Tremblay P. L., Malvankar N. S., Nevin K. P., Lovley D. R., Vargas M..( 2014;). 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 Environ Microbiol 80: 1219––1224. [CrossRef] [PubMed]
    [Google Scholar]
  • Lovley D. R..( 2008;). Extracellular electron transfer: wires, capacitors, iron lungs, and more. . Geobiology 6: 225––231. [CrossRef] [PubMed]
    [Google Scholar]
  • Lovley D. R..( 2011;). Live wires: direct extracellular electron exchange for bioenergy and the bioremediation of energy-related contamination. . Energy Environ Sci 4: 4896––4906. [CrossRef]
    [Google Scholar]
  • Lovley D. R., Reguera G., McCarthy K. D., Tuominem M. T..( 2009;). Providing a bacterium such as Geobacteraceae expressing a conductive proteinaceous pilus; culturing in medium containing an electron acceptor such as iron III oxide; coupling to circuit; self-assembling; no need for metallization. US Patent US 7,498,155 B2, University of Massachusetts.
  • Malvankar N. S., Lovley D. R..( 2012;). Microbial nanowires: a new paradigm for biological electron transfer and bioelectronics. . ChemSusChem 5: 1039––1046. [CrossRef]
    [Google Scholar]
  • Malvankar N. S., Lovley D. R..( 2014;). Microbial nanowires for bioenergy applications. . Curr Opin Biotechnol 27: 88––95. [CrossRef] [PubMed]
    [Google Scholar]
  • Malvankar N. S., Vargas M., Nevin K. P., Franks A. E., Leang C., Kim B.-C., Inoue K., Mester T., Covalla S. F. et al.( 2011;). Tunable metallic-like conductivity in microbial nanowire networks. . Nat Nanotechnol 6: 573––579. [CrossRef]
    [Google Scholar]
  • Malvankar N. S., Tuominen M. T., Lovley D. R..( 2012;). Lack of cytochrome involvement in long-range electron transport through conductive biofilms & nanowires of Geobacter sulfurreducens. . Energy Environ Sci 5: 8651––8659.[CrossRef]
    [Google Scholar]
  • Malvankar N. S., Yalcin S. E., Tuominen M. T., Lovley D. R..( 2014;). Visualization of charge propagation along individual pili proteins using ambient electrostatic force microscopy. . Nat Nanotechnol 9: 1012––1017. [CrossRef] [PubMed]
    [Google Scholar]
  • Malvankar N. S., Vargas M., Nevin K., Tremblay P. L., Evans-Lutterodt K., Nykypanchuk D., Martz E., Tuominen M. T., Lovley D. R..( 2015;). Structural basis for metallic-like conductivity in microbial nanowires. . MBio 6: e00084-15. [CrossRef] [PubMed]
    [Google Scholar]
  • Morita M., Malvankar N. S., Franks A. E., Summers Z. M., Giloteaux L., Rotaru A. E., Rotaru C., Lovley D. R..( 2011;). Potential for direct interspecies electron transfer in methanogenic wastewater digester aggregates. . MBio 2: e00159-11. [CrossRef] [PubMed]
    [Google Scholar]
  • Nwogu N. G..( 2007;). Microbial fuel cells and parameters affecting performance when generating electricity. . MMG 445 Basic Biotechnol eJ 3: 73––79.
     [Google Scholar]
  • Patolsky F., Lieber C. M..( 2005;). Nanowire nanosensors. . Materials Today 8: 20––28. [CrossRef]
    [Google Scholar]
  • Patolsky F., Zheng G., Lieber C. M..( 2006;). Nanowire sensors for medicine and the life sciences. . Nanomedicine 1: 51––65. [CrossRef] [PubMed]
    [Google Scholar]
  • Pelicic V..( 2008;). Type IV pili: e pluribus unum?. Mol Microbiol 68: 827––837. [CrossRef] [PubMed]
    [Google Scholar]
  • Petrov A., Audette G. F..( 2012;). Peptide and protein-based nanotubes for nanobiotechnology. . Wiley Interdiscip Rev Nanomed Nanobiotechnol 4: 575––585. [CrossRef] [PubMed]
    [Google Scholar]
  • Pirbadian S., El-Naggar M. Y..( 2012;). Multistep hopping and extracellular charge transfer in microbial redox chains. . Phys Chem Chem Phys 14: 13802––13808. [CrossRef] [PubMed]
    [Google Scholar]
  • Pirbadian S., Barchinger S. E., Leung K. M., Byun H. S., Jangir Y., Bouhenni R. A., Reed S. B., Romine M. F., Saffarini D. A. et al.( 2014;). Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components. . Proc Natl Acad Sci U S A 111: 12883––12888. [CrossRef] [PubMed]
    [Google Scholar]
  • Pisciotta J. M., Zou Y., Baskakov I. V..( 2010;). Light-dependent electrogenic activity of cyanobacteria. . PLoS One 5: e10821. [CrossRef] [PubMed]
    [Google Scholar]
  • Polizzi N. F., Skourtis S. S., Beratan D. N..( 2012;). Physical constraints on charge transport through bacterial nanowires. . Faraday Discuss 155: 43––61. [CrossRef] [PubMed]
    [Google Scholar]
  • Prochnow A., Heiermann M., Plöchl M., Linke B., Idler C., Amon T., Hobbs P. J..( 2009;). Bioenergy from permanent grassland — a review: 1. Biogas. . Bioresource Technol 100: 4931––4944. [CrossRef]
    [Google Scholar]
  • Proft T., Baker E. N..( 2009;). Pili in Gram-negative and Gram-positive bacteria — structure, assembly and their role in disease. . Cell Mol Life Sci 66: 613––635. [CrossRef] [PubMed]
    [Google Scholar]
  • Rabaey K..( 2010;). Bioelectrochemical Systems: From Extracellular Electron Transfer to Biotechnological Application. UK:: IWA Publishing;.
     [Google Scholar]
  • Reches M., Gazit E..( 2003;). Casting metal nanowires within discrete self-assembled peptide nanotubes. . Science 300: 625––627. [CrossRef] [PubMed]
    [Google Scholar]
  • Reguera G..( 2011;). When microbial conversations get physical. . Trends Microbiol 19: 105––113. [CrossRef] [PubMed]
    [Google Scholar]
  • Reguera G., McCarthy K. D., Mehta T., Nicoll J. S., Tuominen M. T., Lovley D. R..( 2005;). Extracellular electron transfer via microbial nanowires. . Nature 435: 1098––1101. [CrossRef] [PubMed]
    [Google Scholar]
  • Reguera G., Nevin K. P., Nicoll J. S., Covalla S. F., Woodard T. L., Lovley D. R..( 2006;). Biofilm and nanowire production leads to increased current in Geobacter sulfurreducens fuel cells. . Appl Environ Microbiol 72: 7345––7348. [CrossRef] [PubMed]
    [Google Scholar]
  • Reguera G., Cologgi D., Worden R. M., Castro-forero A. A., Steidl R..( 2014;). Microbial nanowires and methods of making and using. US Patent US 2014/0239237 A1, Michigan State University.
  • Remis J. P., Wei D., Gorur A., Zemla M., Haraga J., Allen S., Witkowska H. E., Costerton J. W., Berleman J. E. et al.( 2014;). Bacterial social networks: structure and composition of Myxococcus xanthus outer membrane vesicle chains. . Environ Microbiol 16: 598––610. [CrossRef] [PubMed]
    [Google Scholar]
  • Richardson D. J..( 2000;). Bacterial respiration: a flexible process for a changing environment. . Microbiology 146: 551––571. [CrossRef] [PubMed]
    [Google Scholar]
  • Rosenbaum M., He Z., Angenent L. T..( 2010;). Light energy to bioelectricity: photosynthetic microbial fuel cells. . Curr Opin Biotechnol 21: 259––264. [CrossRef] [PubMed]
    [Google Scholar]
  • Rosenman G., Beker P., Koren I., Yevnin M., Bank-Srour B., Mishina E., Semin S..( 2011;). Bioinspired peptide nanotubes: deposition technology, basic physics and nanotechnology applications. . J Pept Sci 17: 75––87. [CrossRef] [PubMed]
    [Google Scholar]
  • Rotaru A.-E., Shrestha P. M., Liu F., Shrestha M., Shrestha D., Embree M., Zengler K., Wardman C., Nevin K. P., Lovley D. R..( 2014;). 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. [CrossRef]
    [Google Scholar]
  • Scanlon S., Aggeli A..( 2008;). Self-assembling peptide nanotubes. . Nano Today 3: 22––30. [CrossRef]
    [Google Scholar]
  • Shimoyama T., Kato S., Ishii S., Watanabe K..( 2009;). Flagellum mediates symbiosis. . Science 323:. [CrossRef] [PubMed]
    [Google Scholar]
  • Simpson C. F., White F. H., Sandhu T. S..( 1976;). The structure of pili (fimbriae) of Moraxella bovis. . Can J Comp Med 40: 1––4.[PubMed]
    [Google Scholar]
  • Skourtis S. S..( 2013;). Probing protein electron transfer mechanisms from the molecular to the cellular length scales. . Peptide Sci 100: 82––92. [CrossRef]
    [Google Scholar]
  • Steidl R. J., Lampa-Pastirk S., Reguera G..( 2016;). Mechanistic stratification in electroactive biofilms of Geobacter sulfurreducens mediated by pilus nanowires. . Nat Commun 7: 1––7. [CrossRef]
    [Google Scholar]
  • Strik D. P., Timmers R. A., Helder M., Steinbusch K. J., Hamelers H. V., Buisman C. J..( 2011;). Microbial solar cells: applying photosynthetic and electrochemically active organisms. . Trends Biotechnol 29: 41––49. [CrossRef] [PubMed]
    [Google Scholar]
  • Strycharz-Glaven S. M., Tender L. M..( 2012;). Reply to the ‘Comment on ‘‘On electrical conductivity of microbial nanowires & biofilms’’’ by N. S. Malvankar, M. T. Tuominen & D. R. Lovley. . Energy Environ Sci 5: 6250––6255.[CrossRef]
    [Google Scholar]
  • Strycharz-Glaven S. M., Snider R. M., Guiseppi-Elie A., Tender L. M..( 2011;). On the electrical conductivity of microbial nanowires and biofilms. . Energy Environ Sci 4: 4366––4379. [CrossRef]
    [Google Scholar]
  • Summers Z. M., Fogarty H. E., Leang C., Franks A. E., Malvankar N. S., Lovley D. R..( 2010;). Direct exchange of electrons within aggregates of an evolved syntrophic coculture of anaerobic bacteria. . Science 330: 1413––1415. [CrossRef] [PubMed]
    [Google Scholar]
  • Sun W., Shao M., Ren H., Xiao D., Qin X., Deng L., Chen X., Gao J..( 2015;). A new type of electron relay station in proteins: three-piece S: π∴S↔S∴π:S resonance structure. . J Phys Chem C 119: 6998––7005.[CrossRef]
    [Google Scholar]
  • Sure S., Torriero A. A., Gaur A., Li L. H., Chen Y., Tripathi C., Adholeya A., Ackland M. L., Kochar M..( 2015;). Inquisition of Microcystis aeruginosa and Synechocystis nanowires: characterization and modelling. . Antonie van Leeuwenhoek 108: 1213––1225. [CrossRef] [PubMed]
    [Google Scholar]
  • Sure S., Ackland M. L., Gaur A., Gupta P., Adholeya A., Kochar M..( 2016a;). Probing Synechocystis-arsenic interactions through extracellular nanowires. . Front Microbiol 7: 1134. [CrossRef] [PubMed]
    [Google Scholar]
  • Sure S., Torriero A. A., Gaur A., Li L. H., Chen Y., Tripathi C., Adholeya A., Ackland M. L., Kochar M..( 2016b;). Identification and topographical characterisation of microbial nanowires in Nostoc punctiforme. . Antonie van Leeuwenhoek 109: 475––480. [CrossRef] [PubMed]
    [Google Scholar]
  • Tacket C. O., Taylor R. K., Losonsky G., Lim Y., Nataro J. P., Kaper J. B., Levine M. M..( 1998;). Investigation of the roles of toxin-coregulated pili and mannose-sensitive hemagglutinin pili in the pathogenesis of Vibrio cholerae O139 infection. . Infect Immun 66: 692––695.[PubMed]
    [Google Scholar]
  • Tan Y., Adhikari R. Y., Malvankar N. S., Pi S., Ward J. E., Woodard T. L., Nevin K. P., Xia Q., Tuominen M. T. et al.( 2016;). Synthetic biological protein nanowires with high conductivity. . Small 12: 4481––4485. [CrossRef] [PubMed]
    [Google Scholar]
  • Tender L. M..( 2011;). From mud to microbial electrode catalysts & conductive nanomaterials. . MRS Bull 36: 800––805.[CrossRef]
    [Google Scholar]
  • Valdés J., Pedroso I., Quatrini R., Dodson R. J., Tettelin H., Blake R., Eisen J. A., Holmes D. S..( 2008;). Acidithiobacillus ferrooxidans metabolism: from genome sequence to industrial applications. . BMC Genomics 9: 597. [CrossRef] [PubMed]
    [Google Scholar]
  • Vargas M., Malvankar N. S., Tremblay P. L., Leang C., Smith J. A., Patel P., Snoeyenbos-West O., Synoeyenbos-West O., Nevin K. P., Lovley D. R..( 2013;). Aromatic amino acids required for pili conductivity and long-range extracellular electron transport in Geobacter sulfurreducens. . MBio 4: e00105-13. [CrossRef] [PubMed]
    [Google Scholar]
  • Veazey J. P., Reguera G., Tessmer S. H..( 2011;). Electronic properties of conductive pili of the metal-reducing bacterium Geobacter sulfurreducens probed by scanning tunneling microscopy. . Phys Rev E Stat Nonlin Soft Matter Phys 84: 060901. [CrossRef] [PubMed]
    [Google Scholar]
  • Venkidusamy K., Megharaj M., Schröder U., Karouta F., Mohan S., Naidu R..( 2015;). Electron transport through electrically conductive nanofilaments in Rhodopseudomonas palustris strain RP2. . RSC Adv 5: 100790––100798. [CrossRef]
    [Google Scholar]
  • Waleed Shinwari M., Jamal Deen M., Starikov E. B., Cuniberti G..( 2010;). Electrical conductance in biological molecules. . Adv Funct Mater 20: 1865––1883. [CrossRef]
    [Google Scholar]
  • Wang M., Gao J., Müller P., Giese B..( 2009;). Electron transfer in peptides with cysteine and methionine as relay amino acids. . Angew Chem Int Edit 48: 4232––4234. [CrossRef]
    [Google Scholar]
  • Wang K., Wu H., Meng Y., Wei Z..( 2014;). Conducting polymer nanowire arrays for high performance supercapacitors. . Small 10: 14––31. [CrossRef] [PubMed]
    [Google Scholar]
  • Wanger G., Gorby Y., El-Naggar M. Y., Yuzvinsky T. D., Schaudinn C., Gorur A., Sedghizadeh P. P..( 2013;). Electrically conductive bacterial nanowires in bisphosphonate-related osteonecrosis of the jaw biofilms. . Oral Surg Oral Med Oral Pathol Oral Radiol 115: 71––78. [CrossRef] [PubMed]
    [Google Scholar]
  • Wegener G., Krukenberg V., Riedel D., Tegetmeyer H. E., Boetius A..( 2015;). Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria. . Nature 526: 587––590. [CrossRef] [PubMed]
    [Google Scholar]
  • Wei X., Vassallo C. N., Pathak D. T., Wall D..( 2014;). Myxobacteria produce outer membrane-enclosed tubes in unstructured environments. . J Bacteriol 196: 1807––1814. [CrossRef] [PubMed]
    [Google Scholar]
  • Xiao K., Malvankar N. S., Shu C., Martz E., Lovley D. R., Sun X..( 2016;). Low energy atomic models suggesting a pilus structure that could account for electrical conductivity of Geobacter sulfurreducens pili. . Sci Rep 6: 23385. [CrossRef]
    [Google Scholar]
  • Xu D., Watt G. D., Harb J. N., Davis R. C..( 2005;). Electrical conductivity of ferritin proteins by conductive AFM. . Nano Lett 5: 571––577. [CrossRef] [PubMed]
    [Google Scholar]
  • Yan H., Chuang C., Zhugayevych A., Tretiak S., Dahlquist F. W., Bazan G. C..( 2015;). Inter-aromatic distances in Geobacter sulfurreducens pili relevant to biofilm charge transport. . Adv Mater 27: 1908––1911. [CrossRef] [PubMed]
    [Google Scholar]
  • Zhang X. L., Tsui I. S., Yip C. M., Fung A. W., Wong D. K., Dai X., Yang Y., Hackett J., Morris C..( 2000;). Salmonella enterica serovar Typhi uses type IVB pili to enter human intestinal epithelial cells. . Infect Immun 68: 3067––3073. [CrossRef] [PubMed]
    [Google Scholar]
  • Ziadan K. M..( 2012;). Conducting Polymers Application. Croatia:: INTECH Open Access Publisher;.
     [Google Scholar]
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2016-12-21
2019-01-19
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