1887

Abstract

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.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000382
2016-12-21
2022-05-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/162/12/2017.html?itemId=/content/journal/micro/10.1099/mic.0.000382&mimeType=html&fmt=ahah

References

  1. Amdursky N., Marchak D., Sepunaru L., Pecht I., Sheves M., Cahen D. 2014; Electronic transport via proteins. Adv Mater 26:7142–7161 [View Article][PubMed]
    [Google Scholar]
  2. 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 [View Article][PubMed]
    [Google Scholar]
  3. Boesen T., Nielsen L. P. 2013; Molecular dissection of bacterial nanowires. MBio 4:e00270-13 [View Article][PubMed]
    [Google Scholar]
  4. 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 [View Article]
    [Google Scholar]
  5. 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 [View Article][PubMed]
    [Google Scholar]
  6. 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 [View Article][PubMed]
    [Google Scholar]
  7. 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 [View Article][PubMed]
    [Google Scholar]
  8. 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 [View Article][PubMed]
    [Google Scholar]
  9. 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 [View Article]
    [Google Scholar]
  10. 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]
  11. 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 [View Article][PubMed]
    [Google Scholar]
  12. 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 [View Article][PubMed]
    [Google Scholar]
  13. 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 [View Article][PubMed]
    [Google Scholar]
  14. 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 [View Article][PubMed]
    [Google Scholar]
  15. 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 [View Article][PubMed]
    [Google Scholar]
  16. 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 [View Article][PubMed]
    [Google Scholar]
  17. 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 [View Article][PubMed]
    [Google Scholar]
  18. 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 [View Article][PubMed]
    [Google Scholar]
  19. 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 [View Article]
    [Google Scholar]
  20. 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 [View Article][PubMed]
    [Google Scholar]
  21. Gralnick J. A., Newman D. K. 2007; Extracellular respiration. Mol Microbiol 65:1–11 [View Article][PubMed]
    [Google Scholar]
  22. Heckels J. E. 1989; Structure and function of pili of pathogenic Neisseria species. Clin Microbiol Rev 2:S66–S73 [View Article][PubMed]
    [Google Scholar]
  23. 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 [View Article][PubMed]
    [Google Scholar]
  24. 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: [View Article][PubMed]
    [Google Scholar]
  25. 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 [View Article][PubMed]
    [Google Scholar]
  26. 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 [View Article][PubMed]
    [Google Scholar]
  27. 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 [View Article]
    [Google Scholar]
  28. 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 [View Article]
    [Google Scholar]
  29. 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 [View Article][PubMed]
    [Google Scholar]
  30. Li Y., Li H. 2014; Type IV pili of Acidithiobacillus ferrooxidans can transfer electrons from extracellular electron donors. J Basic Microbiol 54:226–231 [View Article][PubMed]
    [Google Scholar]
  31. 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 [View Article][PubMed]
    [Google Scholar]
  32. Lovley D. R. 2008; Extracellular electron transfer: wires, capacitors, iron lungs, and more. Geobiology 6:225–231 [View Article][PubMed]
    [Google Scholar]
  33. 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 [View Article]
    [Google Scholar]
  34. 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
  35. Malvankar N. S., Lovley D. R. 2012; Microbial nanowires: a new paradigm for biological electron transfer and bioelectronics. ChemSusChem 5:1039–1046 [View Article]
    [Google Scholar]
  36. Malvankar N. S., Lovley D. R. 2014; Microbial nanowires for bioenergy applications. Curr Opin Biotechnol 27:88–95 [View Article][PubMed]
    [Google Scholar]
  37. 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 [View Article]
    [Google Scholar]
  38. 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]
  39. 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 [View Article][PubMed]
    [Google Scholar]
  40. 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 [View Article][PubMed]
    [Google Scholar]
  41. 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 [View Article][PubMed]
    [Google Scholar]
  42. Nwogu N. G. 2007; Microbial fuel cells and parameters affecting performance when generating electricity. MMG 445 Basic Biotechnol eJ 3:73–79
    [Google Scholar]
  43. Patolsky F., Lieber C. M. 2005; Nanowire nanosensors. Materials Today 8:20–28 [View Article]
    [Google Scholar]
  44. Patolsky F., Zheng G., Lieber C. M. 2006; Nanowire sensors for medicine and the life sciences. Nanomedicine 1:51–65 [View Article][PubMed]
    [Google Scholar]
  45. Pelicic V. 2008; Type IV pili: e pluribus unum?. Mol Microbiol 68:827–837 [View Article][PubMed]
    [Google Scholar]
  46. Petrov A., Audette G. F. 2012; Peptide and protein-based nanotubes for nanobiotechnology. Wiley Interdiscip Rev Nanomed Nanobiotechnol 4:575–585 [View Article][PubMed]
    [Google Scholar]
  47. Pirbadian S., El-Naggar M. Y. 2012; Multistep hopping and extracellular charge transfer in microbial redox chains. Phys Chem Chem Phys 14:13802–13808 [View Article][PubMed]
    [Google Scholar]
  48. 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 [View Article][PubMed]
    [Google Scholar]
  49. Pisciotta J. M., Zou Y., Baskakov I. V. 2010; Light-dependent electrogenic activity of cyanobacteria. PLoS One 5:e10821 [View Article][PubMed]
    [Google Scholar]
  50. Polizzi N. F., Skourtis S. S., Beratan D. N. 2012; Physical constraints on charge transport through bacterial nanowires. Faraday Discuss 155:43–61 [View Article][PubMed]
    [Google Scholar]
  51. 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 [View Article]
    [Google Scholar]
  52. 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 [View Article][PubMed]
    [Google Scholar]
  53. Rabaey K. 2010 Bioelectrochemical Systems: From Extracellular Electron Transfer to Biotechnological Application UK: IWA Publishing;
    [Google Scholar]
  54. Reches M., Gazit E. 2003; Casting metal nanowires within discrete self-assembled peptide nanotubes. Science 300:625–627 [View Article][PubMed]
    [Google Scholar]
  55. Reguera G. 2011; When microbial conversations get physical. Trends Microbiol 19:105–113 [View Article][PubMed]
    [Google Scholar]
  56. 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 [View Article][PubMed]
    [Google Scholar]
  57. 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 [View Article][PubMed]
    [Google Scholar]
  58. 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
  59. 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 [View Article][PubMed]
    [Google Scholar]
  60. Richardson D. J. 2000; Bacterial respiration: a flexible process for a changing environment. Microbiology 146:551–571 [View Article][PubMed]
    [Google Scholar]
  61. Rosenbaum M., He Z., Angenent L. T. 2010; Light energy to bioelectricity: photosynthetic microbial fuel cells. Curr Opin Biotechnol 21:259–264 [View Article][PubMed]
    [Google Scholar]
  62. 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 [View Article][PubMed]
    [Google Scholar]
  63. 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 [View Article]
    [Google Scholar]
  64. Scanlon S., Aggeli A. 2008; Self-assembling peptide nanotubes. Nano Today 3:22–30 [View Article]
    [Google Scholar]
  65. Shimoyama T., Kato S., Ishii S., Watanabe K. 2009; Flagellum mediates symbiosis. Science 323: [View Article][PubMed]
    [Google Scholar]
  66. 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]
  67. Skourtis S. S. 2013; Probing protein electron transfer mechanisms from the molecular to the cellular length scales. Peptide Sci 100:82–92 [View Article]
    [Google Scholar]
  68. 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 [View Article]
    [Google Scholar]
  69. 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 [View Article][PubMed]
    [Google Scholar]
  70. 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]
  71. 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 [View Article]
    [Google Scholar]
  72. 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 [View Article][PubMed]
    [Google Scholar]
  73. 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]
  74. 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 [View Article][PubMed]
    [Google Scholar]
  75. 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 [View Article][PubMed]
    [Google Scholar]
  76. 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 [View Article][PubMed]
    [Google Scholar]
  77. 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]
  78. 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 [View Article][PubMed]
    [Google Scholar]
  79. Tender L. M. 2011; From mud to microbial electrode catalysts & conductive nanomaterials. MRS Bull 36:800–805 [CrossRef]
    [Google Scholar]
  80. 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 [View Article][PubMed]
    [Google Scholar]
  81. 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 [View Article][PubMed]
    [Google Scholar]
  82. 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 [View Article][PubMed]
    [Google Scholar]
  83. 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 [View Article]
    [Google Scholar]
  84. Waleed Shinwari M., Jamal Deen M., Starikov E. B., Cuniberti G. 2010; Electrical conductance in biological molecules. Adv Funct Mater 20:1865–1883 [View Article]
    [Google Scholar]
  85. 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 [View Article]
    [Google Scholar]
  86. Wang K., Wu H., Meng Y., Wei Z. 2014; Conducting polymer nanowire arrays for high performance supercapacitors. Small 10:14–31 [View Article][PubMed]
    [Google Scholar]
  87. 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 [View Article][PubMed]
    [Google Scholar]
  88. 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 [View Article][PubMed]
    [Google Scholar]
  89. 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 [View Article][PubMed]
    [Google Scholar]
  90. 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 [View Article]
    [Google Scholar]
  91. 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 [View Article][PubMed]
    [Google Scholar]
  92. 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 [View Article][PubMed]
    [Google Scholar]
  93. 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 [View Article][PubMed]
    [Google Scholar]
  94. Ziadan K. M. 2012 Conducting Polymers Application Croatia: INTECH Open Access Publisher;
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000382
Loading
/content/journal/micro/10.1099/mic.0.000382
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error