1887

Abstract

The electrically conductive pili (e-pili) of Geobactersulfurreducens have environmental and practical significance because they can facilitate electron transfer to insoluble Fe(III) oxides; to other microbial species; and through electrically conductive biofilms. E-pili conductivity has been attributed to the truncated PilA monomer, which permits tight packing of aromatic amino acids to form a conductive path along the length of e-pili. In order to better understand the evolution and distribution of e-pili in the microbial world, type IVa PilA proteins from various Gram-negative and Gram-positive bacteria were examined with a particular emphasis on Fe(III)-respiring bacteria. E-pilin genes are primarily restricted to a tight phylogenetic group in the order Desulfuromonadales. The downstream gene in all but one of the Desulfuromonadales that possess an e-pilin gene is a gene previously annotated as ‘pilA–C’ that has characteristics suggesting that it may encode an outer-membrane protein. Other genes associated with pilin function are clustered with e-pilin and ‘pilA–C’ genes in the Desulfuromonadales. In contrast, in the few bacteria outside the Desulfuromonadales that contain e-pilin genes, the other genes required for pilin function may have been acquired through horizontal gene transfer. Of the 95 known Fe(III)-reducing micro-organisms for which genomes are available, 80 % lack e-pilin genes, suggesting that e-pili are just one of several mechanisms involved in extracellular electron transport. These studies provide insight into where and when e-pili are likely to contribute to extracellular electron transport processes that are biogeochemically important and involved in bioenergy conversions.

Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000072
2016-08-25
2019-09-18
Loading full text...

Full text loading...

/deliver/fulltext/mgen/2/8/mgen000072.html?itemId=/content/journal/mgen/10.1099/mgen.0.000072&mimeType=html&fmt=ahah

References

  1. Adhikari R. Y., Malvankar N. S., Tuominen M. T., Lovley D. R.. 2016; Conductivity of individual Geobacter pili. RSC Adv.6:8354–8357 [CrossRef]
    [Google Scholar]
  2. Altschul S., Madden T., Schaffer A., Zhang J., Zhang Z., Miller W., Lipman D.. 1997; Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research25:3389–3402 [CrossRef]
    [Google Scholar]
  3. Ayers M., Howell P. L., Burrows L. L.. 2010; Architecture of the type II secretion and type IV pilus machineries. Future Microbiol5:1203–1218 [CrossRef][PubMed]
    [Google Scholar]
  4. Bernard C. S., Bordi C., Termine E., Filloux A., de Bentzmann S.. 2009; Organization and PprB-dependent control of the Pseudomonas aeruginosa tad locus, involved in Flp pilus biology. J Bacteriol191:1961–1973 [CrossRef][PubMed]
    [Google Scholar]
  5. Bieber D., Ramer S. W., Wu C. Y., Murray W. J., Tobe T., Fernandez R., Schoolnik G. K.. 1998; Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Escherichia coli. Science280:2114–2118 [CrossRef][PubMed]
    [Google Scholar]
  6. Bond D. R., Lovley D. R.. 2003; Electricity production by Geobacter sulfurreducens attached to electrodes. Appl Environ Microbiol69:1548–1555 [CrossRef][PubMed]
    [Google Scholar]
  7. Burrows L. L.. 2012; Pseudomonas aeruginosa twitching motility: type IV pili in action. Annu Rev Microbiol66:493–520 [CrossRef][PubMed]
    [Google Scholar]
  8. Castro L., Vera M., Muñoz JÁ., Blázquez M. L., González F., Sand W., Ballester A.. 2014; Aeromonas hydrophila produces conductive nanowires. Res Microbiol165:794–802 [CrossRef][PubMed]
    [Google Scholar]
  9. Chun A. L.. 2014; Bacterial nanowires: an extended membrane. Nat Nanotechnol9:750 [CrossRef][PubMed]
    [Google Scholar]
  10. Craig L., Pique M. E., Tainer J. A.. 2004; Type IV pilus structure and bacterial pathogenicity. Nat Rev Microbiol2:363–378 [CrossRef][PubMed]
    [Google Scholar]
  11. Craig L., Taylor R. K., Pique M. E., Adair B. D., Arvai A. S., Singh M., Lloyd S. J., Shin D. S., Getzoff E. D. et al. 2003; Type IV pilin structure and assembly: X-ray and EM analyses of Vibrio cholerae toxin-coregulated pilus and Pseudomonas aeruginosa PAK pilin. Mol Cell11:1139–1150[PubMed]
    [Google Scholar]
  12. Craig L., Volkmann N., Arvai A. S., Pique M. E., Yeager M., Egelman E. H., Tainer J. A.. 2006; Type IV pilus structure by cryo-electron microscopy and crystallography: implications for pilus assembly and functions. Mol Cell23:651–662 [CrossRef][PubMed]
    [Google Scholar]
  13. Cuff J. A., Barton G. J.. 2000; Application of multiple sequence alignment profiles to improve protein secondary structure prediction. Proteins40:502–511 [CrossRef][PubMed]
    [Google Scholar]
  14. Dayhoff M. O., Schwartz R. M., Orcutt B. C.. 1978; A Model of Evolutionary Change in Proteins. In Atlas of Protein Sequence and Structure , pp.345–352 Edited by Dayhoff M. O.. Washington DC: National Biomedical Research Foundation;
    [Google Scholar]
  15. Drozdetskiy A., Cole C., Procter J., Barton G. J.. 2015; JPred4: a protein secondary structure prediction server. Nucleic Acids Res43:W389–394 [CrossRef][PubMed]
    [Google Scholar]
  16. 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 Technol210: [CrossRef][PubMed]
    [Google Scholar]
  17. Eddy S. R.. 2008; A probabilistic model of local sequence alignment that simplifies statistical significance estimation. PLoS Comput Biol4:e1000069 [CrossRef][PubMed]
    [Google Scholar]
  18. Eddy S. R.. 2011; Accelerated profile HMM searches. PLoS Comput Biol7:e1002195 [CrossRef][PubMed]
    [Google Scholar]
  19. 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 Phys17:22217–22226 [CrossRef][PubMed]
    [Google Scholar]
  20. Finn R. D., Coggill P., Eberhardt R. Y., Eddy S. R., Mistry J., Mitchell A. L., Potter S. C., Punta M., Qureshi M. et al. 2016; The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res44:D279–285 [CrossRef][PubMed]
    [Google Scholar]
  21. Ford B., Verger D., Dodson K., Volkan E., Kostakioti M., Elam J., Pinkner J., Waksman G., Hultgren S.. 2012; The structure of the PapD–PapGII pilin complex reveals an open and flexible P5 pocket. J Bacteriol194:6390–6397 [CrossRef][PubMed]
    [Google Scholar]
  22. Galdiero S., Falanga A., Cantisani M., Tarallo R., Della Pepa M. E., D'Oriano V., Galdiero M.. 2012; Microbe–host interactions: structure and role of Gram-negative bacterial porins. Curr Protein Pept Sci13:843–854 [CrossRef][PubMed]
    [Google Scholar]
  23. Giltner C. L., Nguyen Y., Burrows L. L.. 2012; Type IV pilin proteins: versatile molecular modules. Microbiol Mol Biol Rev76:740–772 [CrossRef][PubMed]
    [Google Scholar]
  24. 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 A103:11358–11363 [CrossRef][PubMed]
    [Google Scholar]
  25. Gorgel M., Ulstrup J. J., Bøggild A., Jones N. C., Hoffmann S. V., Nissen P., Boesen T.. 2015; High-resolution structure of a type IV pilin from the metal-reducing bacterium Shewanella oneidensis. BMC Struct Biol15:4 [CrossRef][PubMed]
    [Google Scholar]
  26. Hofmann K., Stoffel W.. 1993; TMbase - A database of membrane spanning proteins segments. Biol Chem Hoppe Seyler374:166
    [Google Scholar]
  27. Imam S., Chen Z., Roos D. S., Pohlschröder M.. 2011; Identification of surprisingly diverse type IV pili, across a broad range of Gram-positive bacteria. PLoS One6:e28919 [CrossRef][PubMed]
    [Google Scholar]
  28. Kachlany S. C., Planet P. J., Desalle R., Fine D. H., Figurski D. H., Kaplan J. B.. 2001; flp-1, the first representative of a new pilin gene subfamily, is required for non-specific adherence of Actinobacillus actinomycetemcomitans. Mol Microbiol40:542–554 [CrossRef][PubMed]
    [Google Scholar]
  29. Katoh K., Standley D. M.. 2013; MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol30:772–780 [CrossRef][PubMed]
    [Google Scholar]
  30. Kim S. J., Park S. J., Jung M. Y., Kim J. G., Min U. G., Hong H. J., Rhee S. K.. 2014; Draft genome sequence of an aromatic compound-degrading bacterium, Desulfobacula sp. TS, belonging to the Deltaproteobacteria. FEMS Microbiol Lett360:9–12 [CrossRef][PubMed]
    [Google Scholar]
  31. Krogh A., Larsson B., von Heijne G., Sonnhammer E. L.. 2001; Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol305:567–580 [CrossRef][PubMed]
    [Google Scholar]
  32. Kuever J., Könneke M., Galushko A., Drzyzga O.. 2001; Reclassification of Desulfobacterium phenolicum as Desulfobacula phenolica comb. nov. and description of strain SaxT as Desulfotignum balticum gen. nov., sp. nov. Int J Syst Evol Microbiol51:171–177 [CrossRef][PubMed]
    [Google Scholar]
  33. Le S. Q., Gascuel O.. 2008; An improved general amino acid replacement matrix. Mol Biol Evol25:1307–1320 [CrossRef][PubMed]
    [Google Scholar]
  34. Li Y., Li H.. 2014; Type IV pili of Acidithiobacillus ferrooxidans can transfer electrons from extracellular electron donors. J Basic Microbiol54:226–231 [CrossRef][PubMed]
    [Google Scholar]
  35. 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 Microbiol80:1219–1224 [CrossRef][PubMed]
    [Google Scholar]
  36. Lovley D. R., Malvankar N. S.. 2015; Seeing is believing: novel imaging techniques help clarify microbial nanowire structure and function. Environ Microbiol17:2209–2215 [CrossRef][PubMed]
    [Google Scholar]
  37. Lovley D. R., Phillips E. J.. 1994; Novel processes for anaerobic sulfate production from elemental sulfur by sulfate-reducing bacteria. Appl Environ Microbiol60:2394–2399[PubMed]
    [Google Scholar]
  38. Lovley D. R., Coates J. D., Blunt-Harris E. L., Phillips E. J. P., Woodward J. C.. 1996; Humic substances as electron acceptors for microbial respiration. Nature382:445–448 [CrossRef]
    [Google Scholar]
  39. Lovley D. R., Roden E. E., Phillips E. J. P., Woodward J. C.. 1993; Enzymatic iron and uranium reduction by sulfate-reducing bacteria. Marine Geology113:41–53 [CrossRef]
    [Google Scholar]
  40. Lovley D. R., Ueki T., Zhang T., Malvankar N. S., Shrestha P. M., Flanangan K. A., Aklujkar M. A., Butler J. E., Giloteaux L. et al. 2011; Geobacter: the microbe electric's physiology, ecology, and practical applications. Adv Micro Physiol59:1–100
    [Google Scholar]
  41. Löytynoja A., Goldman N.. 2005; An algorithm for progressive multiple alignment of sequences with insertions. Proc Natl Acad Sci U S A102:10557–10562 [CrossRef][PubMed]
    [Google Scholar]
  42. Malvankar N. S., Lovley D. R.. 2014; Microbial nanowires for bioenergy applications. Curr Opin Biotechnol27:88–95 [CrossRef][PubMed]
    [Google Scholar]
  43. 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 Nanotechnol6:573–579 [CrossRef][PubMed]
    [Google Scholar]
  44. 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. MBio6:e00084 [CrossRef][PubMed]
    [Google Scholar]
  45. 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 Nanotechnol9:1012–1017 [CrossRef][PubMed]
    [Google Scholar]
  46. Marchler-Bauer A., Derbyshire M. K., Gonzales N. R., Lu S., Chitsaz F., Geer L. Y., Geer R. C., He J., Gwadz M. et al. 2015; CDD: NCBI's conserved domain database. Nucleic Acids Res43:D222–226 [CrossRef][PubMed]
    [Google Scholar]
  47. Mattick J. S.. 2002; Type IV pili and twitching motility. Annu Rev Microbiol56:289–314 [CrossRef][PubMed]
    [Google Scholar]
  48. Mouser P. J., N'Guessan A. L., Elifantz H., Holmes D. E., Williams K. H., Wilkins M. J., Long P. E., Lovley D. R.. 2009; Influence of heterogeneous ammonium availability on bacterial community structure and the expression of nitrogen fixation and ammonium transporter genes during in situ bioremediation of uranium-contaminated groundwater. Environ Sci Technol43:4386–4392 [CrossRef][PubMed]
    [Google Scholar]
  49. Nevin K. P., Lovley D. R.. 2000; Potential for nonenzymatic reduction of Fe(III) via electron shuttling in subsurface sediments. Environ. Sci. Technol34:2472–2478 [CrossRef]
    [Google Scholar]
  50. Nevin K. P., Lovley D. R.. 2002; Mechanisms for Fe(III) oxide reduction in sedimentary environments. Geomicrobiol J19:141–159 [CrossRef]
    [Google Scholar]
  51. Nevin K. P., Kim B. C., Glaven R. H., Johnson J. P., Woodard T. L., Methé B. A., Didonato R. J., Covalla S. F., Franks A. E. et al. 2009; Anode biofilm transcriptomics reveals outer surface components essential for high density current production in Geobacter sulfurreducens fuel cells. PLoS One4: [CrossRef][PubMed]
    [Google Scholar]
  52. Nivaskumar M., Francetic O.. 2014; Type II secretion system: a magic beanstalk or a protein escalator. Biochim Biophys Acta1843:1568–1577 [CrossRef][PubMed]
    [Google Scholar]
  53. Petersen T. N., Brunak S., von Heijne G., Nielsen H.. 2011; SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods8:785–786 [CrossRef][PubMed]
    [Google Scholar]
  54. Rabus R., Nordhaus R., Ludwig W., Widdel F.. 1993; Complete oxidation of toluene under strictly anoxic conditions by a new sulfate-reducing bacterium. Appl Environ Microbiol59:1444–1451[PubMed]
    [Google Scholar]
  55. Reardon P. N., Mueller K. T.. 2013; Structure of the type IVa major pilin from the electrically conductive bacterial nanowires of Geobacter sulfurreducens. J Biol Chem288:29260–29266 [CrossRef][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. Nature435:1098–1101 [CrossRef][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 Microbiol72:7345–7348 [CrossRef][PubMed]
    [Google Scholar]
  58. Rollefson J. B., Stephen C. S., Tien M., Bond D. R.. 2011; Identification of an extracellular polysaccharide network essential for cytochrome anchoring and biofilm formation in Geobacter sulfurreducens. J Bacteriol193:1023–1033 [CrossRef][PubMed]
    [Google Scholar]
  59. 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 Sci7:408–415 [CrossRef]
    [Google Scholar]
  60. Rotaru A.-E., Woodard T. L., Nevin K. P., Lovley D. R.. 2015; Link between capacity for current production and syntrophic growth in Geobacter species. Front Microbiol6: [CrossRef][PubMed]
    [Google Scholar]
  61. Sela I., Ashkenazy H., Katoh K., Pupko T.. 2015; GUIDANCE2: accurate detection of unreliable alignment regions accounting for the uncertainty of multiple parameters. Nucleic Acids Res43:W7–W14 [CrossRef][PubMed]
    [Google Scholar]
  62. Shrestha P. M., Rotaru A. E., Aklujkar M., Liu F., Shrestha M., Summers Z. M., Malvankar N., Flores D. C., Lovley D. R.. 2013; Syntrophic growth with direct interspecies electron transfer as the primary mechanism for energy exchange. Environ Microbiol Rep5:904–910 [CrossRef][PubMed]
    [Google Scholar]
  63. Smith J. A., Nevin K. P., Lovley D. R.. 2015; Syntrophic growth via quinone-mediated interspecies electron transfer. Front Microbiol6:121 [CrossRef][PubMed]
    [Google Scholar]
  64. 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. Science330:1413–1415 [CrossRef][PubMed]
    [Google Scholar]
  65. Sun H., Zusman D. R., Shi W.. 2000; Type IV pilus of Myxococcus xanthus is a motility apparatus controlled by the frz chemosensory system. Curr Biol10:1143–1146 [CrossRef][PubMed]
    [Google Scholar]
  66. Szabó Z., Stahl A. O., Albers S., Kissinger J. C., Driessen A. J., Pohlschröder M.. 2007; Identification of diverse archaeal proteins with class III signal peptides cleaved by distinct archaeal prepilin peptidases. J Bacteriol189:772–778 [CrossRef][PubMed]
    [Google Scholar]
  67. Tajima F.. 1989; Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics123:585–595[PubMed]
    [Google Scholar]
  68. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S.. 2013; MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol30:2725–2729 [CrossRef][PubMed]
    [Google Scholar]
  69. Tan Y., Adhikari R. Y., Malvankar N. S., Ward J. E., Nevin K. P., Woodard T. L., Smith J. A., Snoeyenbos-West O. L., Franks A. E. et al. 2016; The Low Conductivity of Geobacter uraniireducens Pili Suggests a Diversity of Extracellular Electron Transfer Mechanisms in the Genus Geobacter. Front Microbiol7:980
    [Google Scholar]
  70. Tomich M., Planet P. J., Figurski D. H.. 2007; The tad locus: postcards from the widespread colonization island. Nat Rev Microbiol5:363–375 [CrossRef][PubMed]
    [Google Scholar]
  71. Tusnády G. E., Simon I.. 2001; The HMMTOP transmembrane topology prediction server. Bioinformatics17:849–850 [CrossRef][PubMed]
    [Google Scholar]
  72. 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. MBio4:e0010500113 [CrossRef][PubMed]
    [Google Scholar]
  73. 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. Physical Review E84: [CrossRef]
    [Google Scholar]
  74. Venkidusamy K., Megharaj M., Schroder U., Karouta F., Mohan S. V, Naidu R.. 2015; Electron transport through electrically conductive nanofilaments in Rhodopseudomonas palustris strain RP2. RSC Adv. 5100790–100798
  75. Voordeckers J. W., Kim B. C., Izallalen M., Lovley D. R.. 2010; Role of Geobacter sulfurreducens outer surface c-type cytochromes in reduction of soil humic acid and anthraquinone-2,6-disulfonate. Appl Environ Microbiol76: 2371–2375 [CrossRef][PubMed]
    [Google Scholar]
  76. Waksman G., Hultgren S. J.. 2009; Structural biology of the chaperone-usher pathway of pilus biogenesis. Nat Rev Microbiol7:765–774 [CrossRef][PubMed]
    [Google Scholar]
  77. Wanger G., Gorby Y., El-Naggar M. Y., Yuzvinsky T. D., Schaudinn C., Gorur A., Sedghizadeh P. P.. 2013; Electrically conductive bacterial nanowires in biphosphonate-related osteonecrosis of the jaw biofilms. Oral and Maxillofacial Path115:71–78
    [Google Scholar]
  78. Yu N. Y., Wagner J. R., Laird M. R., Melli G., Rey S., Lo R., Dao P., Sahinalp S. C., Ester M. et al. 2010; PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics26:1608–1615 [CrossRef][PubMed]
    [Google Scholar]
  79. Zapun A., Missiakas D., Raina S., Creighton T. E.. 1995; Structural and functional characterization of DsbC, a protein involved in disulfide bond formation in Escherichia coli. Biochemistry34:5075–5089 [CrossRef][PubMed]
    [Google Scholar]
  80. Zhuang K., Izallalen M., Mouser P., Richter H., Risso C., Mahadevan R., Lovley D. R.. 2011; Genome-scale dynamic modeling of the competition between Rhodoferax and Geobacter in anoxic subsurface environments. ISME J5:305–316 [CrossRef][PubMed]
    [Google Scholar]
  81. Holmes, Dang, Walker, and Lovley, FigSharehttps://figshare.com/s/87e875d0c5c97c2e5498 2016
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000072
Loading
/content/journal/mgen/10.1099/mgen.0.000072
Loading

Data & Media loading...

Supplementary File 1

PDF

Most Cited This Month

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