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Volume 154, Issue 10

Expression of two distinct types of pili by a hospital-acquired isolate Free

Abstract

Surface filamentous structures designated pili, and implicated in virulence, have been found on the surfaces of several Gram-positive pathogens. This work describes the conditional expression of two phenotypically distinct pilus-like structures, designated PilA and PilB, on the surface of a hospital-adapted bloodstream isolate. is an emerging Gram-positive opportunistic pathogen that can cause severe disease, particularly in immunocompromised patients. Expression of PilA- and PilB-type pili was analysed during different phases of growth in broth culture. During growth, PilA and PilB pilin subunits were expressed around the cross-wall in early-exponential-phase cells. Polymerization and migration of short PilB-type pili towards the poles occurred in cells from the exponential phase and long polymerized pili were expressed at the poles of cells grown to stationary phase. In contrast, PilA-type pili were not expressed in broth culture, but only when cells were grown on solid media. Furthermore, surface expression of the PilA- and PilB-type pili was regulated in a temperature-dependent manner, as polymerization of two distinct types of pili at the surface only occurred when cells were grown at 37 °C; no pili were observed on cells grown at 21 °C. Hospital-aquired isolates were specifically enriched in pilin gene clusters, suggesting that conditional expression of pili may contribute to pathogenesis.

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  • Published Online:
Keyword(s): CWS, cell wall sorting signal , PGC, pilin gene cluster and TEM, transmission electron microscopy
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2008-10-01
2024-04-19
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References

  1. Abbot E. L., Smith W. D., Siou G. P., Chiriboga C., Smith R. J., Wilson J. A., Hirst B. H., Kehoe M. A. 2007; Pili mediate specific adhesion of Streptococcus pyogenes to human tonsil and skin. Cell Microbiol 9:1822–1833
     [Google Scholar]
  2. Bendtsen J. D., Nielsen H., von Heijne G., Brunak S. 2004; Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783–795
     [Google Scholar]
  3. Boekhorst J., de Been M. W., Kleerebezem M., Siezen R. J. 2005; Genome-wide detection and analysis of cell wall-bound proteins with LPxTG-like sorting motifs. J Bacteriol 187:4928–4934
     [Google Scholar]
  4. Cheung A. L., Eberhardt K. J., Fischetti V. A. 1994; A method to isolate RNA from gram-positive bacteria and mycobacteria. Anal Biochem 222:511–514
     [Google Scholar]
  5. Cole R. M., Hahn J. J. 1962; Cell wall replication in Streptococcus pyogenes . Science 135:722–724
     [Google Scholar]
  6. DeDent A. C., McAdow M., Schneewind O. 2007; Distribution of protein A on the surface of Staphylococcus aureus . J Bacteriol 189:4473–4484
     [Google Scholar]
  7. Dramsi S., Caliot E., Bonne I., Guadagnini S., Prevost M. C., Kojadinovic M., Lalioui L., Poyart C., Trieu-Cuot P. 2006; Assembly and role of pili in group B streptococci. Mol Microbiol 60:1401–1413
     [Google Scholar]
  8. Gaspar A. H., Ton-That H. 2006; Assembly of distinct pilus structures on the surface of Corynebacterium diphtheriae . J Bacteriol 188:1526–1533
     [Google Scholar]
  9. Ghuysen J. M. 1968; Use of bacteriolytic enzymes in determination of wall structure and their role in cell metabolism. Bacteriol Rev 32:425–464
     [Google Scholar]
  10. Gianfaldoni C., Censini S., Hilleringmann M., Moschioni M., Facciotti C., Pansegrau W., Masignani V., Covacci A., Rappuoli R. other authors 2007; Streptococcus pneumoniae pilus subunits protect mice against lethal challenge. Infect Immun 75:1059–1062
     [Google Scholar]
  11. Giesbrecht P., Kersten T., Maidhof H., Wecke J. 1998; Staphylococcal cell wall: morphogenesis and fatal variations in the presence of penicillin. Microbiol Mol Biol Rev 62:1371–1414
     [Google Scholar]
  12. Hendrickx A. P., Van Wamel W. J., Posthuma G., Bonten M. J., Willems R. J. 2007; Five genes encoding surface-exposed LPXTG proteins are enriched in hospital-adapted Enterococcus faecium clonal complex 17 isolates. J Bacteriol 189:8321–8332
     [Google Scholar]
  13. Hilleringmann M., Giusti F., Baudner B. C., Masignani V., Covacci A., Rappuoli R., Barocchi M. A., Ferlenghi I. 2008; Pneumococcal pili are composed of protofilaments exposing adhesive clusters of Rrg A. PLoS Pathog 4:e1000026
     [Google Scholar]
  14. Holden N. J., Gally D. L. 2004; Switches, cross-talk and memory in Escherichia coli adherence. J Med Microbiol 53:585–593
     [Google Scholar]
  15. Iwen P. C., Kelly D. M., Linder J., Hinrichs S. H., Dominguez E. A., Rupp M. E., Patil K. D. 1997; Change in prevalence and antibiotic resistance of Enterococcus species isolated from blood cultures over an 8-year period. Antimicrob Agents Chemother 41:494–495
     [Google Scholar]
  16. Kearns D. B., Chu F., Rudner R., Losick R. 2004; Genes governing swarming in Bacillus subtilis and evidence for a phase variation mechanism controlling surface motility. Mol Microbiol 52:357–369
     [Google Scholar]
  17. Lauer P., Rinaudo C. D., Soriani M., Margarit I., Maione D., Rosini R., Taddei A. R., Mora M., Rappuoli R. other authors 2005; Genome analysis reveals pili in Group B Streptococcus . Science 309:105
     [Google Scholar]
  18. Leavis H., Top J., Shankar N., Borgen K., Bonten M., van Embden J., Willems R. J. 2004; A novel putative enterococcal pathogenicity island linked to the esp virulence gene of Enterococcus faecium and associated with epidemicity. J Bacteriol 186:672–682
     [Google Scholar]
  19. Leavis H. L., Bonten M. J., Willems R. J. 2006a; Identification of high-risk enterococcal clonal complexes: global dispersion and antibiotic resistance. Curr Opin Microbiol 9:454–460
     [Google Scholar]
  20. Leavis H. L., Willems R. J., Top J., Bonten M. J. 2006b; High-level ciprofloxacin resistance from point mutations in gyrA and parC confined to global hospital-adapted clonal lineage CC17 of Enterococcus faecium . J Clin Microbiol 44:1059–1064
     [Google Scholar]
  21. Leavis H. L., Willems R. J., Van Wamel W. J., Schuren F. H., Caspers M. P., Bonten M. J. 2007; Insertion sequence-driven diversification creates a globally dispersed emerging multiresistant subspecies of E. faecium . PLoS Pathog 3:e7
     [Google Scholar]
  22. Maisey H. C., Hensler M., Nizet V., Doran K. S. 2007; Group B streptococcal pilus proteins contribute to adherence to and invasion of brain microvascular endothelial cells. J Bacteriol 189:1464–1467
     [Google Scholar]
  23. Maisey H. C., Quach D., Hensler M. E., Liu G. Y., Gallo R. L., Nizet V., Doran K. S. 2008; A group B streptococcal pilus protein promotes phagocyte resistance and systemic virulence. FASEB J 22:1715–1724
     [Google Scholar]
  24. Mandlik A., Swierczynski A., Das A., Ton-That H. 2007; Corynebacterium diphtheriae employs specific minor pilins to target human pharyngeal epithelial cells. Mol Microbiol 64:111–124
     [Google Scholar]
  25. Mandlik A., Swierczynski A., Das A., Ton-That H. 2008; Pili in Gram-positive bacteria: assembly, involvement in colonization and biofilm development. Trends Microbiol 16:33–40
     [Google Scholar]
  26. Marraffini L. A., Schneewind O. 2006; Targeting proteins to the cell wall of sporulating Bacillus anthracis . Mol Microbiol 62:1402–1417
     [Google Scholar]
  27. Murdoch D. R., Mirrett S., Harrell L. J., Monahan J. S., Reller L. B. 2002; Sequential emergence of antibiotic resistance in enterococcal bloodstream isolates over 25 years. Antimicrob Agents Chemother 46:3676–3678
     [Google Scholar]
  28. Murray B. E. 2000; Vancomycin-resistant enterococcal infections. N Engl J Med 342:710–721
     [Google Scholar]
  29. Nallapareddy S. R., Murray B. E. 2006; Ligand-signaled upregulation of Enterococcus faecalis ace transcription, a mechanism for modulating host– E. faecalis interaction. Infect Immun 74:4982–4989
     [Google Scholar]
  30. Nallapareddy S. R., Singh K. V., Sillanpaa J., Garsin D. A., Hook M., Erlandsen S. L., Murray B. E. 2006; Endocarditis and biofilm-associated pili of Enterococcus faecalis . J Clin Invest 116:2799–2807
     [Google Scholar]
  31. Navarre W. W., Schneewind O. 1999; Surface proteins of gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol Mol Biol Rev 63:174–229
     [Google Scholar]
  32. Nelson A. L., Ries J., Bagnoli F., Dahlberg S., Falker S., Rounioja S., Tschop J., Morfeldt E., Ferlenghi I. other authors 2007; RrgA is a pilus-associated adhesin in Streptococcus pneumoniae . Mol Microbiol 66:329–340
     [Google Scholar]
  33. Salton M. R. 1952; Cell wall of Micrococcus lysodeikticus as the substrate of lysozyme. Nature 170:746–747
     [Google Scholar]
  34. Schneewind O., Model P., Fischetti V. A. 1992; Sorting of protein A to the staphylococcal cell wall. Cell 70:267–281
     [Google Scholar]
  35. Schneewind O., Mihaylova-Petkov D., Model P. 1993; Cell wall sorting signals in surface proteins of gram-positive bacteria. EMBO J 12:4803–4811
     [Google Scholar]
  36. Swaminathan A., Mandlik A., Swierczynski A., Gaspar A., Das A., Ton-That H. 2007; Housekeeping sortase facilitates the cell wall anchoring of pilus polymers in Corynebacterium diphtheriae . Mol Microbiol 66:961–974
     [Google Scholar]
  37. Swierczynski A., Ton-That H. 2006; Type III pilus of corynebacteria: pilus length is determined by the level of its major pilin subunit. J Bacteriol 188:6318–6325
     [Google Scholar]
  38. Tendolkar P. M., Baghdayan A. S., Shankar N. 2006; Putative surface proteins encoded within a novel transferable locus confer a high-biofilm phenotype to Enterococcus faecalis . J Bacteriol 188:2063–2072
     [Google Scholar]
  39. Ton-That H., Schneewind O. 2003; Assembly of pili on the surface of Corynebacterium diphtheriae . Mol Microbiol 50:1429–1438
     [Google Scholar]
  40. Ton-That H., Marraffini L. A., Schneewind O. 2004; Sortases and pilin elements involved in pilus assembly of Corynebacterium diphtheriae . Mol Microbiol 53:251–261
     [Google Scholar]
  41. Top J., Willems R., Blok H., de Regt M., Jalink K., Troelstra A., Goorhuis B., Bonten M. 2007; Ecological replacement of Enterococcus faecalis by multiresistant clonal complex 17 Enterococcus faecium . Clin Microbiol Infect 13:316–319
     [Google Scholar]
  42. Treitman A. N., Yarnold P. R., Warren J., Noskin G. A. 2005; Emerging incidence of Enterococcus faecium among hospital isolates (1993 to 2002). J Clin Microbiol 43:462–463
     [Google Scholar]
  43. van der Woude M. W. 2006; Re-examining the role and random nature of phase variation. FEMS Microbiol Lett 254:190–197
     [Google Scholar]
  44. Van Wamel W. J., Hendrickx A. P., Bonten M. J., Top J., Posthuma G., Willems R. J. 2007; Growth condition-dependent Esp expression by Enterococcus faecium affects initial adherence and biofilm formation. Infect Immun 75:924–931
     [Google Scholar]
  45. Willems R. J., Top J., van Santen M., Robinson D. A., Coque T. M., Baquero F., Grundmann H., Bonten M. J. 2005; Global spread of vancomycin-resistant Enterococcus faecium from distinct nosocomial genetic complex. Emerg Infect Dis 11:821–828
     [Google Scholar]
  46. Yeung M. K., Ragsdale P. A. 1997; Synthesis and function of Actinomyces naeslundii T14V type 1 fimbriae require the expression of additional fimbria-associated genes. Infect Immun 65:2629–2639
     [Google Scholar]
  47. Yeung M. K., Donkersloot J. A., Cisar J. O., Ragsdale P. A. 1998; Identification of a gene involved in assembly of Actinomyces naeslundii T14V type 2 fimbriae. Infect Immun 66:1482–1491
     [Google Scholar]
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Expression of two distinct types of pili by a hospital-acquired Enterococcus faecium isolate
Microbiology 154, 3212 (2008); https://doi.org/10.1099/mic.0.2008/020891-0
/content/journal/micro/10.1099/mic.0.2008/020891-0
/content/journal/micro/10.1099/mic.0.2008/020891-0
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