1887

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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2008-10-01
2019-10-20
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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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [Google Scholar]
  5. Cole, R. M. & Hahn, J. J. ( 1962; ). Cell wall replication in Streptococcus pyogenes. Science 135, 722–724.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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 [CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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 [CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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 [CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [Google Scholar]
  26. Marraffini, L. A. & Schneewind, O. ( 2006; ). Targeting proteins to the cell wall of sporulating Bacillus anthracis. Mol Microbiol 62, 1402–1417.[CrossRef]
    [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.[CrossRef]
    [Google Scholar]
  28. Murray, B. E. ( 2000; ). Vancomycin-resistant enterococcal infections. N Engl J Med 342, 710–721.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [Google Scholar]
  33. Salton, M. R. ( 1952; ). Cell wall of Micrococcus lysodeikticus as the substrate of lysozyme. Nature 170, 746–747.[CrossRef]
    [Google Scholar]
  34. Schneewind, O., Model, P. & Fischetti, V. A. ( 1992; ). Sorting of protein A to the staphylococcal cell wall. Cell 70, 267–281.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [Google Scholar]
  39. Ton-That, H. & Schneewind, O. ( 2003; ). Assembly of pili on the surface of Corynebacterium diphtheriae. Mol Microbiol 50, 1429–1438.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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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