1887

Abstract

The role of small-colony variants (SCVs) in the pathogenesis of biofilm-associated infections remains unclear. This study investigated the mechanism behind increased biofilm-forming potential of a menadione-auxotrophic SCV compared with the wild-type parental strain, as recently reported by our laboratory. SCVs displayed an autoaggregative phenotype, with a greater amount of polysaccharide intercellular adhesin (PIA), significantly reduced tricarboxylic acid cycle activity and a decreased susceptibility to aminoglycosides and cell-wall inhibitors compared with wild-type. The biofilms formed by the SCV were highly structured, consisting of large microcolonies separated by channels, and contained more biomass as well as significantly more PIA than wild-type biofilms. The surface hydrophobicity of the two phenotypes was similar. Thus, the autoaggregation and increased biofilm-forming capacity of menadione-auxotrophic SCVs in this study was related to the enhanced production of PIA in these variants.

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2010-05-01
2024-03-28
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References

  1. Acar J. F., Goldstein F. W., Lagrange P. 1978; Human infections caused by thiamine- or menadione-requiring Staphylococcus aureus . J Clin Microbiol 8:142–147
    [Google Scholar]
  2. Al Laham N., Rohde H., Sander G., Fischer A., Hussain M., Heilmann C., Mack D., Proctor R., Peters G. other authors 2007; Augmented expression of polysaccharide intercellular adhesin in a defined Staphylococcus epidermidis mutant with the small-colony-variant phenotype. J Bacteriol 189:4494–4501 [CrossRef]
    [Google Scholar]
  3. Allegrucci M., Sauer K. 2007; Characterization of colony morphology variants isolated from Streptococcus pneumoniae biofilms. J Bacteriol 189:2030–2038 [CrossRef]
    [Google Scholar]
  4. Besier S., Smaczny C., von Mallinckrodt C., Krahl A., Ackermann H., Brade V., Wichelhaus T. A. 2007; Prevalence and clinical significance of Staphylococcus aureus small-colony variants in cystic fibrosis lung disease. J Clin Microbiol 45:168–172 [CrossRef]
    [Google Scholar]
  5. Chuard C., Vaudaux P. E., Proctor R. A., Lew D. P. 1997; Decreased susceptibility to antibiotic killing of a stable small colony variant of Staphylococcus aureus in fluid phase and on fibronectin-coated surfaces. J Antimicrob Chemother 39:603–608 [CrossRef]
    [Google Scholar]
  6. CLSI 2006; Performance Standards for Antimicrobial Susceptibility Testing ; 16th Informational Supplement. CLSI document M100-S16 Wayne, PA: Clinical and Laboratory Standards Institute;
  7. Costerton J. W., Stewart P. S., Greenberg E. P. 1999; Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322 [CrossRef]
    [Google Scholar]
  8. Cramton S. E., Ulrich M., Gotz F., Doring G. 2001; Anaerobic conditions induce expression of polysaccharide intercellular adhesin in Staphylococcus aureus and Staphylococcus epidermidis . Infect Immun 69:4079–4085 [CrossRef]
    [Google Scholar]
  9. Drenkard E., Ausubel F. M. 2002; Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416:740–743 [CrossRef]
    [Google Scholar]
  10. Fux C. A., Costerton J. W., Stewart P. S., Stoodley P. 2005; Survival strategies of infectious biofilms. Trends Microbiol 13:34–40 [CrossRef]
    [Google Scholar]
  11. Haussler S., Ziegler I., Lottel A., von Gotz F., Rohde M., Wehmhohner D., Saravanamuthu S., Tummler B., Steinmetz I. 2003; Highly adherent small-colony variants of Pseudomonas aeruginosa in cystic fibrosis lung infection. J Med Microbiol 52:295–301 [CrossRef]
    [Google Scholar]
  12. Heilmann C., Schweitzer O., Gerke C., Vanittanakom N., Mack D., Gotz F. 1996; Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis . Mol Microbiol 20:1083–1091 [CrossRef]
    [Google Scholar]
  13. Higashi J. M., Sullam P. M. 2006; Staphylococcus aureus biofilms. In Biofilms, Infection, and Antimicrobial Therapy pp 81–108 Edited by Pace J. L., Rupp M. E., Finch R. G. Boca Raton, FL: Taylor and Francis Group;
    [Google Scholar]
  14. Jefferson K. K. 2004; What drives bacteria to produce a biofilm?. FEMS Microbiol Lett 236:163–173 [CrossRef]
    [Google Scholar]
  15. Jefferson K. K., Cerca N. 2006; Bacterial–bacterial cell interactions in biofilms: detection of polysaccharide intercellular adhesins by blotting and confocal microscopy. Methods Mol Biol 341:119–126
    [Google Scholar]
  16. Kahl B. C., Belling G., Becker P., Chatterjee I., Wardecki K., Hilgert K., Cheung A. L., Peters G., Herrmann M. 2005; Thymidine-dependent Staphylococcus aureus small-colony variants are associated with extensive alterations in regulator and virulence gene expression profiles. Infect Immun 73:4119–4126 [CrossRef]
    [Google Scholar]
  17. Kennedy M. C., Emptage M. H., Dreyer J. L., Beinert H. 1983; The role of iron in the activation–inactivation of aconitase. J Biol Chem 258:11098–11105
    [Google Scholar]
  18. Kirisits M. J., Prost L., Starkey M., Parsek M. R. 2005; Characterization of colony morphology variants isolated from Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 71:4809–4821 [CrossRef]
    [Google Scholar]
  19. Kohler C., von Eiff C., Liebeke M., McNamara P. J., Lalk M., Proctor R. A., Hecker M., Engelmann S. 2008; A defect in menadione biosynthesis induces global changes in gene expression in Staphylococcus aureus . J Bacteriol 190:6351–6364 [CrossRef]
    [Google Scholar]
  20. Moisan H., Brouillette E., Jacob C. L., Langlois-Begin P., Michaud S., Malouin F. 2006; Transcription of virulence factors in Staphylococcus aureus small-colony variants isolated from cystic fibrosis patients is influenced by SigB. J Bacteriol 188:64–76 [CrossRef]
    [Google Scholar]
  21. O'Gara J. P. 2007; ica and beyond: biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus . FEMS Microbiol Lett 270:179–188 [CrossRef]
    [Google Scholar]
  22. Otto M. 2008; Staphylococcal biofilms. In Bacterial Biofilms pp 207–228 Edited by Romeo T. Heidelberg: Springer;
    [Google Scholar]
  23. Perez P. F., Minnaard Y., Disalvo E. A., De Antoni G. L. 1998; Surface properties of bifidobacterial strains of human origin. Appl Environ Microbiol 64:21–26
    [Google Scholar]
  24. Proctor R. A., Peters G. 1998; Small colony variants in staphylococcal infections: diagnostic and therapeutic implications. Clin Infect Dis 27:419–422 [CrossRef]
    [Google Scholar]
  25. Proctor R. A., van Langevelde P., Kristjansson M., Maslow J. N., Arbeit R. D. 1995; Persistent and relapsing infections associated with small-colony variants of Staphylococcus aureus . Clin Infect Dis 20:95–102 [CrossRef]
    [Google Scholar]
  26. Proctor R. A., Kahl B., von Eiff C., Vaudaux P. E., Lew D. P., Peters G. 1998; Staphylococcal small colony variants have novel mechanisms for antibiotic resistance. Clin Infect Dis 27:S68–S74 [CrossRef]
    [Google Scholar]
  27. Proctor R. A., von Eiff C., Kahl B. C., Becker K., McNamara P., Herrmann M., Peters G. 2006; Small colony variants: a pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat Rev Microbiol 4:295–305 [CrossRef]
    [Google Scholar]
  28. Singh R., Ray P., Das A., Sharma M. 2009; Role of persisters and small-colony variants in antibiotic resistance of planktonic and biofilm-associated Staphylococcus aureus : an in vitro study. J Med Microbiol 58:1067–1073 [CrossRef]
    [Google Scholar]
  29. Starkey M., Hickman J. H., Ma L., Zhang N., De Long S., Hinz A., Palacios S., Manoil C., Kirisits M. J. other authors 2009; Pseudomonas aeruginosa rugose small-colony variants have adaptations that likely promote persistence in the cystic fibrosis lung. J Bacteriol 191:3492–3503 [CrossRef]
    [Google Scholar]
  30. Stewart P. S., Rani S. A., Gjersing E., Codd S. L., Zheng Z., Pitts B. 2007; Observations of cell cluster hollowing in Staphylococcus epidermidis biofilms. Lett Appl Microbiol 44:454–457 [CrossRef]
    [Google Scholar]
  31. Vaudaux P., Francois P., Bisognano C., Kelley W. L., Lew D. P., Schrenzel J., Proctor R. A., McNamara P. J., Peters G., Von Eiff C. 2002; Increased expression of clumping factor and fibronectin-binding proteins by hemB mutants of Staphylococcus aureus expressing small colony variant phenotypes. Infect Immun 70:5428–5437 [CrossRef]
    [Google Scholar]
  32. von Eiff C., Bettin D., Proctor R. A., Rolauffs B., Lindner N., Winkelmann W., Peters G. 1997; Recovery of small colony variants of Staphylococcus aureus following gentamicin bead placement for osteomyelitis. Clin Infect Dis 25:1250–1251 [CrossRef]
    [Google Scholar]
  33. Vuong C., Kidder J. B., Jacobson E. R., Otto M., Proctor R. A., Somerville G. A. 2005; Staphylococcus epidermidis polysaccharide intercellular adhesin production significantly increases during tricarboxylic acid cycle stress. J Bacteriol 187:2967–2973 [CrossRef]
    [Google Scholar]
  34. Williams I., Venables W. A., Lloyd D., Paul F., Critchley I. 1997; The effects of adherence to silicone surfaces on antibiotic susceptibility in Staphylococcus aureus . Microbiology 143:2407–2413 [CrossRef]
    [Google Scholar]
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