1887

Abstract

Generation of biofilms by the pathogenic yeast is correlated closely with disease. The phenomenon of phenotype switching in 20 isolates of was examined and the relationship with biofilm development was investigated. Four stable and heritable phenotypes were identified – crepe, concentric, smooth and crater. Cells from crepe and concentric phenotypes are almost entirely pseudohyphal, whilst cells from smooth and crater phenotypes are mostly yeast-like. The pseudohyphae from concentric phenotypes are approximately 45 % wider than those from crepe cells. The cell size of the smooth phenotype is smaller than those of the other three phenotypes. On polystyrene surfaces, the concentric phenotype generates up to twofold more biofilm than the crepe and crater phenotypes. Smooth phenotypes generate the least biofilm. Concentric phenotypes also invade agar surfaces more than the crepe and crater phenotypes, whilst smooth phenotypes do not invade at all. The smooth phenotype, however, grows significantly faster than the others. The quorum-sensing molecule farnesol inhibits formation of biofilms by the crepe, concentric and crater phenotypes.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.27739-0
2005-04-01
2019-10-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/151/4/mic1511073.html?itemId=/content/journal/micro/10.1099/mic.0.27739-0&mimeType=html&fmt=ahah

References

  1. Anderson, J. M. & Soll, D. R. ( 1987; ). Unique phenotype of opaque cells in the white-opaque transition of Candida albicans. J Bacteriol 169, 5579–5588.
    [Google Scholar]
  2. Baillie, G. S. & Douglas, L. J. ( 1999; ). Role of dimorphism in the development of Candida albicans biofilms. J Med Microbiol 48, 671–679.[CrossRef]
    [Google Scholar]
  3. Branchini, M. L., Pfaller, M. A., Rhine-Chalberg, J., Frempong, T. & Isenberg, H. D. ( 1994; ). Genotypic variation and slime production among blood and catheter isolates of Candida parapsilosis. J Clin Microbiol 32, 452–456.
    [Google Scholar]
  4. Brockert, P. J., Lachke, S. A., Srikantha, T., Pujol, C., Galask, R. & Soll, D. R. ( 2003; ). Phenotypic switching and mating type switching of Candida glabrata at sites of colonization. Infect Immun 71, 7109–7118.[CrossRef]
    [Google Scholar]
  5. Chandra, J., Kuhn, D. M., Mukherjee, P. K., Hoyer, L. L., McCormick, T. & Ghannoum, M. A. ( 2001; ). Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J Bacteriol 183, 5385–5394.[CrossRef]
    [Google Scholar]
  6. Déziel, E., Comeau, Y. & Villemur, R. ( 2001; ). Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities. J Bacteriol 183, 1195–1204.[CrossRef]
    [Google Scholar]
  7. Dieterich, C., Schandar, M., Noll, M., Johannes, F.-J., Brunner, H., Graeve, T. & Rupp, S. ( 2002; ). In vitro reconstructed human epithelia reveal contributions of Candida albicans EFG1 and CPH1 to adhesion and invasion. Microbiology 148, 497–506.
    [Google Scholar]
  8. Djordjevic, D., Wiedmann, M. & McLandsborough, L. A. ( 2002; ). Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation. Appl Environ Microbiol 68, 2950–2958.[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. Enger, L., Joly, S., Pujol, C., Simonson, P., Pfaller, M. & Soll, D. R. ( 2001; ). Cloning and characterization of a complex DNA fingerprinting probe for Candida parapsilosis. J Clin Microbiol 39, 658–669.[CrossRef]
    [Google Scholar]
  11. Fu, Y., Rieg, G., Fonzi, W. A., Belanger, P. H., Edwards, J. E., Jr & Filler, S. G. ( 1998; ). Expression of the Candida albicans gene ALS1 in Saccharomyces cerevisiae induces adherence to endothelial and epithelial cells. Infect Immun 66, 1783–1786.
    [Google Scholar]
  12. Fu, Y., Ibrahim, A. S., Sheppard, D. C., Chen, Y.-C., French, S. W., Cutler, J. E., Filler, S. G. & Edwards, J. E., Jr ( 2002; ). Candida albicans Als1p: an adhesin that is a downstream effector of the EFG1 filamentation pathway. Mol Microbiol 44, 61–72.[CrossRef]
    [Google Scholar]
  13. García-Sánchez, S., Aubert, S., Iraqui, I., Janbon, G., Ghigo, J.-M. & d'Enfert, C. ( 2004; ). Candida albicans biofilms: a developmental state associated with specific and stable gene expression patterns. Eukaryot Cell 3, 536–545.[CrossRef]
    [Google Scholar]
  14. Hajjeh, R. A., Sofair, A. N., Harrison, L. H. & 13 other authors ( 2004; ). Incidence of bloodstream infections due to Candida species and in vitro susceptibilities of isolates collected from 1998 to 2000 in a population-based active surveillance program. J Clin Microbiol 42, 1519–1527.[CrossRef]
    [Google Scholar]
  15. Hall-Stoodley, L., Costerton, J. W. & Stoodley, P. ( 2004; ). Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2, 95–108.[CrossRef]
    [Google Scholar]
  16. Häußler, S. ( 2004; ). Biofilm formation by the small colony variant phenotype of Pseudomonas aeruginosa. Environ Microbiol 6, 546–551.[CrossRef]
    [Google Scholar]
  17. Hawser, S. P. & Douglas, L. J. ( 1994; ). Biofilm formation by Candida species on the surface of catheter materials in vitro. Infect Immun 62, 915–921.
    [Google Scholar]
  18. Hornby, J. M., Jensen, E. C., Lisec, A. D., Tasto, J. J., Jahnke, B., Shoemaker, R., Dussault, P. & Nickerson, K. W. ( 2001; ). Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl Environ Microbiol 67, 2982–2992.[CrossRef]
    [Google Scholar]
  19. Jabra-Rizk, M. A., Falkler, W. A. & Meiller, T. F. ( 2004; ). Fungal biofilms and drug resistance. Emerg Infect Dis 10, 14–19.[CrossRef]
    [Google Scholar]
  20. Kennedy, M. J., Rogers, A. L., Hanselmen, L. R., Soll, D. R. & Yancey, R. J., Jr ( 1988; ). Variation in adhesion and cell surface hydrophobicity in Candida albicans white and opaque phenotypes. Mycopathologia 102, 149–156.[CrossRef]
    [Google Scholar]
  21. Kruppa, M., Krom, B. P., Chauhan, N., Bambach, A. V., Cihlar, R. L. & Calderone, R. A. ( 2004; ). The two-component signal transduction protein Chk1p regulates quorum sensing in Candida albicans. Eukaryot Cell 3, 1062–1065.[CrossRef]
    [Google Scholar]
  22. Kuchma, S. L. & O'Toole, G. A. ( 2000; ). Surface-induced and biofilm-induced changes in gene expression. Curr Opin Biotechnol 11, 429–433.[CrossRef]
    [Google Scholar]
  23. Kuhn, D. M., Chandra, J., Mukherjee, P. K. & Ghannoum, M. A. ( 2002; ). Comparison of biofilms formed by Candida albicans and Candida parapsilosis on bioprosthetic surfaces. Infect Immun 70, 878–888.[CrossRef]
    [Google Scholar]
  24. Kumamoto, C. A. ( 2002; ). Candida biofilms. Curr Opin Microbiol 5, 608–611.[CrossRef]
    [Google Scholar]
  25. Lewis, R. E., Lo, H.-J., Raad, I. I. & Kontoyiannis, D. P. ( 2002; ). Lack of catheter infection by the efg1/efg1 cph1/cph1 double-null mutant, a Candida albicans strain that is defective in filamentous growth. Antimicrob Agents Chemother 46, 1153–1155.[CrossRef]
    [Google Scholar]
  26. Lott, T. J., Kuykendall, R. J., Welbel, S. F., Pramanik, A. & Lasker, B. A. ( 1993; ). Genomic heterogeneity in the yeast Candida parapsilosis. Curr Genet 23, 463–467.[CrossRef]
    [Google Scholar]
  27. Odds, F. C. ( 1988; ). Candida and Candidosis, 2nd edn. London: Baillière Tindall.
  28. Pfaller, M. A. & Diekema, D. J. ( 2004; ). Twelve years of fluconazole in clinical practice: global trends in species distribution and fluconazole susceptibility of bloodstream isolates of Candida. Clin Microbiol Infect 10 (Suppl. 1), 11–23.[CrossRef]
    [Google Scholar]
  29. Ramage, G., Vande Walle, K., Wickes, B. L. & López-Ribot, J. L. ( 2001; ). Standardized method for in vitro antifungal susceptibility testing of Candida albicans biofilms. Antimicrob Agents Chemother 45, 2475–2479.[CrossRef]
    [Google Scholar]
  30. Ramage, G., Saville, S. P., Wickes, B. L. & López-Ribot, J. L. ( 2002a; ). Inhibition of Candida albicans biofilm formation by farnesol, a quorum-sensing molecule. Appl Environ Microbiol 68, 5459–5463.[CrossRef]
    [Google Scholar]
  31. Ramage, G., VandeWalle, K., López-Ribot, J. & Wickes, B. L. ( 2002b; ). The filamentation pathway controlled by the Efg1 regulator protein is required for normal biofilm formation and development in Candida albicans. FEMS Microbiol Lett 214, 95–100.[CrossRef]
    [Google Scholar]
  32. Rashid, M. H., Rajanna, C., Ali, A. & Karaolis, D. K. R. ( 2003; ). Identification of genes involved in the switch between the smooth and rugose phenotypes of Vibrio cholerae. FEMS Microbiol Lett 227, 113–119.[CrossRef]
    [Google Scholar]
  33. Rashid, M. H., Rajanna, C., Zhang, D., Pasquale, V., Magder, L. S., Ali, A., Dumontet, S. & Karaolis, D. K. R. ( 2004; ). Role of exopolysaccharide, the rugose phenotype and VpsR in the pathogenesis of epidemic Vibrio cholerae. FEMS Microbiol Lett 230, 105–113.[CrossRef]
    [Google Scholar]
  34. Ren, D., Bedzyk, L. A., Setlow, P., Thomas, S. M., Ye, R. W. & Wood, T. K. ( 2004a; ). Gene expression in Bacillus subtilis surface biofilms with and without sporulation and the importance of yveR for biofilm maintenance. Biotechnol Bioeng 86, 344–364.[CrossRef]
    [Google Scholar]
  35. Ren, D., Bedzyk, L. A., Thomas, S. M., Ye, R. W. & Wood, T. K. ( 2004b; ). Gene expression in Escherichia coli biofilms. Appl Microbiol Biotechnol 64, 515–524.[CrossRef]
    [Google Scholar]
  36. Roilides, E., Farmaki, E., Evdoridou, J. & 9 other authors ( 2004; ). Neonatal candidiasis: analysis of epidemiology, drug susceptibility, and molecular typing of causative isolates. Eur J Clin Microbiol Infect Dis 23, 745–750.[CrossRef]
    [Google Scholar]
  37. Sato, T., Watanabe, T., Mikami, T. & Matsumoto, T. ( 2004; ). Farnesol, a morphogenetic autoregulatory substance in the dimorphic fungus Candida albicans, inhibits hyphae growth through suppression of a mitogen-activated protein kinase cascade. Biol Pharm Bull 27, 751–752.[CrossRef]
    [Google Scholar]
  38. Schembri, M. A., Kjærgaard, K. & Klemm, P. ( 2003; ). Global gene expression in Escherichia coli biofilms. Mol Microbiol 48, 253–267.[CrossRef]
    [Google Scholar]
  39. Schoolnik, G. K., Voskuil, M. I., Schnappinger, D., Yildiz, F. H., Meibom, K., Dolganov, N. A., Wilson, M. A. & Chong, K. H. ( 2001; ). Whole genome DNA microarray expression analysis of biofilm development by Vibrio cholerae O1 E1 Tor. Methods Enzymol 336, 3–18.
    [Google Scholar]
  40. Shchepin, R., Hornby, J. M., Burger, E., Niessen, T., Dussault, P. & Nickerson, K. W. ( 2003; ). Quorum sensing in Candida albicans: probing farnesol's mode of action with 40 natural and synthetic farnesol analogs. Chem Biol 10, 743–750.[CrossRef]
    [Google Scholar]
  41. Shin, J. H., Kee, S. J., Shin, M. G., Kim, S. H., Shin, D. H., Lee, S. K., Suh, S. P. & Ryang, D. W. ( 2002; ). Biofilm production by isolates of Candida species recovered from nonneutropenic patients: comparison of bloodstream isolates with isolates from other sources. J Clin Microbiol 40, 1244–1248.[CrossRef]
    [Google Scholar]
  42. Slutsky, B., Buffo, J. & Soll, D. R. ( 1985; ). High-frequency switching of colony morphology in Candida albicans. Science 230, 666–669.[CrossRef]
    [Google Scholar]
  43. Soll, D. R., Morrow, B. & Srikantha, T. ( 1993; ). High-frequency phenotypic switching in Candida albicans. Trends Genet 9, 61–65.[CrossRef]
    [Google Scholar]
  44. Stepanovic, S., Vukovic, D., Jesic, M. & Ranin, L. ( 2004; ). Influence of acetylsalicylic acid (aspirin) on biofilm production by Candida species. J Chemother 16, 134–138.[CrossRef]
    [Google Scholar]
  45. Tavanti, A., Davidson, A. D., Gow, N. A. R., Maiden, M. C. J. & Odds, F. C. ( 2005; ). Candida orthopsilosis and Candida metapsilosis spp. nov. to replace Candida parapsilosis groups II and III. J Clin Microbiol 43, 284–292.[CrossRef]
    [Google Scholar]
  46. Vargas, K., Wertz, P. W., Drake, D., Morrow, B. & Soll, D. R. ( 1994; ). Differences in adhesion of Candida albicans 3153A cells exhibiting switch phenotypes to buccal epithelium and stratum corneum. Infect Immun 62, 1328–1335.
    [Google Scholar]
  47. Weems, J. J., Jr ( 1992; ). Candida parapsilosis: epidemiology, pathogenicity, clinical manifestations, and antimicrobial susceptibility. Clin Infect Dis 14, 756–766.[CrossRef]
    [Google Scholar]
  48. Yildiz, F. H., Dolganov, N. A. & Schoolnik, G. K. ( 2001; ). VpsR, a member of the response regulators of the two-component regulatory systems, is required for expression of vps biosynthesis genes and EPSETr-associated phenotypes in Vibrio cholerae O1 El Tor. J Bacteriol 183, 1716–1726.[CrossRef]
    [Google Scholar]
  49. Zhao, X., Oh, S.-H., Cheng, G., Green, C. B., Nuessen, J. A., Yeater, K., Leng, R. P., Brown, A. J. P. & Hoyer, L. L. ( 2004; ). ALS3 and ALS8 represent a single locus that encodes a Candida albicans adhesin; functional comparisons between Als3p and Als1p. Microbiology 150, 2415–2428.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.27739-0
Loading
/content/journal/micro/10.1099/mic.0.27739-0
Loading

Data & Media loading...

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