1887

Abstract

causes infections in a wide variety of hosts and is the leading cause of mortality in cystic fibrosis (CF) patients. Although most clinical isolates of share common virulence determinants, it is known that strains evolve and change phenotypically during CF lung infections. These changes can include alterations in the levels of -acyl homoserine lactones (HSLs), which are secreted signal molecules. In the CF lung, fungi, especially and , may coexist with but the implications for disease are not known. Recent studies have established that signalling can occur between and , with the bacterial molecule 3-oxo-C12HSL affecting morphology, and the fungal metabolite farnesol reducing levels of the quinolone signal and pyocyanin in . Whether these interactions are common and typical in clinical strains of was addressed using CF isolates that produced varied levels of HSLs. It was found that, whereas some clinical strains affected morphology, others did not. This correlated closely with the amounts of 3-oxo-C12HSL produced by the isolates. Furthermore, it was established that signalling is bidirectional and that the molecule farnesol inhibits swarming motility in CF strains. This work demonstrates that clinical isolates of these opportunistic pathogens can interact in strain-specific ways via secreted signals and illustrates the importance of studying these interactions to fully understand the microbial contribution to disease in polymicrobial infections.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.47705-0
2008-05-01
2019-10-22
Loading full text...

Full text loading...

/deliver/fulltext/jmm/57/5/563.html?itemId=/content/journal/jmm/10.1099/jmm.0.47705-0&mimeType=html&fmt=ahah

References

  1. Adams, C., Morris-Quinn, M., McConnell, F., West, J., Lucey, B., Shortt, C., Cryan, B., Watson, J. B. & O'Gara, F. ( 1998; ). Epidemiology and clinical impact of Pseudomonas aeruginosa infection in cystic fibrosis using AP-PCR fingerprinting. J Infect 37, 151–158.[CrossRef]
    [Google Scholar]
  2. Bakare, N., Rickerts, V., Bargon, J. & Just-Nubling, G. ( 2003; ). Prevalence of Aspergillus fumigatus and other fungal species in the sputum of adult patients with cystic fibrosis. Mycoses 46, 19–23.[CrossRef]
    [Google Scholar]
  3. Bauernfeind, A., Bertele, R. M., Harms, K., Horl, G., Jungwirth, R., Petermuller, C., Przyklenk, B. & Weisslein-Pfister, C. ( 1987; ). Qualitative and quantitative microbiological analysis of sputa of 102 patients with cystic fibrosis. Infection 15, 270–277.[CrossRef]
    [Google Scholar]
  4. Baysse, C., Cullinane, M., Denervaud, V., Burrowes, E., Dow, J. M., Morrissey, J. P., Tam, L., Trevors, J. T. & O'Gara, F. ( 2005; ). Modulation of quorum sensing in Pseudomonas aeruginosa through alteration of membrane properties. Microbiology 151, 2529–2542.[CrossRef]
    [Google Scholar]
  5. Beatson, S. A., Whitchurch, C. B., Semmler, A. B. & Mattick, J. S. ( 2002; ). Quorum sensing is not required for twitching motility in Pseudomonas aeruginosa. J Bacteriol 184, 3598–3604.[CrossRef]
    [Google Scholar]
  6. Biswas, S., Van Dijck, P. & Datta, A. ( 2007; ). Environmental sensing and signal transduction pathways regulating morphopathogenic determinants of Candida albicans. Microbiol Mol Biol Rev 71, 348–376.[CrossRef]
    [Google Scholar]
  7. Burns, J. L., Van Dalfsen, J. M., Shawar, R. M., Otto, K. L., Garber, R. L., Quan, J. M., Montgomery, A. B., Albers, G. M., Ramsey, B. W. & Smith, A. L. ( 1999; ). Effect of chronic intermittent administration of inhaled tobramycin on respiratory microbial flora in patients with cystic fibrosis. J Infect Dis 179, 1190–1196.[CrossRef]
    [Google Scholar]
  8. Burrowes, E., Baysse, C., Adams, C. & O'Gara, F. ( 2006; ). Influence of the regulatory protein RsmA on cellular functions in Pseudomonas aeruginosa PAO1, as revealed by transcriptome analysis. Microbiology 152, 405–418.[CrossRef]
    [Google Scholar]
  9. Calderone, R. A. & Fonzi, W. A. ( 2001; ). Virulence factors of Candida albicans. Trends Microbiol 9, 327–335.[CrossRef]
    [Google Scholar]
  10. Calfee, M. W., Shelton, J. G., McCubrey, J. A. & Pesci, E. C. ( 2005; ). Solubility and bioactivity of the Pseudomonas quinolone signal are increased by a Pseudomonas aeruginosa-produced surfactant. Infect Immun 73, 878–882.[CrossRef]
    [Google Scholar]
  11. Cugini, C., Calfee, M. W., Farrow, J. M., III, Morales, D. K., Pesci, E. C. & Hogan, D. A. ( 2007; ). Farnesol, a common sesquiterpene, inhibits PQS production in Pseudomonas aeruginosa. Mol Microbiol 65, 896–906.[CrossRef]
    [Google Scholar]
  12. Diggle, S. P., Winzer, K., Chhabra, S. R., Worrall, K. E., Camara, M. & Williams, P. ( 2003; ). The Pseudomonas aeruginosa quinolone signal molecule overcomes the cell density-dependency of the quorum sensing hierarchy, regulates rhl-dependent genes at the onset of stationary phase and can be produced in the absence of LasR. Mol Microbiol 50, 29–43.[CrossRef]
    [Google Scholar]
  13. Diggle, S. P., Cornelis, P., Williams, P. & Camara, M. ( 2006; ). 4-Quinolone signalling in Pseudomonas aeruginosa: old molecules, new perspectives. Int J Med Microbiol 296, 83–91.[CrossRef]
    [Google Scholar]
  14. Diggle, S. P., Matthijs, S., Wright, V. J., Fletcher, M. P., Chhabra, S. R., Lamont, I. L., Kong, X., Hider, R. C., Cornelis, P. & other authors ( 2007; ). The Pseudomonas aeruginosa 4-quinolone signal molecules HHQ and PQS play multifunctional roles in quorum sensing and iron entrapment. Chem Biol 14, 87–96.[CrossRef]
    [Google Scholar]
  15. Drenkard, E. & Ausubel, F. M. ( 2002; ). Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416, 740–743.[CrossRef]
    [Google Scholar]
  16. Enjalbert, B. & Whiteway, M. ( 2005; ). Release from quorum-sensing molecules triggers hyphal formation during Candida albicans resumption of growth. Eukaryot Cell 4, 1203–1210.[CrossRef]
    [Google Scholar]
  17. Finnan, S., Morrissey, J. P., O'Gara, F. & Boyd, E. F. ( 2004; ). Genome diversity of Pseudomonas aeruginosa isolates from cystic fibrosis patients and the hospital environment. J Clin Microbiol 42, 5783–5792.[CrossRef]
    [Google Scholar]
  18. Giamarellou, H. ( 2000; ). Therapeutic guidelines for Pseudomonas aeruginosa infections. Int J Antimicrob Agents 16, 103–106.[CrossRef]
    [Google Scholar]
  19. Gillum, A. M., Tsay, E. Y. & Kirsch, D. R. ( 1984; ). Isolation of the Candida albicans gene for orotidine-5′-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations. Mol Gen Genet 198, 179–182.[CrossRef]
    [Google Scholar]
  20. Govan, J. R. & Deretic, V. ( 1996; ). Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol Rev 60, 539–574.
    [Google Scholar]
  21. Gow, N. A. ( 1997; ). Germ tube growth of Candida albicans. Curr Top Med Mycol 8, 43–55.
    [Google Scholar]
  22. Gow, N. A., Brown, A. J. & Odds, F. C. ( 2002; ). Fungal morphogenesis and host invasion. Curr Opin Microbiol 5, 366–371.[CrossRef]
    [Google Scholar]
  23. Gupta, N., Haque, A., Mukhopadhyay, G., Narayan, R. P. & Prasad, R. ( 2005; ). Interactions between bacteria and Candida in the burn wound. Burns 31, 375–378.[CrossRef]
    [Google Scholar]
  24. Heurlier, K., Denervaud, V. & Haas, D. ( 2006; ). Impact of quorum sensing on fitness of Pseudomonas aeruginosa. Int J Med Microbiol 296, 93–102.[CrossRef]
    [Google Scholar]
  25. Hogan, D. A. ( 2006a; ). Quorum sensing: alcohols in a social situation. Curr Biol 16, R457–R458.[CrossRef]
    [Google Scholar]
  26. Hogan, D. A. ( 2006b; ). Talking to themselves: autoregulation and quorum sensing in fungi. Eukaryot Cell 5, 613–619.[CrossRef]
    [Google Scholar]
  27. Hogan, D. A. & Kolter, R. ( 2002; ). Pseudomonas-Candida interactions: an ecological role for virulence factors. Science 296, 2229–2232.[CrossRef]
    [Google Scholar]
  28. Hogan, D. A., Vik, A. & Kolter, R. ( 2004; ). A Pseudomonas aeruginosa quorum-sensing molecule influences Candida albicans morphology. Mol Microbiol 54, 1212–1223.[CrossRef]
    [Google Scholar]
  29. Holloway, B. W. & Morgan, A. F. ( 1986; ). Genome organization in Pseudomonas. Annu Rev Microbiol 40, 79–105.[CrossRef]
    [Google Scholar]
  30. 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]
  31. Hube, B. ( 2006; ). Infection-associated genes of Candida albicans. Future Microbiol 1, 209–218.[CrossRef]
    [Google Scholar]
  32. Hughes, W. T. & Kim, H. K. ( 1973; ). Mycoflora in cystic fibrosis: some ecologic aspects of Pseudomonas aeruginosa and Candida albicans. Mycopathol Mycol Appl 50, 261–269.[CrossRef]
    [Google Scholar]
  33. Kaleli, I., Cevahir, N., Demir, M., Yildirim, U. & Sahin, R. ( 2007; ). Anticandidal activity of Pseudomonas aeruginosa strains isolated from clinical specimens. Mycoses 50, 74–78.[CrossRef]
    [Google Scholar]
  34. Kerr, J. ( 1994a; ). Inhibition of fungal growth by Pseudomonas aeruginosa and Pseudomonas cepacia isolated from patients with cystic fibrosis. J Infect 28, 305–310.[CrossRef]
    [Google Scholar]
  35. Kerr, J. R. ( 1994b; ). Suppression of fungal growth exhibited by Pseudomonas aeruginosa. J Clin Microbiol 32, 525–527.
    [Google Scholar]
  36. Liu, H. ( 2001; ). Transcriptional control of dimorphism in Candida albicans. Curr Opin Microbiol 4, 728–735.[CrossRef]
    [Google Scholar]
  37. Liu, H. ( 2002; ). Co-regulation of pathogenesis with dimorphism and phenotypic switching in Candida albicans, a commensal and a pathogen. Int J Med Microbiol 292, 299–311.[CrossRef]
    [Google Scholar]
  38. Martin, C., Ichou, M. A., Massicot, P., Goudeau, A. & Quentin, R. ( 1995; ). Genetic diversity of Pseudomonas aeruginosa strains isolated from patients with cystic fibrosis revealed by restriction fragment length polymorphism of the rRNA gene region. J Clin Microbiol 33, 1461–1466.
    [Google Scholar]
  39. McGrath, S., Wade, D. S. & Pesci, E. C. ( 2004; ). Dueling quorum sensing systems in Pseudomonas aeruginosa control the production of the Pseudomonas quinolone signal (PQS). FEMS Microbiol Lett 230, 27–34.[CrossRef]
    [Google Scholar]
  40. Mitchell, A. P. ( 1998; ). Dimorphism and virulence in Candida albicans. Curr Opin Microbiol 1, 687–692.[CrossRef]
    [Google Scholar]
  41. Naglik, J., Albrecht, A., Bader, O. & Hube, B. ( 2004; ). Candida albicans proteinases and host/pathogen interactions. Cell Microbiol 6, 915–926.[CrossRef]
    [Google Scholar]
  42. Navarathna, D. H., Hornby, J. M., Krishnan, N., Parkhurst, A., Duhamel, G. E. & Nickerson, K. W. ( 2007a; ). Effect of farnesol on a mouse model of systemic candidiasis, determined by use of a DPP3 knockout mutant of Candida albicans. Infect Immun 75, 1609–1618.[CrossRef]
    [Google Scholar]
  43. Navarathna, D. H., Nickerson, K. W., Duhamel, G. E., Jerrels, T. R. & Petro, T. M. ( 2007b; ). Exogenous farnesol interferes with the normal progression of cytokine expression during candidiasis in a mouse model. Infect Immun 75, 4006–4011.[CrossRef]
    [Google Scholar]
  44. Nguyen, D. & Singh, P. K. ( 2006; ). Evolving stealth: genetic adaptation of Pseudomonas aeruginosa during cystic fibrosis infections. Proc Natl Acad Sci U S A 103, 8305–8306.[CrossRef]
    [Google Scholar]
  45. Nickerson, K. W., Atkin, A. L. & Hornby, J. M. ( 2006; ). Quorum sensing in dimorphic fungi: farnesol and beyond. Appl Environ Microbiol 72, 3805–3813.[CrossRef]
    [Google Scholar]
  46. Oliver, A., Canton, R., Campo, P., Baquero, F. & Blazquez, J. ( 2000; ). High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288, 1251–1254.[CrossRef]
    [Google Scholar]
  47. Pfaller, M. A. & Diekema, D. J. ( 2007; ). Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev 20, 133–163.[CrossRef]
    [Google Scholar]
  48. Rahme, L. G., Stevens, E. J., Wolfort, S. F., Shao, J., Tompkins, R. G. & Ausubel, F. M. ( 1995; ). Common virulence factors for bacterial pathogenicity in plants and animals. Science 268, 1899–1902.[CrossRef]
    [Google Scholar]
  49. Rahme, L. G., Ausubel, F. M., Cao, H., Drenkard, E., Goumnerov, B. C., Lau, G. W., Mahajan-Miklos, S., Plotnikova, J., Tan, M. W. & other authors ( 2000; ). Plants and animals share functionally common bacterial virulence factors. Proc Natl Acad Sci U S A 97, 8815–8821.[CrossRef]
    [Google Scholar]
  50. Ravn, L., Christensen, A. B., Molin, S., Givskov, M. & Gram, L. ( 2001; ). Methods for detecting acylated homoserine lactones produced by Gram-negative bacteria and their application in studies of AHL-production kinetics. J Microbiol Methods 44, 239–251.[CrossRef]
    [Google Scholar]
  51. 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]
  52. Schuster, M. & Greenberg, E. P. ( 2006; ). A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Int J Med Microbiol 296, 73–81.[CrossRef]
    [Google Scholar]
  53. Shaw, P. D., Ping, G., Daly, S. L., Cha, C., Cronan, J. E., Jr, Rinehart, K. L. & Farrand, S. K. ( 1997; ). Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography. Proc Natl Acad Sci U S A 94, 6036–6041.[CrossRef]
    [Google Scholar]
  54. Shiner, E. K., Rumbaugh, K. P. & Williams, S. C. ( 2005; ). Inter-kingdom signaling: deciphering the language of acyl homoserine lactones. FEMS Microbiol Rev 29, 935–947.[CrossRef]
    [Google Scholar]
  55. Smith, R. S. & Iglewski, B. H. ( 2003; ). P. aeruginosa quorum-sensing systems and virulence. Curr Opin Microbiol 6, 56–60.[CrossRef]
    [Google Scholar]
  56. Smith, J. J., Travis, S. M., Greenberg, E. P. & Welsh, M. J. ( 1996; ). Cystic fibrosis airway epithelia fail to kill bacteria because of abnormal airway surface fluid. Cell 85, 229–236.[CrossRef]
    [Google Scholar]
  57. Smith, E. E., Buckley, D. G., Wu, Z., Saenphimmachak, C., Hoffman, L. R., D'Argenio, D. A., Miller, S. I., Ramsey, B. W., Speert, D. P. & other authors ( 2006; ). Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci U S A 103, 8487–8492.[CrossRef]
    [Google Scholar]
  58. Tan, M. W. & Ausubel, F. M. ( 2000; ). Caenorhabditis elegans: a model genetic host to study Pseudomonas aeruginosa pathogenesis. Curr Opin Microbiol 3, 29–34.[CrossRef]
    [Google Scholar]
  59. Wade, D. S., Calfee, M. W., Rocha, E. R., Ling, E. A., Engstrom, E., Coleman, J. P. & Pesci, E. C. ( 2005; ). Regulation of Pseudomonas quinolone signal synthesis in Pseudomonas aeruginosa. J Bacteriol 187, 4372–4380.[CrossRef]
    [Google Scholar]
  60. Whitchurch, C. B., Beatson, S. A., Comolli, J. C., Jakobsen, T., Sargent, J. L., Bertrand, J. J., West, J., Klausen, M., Waite, L. L. & other authors ( 2005; ). Pseudomonas aeruginosa fimL regulates multiple virulence functions by intersecting with Vfr-modulated pathways. Mol Microbiol 55, 1357–1378.[CrossRef]
    [Google Scholar]
  61. Whiteway, M. ( 2000; ). Transcriptional control of cell type and morphogenesis in Candida albicans. Curr Opin Microbiol 3, 582–588.[CrossRef]
    [Google Scholar]
  62. Whiteway, M. & Oberholzer, U. ( 2004; ). Candida morphogenesis and host-pathogen interactions. Curr Opin Microbiol 7, 350–357.[CrossRef]
    [Google Scholar]
  63. Williams, P. ( 2002; ). Quorum sensing: an emerging target for antibacterial chemotherapy? Expert Opin Ther Targets 6, 257–274.[CrossRef]
    [Google Scholar]
  64. Wolfgang, M. C., Kulasekara, B. R., Liang, X., Boyd, D., Wu, K., Yang, Q., Miyada, C. G. & Lory, S. ( 2003; ). Conservation of genome content and virulence determinants among clinical and environmental isolates of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 100, 8484–8489.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.47705-0
Loading
/content/journal/jmm/10.1099/jmm.0.47705-0
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