1887

Abstract

Multiple bacterial species often coexist as communities, and compete for environmental resources. Here, we describe how an opportunistic pathogen, , uses extracellular products to interact with the nosocomial pathogen . biofilms and planktonic cultures were challenged with supernatant cultures overnight. Results indicated that quorum-sensing-controlled factors from supernatant inhibited growth in planktonic cultures. We also found that extracellular products, mainly polysaccharides, disrupted established biofilms. Cellulase-treated supernatant, and supernatant from , and mutants, which are deficient in polysaccharide biosynthesis, diminished the disruption of biofilms. In contrast, supernatant in overnight cultures had no effect on established biofilms and planktonic growth. These findings reveal that extracellular products are important microbial competition factors that overcome competition with , and the results may provide clues for the development of a novel strategy for controlling biofilms.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.028001-0
2009-07-01
2019-10-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/7/2148.html?itemId=/content/journal/micro/10.1099/mic.0.028001-0&mimeType=html&fmt=ahah

References

  1. Allesen-Holm, M., Barken, K. B., Yang, L., Klausen, M., Webb, J. S., Kjelleberg, S., Molin, S., Givskov, M. & Tolker-Nielsen, T. ( 2006; ). A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol Microbiol 59, 1114–1128.[CrossRef]
    [Google Scholar]
  2. Burgess, J. G., Jordan, E. M., Bregu, M., Mearns-Spragg, A. & Boyd, K. G. ( 1999; ). Microbial antagonism: a neglected avenue of natural products research. J Biotechnol 70, 27–32.[CrossRef]
    [Google Scholar]
  3. Christensen, G. D., Simpson, W. A., Younger, J. J., Baddour, L. M., Barrett, F. F., Melton, D. M. & Beachey, E. H. ( 1985; ). Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices. J Clin Microbiol 22, 996–1006.
    [Google Scholar]
  4. Costerton, J. W., Lewandowski, Z., Caldwell, D. E., Korber, D. R. & Lappin-Scott, H. M. ( 1995; ). Microbial biofilms. Annu Rev Microbiol 49, 711–745.[CrossRef]
    [Google Scholar]
  5. D'Argenio, D. A., Calfee, M. W., Rainey, P. B. & Pesci, E. C. ( 2002; ). Autolysis and autoaggregation in Pseudomonas aeruginosa colony morphology mutants. J Bacteriol 184, 6481–6489.[CrossRef]
    [Google Scholar]
  6. Davies, D. G. & Marques, C. N. ( 2009; ). A fatty acid messenger is responsible for inducing dispersion in microbial biofilms. J Bacteriol 191, 1393–1403.[CrossRef]
    [Google Scholar]
  7. Deziel, E., Lepine, F., Milot, S., He, J., Mindrinos, M. N., Tompkins, R. G. & Rahme, L. G. ( 2004; ). Analysis of Pseudomonas aeruginosa 4-hydroxy-2-alkylquinolines (HAQs) reveals a role for 4-hydroxy-2-heptylquinoline in cell-to-cell communication. Proc Natl Acad Sci U S A 101, 1339–1344.[CrossRef]
    [Google Scholar]
  8. 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]
  9. Donlan, R. M. ( 2001; ). Biofilms and device-associated infections. Emerg Infect Dis 7, 277–281.[CrossRef]
    [Google Scholar]
  10. Friedman, L. & Kolter, R. ( 2004a; ). Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix. J Bacteriol 186, 4457–4465.[CrossRef]
    [Google Scholar]
  11. Friedman, L. & Kolter, R. ( 2004b; ). Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol Microbiol 51, 675–690.
    [Google Scholar]
  12. Gilsdorf, J. R., Wilson, K. & Beals, T. F. ( 1989; ). Bacterial colonization of intravenous catheter materials in vitro and in vivo. Surgery 106, 37–44.
    [Google Scholar]
  13. Govan, J. R. & Deretic, V. ( 1996; ). Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol Rev 60, 539–574.
    [Google Scholar]
  14. 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]
  15. 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]
  16. Henriques, M., Sousa, C., Lira, M., Elisabete, M., Oliveira, R., Oliveira, R. & Azeredo, J. ( 2005; ). Adhesion of Pseudomonas aeruginosa and Staphylococcus epidermidis to silicone-hydrogel contact lenses. Optom Vis Sci 82, 446–450.[CrossRef]
    [Google Scholar]
  17. Hentzer, M., Wu, H., Andersen, J. B. & other authors ( 2003; ). Attenuation of Pseudomonas aeruginosa virulence by quorum-sensing inhibitors. EMBO J 22, 3803–3815.[CrossRef]
    [Google Scholar]
  18. Herrero, M., de Lorenzo, V. & Timmis, K. N. ( 1990; ). Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in Gram-negative bacteria. J Bacteriol 172, 6557–6567.
    [Google Scholar]
  19. Hoang, T. T., Karkhoff-Schweizer, R. R., Kutchma, A. J. & Schweizer, H. P. ( 1998; ). A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212, 77–86.[CrossRef]
    [Google Scholar]
  20. Irie, Y., O'Toole, G. A. & Yuk, M. H. ( 2005; ). Pseudomonas aeruginosa rhamnolipids disperse Bordetella bronchiseptica biofilms. FEMS Microbiol Lett 250, 237–243.[CrossRef]
    [Google Scholar]
  21. Jackson, K. D., Starkey, M., Kremer, S., Parsek, M. R. & Wozniak, D. J. ( 2004; ). Identification of psl, a locus encoding a potential exopolysaccharide that is essential for Pseudomonas aeruginosa PAO1 biofilm formation. J Bacteriol 186, 4466–4475.[CrossRef]
    [Google Scholar]
  22. Jacobs, M. A., Alwood, A., Thaipisuttikul, I. & other authors ( 2003; ). Comprehensive transposon mutant library of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 100, 14339–14344.[CrossRef]
    [Google Scholar]
  23. Kessler, E., Safrin, M., Olson, J. C. & Ohman, D. E. ( 1993; ). Secreted LasA of Pseudomonas aeruginosa is a staphylolytic protease. J Biol Chem 268, 7503–7508.
    [Google Scholar]
  24. Latifi, A., Winson, M. K., Foglino, M., Bycroft, B. W., Stewart, G. S., Lazdunski, A. & Williams, P. ( 1995; ). Multiple homologues of LuxR and LuxI control expression of virulence determinants and secondary metabolites through quorum-sensing in Pseudomonas aeruginosa PAO1. Mol Microbiol 17, 333–343.[CrossRef]
    [Google Scholar]
  25. Lepine, F., Milot, S., Deziel, E., He, J. & Rahme, L. G. ( 2004; ). Electrospray/mass spectrometric identification and analysis of 4-hydroxy-2-alkylquinolines (HAQs) produced by Pseudomonas aeruginosa. J Am Soc Mass Spectrom 15, 862–869.[CrossRef]
    [Google Scholar]
  26. Li, M., Guan, M., Jiang, X. F., Yuan, F. Y., Xu, M., Zhang, W. Z. & Lu, Y. ( 2004; ). Genetic polymorphism of the accessory gene regulator (agr) locus in Staphylococcus epidermidis and its association with pathogenicity. J Med Microbiol 53, 545–549.[CrossRef]
    [Google Scholar]
  27. Machan, Z. A., Taylor, G. W., Pitt, T. L., Cole, P. J. & Wilson, R. ( 1992; ). 2-Heptyl-4-hydroxyquinoline N-oxide, an antistaphylococcal agent produced by Pseudomonas aeruginosa. J Antimicrob Chemother 30, 615–623.[CrossRef]
    [Google Scholar]
  28. Mashburn, L. M. & Whiteley, M. ( 2005; ). Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 437, 422–425.[CrossRef]
    [Google Scholar]
  29. McKnight, S. L., Iglewski, B. H. & Pesci, E. C. ( 2000; ). The Pseudomonas quinolone signal regulates rhl quorum-sensing in Pseudomonas aeruginosa. J Bacteriol 182, 2702–2708.[CrossRef]
    [Google Scholar]
  30. Nouwens, A. S., Beatson, S. A., Whitchurch, C. B., Walsh, B. J., Schweizer, H. P., Mattick, J. S. & Cordwell, S. J. ( 2003; ). Proteome analysis of extracellular proteins regulated by the las and rhl quorum-sensing systems in Pseudomonas aeruginosa PAO1. Microbiology 149, 1311–1322.[CrossRef]
    [Google Scholar]
  31. Pamp, S. J. & Tolker-Nielsen, T. ( 2007; ). Multiple roles of biosurfactants in structural biofilm development by Pseudomonas aeruginosa. J Bacteriol 189, 2531–2539.[CrossRef]
    [Google Scholar]
  32. Passador, L., Cook, J. M., Gambello, M. J., Rust, L. & Iglewski, B. H. ( 1993; ). Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication. Science 260, 1127–1130.[CrossRef]
    [Google Scholar]
  33. Pesci, E. C., Pearson, J. P., Seed, P. C. & Iglewski, B. H. ( 1997; ). Regulation of las and rhl quorum-sensing in Pseudomonas aeruginosa. J Bacteriol 179, 3127–3132.
    [Google Scholar]
  34. Qin, Z., Yang, X., Yang, L., Jiang, J., Ou, Y., Molin, S. & Qu, D. ( 2007; ). Formation and properties of in vitro biofilms of ica-negative Staphylococcus epidermidis clinical isolates. J Med Microbiol 56, 83–93.[CrossRef]
    [Google Scholar]
  35. Rasmussen, T. B. & Givskov, M. ( 2006; ). Quorum-sensing inhibitors as anti-pathogenic drugs. Int J Med Microbiol 296, 149–161.
    [Google Scholar]
  36. Rupp, M. E. & Archer, G. L. ( 1994; ). Coagulase-negative staphylococci: pathogens associated with medical progress. Clin Infect Dis 19, 231–243.[CrossRef]
    [Google Scholar]
  37. Schooling, S. R. & Beveridge, T. J. ( 2006; ). Membrane vesicles: an overlooked component of the matrices of biofilms. J Bacteriol 188, 5945–5957.[CrossRef]
    [Google Scholar]
  38. Shrout, J. D., Chopp, D. L., Just, C. L., Hentzer, M., Givskov, M. & Parsek, M. R. ( 2006; ). The impact of quorum-sensing and swarming motility on Pseudomonas aeruginosa biofilm formation is nutritionally conditional. Mol Microbiol 62, 1264–1277.[CrossRef]
    [Google Scholar]
  39. Smith, V. H. ( 2002; ). Effects of resource supplies on the structure and function of microbial communities. Antonie Van Leeuwenhoek 81, 99–106.[CrossRef]
    [Google Scholar]
  40. Valle, J., Da Re, S., Henry, N., Fontaine, T., Balestrino, D., Latour-Lambert, P. & Ghigo, J. M. ( 2006; ). Broad-spectrum biofilm inhibition by a secreted bacterial polysaccharide. Proc Natl Acad Sci U S A 103, 12558–12563.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.028001-0
Loading
/content/journal/micro/10.1099/mic.0.028001-0
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