1887

Abstract

has long been known to produce phenotypic variants during chronic mucosal surface infections. These variants are thought to be generated to ensure bacterial survival against the diverse challenges in the mucosal environment. Studies have begun to elucidate the mechanisms by which these variants emerge ; however, too little information exists on phenotypic variation to draw any links between variants generated and . Consequently, in this study, the gene, which has previously been linked to the generation of small colony variants (SCVs) , was studied in an mucosal surface infection model. More specifically, the rat prostate served as a model mucosal surface to test for the appearance of SCVs following infections with strains. As in studies, deletion of the gene led to SCV production . The appearance of these SCVs was important for the sustainability of a chronic infection. In the subset of rats in which did not convert to SCVs, clearance of the bacteria took place and healing of the tissue ensued. When comparing the SCVs that arose at the mucosal surface (MS-SCVs) with SCVs (IV-SCVs) from the same parent, some differences between the phenotypic variants were observed. Whereas both MS-SCVs and IV-SCVs formed dense biofilms, MS-SCVs exhibited a less diverse resistance profile to antimicrobial agents than IV-SCVs. Additionally, MS-SCVs were better suited to initiate an infection in the rat model than IV-SCVs. Together, these observations suggest that phenotypic variation can be important for maintenance of infection, and that variants may differ from variants generated from the same genetic parent.

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2010-12-01
2020-11-27
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References

  1. Boles B. R., Singh P. K. 2008; Endogenous oxidative stress produces diversity and adaptability in biofilm communities. Proc Natl Acad Sci U S A 105:12503–12508
    [Google Scholar]
  2. Boles B. R., Thoendel M., Singh P. K. 2004; Self-generated diversity produces “insurance effects” in biofilm communities. Proc Natl Acad Sci U S A 101:16630–16635
    [Google Scholar]
  3. Ceri H., Olson M. E., Nickel J. C. 1999a; Prostatitis: role of the animal model. In Textbook of Prostatitis pp 109–114 Edited by Nickel J. C. Oxford: Isis Medical Media;
    [Google Scholar]
  4. Ceri H., Olson M. E., Stremick C., Read R. R., Morck D., Buret A. 1999b; The Calgary Biofilm Device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J Clin Microbiol 37:1771–1776
    [Google Scholar]
  5. Ceri H., Schmidt S., Olson M. E., Nickel J. C., Benediktsson H. 1999c; Specific mucosal immunity in the pathophysiology of bacterial prostatitis in a rat model. Can J Microbiol 45:849–855
    [Google Scholar]
  6. Chieda Y., Iiyama K., Yasunaga-Aoki C., Lee J. M., Kusakabe T., Shimizu S. 2005; Pathogenicity of gacA mutant of Pseudomonas aeruginosa PA01 in the silkworm, Bombyx mori . FEMS Microbiol Lett 244:181–186
    [Google Scholar]
  7. Coleman F. T., Mueschenborn S., Meluleni G., Ray C., Carey V. J., Vargas S. O., Cannon C. L., Ausubel F. M., Pier G. B. 2003; Hypersusceptibility of cystic fibrosis mice to chronic Pseudomonas aeruginosa oropharyngeal colonization and lung infection. Proc Natl Acad Sci U S A 100:1949–1954
    [Google Scholar]
  8. Costerton J. W., Stewart P. S., Greenberg E. P. 1999; Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322
    [Google Scholar]
  9. D'Argenio D. A., Gallagher L. A., Berg C. A., Manoil C. 2001; Drosophila as a model host for Pseudomonas aeruginosa infection. J Bacteriol 183:1466–1471
    [Google Scholar]
  10. Davies J. A., Harrison J. J., Marques L. L., Foglia G. R., Stremick C. A., Storey D. G., Turner R. J., Olson M. E., Ceri H. 2007; The GacS sensor kinase controls phenotypic reversion of small colony variants isolated from biofilms of Pseudomonas aeruginosa PA14. FEMS Microbiol Ecol 59:32–46
    [Google Scholar]
  11. 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
    [Google Scholar]
  12. Drenkard E., Ausubel F. M. 2002; Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416:740–743
    [Google Scholar]
  13. Foglia G. R., Marques L. L. R., Harrison J. J., Turner R. J., Olson M. E., Ceri H. 2005; GacS as a phase dependent on/off switch for stress tolerance in pseudomonads?. Phytopathology 95:S30
    [Google Scholar]
  14. Govan J. R., Deretic V. 1996; Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia . Microbiol Rev 60:539–574
    [Google Scholar]
  15. Harrison J. J., Ceri H., Stremick C. A., Turner R. J. 2004; Biofilm susceptibility to metal toxicity. Environ Microbiol 6:1220–1227
    [Google Scholar]
  16. Harrison J. J., Ceri H., Yerly J., Stremick C. A., Hu Y., Martinuzzi R., Turner R. J. 2006; The use of microscopy and three-dimensional visualization to evaluate the structure of microbial biofilms cultivated in the Calgary Biofilm Device. Biol Proced Online 8:194–215
    [Google Scholar]
  17. Harrison J. J., Ceri H., Turner R. J. 2007; Multimetal resistance and tolerance in microbial biofilms. Nat Rev Microbiol 5:928–938
    [Google Scholar]
  18. Harrison J. J., Tremaroli V., Stan M. A., Chan C. S., Vacchi-Suzzi C., Heyne B. J., Parsek M. R., Ceri H., Turner R. J. 2009; Chromosomal antioxidant genes have metal ion-specific roles as determinants of bacterial metal tolerance. Environ Microbiol 11:2491–2509
    [Google Scholar]
  19. Harrison J. J., Stremick C. A., Turner R. J., Allan N. D., Olson M. E., Ceri H. 2010; Microtiter susceptibility testing of microbes growing on peg lids: a miniaturized biofilm model for high-throughput screening. Nat Protoc 5:1236–1254
    [Google Scholar]
  20. Häussler S., Tummler B., Weissbrodt H., Rohde M., Steinmetz I. 1999; Small-colony variants of Pseudomonas aeruginosa in cystic fibrosis. Clin Infect Dis 29:621–625
    [Google Scholar]
  21. Häussler 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
    [Google Scholar]
  22. Hickman J. W., Tifrea D. F., Harwood C. S. 2005; A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci U S A 102:14422–14427
    [Google Scholar]
  23. 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
    [Google Scholar]
  24. Mahajan-Miklos S., Tan M. W., Rahme L. G., Ausubel F. M. 1999; Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa Caenorhabditis elegans pathogenesis model. Cell 96:47–56
    [Google Scholar]
  25. Meissner A., Wild V., Simm R., Rohde M., Erck C., Bredenbruch F., Morr M., Romling U., Haussler S. 2007; Pseudomonas aeruginosa cupA -encoded fimbriae expression is regulated by a GGDEF and EAL domain-dependent modulation of the intracellular level of cyclic diguanylate. Environ Microbiol 9:2475–2485
    [Google Scholar]
  26. Mullane K. M., Kraemer R., Smith B. 1985; Myeloperoxidase activity as a quantitative assessment of neutrophil infiltration into ischemic myocardium. J Pharmacol Methods 14:157–167
    [Google Scholar]
  27. Nelson L. K., D'Amours G. H., Sproule-Willoughby K. M., Morck D. W., Ceri H. 2009; Pseudomonas aeruginosa las and rhl quorum-sensing systems are important for infection and inflammation in a rat prostatitis model. Microbiology 155:2612–2619
    [Google Scholar]
  28. Nickel J. C., Olson M. E., Barabas A., Benediktsson H., Dasgupta M. K., Costerton J. W. 1990; Pathogenesis of chronic bacterial prostatitis in an animal model. Br J Urol 66:47–54
    [Google Scholar]
  29. 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
    [Google Scholar]
  30. Parkins M. D., Ceri H., Storey D. G. 2001; Pseudomonas aeruginosa GacA, a factor in multihost virulence, is also essential for biofilm formation. Mol Microbiol 40:1215–1226
    [Google Scholar]
  31. Pedersen S. S., Hoiby N., Espersen F., Koch C. 1992; Role of alginate in infection with mucoid Pseudomonas aeruginosa in cystic fibrosis. Thorax 47:6–13
    [Google Scholar]
  32. Phan V., Belas R., Gilmore B. F., Ceri H. 2008; ZapA a virulence factor in a rat model of Proteus mirabilis induced acute and chronic prostatitis. Infect Immun 76:4859–4864
    [Google Scholar]
  33. Rahme L. G., Stevens E. J., Wolfort S. F., Shao J., Tompkins R. G., Ausubel F. M. 1995; Common virulence factors for bacterial pathogenecity in plants and animals. Science 268:1899–1902
    [Google Scholar]
  34. 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
    [Google Scholar]
  35. Rainey P. B., Travisano M. 1998; Adaptive radiation in a heterogeneous environment. Nature 394:69–72
    [Google Scholar]
  36. Rippere-Lampe K. E., Lang M., Ceri H., Olson M., Lockman H. A., O'Brien A. D. 2001; Cytotoxic necrotizing factor type 1-positive Escherichia coli causes increased inflammation and tissue damage to the prostate in a rat prostatitis model. Infect Immun 69:6515–6519
    [Google Scholar]
  37. Sánchez-Contreras M., Martin M., Villacieros M., O'Gara F., Bonilla I., Rivilla R. 2002; Phenotypic selection and phase variation occur during alfalfa root colonization by Pseudomonas fluorescens F113. J Bacteriol 184:1587–1596
    [Google Scholar]
  38. Schmidt-Eisenlohr H., Gast A., Baron C. 2003; Inactivation of gacS does not affect the competitiveness of Pseudomonas chlororaphis in the Arabidopsis thaliana rhizosphere. Appl Environ Microbiol 69:1817–1826
    [Google Scholar]
  39. Schneider M., Muhlemann K., Droz S., Couzinet S., Casaulta C., Zimmerli S. 2008; Clinical characteristics associated with isolation of small-colony variants of Staphylococcus aureus and Pseudomonas aeruginosa from respiratory secretions of patients with cystic fibrosis. J Clin Microbiol 46:1832–1834
    [Google Scholar]
  40. Singh P. K., Schaefer A. L., Parsek M. R., Moninger T. O., Welsh M. J., Greenberg E. P. 2000; Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407:762–764
    [Google Scholar]
  41. 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
    [Google Scholar]
  42. Tan M. W., Rahme L. G., Sternberg J. A., Tompkins R. G., Ausubel F. M. 1999; Pseudomonas aeruginosa killing of Caenorhabditis elegans used to identify P. aeruginosa virulence factors. Proc Natl Acad Sci U S A 96:2408–2413
    [Google Scholar]
  43. von Götz F., Häussler S., Jordan D., Saravanamuthu S. S., Wehmhöner D., Strüssmann A., Lauber J., Attree I., Buer J. other authors 2004; Expression analysis of a highly adherent and cytotoxic small colony variant of Pseudomonas aeruginosa isolated from a lung of a patient with cystic fibrosis. J Bacteriol 186:3837–3847
    [Google Scholar]
  44. Zierdt C. H., Schmidt P. J. 1964; Dissociation in Pseudomonas aeruginosa . J Bacteriol 87:1003–1010
    [Google Scholar]
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