1887

Abstract

Bacteria have evolved a set of regulatory pathways to adapt to the dynamic nutritional environment during the course of infection. However, the underlying mechanism of the regulatory effects by nutritional cues on bacterial pathogenesis is unclear. In the present study, we showed that the catabolite repression control protein regulates the quinolone signal quorum sensing, which further controls synthesis of virulence factor pyocyanin, biofilm formation and survival during infection models. Our study suggests that deregulation of the catabolite repression by might enhance its fitness during cystic fibrosis infections.

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2013-09-01
2020-06-01
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References

  1. Almengor A. C., Kinkel T. L., Day S. J., McIver K. S..( 2007;). The catabolite control protein CcpA binds to Pmga and influences expression of the virulence regulator Mga in the Group A streptococcus. J Bacteriol189:8405–8416 [CrossRef][PubMed]
    [Google Scholar]
  2. Banin E., Vasil M. L., Greenberg E. P..( 2005;). Iron and Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci U S A102:11076–11081 [CrossRef][PubMed]
    [Google Scholar]
  3. D’Argenio D. A., Calfee M. W., Rainey P. B., Pesci E. C..( 2002;). Autolysis and autoaggregation in Pseudomonas aeruginosa colony morphology mutants. J Bacteriol184:6481–6489 [CrossRef][PubMed]
    [Google Scholar]
  4. Das T., Kutty S. K., Kumar N., Manefield M..( 2013;). Pyocyanin facilitates extracellular DNA binding to Pseudomonas aeruginosa influencing cell surface properties and aggregation. PLoS ONE8:e58299 [CrossRef][PubMed]
    [Google Scholar]
  5. Diggle S. P., Lumjiaktase P., Dipilato F., Winzer K., Kunakorn M., Barrett D. A., Chhabra S. R., Cámara M., Williams P..( 2006;). Functional genetic analysis reveals a 2-alkyl-4-quinolone signalling system in the human pathogen Burkholderia pseudomallei and related bacteria. Chem Biol13:701–710 [CrossRef][PubMed]
    [Google Scholar]
  6. Essar D. W., Eberly L., Hadero A., Crawford I. P..( 1990;). Identification and characterization of genes for a second anthranilate synthase in Pseudomonas aeruginosa: interchangeability of the two anthranilate synthases and evolutionary implications. J Bacteriol172:884–900[PubMed]
    [Google Scholar]
  7. Fletcher M. P., Diggle S. P., Cámara M., Williams P..( 2007;). Biosensor-based assays for PQS, HHQ and related 2-alkyl-4-quinolone quorum sensing signal molecules. Nat Protoc2:1254–1262 [CrossRef][PubMed]
    [Google Scholar]
  8. Gallagher L. A., McKnight S. L., Kuznetsova M. S., Pesci E. C., Manoil C..( 2002;). Functions required for extracellular quinolone signaling by Pseudomonas aeruginosa. J Bacteriol184:6472–6480 [CrossRef][PubMed]
    [Google Scholar]
  9. Gilbreth S. E., Benson A. K., Hutkins R. W..( 2004;). Catabolite repression and virulence gene expression in Listeria monocytogenes. Curr Microbiol49:95–98 [CrossRef][PubMed]
    [Google Scholar]
  10. Görke B., Stülke J..( 2008;). Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat Rev Microbiol6:613–624 [CrossRef][PubMed]
    [Google Scholar]
  11. Hoffman L. R., Richardson A. R., Houston L. S., Kulasekara H. D., Martens-Habbena W., Klausen M., Burns J. L., Stahl D. A., Hassett D. J..& other authors ( 2010;). Nutrient availability as a mechanism for selection of antibiotic tolerant Pseudomonas aeruginosa within the CF airway. PLoS Pathog6:e1000712 [CrossRef][PubMed]
    [Google Scholar]
  12. Jensen P. O., Givskov M., Bjarnsholt T., Moser C..( 2010;). The immune system vs. Pseudomonas aeruginosa biofilms. FEMS Immunol Med Microbiol59:292–305[PubMed]
    [Google Scholar]
  13. Klausen M., Aaes-Jørgensen A., Molin S., Tolker-Nielsen T..( 2003;). Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms. Mol Microbiol50:61–68 [CrossRef][PubMed]
    [Google Scholar]
  14. Linares J. F., Moreno R., Fajardo A., Martínez-Solano L., Escalante R., Rojo F., Martínez J. L..( 2010;). The global regulator Crc modulates metabolism, susceptibility to antibiotics and virulence in Pseudomonas aeruginosa. Environ Microbiol12:3196–3212 [CrossRef][PubMed]
    [Google Scholar]
  15. Lyczak J. B., Cannon C. L., Pier G. B..( 2000;). Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect2:1051–1060 [CrossRef][PubMed]
    [Google Scholar]
  16. McAdam P. R., Holmes A., Templeton K. E., Fitzgerald J. R..( 2011;). Adaptive evolution of Staphylococcus aureus during chronic endobronchial infection of a cystic fibrosis patient. PLoS ONE6:e24301 [CrossRef][PubMed]
    [Google Scholar]
  17. Nudler E., Mironov A. S..( 2004;). The riboswitch control of bacterial metabolism. Trends Biochem Sci29:11–17 [CrossRef][PubMed]
    [Google Scholar]
  18. O’Toole G. A., Gibbs K. A., Hager P. W., Phibbs P. V. Jr, Kolter R..( 2000;). The global carbon metabolism regulator Crc is a component of a signal transduction pathway required for biofilm development by Pseudomonas aeruginosa. J Bacteriol182:425–431 [CrossRef][PubMed]
    [Google Scholar]
  19. Palmer K. L., Mashburn L. M., Singh P. K., Whiteley M..( 2005;). Cystic fibrosis sputum supports growth and cues key aspects of Pseudomonas aeruginosa physiology. J Bacteriol187:5267–5277 [CrossRef][PubMed]
    [Google Scholar]
  20. Palmer K. L., Aye L. M., Whiteley M..( 2007;). Nutritional cues control Pseudomonas aeruginosa multicellular behavior in cystic fibrosis sputum. J Bacteriol189:8079–8087 [CrossRef][PubMed]
    [Google Scholar]
  21. Pearson J. P., Pesci E. C., Iglewski B. H..( 1997;). Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. J Bacteriol179:5756–5767[PubMed]
    [Google Scholar]
  22. Pesci E. C., Milbank J. B., Pearson J. P., McKnight S., Kende A. S., Greenberg E. P., Iglewski B. H..( 1999;). Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A96:11229–11234 [CrossRef][PubMed]
    [Google Scholar]
  23. Rohmer L., Hocquet D., Miller S. I..( 2011;). Are pathogenic bacteria just looking for food? Metabolism and microbial pathogenesis. Trends Microbiol19:341–348 [CrossRef][PubMed]
    [Google Scholar]
  24. 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 Microbiol62:1264–1277 [CrossRef][PubMed]
    [Google Scholar]
  25. Silo-Suh L., Suh S. J., Phibbs P. V., Ohman D. E..( 2005;). Adaptations of Pseudomonas aeruginosa to the cystic fibrosis lung environment can include deregulation of zwf, encoding glucose-6-phosphate dehydrogenase. J Bacteriol187:7561–7568 [CrossRef][PubMed]
    [Google Scholar]
  26. Song Z., Wu H., Ciofu O., Kong K. F., Høiby N., Rygaard J., Kharazmi A., Mathee K..( 2003;). Pseudomonas aeruginosa alginate is refractory to Th1 immune response and impedes host immune clearance in a mouse model of acute lung infection. J Med Microbiol52:731–740 [CrossRef][PubMed]
    [Google Scholar]
  27. Sonnleitner E., Valentini M., Wenner N., Haichar F. Z., Haas D., Lapouge K..( 2012;). Novel targets of the CbrAB/Crc carbon catabolite control system revealed by transcript abundance in Pseudomonas aeruginosa. PLoS ONE7:e44637 [CrossRef][PubMed]
    [Google Scholar]
  28. Sternberg C., Tolker-Nielsen T..( 2006;). Growing and analyzing biofilms in flow cells. Curr Protoc Microbiol [CrossRef][PubMed]
    [Google Scholar]
  29. Stover C. K., Pham X. Q., Erwin A. L., Mizoguchi S. D., Warrener P., Hickey M. J., Brinkman F. S., Hufnagle W. O., Kowalik D. J..& other authors ( 2000;). Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature406:959–964 [CrossRef][PubMed]
    [Google Scholar]
  30. Wagner V. E., Bushnell D., Passador L., Brooks A. I., Iglewski B. H..( 2003;). Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment. J Bacteriol185:2080–2095 [CrossRef][PubMed]
    [Google Scholar]
  31. Wang J. D., Levin P. A..( 2009;). Metabolism, cell growth and the bacterial cell cycle. Nat Rev Microbiol7:822–827 [CrossRef][PubMed]
    [Google Scholar]
  32. Wolff J. A., MacGregor C. H., Eisenberg R. C., Phibbs P. V. Jr.( 1991;). Isolation and characterization of catabolite repression control mutants of Pseudomonas aeruginosa PAO. J Bacteriol173:4700–4706[PubMed]
    [Google Scholar]
  33. Yang L., Barken K. B., Skindersoe M. E., Christensen A. B., Givskov M., Tolker-Nielsen T..( 2007;). Effects of iron on DNA release and biofilm development by Pseudomonas aeruginosa. Microbiology153:1318–1328 [CrossRef][PubMed]
    [Google Scholar]
  34. Yang L., Nilsson M., Gjermansen M., Givskov M., Tolker-Nielsen T..( 2009;). Pyoverdine and PQS mediated subpopulation interactions involved in Pseudomonas aeruginosa biofilm formation. Mol Microbiol74:1380–1392 [CrossRef][PubMed]
    [Google Scholar]
  35. Yang L., Jelsbak L., Marvig R. L., Damkiær S., Workman C. T., Rau M. H., Hansen S. K., Folkesson A., Johansen H. K..& other authors ( 2011a;). Evolutionary dynamics of bacteria in a human host environment. Proc Natl Acad Sci U S A108:7481–7486 [CrossRef][PubMed]
    [Google Scholar]
  36. Yang L., Liu Y., Markussen T., Høiby N., Tolker-Nielsen T., Molin S..( 2011b;). Pattern differentiation in co-culture biofilms formed by Staphylococcus aureus and Pseudomonas aeruginosa. FEMS Immunol Med Microbiol62:339–347 [CrossRef][PubMed]
    [Google Scholar]
  37. Yang L., Rau M. H., Yang L., Høiby N., Molin S., Jelsbak L..( 2011c;). Bacterial adaptation during chronic infection revealed by independent component analysis of transcriptomic data. BMC Microbiol11:184 [CrossRef][PubMed]
    [Google Scholar]
  38. Zhang L., Chiang W. C., Gao Q., Givskov M., Tolker-Nielsen T., Yang L., Zhang G..( 2012;). The catabolite repression control protein Crc plays a role in the development of antimicrobial-tolerant subpopulations in Pseudomonas aeruginosa biofilms. Microbiology158:3014–3019 [CrossRef][PubMed]
    [Google Scholar]
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