Cooperation and cheating in Pseudomonas aeruginosa: The roles of the las, rhl and pqs quorum-sensing systems

ISME Journal

Volumn 5, Issue 8, 2011, Pages 1332-1343

  Wilder, Cara N ^a   Diggle, Stephen P ^b   Schuster, Martin ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

cheating; cooperation; Pseudomonas aeruginosa; quorum

Indexed keywords

BACTERIAL PROTEIN; LASR PROTEIN, PSEUDOMONAS AERUGINOSA; TRANSACTIVATOR PROTEIN;

BACTERIUM; DEVELOPMENTAL BIOLOGY; FREQUENCY ANALYSIS; GENE EXPRESSION; MUTATION; VIRULENCE; WILD POPULATION;

ARTICLE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION; PSEUDOMONAS AERUGINOSA; QUORUM SENSING;

BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MUTATION; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; TRANS-ACTIVATORS;

PSEUDOMONAS AERUGINOSA;

EID: 79960558506     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2011.13     Document Type: Article

References (57)

1. Bredenbruch F, Geffers R, Nimtz M, Buer J, Haussler S. (2006). The Pseudomonas aeruginosa quinolone signal (PQS) has an iron-chelating activity. Environ Microbiol 8: 1318-1329. (Pubitemid 44025327)
2. Brint JM, Ohman DE. (1995). Synthesis of multiple exoproducts in Pseudomonas aeruginosa is under the control of RhlR-RhlI, another set of regulators in strain PAO1 with homology to the autoinducer-responsive LuxR-LuxI family. J Bacteriol 177: 7155-7163.
3. Choi KH, Schweizer HP. (2006). Mini-Tn7 insertion in bacteria with secondary, non-glmS-linked attTn7 sites: example Proteus mirabilis HI4320. Nat Protoc 1: 170-178.
4. D'Argenio DA, Calfee MW, Rainey PB, Pesci EC. (2002). Autolysis and autoaggregation in Pseudomonas aeru-ginosa colony morphology mutants. J Bacteriol 184: 6481-6489. (Pubitemid 35332551)
5. D'Argenio DA, Wu M, Hoffman LR, Kulasekara HD, Deziel E, Smith EE et al. (2007). Growth phenotypes of Pseudomonas aeruginosa lasR mutants adapted to the airways of cystic fibrosis patients. Mol Microbiol 64: 512-533. (Pubitemid 46632635)
6. Dekimpe V, Deziel E. (2009). Revisiting the quorum-sensing hierarchy in Pseudomonas aeruginosa: the transcriptional regulator RhlR regulates LasR-specific factors. Microbiology 155: 712-723.
7. Deziel E, Gopalan S, Tampakaki AP, Lepine F, Padfield KE, Saucier M et al. (2005). The contribution of MvfR to Pseudomonas aeruginosa pathogenesis and quorum sensing circuitry regulation: multiple quorum sensing-regulated genes are modulated without affecting lasRI, rhlRI or the production of N-acyl-L-homoserine lactones. Mol Microbiol 55: 998-1014. (Pubitemid 40299172)
8. Diggle SP, Gardner A, West SA, Griffin AS. (2007a). Evolutionary theory of bacterial quorum sensing: when is a signal not a signal? Philos Trans R Soc Lond B Biol Sci 362: 1241-1249. (Pubitemid 47075155)
9. Diggle SP, Griffin AS, Campbell GS, West SA. (2007b). Cooperation and conflict in quorum-sensing bacterial populations. Nature 450: 411-414. (Pubitemid 350126749)
10. Diggle SP, Matthijs S, Wright VJ, Fletcher MP, Chhabra SR, Lamont IL et al. (2007c). The Pseudomonas aerugino-sa 4-quinolone signal molecules HHQ and PQS play multifunctional roles in quorum sensing and iron entrapment. Chem Biol 14: 87-96. (Pubitemid 46138049)
11. Diggle SP, Winzer K, Chhabra SR, Worrall KE, 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. (Pubitemid 37222784)
12. Fletcher MP, Diggle SP, Camara M, Williams P. (2007). Biosensor-based assays for PQS, HHQ and related 2-alkyl-4-quinolone quorum sensing signal molecules. Nat Protoc 2: 1254-1262. (Pubitemid 46901302)
13. Fong YM, Minei JP, Marano MA, Moldawer LL, Wei H, Shires III GT et al. (1991). Skeletal muscle amino acid and myofibrillar protein mRNA response to thermal injury and infection. Am J Physiol 261: R536-R542.
14. Fothergill JL, Panagea S, Hart CA, Walshaw MJ, Pitt TL, Winstanley C. (2007). Widespread pyocyanin overproduction among isolates of a cystic fibrosis epidemic strain. BMC Microbiol 7: 45.
15. Haussler S, Becker T. (2008). The pseudomonas quinolone signal (PQS) balances life and death in Pseudomonas aeruginosa populations. PLoS Pathog 4: e1000166.
16. Hentzer M, Wu H, Andersen JB, Riedel K, Rasmussen TB, Bagge N et al. (2003). Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J 22: 3803-3815. (Pubitemid 36975709)
17. Heurlier K, Denervaud V, Haas D. (2006). Impact of quorum sensing on fitness of Pseudomonas aeruginosa. Int J Med Microbiol 296: 93-102. (Pubitemid 43375991)
18. Heurlier K, Denervaud V, Haenni M, Guy L, Krishnapillai V, Haas D. (2005). Quorum-sensing-negative (lasR) mutants of Pseudomonas aeruginosa avoid cell lysis and death. J Bacteriol 187: 4875-4883. (Pubitemid 40962204)
19. Hoang TT, Karkhoff-Schweizer RR, Kutchma AJ, Schweizer HP. (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 28: 77-86. (Pubitemid 28269135)
20. Hoffman LR, Kulasekara HD, Emerson J, Houston LS, Burns JL, Ramsey BW et al. (2009). Pseudomonas aeruginosa lasR mutants are associated with cystic fibrosis lung disease progression. J Cyst Fibros 8: 66-70.
21. Holloway JB, Krishnapillai V, Morgan AF. (1979). Chromosomal genetics of Pseudomonas. Microbiol Rev 43: 73-102. (Pubitemid 9169387)
22. Inglis RF, Gardner A, Cornelis P, Buckling A. (2009). Spite and virulence in the bacterium Pseudomonas aeruginosa. Proc Natl Acad Sci USA 106: 5703-5707.
23. Juhas M, Eberl L, Tummler B. (2005). Quorum sensing: the power of cooperation in the world of Pseudomonas. Environ Microbiol 7: 459-471. (Pubitemid 40441020)
24. Keller L, Surette MG. (2006). Communication in bacteria: an ecological and evolutionary perspective. Nat Rev Microbiol 4: 249-258.
25. Kohler T, Buckling A, van Delden C. (2009). Cooperation and virulence of clinical Pseudomonas aeruginosa populations. Proc Natl Acad Sci USA 106: 6339-6344.
26. Kohler T, Curty LK, Barja F, van Delden C, Pechere JC. (2000). Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. J Bacteriol 182: 5990-5996.
27. Latifi A, Foglino M, Tanaka K, Williams P, Lazdunski A. (1996). A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhIR (VsmR) to expression of the stationary-phase sigma factor RpoS. Mol Microbiol 21: 1137-1146. (Pubitemid 26313241)
28. Lee JH, Lequette Y, Greenberg EP. (2006). Activity of purified QscR, a Pseudomonas aeruginosa orphan quorum-sensing transcription factor. Mol Microbiol 59: 602-609.
29. Lehmann L, Keller L. (2006). The evolution of cooperation and altruism-a general framework and a classification of models. J Evol Biol 19: 1365-1376.
30. Lenski RE. (1991). Quantifying fitness and gene stability in microorganisms. Biotechnology 15: 173-192.
31. MacLean RC, Gudelj I. (2006). Resource competition and social conflict in experimental populations of yeast. Nature 441: 498-501. (Pubitemid 44050149)
32. McGrath S, Wade DS, Pesci EC. (2004). Dueling quorum sensing systems in Pseudomonas aeruginosa control the production of the Pseudomonas quinolone signal (PQS). FEMS Microbiol Lett 230: 27-34. (Pubitemid 38091735)
33. Medina G, Juarez K, Diaz R, Soberon-Chavez G. (2003). Transcriptional regulation of Pseudomonas aerugino-sa rhlR, encoding a quorum-sensing regulatory protein. Microbiology 149: 3073-3081. (Pubitemid 37441990)
34. Molofsky J, Bever JD, Antonovics J. (2001). Coexistence under positive frequency dependence. Proc Biol Sci 268: 273-277. (Pubitemid 32154507)
35. Newman JR, Fuqua C. (1999). Broad-host-range expression vectors that carry the L-arabinose-inducible Escher-ichia coli araBAD promoter and the araC regulator. Gene 227: 197-203. (Pubitemid 29104855)
36. Ng WL, Bassler BL. (2009). Bacterial quorum-sensing network architectures. Annu Rev Genet 43: 197-222.
37. Pearson JP, Pesci EC, Iglewski BH. (1997). Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. J Bacteriol 179: 5756-5767. (Pubitemid 27398275)
38. Pesci EC, Pearson JP, Seed PC, Iglewski BH. (1997). Regulation of las and rhl quorum sensing in Pseudo-monas aeruginosa. J Bacteriol 179: 3127-3132. (Pubitemid 27202984)
39. Rampioni G, Pustelny C, Fletcher MP, Wright VJ, Bruce M, Rumbaugh KP et al. (2010). Transcriptomic analysis reveals a global alkyl-quinolone-independent regulatory role for PqsE in facilitating the environmental adaptation of Pseudomonas aeruginosa to plant and animal hosts. Environ Microbiol 12: 1659-1673.
40. Ross-Gillespie A, Gardner A, West SA, Griffin AS. (2007a). Frequency dependence and cooperation: theory and a test with bacteria. Am Nat 170: 331-342. (Pubitemid 47312840)
41. Ross-Gillespie A, Gardner A, West SA, Griffin AS. (2007b). Frequency dependence and cooperation: theory and a test with bacteria. Am Nat 170: 331-342. (Pubitemid 47312840)
42. Rumbaugh KP, Diggle SP, Watters CM, Ross-Gillespie A, Griffin AS, West SA. (2009). Quorum sensing and the social evolution of bacterial virulence. Curr Biol 19: 341-345.
43. Sandoz K, Mitzimberg S, Schuster M. (2007). Social cheating in Pseudomonas aeruginosa quorum sensing. Proc Natl Acad Sci USA 104: 15876-15881. (Pubitemid 350035392)
44. Schuster M, Greenberg EP. (2006). A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Int J Med Microbiol 296: 73-81. (Pubitemid 43375989)
45. Schuster M, Greenberg EP. (2007). Early activation of quorum sensing in Pseudomonas aeruginosa reveals the architecture of a complex regulon. BMC Genomics 8: 287.
46. Schuster M, Lohstroh CP, Ogi T, Greenberg EP. (2003). Identification, timing and signal specificity of Pseu-domonas aeruginosa quorum-controlled genes: a transcriptome analysis. J Bacteriol 185: 2066-2079. (Pubitemid 36363167)
47. Smith EE, Buckley DG, Wu Z, Saenphimmachak C, Hoffman LR, D'Argenio DA et al. (2006). Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci USA 103: 8487-8492. (Pubitemid 43838482)
48. Tingpej P, Smith L, Rose B, Zhu H, Conibear T, Al Nassafi K et al. (2007). Phenotypic characterization of clonal and nonclonal Pseudomonas aeruginosa strains isolated from lungs of adults with cystic fibrosis. J Clin Microbiol 45: 1697-1704. (Pubitemid 46933894)
49. Van Delden C, Pesci EC, Pearson JP, Iglewski BH. (1998). Starvation selection restores elastase and rhamnolipid production in a Pseudomonas aeruginosa quorum-sensing mutant. Infect Immun 66: 4499-4502. (Pubitemid 28402731)
50. Wade DS, Calfee MW, Rocha ER, Ling EA, Engstrom E, Coleman JP et al. (2005). Regulation of Pseudomonas quinolone signal synthesis in Pseudomonas aeruginosa. J Bacteriol 187: 4372-4380. (Pubitemid 40880947)
51. Wagner VE, Bushnell D, Passador L, Brooks AI, Iglewski BH. (2003). Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment. J Bacteriol 185: 2080-2095. (Pubitemid 36363168)
52. West SA, Buckling A. (2003). Cooperation, virulence and siderophore production in bacterial parasites. Proc Biol Sci 270: 37-44. (Pubitemid 36140420)
53. West SA, Griffin AS, Gardner A. (2007). Evolutionary explanations for cooperation. Curr Biol 17: R661-R672. (Pubitemid 47259365)
54. West SA, Griffin AS, Gardner A, Diggle SP. (2006). Social evolution theory for microorganisms. Nat Rev Microbiol 4: 597-607. (Pubitemid 44317022)
55. Williams P, Winzer K, Chan WC, Camara M. (2007). Look who's talking: communication and quorum sensing in the bacterial world. Philos Trans R Soc Lond B Biol Sci 362: 1119-1134. (Pubitemid 47075145)
56. Xiao G, Deziel E, He J, Lepine F, Lesic B, Castonguay MH et al. (2006). MvfR, a key Pseudomonas aeruginosa pathogenicity LTTR-class regulatory protein, has dual ligands. Mol Microbiol 62: 1689-1699. (Pubitemid 44813813)
57. Yates EA, Philipp B, Buckley C, Atkinson S, Chhabra SR, Sockett RE et al. (2002). N-acylhomoserine lactones undergo lactonolysis in a pH-, temperature-, and acyl chain length-dependent manner during growth of Yersinia pseudotuberculosis and Pseudomonas aeru-ginosa. Infect Immun 70: 5635-5646.