Impact of quorum sensing on fitness of Pseudomonas aeruginosa

International Journal of Medical Microbiology

Volumn 296, Issue 2-3, 2006, Pages 93-102

  Heurlier, Karin ^a   Dénervaud, Valérie ^b   Haas, Dieter ^b  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Cell death; N acyl homoserine lactones; Nucleoside hydrolase; Pseudomonas aeruginosa; Quorum sensing; S adenosyl methionine; Stationary phase

Indexed keywords

ADENOSINE; HYPOXANTHINE; INOSINE; LACTONE DERIVATIVE; N ACYLHOMOSERINE LACTONE; S ADENOSYLMETHIONINE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

BACTERIAL VIRULENCE; BACTERIUM ISOLATE; BIOSYNTHESIS; CELL COMMUNICATION; LASR GENE; NONHUMAN; PROTEOMICS; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; RECYCLING; REGULATOR GENE; REVIEW; TRANSCRIPTOMICS; WILD TYPE;

EID: 33644865643     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2006.01.043     Document Type: Review

References (76)

1. M. Alaminos, and J.L. Ramos The methionine biosynthetic pathway from homoserine in Pseudomonas putida involves the metW, metX, metZ, metH and metE gene products Arch. Microbiol. 176 2001 151 154
2. C. Arevalo-Ferro, M. Hentzer, G. Reil, A. Gorg, S. Kjelleberg, M. Givskov, K. Riedel, and L. Eberl Identification of quorum-sensing regulated proteins in the opportunistic pathogen Pseudomonas aeruginosa by proteomics Environ. Microbiol. 5 2003 1350 1369
3. S.A. Beatson, C.B. Whitchurch, A.B.T. Semmler, and J.S. Mattick Quorum sensing is not required for twitching motility in Pseudomonas aeruginosa J. Bacteriol. 184 2002 3598 3604
4. S. Bleves, C. Soscia, P. Nogueira-Orlandi, A. Lazdunski, and A. Filloux Quorum sensing negatively controls type III secretion regulon expression in Pseudomonas aeruginosa PAO1 J. Bacteriol. 187 2005 3898 3902
5. N. Bollinger, D.J. Hassett, B.H. Iglewski, J.W. Costerton, and T.R. McDermott Gene expression in Pseudomonas aeruginosa: evidence of iron override effects on quorum sensing and biofilm-specific gene regulation J. Bacteriol. 183 2001 1990 1996
6. J.T. Byers, C. Lucas, G.P.C. Salmond, and M. Welch Nonenzymatic turnover of an Erwinia carotovora quorum-sensing signaling molecule J. Bacteriol. 184 2002 1163 1171
7. S. Cabrol, A. Olliver, G.B. Pier, A. Andremont, and R. Ruimy Transcription of quorum-sensing system genes in clinical and environmental isolates of Pseudomonas aeruginosa J. Bacteriol. 185 2003 7222 7230
8. A. Carlier, R. Chevrot, Y. Dessaux, and D. Faure The assimilation of gamma-butyrolactone in Agrobacterium tumefaciens C58 interferes with the accumulation of the N-acyl-homoserine lactone signal Mol. Plant Microbe Interact. 17 2004 951 957
9. C. Cha, P. Gao, Y.C. Chen, P.D. Shaw, and S.K. Farrand Production of acyl-homoserine lactone quorum-sensing signals by Gram-negative plant-associated bacteria Mol. Plant Microbe Interact. 11 1998 1119 1129
10. C.E. Chambers, M.B. Visser, U. Schwab, and P.A. Sokol Identification of N-acylhomoserine lactones in mucopurulent respiratory secretions from cystic fibrosis patients FEMS Microbiol. Lett. 244 2005 297 304
11. C.-C. Chen, L. Riadi, S.-J. Suh, D. Ohman, and L.-K. Ju Degradation and synthesis kinetics of quorum-sensing autoinducer in Pseudomonas aeruginosa cultivation J. Biotechnol. 117 2005 1 10
12. P. Cornelis, and S. Aendekerk A new regulator linking quorum sensing and iron uptake in Pseudomonas aeruginosa Microbiology 150 2004 752 756
13. D.A. D'Argenio, M.W. Calfee, P.B. Rainey, and E.C. Pesci Autolysis and autoaggregation in Pseudomonas aeruginosa colony morphology mutants J. Bacteriol. 184 2002 6481 6489
14. V. Dénervaud, P. TuQuoc, D. Blanc, S. Favre-Bonté, V. Krishnapillai, C. Reimmann, D. Haas, and C. van Delden Characterization of cell-to-cell signaling-deficient Pseudomonas aeruginosa strains colonizing intubated patients J. Clin. Microbiol. 42 2004 554 562
15. C.K. Dumenyo, A. Mukherjee, W. Chun, and A.K. Chatterjee Genetic and physiological evidence for the production of N-acyl homoserine lactones by Pseudomonas syringae pv. syringae and other fluorescent plant pathogenic Pseudomonas species Eur. J. Plant Pathol. 104 1998 569 582
16. M. Elasri, S. Delorme, P. Lemanceau, G. Stewart, B. Laue, E. Glickmann, P.M. Oger, and Y. Dessaux Acyl-homoserine lactone production is more common among plant-associated Pseudomonas spp. than among soilborne Pseudomonas spp Appl. Environ. Microbiol. 67 2001 1198 1209
17. S. Favre-Bonté, J.-C. Pache, J. Robert, D. Blanc, J.-C. Pechère, and C. van Delden Detection of Pseudomonas aeruginosa cell-to-cell signals in lung tissue of cystic fibrosis patients Microb. Pathog. 32 2002 143 147
18. V. Finck-Barbancon, J. Goranson, L. Zhu, T. Sawa, J.P. Wiener-Kronish, S.M. Fleiszig, C. Wu, L. Mende-Mueller, and D.W. Frank ExoU expression by Pseudomonas aeruginosa correlates with acute cytotoxicity and epithelial injury Mol. Microbiol. 25 1997 547 557
19. M. Foglino, F. Borne, M. Bally, G. Ball, and J. Patte A direct sulfhydrylation pathway is used for methionine biosynthesis in Pseudomonas aeruginosa Microbiology 141 1995 431 439
20. M.J. Gambello, and B.J. Iglewski Cloning and characterization of the Pseudomonas aeruginosa lasR gene, a transcriptional activator of elastase expression J. Bacteriol. 173 1991 3000 3009
21. O. Geisenberger, M. Givskov, K. Riedel, N. Høiby, B. Tümmler, and L. Eberl Production of N-acyl-homoserine lactones by Pseudomonas aeruginosa isolates from chronic lung infections associated with cystic fibrosis FEMS Microbiol. Lett. 184 2000 273 278
22. A. Goodman, B. Kulasekara, A. Rietsch, D. Boyd, R. Smith, and S. Lory A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa Dev. Cell 7 2004 745 754
23. K.M. Gray, and J.R. Garey The evolution of bacterial LuxI and LuxR quorum sensing regulators Microbiology 147 2001 2379 2387
24. A. Hamood, J. Griswold, and J. Colmer Characterization of elastase-deficient clinical isolates of Pseudomonas aeruginosa Infect. Immun. 64 1996 3154 3160
25. S. Häussler, I. Ziegler, A. Lottel, F. von Götz, M. Rohde, D. Wehmhohner, S. Saravanamuthu, B. Tümmler, and I. Steinmetz Highly adherent small-colony variants of Pseudomonas aeruginosa in cystic fibrosis lung infection J. Med. Microbiol. 52 2003 295 301
26. M. Hentzer, H. Wu, J.B. Andersen, K. Riedel, T.B. Rasmussen, N. Bagge, N. Kumar, M.A. Schembri, Z. Song, P. Kristoffersen, M. Manefield, J.W. Costerton, S. Molin, L. Eberl, P. Steinberg, S. Kjelleberg, N. Høiby, and M. Givskov Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors EMBO J. 22 2003 3803 3815
27. K. Heurlier, V. Dénervaud, M. Haenni, L. Guy, V. Krishnapillai, and D. Haas Quorum sensing-negative (lasR) mutants of Pseudomonas aeruginosa avoid cell lysis and death J. Bacteriol. 187 2005 4875 4883
28. M. Hogardt, M. Roeder, A.M. Schreff, L. Eberl, and J. Heesemann Expression of Pseudomonas aeruginosa exoS is controlled by quorum sensing and RpoS Microbiology 150 2004 843 851
29. J.J. Huang, J.-I. Han, L.-H. Zhang, and J.R. Leadbetter Utilization of acyl-homoserine lactone quorum signals for growth by a soil pseudomonad and Pseudomonas aeruginosa PAO1 Appl. Environ. Microbiol. 69 2003 5941 5949
30. J.J. Huang, A. Petersen, M. Whiteley, and J.R. Leadbetter Identification of QuiP, the product of gene PA1032, as the second acyl-homoserine lactone acylase of pseudomonas aeruginosa PAO1 Appl. Environ. Microbiol. 72 2006 1190 1197
31. M. Juhas, L. Wiehlmann, B. Huber, D. Jordan, J. Lauber, P. Salunkhe, A.S. Limpert, F. von Götz, I. Steinmetz, L. Eberl, and B. Tümmler Global regulation of quorum sensing and virulence by VqsR in Pseudomonas aeruginosa Microbiology 150 2004 831 841
32. M. Juhas, L. Eberl, and B. Tümmler Quorum sensing: the power of cooperation in the world of Pseudomonas Environ. Microbiol. 7 2005 459 471
33. G.F. Kaufmann, R. Sartorio, S.-H. Lee, C.J. Rogers, M.M. Meijler, J.A. Moss, B. Clapham, A.P. Brogan, T.J. Dickerson, and K.D. Janda Revisiting quorum sensing: discovery of additional chemical and biological functions for 3-oxo-N-acylhomoserine lactones Proc. Natl. Acad. Sci. USA 102 2005 309 314
34. E.-J. Kim, W. Wang, W.-D. Deckwer, and A.-P. Zeng Expression of the quorum-sensing regulatory protein LasR is strongly affected by iron and oxygen concentrations in cultures of Pseudomonas aeruginosa irrespective of cell density Microbiology 151 2005 1127 1138
35. I.L. Lamont, and L.W. Martin Identification and characterization of novel pyoverdine synthesis genes in Pseudomonas aeruginosa Microbiology 149 2003 833 842
36. B. Lee, J.A. Haagensen, O. Ciofu, J.B. Andersen, N. Hoiby, and S. Molin Heterogeneity of biofilms formed by nonmucoid Pseudomonas aeruginosa isolates from patients with cystic fibrosis J. Clin. Microbiol. 43 2005 5247 5255
37. V.T. Lee, R.S. Smith, B. Tümmler, and S. Lory Activities of Pseudomonas aeruginosa effectors secreted by the type III secretion system in vitro and during infection Infect. Immun. 73 2005 1695 1705
38. P. Lesprit, F. Faurisson, O. Join-Lambert, F. Roudot-Thoraval, M. Foglino, C. Vissuzaine, and C. Carbon Role of the quorum-sensing system in experimental pneumonia due to Pseudomonas aeruginosa in rats Am. J. Respir. Crit. Care Med. 167 2003 1478 1482
39. P.V. Liu Extracellular toxins of Pseudomonas aeruginosa J. Infect. Dis. 130 1974 S94 S99
40. J. Loh, E.A. Pierson, L.S. Pierson, G. Stacey, and A. Chatterjee Quorum sensing in plant-associated bacteria Curr. Opin. Plant Biol. 5 2002 285 290
41. M. Manefield, and S.L. Turner Quorum sensing in context: out of molecular biology and into microbial ecology Microbiology 148 2002 3762 3764
42. H. Matsumoto, S. Ohta, R. Kobayashi, and Y. Terawaki Chromosomal location of genes participating in the degradation of purines in Pseudomonas aeruginosa Mol. Gen. Genet. 167 1978 165 176
43. B. Middleton, H.C. Rodgers, M. Cámara, A.J. Knox, P. Williams, and A. Hardman Direct detection of N-acylhomoserine lactones in cystic fibrosis sputum FEMS Microbiol. Lett. 207 2002 1 7
44. M.I. More, L.D. Finger, J.L. Stryker, C. Fuqua, A. Eberhard, and S.C. Winans Enzymatic synthesis of a quorum-sensing autoinducer through use of defined substrates Science 272 1996 1655 1658
45. T.I. Nicas, and B.H. Iglewski The contribution of exoproducts to virulence of Pseudomonas aeruginosa Can. J. Microbiol. 31 1985 387 392
46. M.R. Parsek, D.L. Val, B.L. Hanzelka, J.E. Cronan Jr., and E.P. Greenberg Acyl homoserine-lactone quorum-sensing signal generation Proc. Natl. Acad. Sci. USA 96 1999 4360 4365
47. J.P. Pearson, C. van Delden, and B.J. Iglewski Active efflux and diffusion are involved in transport of Pseudomonas aeruginosa cell-to-cell signals J. Bacteriol. 181 1999 1203 1210
48. J.P. Pearson, M. Feldman, B.H. Iglewski, and A. Prince Pseudomonas aeruginosa cell-to-cell signaling is required for virulence in a model of acute pulmonary infection Infect. Immun. 68 2000 4331 4334
49. M. Preston, P. Seed, D. Toder, B. Iglewski, D. Ohman, J. Gustin, J. Goldberg, and G. Pier Contribution of proteases and LasR to the virulence of Pseudomonas aeruginosa during corneal infections Infect. Immun. 65 1997 3086 3090
50. K. Riedel, M. Hentzer, O. Geisenberger, B. Huber, A. Steidle, H. Wu, N. Høiby, M. Givskov, S. Molin, and L. Eberl N-acylhomoserine-lactone- mediated communication between Pseudomonas aeruginosa and Burkholderia cepacia in mixed biofilms Microbiology 147 2001 3249 3262
51. K.P. Rumbaugh, J.A. Griswold, and A.N. Hamood Pseudomonas aeruginosa strains obtained from patients with tracheal, urinary tract and wound infection: variations in virulence factors and virulence genes J. Hosp. Infect. 43 1999 211 218
52. K.P. Rumbaugh, J.A. Griswold, B.H. Iglewski, and A.N. Hamood Contribution of quorum sensing to the virulence of Pseudomonas aeruginosa in burn wound infections Infect. Immun. 67 1999 5854 5862
53. P. Salunkhe, C.H.M. Smart, J.A.W. Morgan, S. Panagea, M.J. Walshaw, C.A. Hart, R. Geffers, B. Tümmler, and C. Winstanley A cystic fibrosis epidemic strain of Pseudomonas aeruginosa displays enhanced virulence and antimicrobial resistance J. Bacteriol. 187 2005 4908 4920
54. T. Sawa, M. Ohara, K. Kurahashi, S.S. Twining, D.W. Frank, D.B. Doroques, T. Long, M.A. Gropper, and J.P. Wiener-Kronish In vitro cellular toxicity predicts Pseudomonas aeruginosa virulence in lung infections Infect. Immun. 66 1998 3242 3249
55. J.A. Schaber, N.L. Carty, N.A. McDonald, E.D. Graham, R. Cheluvappa, J.A. Griswold, and A.N. Hamood Analysis of quorum sensing-deficient clinical isolates of Pseudomonas aeruginosa J. Med. Microbiol. 53 2004 841 853
56. M. Schuster, and E.P. Greenberg A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa Int. J. Med. Microbiol. 296 2006 73 81
57. M. Schuster, C.P. Lostroh, T. Ogi, and E.P. Greenberg Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis J. Bacteriol. 185 2003 2066 2079
58. M. Schuster, A.C. Hawkins, C.S. Harwood, and E.P. Greenberg The Pseudomonas aeruginosa RpoS regulon and its relationship to quorum sensing Mol. Microbiol. 51 2004 973 985
59. A. Sekowska, V. Dénervaud, H. Ashida, K. Michoud, D. Haas, A. Yokota, and A. Danchin Bacterial variations on the methionine salvage pathway BMC Microbiol. 4 2004 9
60. P.D. Shaw, G. Ping, S.L. Daly, C. Cha, J.E. Cronan Jr., K.L. Rinehart, and S.K. Farrand Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography Proc. Natl. Acad. Sci. USA 94 1997 6036 6041
61. M.W. Silby, S.R. Giddens, and H.K. Mahanty Mutation of a LysR-type regulator of antifungal activity results in a growth advantage in stationary phase phenotype in Pseudomonas aureofaciens PA147-2 Appl. Environ. Microbiol. 71 2005 569 573
62. E.V. Sokurenko, V. Tchesnokova, A.T. Yeung, C.A. Oleykowski, E. Trintchina, K.T. Hughes, R.A. Rashid, J.M. Brint, S.L. Moseley, and S. Lory Detection of simple mutations and polymorphisms in large genomic regions Nucl. Acids Res. 29 2001 E111
63. G.V. Stauffer Biosynthesis of serine, glycine, and one-carbon units F.C. Neidhardt Escherichia coli and Salmonella. Cellular and molecular biology 1996 ASM Press Washington, DC 506 513
64. A. Stintzi, K. Evans, J.-M. Meyer, and K. Poole Quorum-sensing and siderophore biosynthesis in Pseudomonas aeruginosa: lasR/lasI mutants exhibit reduced pyoverdine biosynthesis FEMS Microbiol. Lett. 166 1998 341 345
65. H. Tabor, C.W. Tabor, and S.M. Rosenthal The biochemistry of the polyamines: spermidine and spermine Annu. Rev. Biochem. 30 1961 579 604
66. C. Van Delden, and B. Iglewski Cell-to-cell signaling and Pseudomonas aeruginosa infections Emerg. Infect. Dis. 4 1998 551 560
67. V.E. Wagner, D. Bushnell, L. Passador, A.I. Brooks, and B.H. Iglewski Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment J. Bacteriol. 185 2003 2080 2095
68. Y.-J. Wang, and J.R. Leadbetter Rapid acyl-homoserine lactone quorum signal biodegradation in diverse soils Appl. Environ. Microbiol. 71 2005 1291 1299
69. M. Whiteley, K.M. Lee, and E.P. Greenberg Identification of genes controlled by quorum sensing in Pseudomonas aeruginosa Proc. Natl. Acad. Sci. USA 96 1999 13904 13909
70. K. Winzer, and P. Williams Quorum sensing and the regulation of virulence gene expression in pathogenic bacteria Int. J. Med. Microbiol. 291 2001 131 143
71. H. Withers, S. Swift, and P. Williams Quorum sensing as an integral component of gene regulatory networks in Gram-negative bacteria Curr. Opin. Microbiol. 4 2001 186 193
72. H. Wu, Z. Song, M. Givskov, G. Döring, D. Worlitzsch, K. Mathee, J. Rygaard, and N. Høiby Pseudomonas aeruginosa mutations in lasI and rhlI quorum sensing systems result in milder chronic lung infection Microbiology 147 2001 1105 1113
73. E.A. Yates, B. Philipp, C. Buckley, S. Atkinson, S.R. Chhabra, R.E. Sockett, M. Goldner, Y. Dessaux, M. Camara, H. Smith, and P. Williams N-acylhomoserine lactones undergo lactonolysis in a pH-, temperature-, and acyl chain length-dependent manner during growth of Yersinia pseudotuberculosis and Pseudomonas aeruginosa Infect. Immun. 70 2002 5635 5646
74. H. Zhu, S.J. Thuruthyil, and M.D.P. Willcox Determination of quorum-sensing signal molecules and virulence factors of Pseudomonas aeruginosa isolates from contact lens-induced microbial keratitis J. Med. Microbiol. 51 2002 1063 1070
75. H. Zhu, R. Bandara, T.C.R. Conibear, S.J. Thuruthyil, S.A. Rice, S. Kjelleberg, M. Givskov, and M.D.P. Willcox Pseudomonas aeruginosa with LasI quorum-sensing deficiency during corneal infection Invest. Ophthalmol. Vis. Sci. 45 2004 1897 1903
76. C.H. Zierdt, and P.J. Schmidt Dissociation in Pseudomonas aeruginosa J. Bacteriol. 87 1964 1003 1010