Acyl-homoserine lactone quorum sensing: From evolution to application

Annual Review of Microbiology

Volumn 67, Issue , 2013, Pages 43-63

  Schuster, Martin ^a   Joseph Sexton, D ^a   Diggle, Stephen P ^b   Peter Greenberg, E ^c  

^a OREGON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Cheating; Cooperation; Pseudomonas; Public good; QS inhibition

Indexed keywords

N ACYLHOMOSERINE LACTONE; PYOVERDINE; VIRULENCE FACTOR;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; CELL DENSITY; COOPERATION; GENE EXPRESSION; KIN SELECTION; MOLECULAR EVOLUTION; NONHUMAN; PLEIOTROPY; POPULATION DENSITY; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; REGULATORY MECHANISM; SOCIAL BEHAVIOR; SOCIAL INTERACTION; VIBRIO FISCHERI;

ACYL-BUTYROLACTONES; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; BIOLOGICAL EVOLUTION; INDUSTRIAL MICROBIOLOGY; PSEUDOMONAS AERUGINOSA; QUORUM SENSING;

EID: 84882745417     PISSN: 00664227     EISSN: 15453251     Source Type: Book Series    
DOI: 10.1146/annurev-micro-092412-155635     Document Type: Article

References (129)

1. André J-B, Godelle B. 2005. Multicellular organization in bacteria as a target for drug therapy. Ecol. Lett. 8:800-10
2. Allewelt M, Coleman FT, Grout M, Priebe GP, Pier GB. 2000. Acquisition of expression of the Pseudomonas aeruginosa ExoU cytotoxin leads to increased bacterial virulence in a murine model of acute pneumonia and systemic spread. Infect. Immun. 68:3998-4004
3. Antunes LC, Schaefer AL, Ferreira RB, Qin N, Stevens AM, et al. 2007. Transcriptome analysis of the Vibrio fischeri LuxR-LuxI regulon. J. Bacteriol. 189:8387-91
4. Banin E, Lozinski A, Brady KM, Berenshtein E, Butterfield PW, et al. 2008. The potential of desferrioxamine-gallium as an anti-Pseudomonas therapeutic agent. Proc. Natl. Acad. Sci. USA 105:16761-66
5. Barczak AK, Hung DT. 2009. Productive steps toward an antimicrobial targeting virulence. Curr. Opin. Microbiol. 12:490-96
6. Bjarnsholt T, Givskov M. 2007. Quorum-sensing blockade as a strategy for enhancing host defences against bacterial pathogens. Philos. Trans. R. Soc. Lond. B 362:1213-22
7. Boedicker JQ, Vincent ME, Ismagilov RF. 2009. Microfluidic confinement of single cells of bacteria in small volumes initiates high-density behavior of quorum sensing and growth and reveals its variability. Angew. Chem. Int. Ed. 48:5908-11
8. Brown SP, Cornforth DM, Mideo N. 2012. Evolution of virulence in opportunistic pathogens: generalism, plasticity, and control. Trends Microbiol. 20:336-42
9. Brown SP, West SA, Diggle SP, Griffin AS. 2009. Social evolution in microorganisms and a Trojan horse approach to medical intervention strategies. Philos. Trans. R. Soc. Lond. B 364:3157-68
10. Cabrol S, Olliver A, Pier GB, Andremont A, Ruimy R. 2003. Transcription of quorum-sensing system genes in clinical and environmental isolates of Pseudomonas aeruginosa. J. Bacteriol. 185:7222-30
11. Cegelski L, Marshall GR, Eldridge GR, Hultgren SJ. 2008. The biology and future prospects of antivirulence therapies. Nat. Rev. Microbiol. 6:17-27
12. Clatworthy AE, Pierson E, Hung DT. 2007. Targeting virulence: a new paradigm for antimicrobial therapy. Nat. Chem. Biol. 3:541-48
13. Connell JL, Wessel AK, Parsek MR, Ellington AD, Whiteley M, Shear JB. 2010. Probing prokaryotic social behaviors with bacterial "lobster traps". mBio 1:e00202-10
14. Costerton JW, Stewart PS, Greenberg EP. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-22
15. Czaran T, Hoekstra RF. 2009. Microbial communication, cooperation and cheating: Quorum sensing drives the evolution of cooperation in bacteria. PLoS ONE 4:e6655
16. D'Argenio DA, Wu M, Hoffman LR, Kulasekara HD, Deziel E, et al. 2007. Growth phenotypes of Pseudomonas aeruginosa lasR mutants adapted to the airways of cystic fibrosis patients. Mol. Microbiol. 64:512-33
17. Dandekar AA, Chugani S, Greenberg EP. 2012. Bacterial quorum sensing and metabolic incentives to cooperate. Science 338:264-66
18. Darch SE, West SA, Winzer K, Diggle SP. 2012. Density-dependent fitness benefits in quorumsensing bacterial populations. Proc. Natl. Acad. Sci. USA 109:8259-63
19. Defoirdt T, Boon N, Bossier P. 2010. Can bacteria evolve resistance to quorum sensing disruption? PLoS Pathog. 6:e1000989
20. Denervaud V, TuQuoc P, Blanc D, Favre-Bonte S, Krishnapillai V, et al. 2004. Characterization of cellto- cell signaling-deficient Pseudomonas aeruginosa strains colonizing intubated patients. J. Clin.Microbiol. 42:554-62
21. Desai JD, Banat IM. 1997. Microbial production of surfactants and their commercial potential. Microbiol. Mol. Biol. Rev. 61:47-64
22. Diggle SP. 2010. Microbial communication and virulence: lessons from evolutionary theory. Microbiology 156:3503-12
23. Diggle SP, Gardner A, West SA, Griffin AS. 2007. Evolutionary theory of bacterial quorum sensing: When is a signal not a signal? Philos. Trans. R. Soc. Lond. B 362:1241-49
24. Diggle SP, Griffin AS, Campbell GS, West SA. 2007. Cooperation and conflict in quorum-sensing bacterial populations. Nature 450:411-14
25. Dulla G, Lindow SE. 2008. Quorum size of Pseudomonas syringae is small and dictated by water availability on the leaf surface. Proc. Natl. Acad. Sci. USA 105:3082-87
26. Eberhard A. 1972. Inhibition and activation of bacterial luciferase synthesis. J. Bacteriol. 109:1101-5
27. Eberhard A, Burlingame AL, EberhardC, KenyonGL, Nealson KH, Oppenheimer NJ. 1981. Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry 20:2444-49
28. Engebrecht J, Nealson K, Silverman M. 1983. Bacterial bioluminescence: isolation and genetic analysis of functions from Vibrio fischeri. Cell 32:773-81
29. Fiegna F, Yu YT, Kadam SV, Velicer GJ. 2006. Evolution of an obligate social cheater to a superior cooperator. Nature 441:310-14
30. Foster KR, Parkinson K, Thompson CR. 2007. What can microbial genetics teach sociobiology? Trends Genet. 23:74-80
31. Foster KR, Shaulsky G, Strassmann JE, Queller DC, Thompson CR. 2004. Pleiotropy as a mechanism to stabilize cooperation. Nature 431:693-96
32. Fothergill JL, Panagea S, Hart CA, Walshaw MJ, Pitt TL, Winstanley C. 2007. Widespread pyocyanin over-production among isolates of a cystic fibrosis epidemic strain. BMC Microbiol. 7:45
33. Fuqua WC, Winans SC, Greenberg EP. 1994. Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J. Bacteriol. 176:269-75
34. Gardner A, West SA, Wild G. 2011. The genetical theory of kin selection. J. Evol. Biol. 24:1020-43
35. Geske GD, Wezeman RJ, Siegel AP, Blackwell HE. 2005. Small molecule inhibitors of bacterial quorum sensing and biofilm formation. J. Am. Chem. Soc. 127:12762-63
36. Gilbert KB, Kim TH, Gupta R, Greenberg EP, Schuster M. 2009. Global position analysis of the Pseudomonas aeruginosa quorum-sensing transcription factor LasR. Mol. Microbiol. 73:1072-85
37. Givskov M, de Nys R, Manefield M, Gram L, Maximilien R, et al. 1996. Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling. J. Bacteriol. 178:6618-22
38. Greenwald J, Zeder-Lutz G, Hagege A, Celia H, Pattus F. 2008. The metal dependence of pyoverdine interactions with its outer membrane receptor FpvA. J. Bacteriol. 190:6548-58
39. Hamilton WD. 1964. The genetical evolution of social behaviour. I. J. Theor. Biol. 7:1-16
40. Hamilton WD. 1964. The genetical evolution of social behaviour. II. J. Theor. Biol. 7:17-52
41. Hamood AN, Griswold J, Colmer J. 1996. Characterization of elastase-deficient clinical isolates of Pseudomonas aeruginosa. Infect. Immunity 64:3154-60
42. Hardin G. 1968. The tragedy of the commons. Science 162:1243-48
43. Hastings JW. 2010. Quorum sensing is not a misnomer. Microbe 5:189
44. Heeb S, Fletcher MP, Chhabra SR, Diggle SP, Williams P, Camara M. 2011. Quinolones: from antibiotics to autoinducers. FEMS Microbiol. Rev. 35:247-74
45. Hense BA, Kuttler C, Muller J, Rothballer M, Hartmann A, Kreft JU. 2007. Does efficiency sensing unify diffusion and quorum sensing? Nat. Rev. Microbiol. 5:230-39
46. HentzerM, Givskov M. 2003. Pharmacological inhibition of quorum sensing for the treatment of chronic bacterial infections. J. Clin. Invest. 112:1300-7
47. HentzerM, RiedelK, RasmussenTB, Heydorn A, Andersen JB, et al. 2002. Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology 148:87-102
48. Hentzer M, Wu H, Andersen JB, Riedel K, Rasmussen TB, et al. 2003. Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J. 22:3803-15
49. Heurlier K, Denervaud V, Haas D. 2006. Impact of quorum sensing on fitness of Pseudomonas aeruginosa. Int. J. Med. Microbiol. 296:93-102
50. 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. 187:4875-83
51. Hoffman LR, Kulasekara HD, Emerson J, Houston LS, Burns JL, et al. 2009. Pseudomonas aeruginosa lasR mutants are associated with cystic fibrosis lung disease progression. J. Cyst. Fibros. 8:66-70
52. Huse HK, Kwon T, Zlosnik JEA, Speert DP, Marcotte EM, Whiteley M. 2010. Parallel evolution in Pseudomonas aeruginosa over 39, 000 generations in vivo. mBio 1(4):e00199-10
53. Joelsson A, Liu Z, Zhu J. 2006. Genetic and phenotypic diversity of quorum-sensing systems in clinical and environmental isolates of Vibrio cholerae. Infect. Immun. 74:1141-47
54. Kalia VC, Purohit HJ. 2011. Quenching the quorum sensing system: potential antibacterial drug targets. Crit. Rev. Microbiol. 37:121-40
55. Kaplan HB, Greenberg EP. 1985. Diffusion of autoinducer is involved in regulation of the Vibrio fischeri luminescence system. J. Bacteriol. 163:1210-14
56. Keller L, Surette MG. 2006. Communication in bacteria: an ecological and evolutionary perspective. Nat. Rev. Microbiol. 4:249-58
57. Kleerebezem M, Quadri LE, Kuipers OP, de VosWM. 1997. Quorum sensing by peptide pheromones and two-component signal-transduction systems in gram-positive bacteria. Mol. Microbiol. 24:895-904
58. Koch B, Liljefors T, Persson T, Nielsen J, Kjelleberg S, GivskovM. 2005. The LuxR receptor: the sites of interaction with quorum-sensing signals and inhibitors. Microbiology 151:3589-602
59. Kohler T, Buckling A, van Delden C. 2009. Cooperation and virulence of clinical Pseudomonas aeruginosa populations. Proc. Natl. Acad. Sci. USA 106:6339-44
60. Kohler T, Perron GG, Buckling A, van Delden C. 2010. Quorum sensing inhibition selects for virulence and cooperation in Pseudomonas aeruginosa. PLoS Pathog. 6:e1000883
61. KoulmanA, Lee TV, FraserK, Johnson L, ArcusV, et al. 2012. Identification of extracellular siderophores and a related peptide from the endophytic fungus Epichloë festucae in culture and endophyte-infected Lolium perenne. Phytochemistry 75:128-39
62. Kreft JU. 2004. Biofilms promote altruism. Microbiology 150:2751-60
63. Kuemmerli R, Brown SP. 2010. Molecular and regulatory properties of a public good shape the evolution of cooperation. Proc. Natl. Acad. Sci. USA 107:18921-26
64. Lamont IL, Beare PA, Ochsner U, Vasil AI, Vasil ML. 2002. Siderophore-mediated signaling regulates virulence factor production in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 99:7072-77
65. Lee JH, Lequette Y, Greenberg EP. 2006. Activity of purified QscR, a Pseudomonas aeruginosa orphan quorum-sensing transcription factor. Mol. Microbiol. 59:602-9
66. Lequette Y, Lee JH, Ledgham F, Lazdunski A, Greenberg EP. 2006. A distinct QscR regulon in the Pseudomonas aeruginosa quorum-sensing circuit. J. Bacteriol. 188:3365-70
67. Lesprit P, Faurisson F, Join-LambertO, Roudot-Thoraval F, FoglinoM, et al. 2003. Role of the quorumsensing system in experimental pneumonia due to Pseudomonas aeruginosa in rats. Am. J. Respir. Crit. Care Med. 167:1478-82
68. LindemannA, Pessi G, Schaefer AL, MattmannME, ChristensenQH, et al. 2011. Isovaleryl-homoserine lactone, an unusual branched-chain quorum-sensing signal from the soybean symbiont Bradyrhizobium japonicum. Proc. Natl. Acad. Sci. USA 108:16765-70
69. Lyczak JB, Cannon CL, Pier GB. 2000. Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect. 2:1051-60
70. Maeda T, Garcia-Contreras R, Pu M, Sheng L, Garcia LR, et al. 2012. Quorum quenching quandary: resistance to antivirulence compounds. ISME J. 6:493-501
71. Majerczyk CD, Greenberg EP, Chandler JR. 2013. Quorum sensing in Burkholderia. In Regulation of Bacterial Virulence, ed. ML Vasil, AJ Darwin. Washington, DC: ASM Press. In press
72. Manefield M, Rasmussen TB, HenzterM, Andersen JB, Steinberg P, et al. 2002. Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover. Microbiology 148:1119-27
73. Maynard-Smith J, Harper D. 2003. Animal Signals. Oxford, UK: Oxford Univ. Press
74. Mellbye B, Schuster M. 2011. The sociomicrobiology of antivirulence drug resistance: a proof of concept. mBio 2(5):e00131-11
75. Meyer JM, Geoffroy VA, BaidaN, Gardan L, IzardD, et al. 2002. Siderophore typing, a powerful tool for the identification of fluorescent and nonfluorescent pseudomonads. Appl. Environ.Microbiol. 68:2745-53
76. Meyer JM, Stintzi A, DeVos D, Cornelis P, Tappe R, et al. 1997. Use of siderophores to type pseudomonads: the three Pseudomonas aeruginosa pyoverdine systems. Microbiology 143:35-43
77. Muh U, Hare BJ, Duerkop BA, Schuster M, Hanzelka BL, et al. 2006. A structurally unrelated mimic of a Pseudomonas aeruginosa acyl-homoserine lactone quorum-sensing signal. Proc. Natl. Acad. Sci. USA 103:16948-52
78. Muh U, Schuster M, Heim R, Singh A, Olson ER, Greenberg EP. 2006. Novel Pseudomonas aeruginosa quorum-sensing inhibitors identified in an ultra-high-throughput screen. Antimicrob. Agents Chemother. 50:3674-79
79. Ochsner UA, Wilderman PJ, Vasil AI, Vasil ML. 2002. GeneChip expression analysis of the iron starvation response in Pseudomonas aeruginosa: identification of novel pyoverdine biosynthesis genes. Mol. Microbiol. 45:1277-87
80. Pai A, Tanouchi Y, You L. 2012. Optimality and robustness in quorum sensing (QS)-mediated regulation of a costly public good enzyme. Proc. Natl. Acad. Sci. USA 109:19810-15
81. Pai A, You L. 2009. Optimal tuning of bacterial sensing potential. Mol. Syst. Biol. 5:286
82. Patel NJ, Zaborina O, Wu L, Wang Y, Wolfgeher DJ, et al. 2007. Recognition of intestinal epithelial HIF-1áctivation by Pseudomonas aeruginosa. Am. J. Physiol. Gastrointest. Liver Physiol. 292:G134-42
83. Pearson JP, Feldman M, Iglewski BH, Prince A. 2000. Pseudomonas aeruginosa cell-to-cell signaling is required for virulence in a model of acute pulmonary infection. Infect. Immun. 68:4331-34
84. Popat R, Crusz SA, Messina M, Williams P, West SA, Diggle SP. 2012. Quorum-sensing and cheating in bacterial biofilms. Proc. R. Soc. B 279:4765-71
85. Queller DC, Goodnight KF. 1989. Estimating relatedness using genetic markers. Evolution 43:258-75
86. Rasko DA, Sperandio V. 2010. Anti-virulence strategies to combat bacteria-mediated disease. Nat. Rev. Drug Discov. 9:117-28
87. Redfield RJ. 2002. Is quorum sensing a side effect of diffusion sensing? Trends Microbiol. 10:365-70
88. Ross-Gillespie A, Gardner A, West SA, Griffin AS. 2007. Frequency dependence and cooperation: theory and a test with bacteria. Am. Nat. 170:331-42
89. 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. 19:341-45
90. Rumbaugh KP, Griswold JA, Hamood AN. 2000. The role of quorum sensing in the in vivo virulence of Pseudomonas aeruginosa. Microbes Infect. 2:1721-31
91. Rumbaugh KP, Griswold JA, Iglewski BH, Hamood AN. 1999. Contribution of quorum sensing to the virulence of Pseudomonas aeruginosa in burn wound infections. Infect. Immun. 67:5854-62
92. Rumbaugh KP, Trivedi U, Watters C, Burton-Chellew MN, Diggle SP, West SA. 2012. Kin selection, quorum sensing and virulence in pathogenic bacteria. Proc. R. Soc. B 279:3584-88
93. Salunkhe P, Smart CHM, Morgan JAW, Panagea S, WalshawMJ, et al. 2005. A cystic fibrosis epidemic strain of Pseudomonas aeruginosa displays enhanced virulence and antimicrobial resistance. J. Bacteriol. 187:4908-20
94. Sandoz KM, Mitzimberg SM, Schuster M. 2007. Social cheating in Pseudomonas aeruginosa quorum sensing. Proc. Natl. Acad. Sci. USA 104:15876-81
95. Schaber JA, Carty NL, McDonald NA, Graham ED, Cheluvappa R, et al. 2004. Analysis of quorum sensing-deficient clinical isolates of Pseudomonas aeruginosa. J. Med. Microbiol. 53:841-53
96. Schuster M, Greenberg EP. 2006. A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Int. J. Med. Microbiol. 296:73-81
97. Schuster M, Lostroh CP, Ogi T, Greenberg EP. 2003. Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J. Bacteriol. 185:2066-79
98. Shompole S, Henon KT, Liou LE, Dziewanowska K, Bohach GA, Bayles KW. 2003. Biphasic intracellular expression of Staphylococcus aureus virulence factors and evidence for Agr-mediated diffusion sensing. Mol. Microbiol. 49:919-27
99. Shopsin B, Drlica-Wagner A, Mathema B, Adhikari RP, Kreiswirth BN, Novick RP. 2008. Prevalence of agr dysfunction among colonizing Staphylococcus aureus strains. J. Infect. Dis. 198:1171-74
100. Shopsin B, Eaton C, Wasserman GA, Mathema B, Adhikari RP, et al. 2010. Mutations in agr do not persist in natural populations of methicillin-resistant Staphylococcus aureus. J. Infect. Dis. 202:1593-99
101. Silby MW, Winstanley C, Godfrey SAC, Levy SB, Jackson RW. 2011. Pseudomonas genomes: diverse and adaptable. FEMS Microbiol. Rev. 35:652-80
102. Smith EE, Buckley DG, Wu Z, Saenphimmachak C, Hoffman LR, et al. 2006. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc. Natl. Acad. Sci. USA 103:8487-92
103. Smith KM, Bu Y, Suga H. 2003. Induction and inhibition of Pseudomonas aeruginosa quorum sensing by synthetic autoinducer analogs. Chem. Biol. 10:81-89
104. Smith RS, Harris SG, Phipps R, Iglewski B. 2002. The Pseudomonas aeruginosa quorum-sensing molecule N-(3-oxododecanoyl)homoserine lactone contributes to virulence and induces inflammation in vivo. J. Bacteriol. 184:1132-39
105. Sokurenko EV, Tchesnokova V, Yeung AT, Oleykowski CA, Trintchina E, et al. 2001. Detection of simple mutations and polymorphisms in large genomic regions. Nucleic Acids Res. 29:e111
106. Stintzi A, Evans K, Meyer JM, Poole K. 1998. Quorum-sensing and siderophore biosynthesis in Pseudomonas aeruginosa: lasR/lasI mutants exhibit reduced pyoverdine biosynthesis. FEMS Microbiol. Lett. 166:341-45
107. Tingpej P, Smith L, Rose B, Zhu H, Conibear T, et al. 2007. Phenotypic characterization of clonal and nonclonal Pseudomonas aeruginosa strains isolated from lungs of adults with cystic fibrosis. J. Clin. Microbiol. 45:1697-704
108. Tomasz A. 1965. Control of the competent state in Pneumococcus by a hormone-like cell product: an example for a new type of regulatory mechanism in bacteria. Nature 208:155-59
109. Traber KE, Lee E, Benson S, Corrigan R, Cantera M, et al. 2008. agr function in clinical Staphylococcus aureus isolates. Microbiology 154:2265-74
110. Travisano M, Velicer GJ. 2004. Strategies of microbial cheater control. Trends Microbiol. 12:72-78
111. van Delden C, Comte R, Bally AM. 2001. Stringent response activates quorum sensing and modulates cell density-dependent gene expression in Pseudomonas aeruginosa. J. Bacteriol. 183:5376-84
112. 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. 66:4499-502
113. von Bodman SB, Bauer WD, Coplin DL. 2003. Quorum sensing in plant-pathogenic bacteria. Annu. Rev. Phytopathol. 41:455-82
114. 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. 185:2080-95
115. West SA, Griffin AS, Gardner A. 2007. Evolutionary explanations for cooperation. Curr. Biol. 17:R661-72
116. West SA, Griffin AS, Gardner A, Diggle SP. 2006. Social evolution theory for microorganisms. Nat. Rev. Microbiol. 4:597-607
117. West SA, Winzer K, Gardner A, Diggle SP. 2012. Quorum sensing and the confusion about diffusion. Trends Microbiol. 20:586-94
118. Whitehead NA, Barnard AM, Slater H, Simpson NJ, Salmond GP. 2001. Quorum-sensing in gramnegative bacteria. FEMS Microbiol. Rev. 25:365-404
119. Wilder CN, AlladaG, SchusterM. 2009. Instantaneous within-patient diversity of Pseudomonas aeruginosa quorum-sensing populations from cystic fibrosis lung infections. Infect. Immun. 77:5631-39
120. Wilder CN, Diggle SP, Schuster M. 2011. Cooperation and cheating in Pseudomonas aeruginosa: the roles of the las, rhl, and pqs quorum-sensing systems. ISME J. 5:1332-43
121. Williams P, CamaraM. 2009. Quorum sensing and environmental adaptation in Pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules. Curr. Opin. Microbiol. 12:182-91
122. Wu H, Song Z, Givskov M, Doring G, Worlitzsch D, et al. 2001. Pseudomonas aeruginosa mutations in lasI and rhlI quorum sensing systems result in milder chronic lung infection. Microbiology 147:1105-13
123. Wu H, Song Z, Hentzer M, Andersen JB, Molin S, et al. 2004. Synthetic furanones inhibit quorumsensing and enhance bacterial clearance in Pseudomonas aeruginosa lung infection in mice. J. Antimicrob. Chemother. 53:1054-61
124. Xavier JB, Foster KR. 2007. Cooperation and conflict in microbial biofilms. Proc. Natl. Acad. Sci. USA 104:876-81
125. Xavier JB, Kim W, Foster KR. 2011. A molecular mechanism that stabilizes cooperative secretions in Pseudomonas aeruginosa. Mol. Microbiol. 79:166-79
126. ZhuH, Bandara R, Conibear TCR, Thuruthyil SJ, Rice SA, et al. 2004. Pseudomonas aeruginosa with LasI quorum-sensing deficiency during corneal infection. Investig. Ophthalmol. Visual Sci. 45:1897-903
127. Zhu H, Thuruthyil SJ, Willcox MDP. 2002. Determination of quorum-sensing signal molecules and virulence factors of Pseudomonas aeruginosa isolates from contact lens-induced microbial keratitis. J. Med. Microbiol. 51:1063-70
128. Zhu J, Beaber JW, Moré MI, Fuqua C, Eberhard A, Winans SC. 1998. Analogs of the autoinducer 3-oxooctanoyl-homoserine lactone strongly inhibit activity of the TraR protein of Agrobacterium tumefaciens. J. Bacteriol. 180:5398-405
129. Tomás M, Doumith M, Warner M, Turton JF, Beceiro A, et al. 2010. Efflux pumps, OprD porin, AmpC β-lactamase, and multiresistance in Pseudomonas aeruginosa isolates from cystic fibrosis patients. Antimicrob. Agents Chemother. 54:2219-24