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Chapter 20 : More than Just a Quorum: Integration of Stress and Other Environmental Cues in Acyl-Homoserine Lactone Signaling

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More than Just a Quorum: Integration of Stress and Other Environmental Cues in Acyl-Homoserine Lactone Signaling, Page 1 of 2

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Abstract:

Many bacteria employ chemical communication to coordinate group behaviors, a process that has been termed quorum sensing (QS). Although many different classes of bacteria use QS, the mechanism that has emerged as common in gram-negative proteobacteria is based on acyl-homoserine lactone (acyl-HSL) signal molecules. QS is an important field of study because of its important regulatory roles in pathogenic and environmental bacteria. Acyl-homoserine lactone (Acyl-HSL) QS controls virulence in many plant and animal pathogens such as , , and . This chapter focuses on the integration of acyl-HSL QS and such stress responses. In , QS controls the expression of numerous virulence factors such as extracellular enzymes (LasB elastase, LasA protease, alkaline protease), secondary metabolites (pyocyanin, hydrogen cyanide, pyoverdin), and toxins (exotoxin A). Microarray studies revealed that the and systems together control the expression of more than 300 genes. The majority of the associated genes are predicted to encode secreted factors and secretion machinery, confirming the notion that the core function of QS is to control the expression of extracellular factors. Indeed, a recent population analysis of concurrently isolated from individual Cystic fibrosis (CF) lung infections revealed great heterogeneity of QS phenotypes and genotypes within as well as among patients. This finding suggests that a single selective mechanism, whether of social or nonsocial nature, is unlikely to explain the emergence of QS variants during CF infection.

Citation: Mellbye B, Schuster M. 2011. More than Just a Quorum: Integration of Stress and Other Environmental Cues in Acyl-Homoserine Lactone Signaling, p 349-363. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch20

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Figure 1.

Structures of selected homoserine lactone and alkylquinolone signals.

Citation: Mellbye B, Schuster M. 2011. More than Just a Quorum: Integration of Stress and Other Environmental Cues in Acyl-Homoserine Lactone Signaling, p 349-363. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch20
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Image of Figure 2.
Figure 2.

Signal integration in the acyl-HSL and AQ-QS systems of . The three QS systems and AQ are highlighted. The small circles associated with each system refer to the signal molecules 3OC12-HSL (dark gray), C4-HSL (light gray), and HHQ and PQS (white and black, respectively). Solid arrows and T bars indicate positive and negative regulation, respectively. Dotted lines indicate indirect regulation. For simplicity, only protein components are shown and regulatory effects on individual components within a QS system are generally not distinguished. LasI generates 3OC12-HSL that is bound by LasR. RsaL is activated by LasR-3OC12-HSL and acts to maintain 3OC12-HSL homeostasis by negatively regulating . LasR-3OC12-HSL activates , numerous target genes as well as the and AQ systems. RhlR binds C4-HSL generated by RhlI and activates further expression and negatively regulates the AQ-dependent QS system. Both acyl-HSL QS systems are controlled at both the transcriptional and posttranscriptional level by regulators including VqsR; GidA; and a regulatory pathway involving the two-component system GacAS, the RNA-binding protein RsmA, and the small RNA RsmZ. Vfr, a cAMP-binding protein, responds to increased cAMP production during calcium limitation and positively regulates LasR. An orphan LuxR homolog, QscR, negatively regulates acyl-HSL QS and controls other genes in response to endogenous and perhaps exogenous acyl-HSLs. In the AQ system, products of generate HHQ, which is converted to PQS by another protein, PqsH. The LysR-type regulator PqsR responds to either HHQ or PQS. AQ biosynthesis is positively regulated by PqsR. Expression of AQ-PqsR-dependent target genes can also be mediated through another component, PqsE, which is not shown. The response regulator PhoB regulates transcription of during phosphate-limiting conditions. Under iron-limiting conditions, Fur indirectly affects PQS production through de-repression of two small RNAs. Starvation and stress conditions lead to induction of the stringent response and RpoS that directly and indirectly control QS gene expression.

Citation: Mellbye B, Schuster M. 2011. More than Just a Quorum: Integration of Stress and Other Environmental Cues in Acyl-Homoserine Lactone Signaling, p 349-363. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch20
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References

/content/book/10.1128/9781555816841.ch20
1. Aguilar, C., I. Bertani, and, V. Venturi. 2003. Quorum-sensing system and stationary-phase sigma factor (rpoS) of the onion pathogen Burkholderia cepacia genomovar I type strain, ATCC 25416. Appl. Environ. Microbiol. 69:17391747.
2. Ahmer, B. M. 2004. Cell-to-cell signalling in Escherichia coli and Salmonella enterica. Mol. Microbiol. 52:933945.
3. Albus, A. M.,, E.C. Pesci,, L.J. Runyen-Janecky, S. E. West, and, B.H. Iglewski. 1997. Vfr controls quorum sensing in Pseudomonas aeruginosa. J. Bacteriol. 179:39283935.
4. Alvarez-Ortega, C., and, C.S. Harwood. 2007. Responses of Pseudomonas aeruginosa to low oxygen indicate that growth in the cystic fibrosis lung is by aerobic respiration. Mol. Microbiol. 65:582.
5. Anba, J.,, M. Bidaud,, M.L. Vasil, and, A. Lazdunski. 1990. Nucleotide sequence of the Pseudomonas aeruginosa phoB gene, the regulatory gene for the phosphate regulon. J. Bacteriol. 172:46854689.
6. Barnard, A. M.,, S.D. Bowden,, T. Burr,, S. J. Coulthurst,, R. E. Monson, and, G.P. Salmond. 2007. Quorum sensing, virulence and secondary metabolite production in plant soft-rotting bacteria. Philos. Trans. R. Soc. Lond. B Biol. Sci. 362:11651183.
7. Bazire, A.,, A. Dheilly,, F. Diab,, D. Morin,, M. Jebbar,, D. Haras,, and A. Dufour. 2005. Osmotic stress and phosphate limitation alter production of cell-to-cell signal molecules and rhamnolipid biosurfactant by Pseudomonas aeruginosa. FEMS Microbiol. Lett. 253:125131.
8. Beck von Bodman, S.,, G. T. Hayman, and, S.K. Farrand. 1992. Opine catabolism and conjugal transfer of the nopaline Ti plasmid pTiC58 are coordinately regulated by a single repressor. Proc. Natl. Acad. Sci. USA 89:643647.
9. Bjarnsholt, T., and, M. Givskov. 2007. The role of quorum sensing in the pathogenicity of the cunning aggressor Pseudomonas aeruginosa. Anal. Bioanal. Chem. 387:409414.
10. Bollinger, N.,, D.J. Hassett,, B.H. Iglewski,, J.W. Costerton, and, T.R. McDermott. 2001. Gene expression in Pseudomonas aeruginosa: evidence of iron override effects on quorum sensing and biofilm-specific gene regulation. J. Bacteriol. 183:19901996.
11. Boyer, M., and, F. Wisniewski-Dye. 2009. Cell-cell signalling in bacteria: not simply a matter of quorum. FEMS Microbiol. Ecol. 70:119.
12. Braeken, K.,, M. Moris,, R. Daniels, J. Vanderleyden, and, J. Michiels. 2006. New horizons for (p)ppGpp in bacterial and plant physiology. Trends Microbiol. 14:4554.
13. Bredenbruch, F.,, M. Nimtz,, V. Wray,, M. Morr,, R. Muller,, and S. Haussler. 2005. Biosynthetic pathway of Pseudomonas aeruginosa 4–hydroxy-2–alkylquinolines. J. Bacteriol. 187:36303635.
14. Bredenbruch, F.,, R. Geffers,, M. Nimtz, J. Buer, and, S. Haussler. 2006. The Pseudomonas aeruginosa quinolone signal (PQS) has an iron-chelating activity. Environ. Microbiol. 8:13181329.
15. Brint, J. M., and, D.E. Ohman. 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. 177:71557163.
16. Cabrol, S.,, A. Olliver,, G.B. Pier,, A. Andremont,, and R. Ruimy. 2003. Transcription of quorum-sensing system genes in clinical and environmental isolates of Pseudomonas aeruginosa. J. Bacteriol. 185:72227230.
17. Case, R. J.,, M. Labbate, and, S. Kjelleberg. 2008. AHL-driven quorum-sensing circuits: their frequency and function among the Proteobacteria. ISME J. 2:345349.
18. Chugani, S. A.,, M. Whiteley, K. M. Lee,, D.D. Argenio,, C. Manoil, and, E.P. Greenberg. 2001. QscR, a modulator of quorumsensing signal synthesis and virulence in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 98:27522757.
19. Comolli, J. C., and, T.J. Donohue. 2004. Differences in two Pseudomonas aeruginosa cbb3 cytochrome oxidases. Mol. Microbiol. 51:11931203.
20. Cornelis, P., S. Matthijs, and, L. Van Oeffelen. 2009. Iron uptake regulation in Pseudomonas aeruginosa. Biometals 22:1522.
21. Czaran, T., and, R.F. Hoekstra. 2009. Microbial communication, cooperation and cheating: quorum sensing drives the evolution of cooperation in bacteria. PLoS ONE 4: e6655.
22. D’Argenio, D. A.,, M. Wu,, L. R. Hoffman,, H.D. Kulasekara,, E. Deziel,, E. E. Smith,, H. Nguyen,, R. K. Ernst,, T. J. Larson Freeman,, D. H. Spencer,, M. Brittnacher,, H. S. Hayden,, S. Selgrade,, M. Klausen,, D. R. Goodlett,, J. L. Burns,, B. W. Ramsey, and, S.I. Miller. 2007. Growth phenotypes of Pseudomonas aeruginosa lasR mutants adapted to the airways of cystic fibrosis patients. Mol. Microbiol. 64:512533.
23. Davies, D. G.,, M.R. Parsek,, J.P. Pearson,, B. H. Iglewski,, J. W. Costerton, and, E.P. Greenberg. 1998. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295298.
24. de Kievit, T. R. 2009. Quorum sensing in Pseudomonas aeruginosa biofilms. Environ. Microbiol. 11:279288.
25. de Kievit, T. R.,, Y. Kakai,, J. K. Register,, E.C. Pesci, and, B.H. Iglewski. 2002. Role of the Pseudomonas aeruginosa las and rhl quorum-sensing systems in rhlI regulation. FEMS Microbiol. Lett. 212:101106.
26. Dekimpe, V., and, E. Deziel. 2009. Revisiting the quorum-sensing hierarchy in Pseudomonas aeruginosa: the transcriptional regulator RhlR regulates LasR-specific factors. Microbiology 155:712723.
27. Devine, J. H.,, G. S. Shadel, and, T.O. Baldwin. 1989. Identification of the operator of the lux regulon from the Vibrio fischeri strain ATCC7744. Proc. Natl. Acad. Sci. USA 86:56885692.
28. Deziel, E., F. Lepine,, S. Milot,, J. He,, M.N. Mindrinos,, R. G. Tompkins, and, L.G. Rahme. 2004. Analysis of Pseudomonas aeruginosa 4–hydroxy-2–alkylquinolines (HAQs) reveals a role for 4–hydroxy-2–heptylquinoline in cell-to-cell communication. Proc. Natl. Acad. Sci. USA 101:13391344.
29. Deziel, E.,, S. Gopalan,, A.P. Tampakaki,, F. Lepine,, K. E. Padfield,, M. Saucier,, G. Xiao, and, L.G. Rahme. 2005. The contribution of MvfR to Pseudomonas aeruginosa pathogenesis and quorum sensing circuitry regulation: multiple quorum sensingregulated genes are modulated without affecting lasRI, rhlRI or the production of N-acyl-L-homoserine lactones. Mol. Microbiol. 55:9981014.
30. Diggle, S. P.,, A. Gardner,, S. A. West, and, A.S. Griffin. 2007a. Evolutionary theory of bacterial quorum sensing: when is a signal not a signal? Philos. Trans. R. Soc. Lond. B Biol. Sci. 362:12411249.
31. Diggle, S. P.,, A.S. Griffin,, G.S. Campbell, and, S.A. West. 2007b. Cooperation and conflict in quorum-sensing bacterial populations. Nature 450:411414.
32. Diggle, S. P.,, K. Winzer,, A. Lazdunski,, P. Williams,, and M. Camara. 2002. Advancing the quorum in Pseudomonas aeruginosa: MvaT and the regulation of N-acylhomoserine lactone production and virulence gene expression. J. Bacteriol. 184:25762586.
33. Diggle, S. P.,, K. Winzer,, S. R. Chhabra,, K.E. Worrall,, M. Camara,, and P. Williams. 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. 50:2943.
34. Diggle, S. P.,, S. Matthijs,, V. J. Wright,, M.P. Fletcher,, S. R. Chhabra,, I. L. Lamont,, X. Kong,, R. C. Hider,, P. Cornelis,, M. Camara,, and P. Williams. 2007c. The Pseudomonas aeruginosa 4–quinolone signal molecules HHQ and PQS play multifunctional roles in quorum sensing and iron entrapment. Chem. Biol. 14:8796.
35. Duan, K., and, M.G. Surette. 2007. Environmental regulation of Pseudomonas aeruginosa PAO1 Las and Rhl quorum-sensing systems. J. Bacteriol. 189:48274836.
36. Dubern, J. F., and, S.P. Diggle. 2008. Quorum sensing by 2–alkyl-4–quinolones in Pseudomonas aeruginosa and other bacterial species. Mol. Biosyst. 4:882888.
37. Dunlap, P. V., and, E.P. Greenberg. 1988. Control of Vibrio fischeri lux gene transcription by a cyclic AMP receptor protein-LuxR protein regulatory circuit. J. Bacteriol. 170:40404046.
38. Dunlap, P. V. 1992. Mechanism for iron control of the Vibrio fischeri luminescence system: involvement of cyclic AMP and cyclic AMP receptor protein and modulation of DNA level. J. Biolumin. Chemilumin. 7:203214.
39. Dunlap, P. V., and, A. Kuo. 1992. Cell density-dependent modulation of the Vibrio fischeri luminescence system in the absence of autoinducer and LuxR protein. J. Bacteriol. 174:24402448.
40. Eberhard, A. 1972. Inhibition and activation of bacterial luciferase synthesis. J. Bacteriol. 109:11011105.
41. Eberhard, A.,, A.L. Burlingame,, C. Eberhard, G. L. Kenyon,, K.H. Nealson, and, N.J. Oppenheimer. 1981. Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry 20:24442449.
42. Eberl, L. 2006. Quorum sensing in the genus Burkholderia. Int. J. Med. Microbiol. 296:103110.
43. Engebrecht, J., K. Nealson, and, M. Silverman. 1983. Bacterial bioluminescence: isolation and genetic analysis of functions from Vibrio fischeri. Cell 32:773781.
44. Engebrecht, J., and, M. Silverman. 1984. Identification of genes and gene products necessary for bacterial bioluminescence. Proc. Natl. Acad. Sci. USA 81:41544158.
45. Ennis, H. L.,, D.N. Dao,, S.U. Pukatzki, and, R.H. Kessin. 2000. Dictyostelium amoebae lacking an F-box protein form spores rather than stalk in chimeras with wild type. Proc. Natl. Acad. Sci. USA 97:32923297.
46. Erickson, D. L.,, J.L. Lines,, E.C. Pesci, V. Venturi, and, D.G. Storey. 2004. Pseudomonas aeruginosa relA contributes to virulence in Drosophila melanogaster. Infect. Immun. 72:56385645.
47. Farrow, J. M.,, 3rd, Z.M. Sund,, M.L. Ellison,, D. S. Wade, J. P. Coleman, and, E.C. Pesci. 2008. PqsE functions independently of PqsR-Pseudomonas quinolone signal and enhances the rhl quorum-sensing system. J. Bacteriol. 190:70437051.
48. Ferluga, S., and, V. Venturi. 2009. OryR is a LuxR-family protein involved in interkingdom signaling between pathogenic Xanthomonas oryzae pv. oryzae and rice. J. Bacteriol. 191:890897.
49. Foster, K. R., K. Parkinson, and, C.R. Thompson. 2007. What can microbial genetics teach sociobiology? Trends Genet. 23:7480.
50. Fothergill, J. L.,, S. Panagea,, C. A. Hart,, M.J. Walshaw,, T. L. Pitt,, and C. Winstanley. 2007. Widespread pyocyanin over-production among isolates of a cystic fibrosis epidemic strain. BMC Microbiol. 7:45.
51. Fujita, M.,, K. Tanaka,, H. Takahashi, and, A. Amemura. 1994. Transcription of the principal sigma-factor genes, rpoD and rpoS, in Pseudomonas aeruginosa is controlled according to the growth phase. Mol Microbiol 13:10711077.
52. Fuqua, C., and, E.P. Greenberg. 2002. Listening in on bacteria: acylhomoserine lactone signalling. Nat. Rev. Mol. Cell. Biol. 3:685695.
53. Fuqua, W. C.,, S. C. Winans, and, E.P. Greenberg. 1994. Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J. Bacteriol. 176:269275.
54. Gallagher, L. A.,, S.L. McKnight,, M.S. Kuznetsova,, E. C. Pesci,, and C. Manoil. 2002. Functions required for extracellular quinolone signaling by Pseudomonas aeruginosa. J. Bacteriol. 184:64726480.
55. Gambello, M. J., and, B.H. Iglewski. 1991. Cloning and characterization of the Pseudomonas aeruginosa lasR gene, a transcriptional activator of elastase expression. J. Bacteriol. 173:30003009.
56. Gentry, D. R., and, M. Cashel. 1996. Mutational analysis of the Escherichia coli spoT gene identifies distinct but overlapping regions involved in ppGpp synthesis and degradation. Mol. Microbiol. 19:13731384.
57. Gilbert, K. B.,, T.H. Kim,, R. Gupta,, E. P. Greenberg,, and M. Schuster. 2009. Global position analysis of the Pseudomonas aeruginosa quorum-sensing transcription factor LasR. Mol. Microbiol. 73:10721085.
58. Girard, G., and, G.V. Bloemberg. 2008. Central role of quorum sensing in regulating the production of pathogenicity factors in Pseudomonas aeruginosa. Future Microbiol. 3:97106.
59. Gooderham, W. J., and, R.E. Hancock. 2009. Regulation of virulence and antibiotic resistance by two-component regulatory systems in Pseudomonas aeruginosa. FEMS Microbiol. Rev. 33:279294.
60. Greig, D., and, M. Travisano. 2004. The Prisoner’s Dilemma and polymorphism in yeast SUC genes. Proc. Biol. Sci. 271: S2526.
61. Griffin, A. S.,, S.A. West, and, A. Buckling. 2004. Cooperation and competition in pathogenic bacteria. Nature 430:10241027.
62. Gupta, R.,, T.R. Gobble, and, M. Schuster. 2009. GidA posttranscriptionally regulates rhl quorum sensing in Pseudomonas aeruginosa. J. Bacteriol. 191: 57855792.
63. Hall-Stoodley, L.,, J.W. Costerton, and, P. Stoodley. 2004. Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2:95108.
64. Hamilton, W. D. 1964. The genetical evolution of social behaviour 1 & 2. J. Theor. Biol. 7:152.
65. Hanzelka, B. L., and, E.P. Greenberg. 1996. Quorum sensing in Vibrio fischeri: evidence that S-adenosylmethionine is the amino acid substrate for autoinducer synthesis. J. Bacteriol. 178:52915294.
66. Hengge, R. 2008. The two-component network and the general stress sigma factor RpoS (sigma S) in Escherichia coli. Adv. Exp. Med. Biol. 631:4053.
67. Hense, B. A.,, C. Kuttler,, J. Muller,, M. Rothballer, A. Hartmann, and, J.U. Kreft. 2007. Does efficiency sensing unify diffusion and quorum sensing? Nat. Rev. Microbiol. 5:230239.
68. Hentzer, M.,, 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. Hoiby,, and M. Givskov. 2003. Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J. 22:38033815.
69. Heurlier, K., V. Denervaud, and, D. Haas. 2006. Impact of quorum sensing on fitness of Pseudomonas aeruginosa. Int. J. Med. Microbiol. 296:93102.
70. Heurlier, K.,, V. Denervaud,, M. Haenni,, L. Guy,, V. Krishnapillai,, and D. Haas. 2005. Quorum-sensing-negative (lasR) mutants of Pseudomonas aeruginosa avoid cell lysis and death. J. Bacteriol. 187:48754883.
71. Hoffman, L. R.,, H.D. Kulasekara,, J. Emerson,, L. S. Houston,, J. L. Burns,, B. W. Ramsey, and, S.I. Miller. 2009. Pseudomonas aeruginosa lasR mutants are associated with cystic fibrosis lung disease progression. J. Cyst. Fibros. 8:6670.
72. Huber, B.,, K. Riedel,, M. Kothe,, M. Givskov,, S. Molin,, and L. Eberl. 2002. Genetic analysis of functions involved in the late stages of biofilm development in Burkholderia cepacia H111. Mol. Microbiol. 46:411426.
73. Hunt, T. A.,, W.T. Peng,, I. Loubens, and, D.G. Storey. 2002. The Pseudomonas aeruginosa alternative sigma factor PvdS controls exotoxin A expression and is expressed in lung infections associated with cystic fibrosis. Microbiology 148:31833193.
74. Jensen, V.,, D. Lons,, C. Zaoui,, F. Bredenbruch,, A. Meissner,, G. Dieterich,, R. Munch,, and S. Haussler. 2006. RhlR expression in Pseudomonas aeruginosa is modulated by the Pseudomonas quinolone signal via PhoB-dependent and -independent pathways. J. Bacteriol. 188:86018606.
75. Jorgensen, F., M. Bally,, V. Chapon-Herve, G. Michel,, A. Lazdunski, P. Williams, and, G.S. Stewart. 1999. RpoS-dependent stress tolerance in Pseudomonas aeruginosa. Microbiology 145:835844.
76. Juhas, M., L. Eberl, and, B. Tummler. 2005. Quorum sensing: the power of cooperation in the world of Pseudomonas. Environ. Microbiol. 7:459471.
77. Juhas, M.,, L. Wiehlmann,, B. Huber,, D. Jordan,, J. Lauber,, P. Salunkhe,, A. S. Limpert,, F. von Gotz,, I. Steinmetz,, L. Eberl,, and B. Tummler. 2004. Global regulation of quorum sensing and virulence by VqsR in Pseudomonas aeruginosa. Microbiology 150:831841.
78. Kanack, K. J.,, L.J. Runyen-Janecky,, E.P. Ferrell,, S. J. Suh, and, S.E. West. 2006. Characterization of DNA-binding specificity and analysis of binding sites of the Pseudomonas aeruginosa global regulator, Vfr, a homologue of the Escherichia coli cAMP receptor protein. Microbiology 152:34853496.
79. Kaplan, H. B., and, E.P. Greenberg. 1985. Diffusion of autoinducer is involved in regulation of the Vibrio fischeri luminescence system. J. Bacteriol. 163:12101214.
80. Keller, L., and, M.G. Surette. 2006. Communication in bacteria: an ecological and evolutionary perspective. Nat. Rev. Microbiol. 4:249258.
81. Kim, E. J.,, W. Wang,, W. D. Deckwer, and, A.P. Zeng. 2005. 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 151:11271138.
82. Kiratisin, P.,, K.D. Tucker, and, L. Passador. 2002. LasR, a transcriptional activator of Pseudomonas aeruginosa virulence genes, functions as a multimer. J. Bacteriol. 184:49124919.
83. Kirisits, M. J., and, M.R. Parsek. 2006. Does Pseudomonas aeruginosa use intercellular signalling to build biofilm communities? Cell. Microbiol. 8:18411849.
84. Kohler, T., A. Buckling, and, C. van Delden. 2009. Cooperation and virulence of clinical Pseudomonas aeruginosa populations. Proc. Natl. Acad. Sci. USA 106:63396344.
85. Kulasekara, B. R., and, S. Lory. 2004. The genome of Pseudomonas aeruginosa. In J. L. Ramos (ed), Pseudomonas: Genome, Life Style and Molecular Architecture, Vol. 1. Kluwer Academic, New York, NY.
86. Lamarche, M. G.,, B.L. Wanner,, S. Crepin,, and J. Harel. 2008. The phosphate regulon and bacterial virulence: a regulatory network connecting phosphate homeostasis and pathogenesis. FEMS Microbiol. Rev. 32:461473.
87. Lapouge, K.,, M. Schubert,, F.H. Allain, and, D. Haas. 2008. Gac/Rsm signal transduction pathway of gamma-proteobacteria: from RNA recognition to regulation of social behaviour. Mol. Microbiol. 67:241253.
88. Latifi, A.,, M. Foglino,, K. Tanaka, P. Williams, and, A. Lazdunski. 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. 21:11371146.
89. Latifi, A.,, M.K. Winson,, M. Foglino,, B. W. Bycroft,, G.S. Stewart,, A. Lazdunski,, and P. Williams. 1995. Multiple homologues of LuxR and LuxI control expression of virulence determinants and secondary metabolites through quorum sensing in Pseudomonas aeruginosa PAO1. Mol. Microbiol. 17:333343.
90. Lee, J. H., Y. Lequette, and, E.P. Greenberg. 2006. Activity of purified QscR, a Pseudomonas aeruginosa orphan quorum-sensing transcription factor. Mol. Microbiol. 59:602609.
91. Leoni, L.,, N. Orsi,, V. de Lorenzo, and, P. Visca. 2000. Functional analysis of PvdS, an iron starvation sigma factor of Pseudomonas aeruginosa. J. Bacteriol. 182:14811491.
92. Lequette, Y.,, J. H. Lee,, F. Ledgham,, A. Lazdunski, and, E.P. Greenberg. 2006. A distinct QscR regulon in the Pseudomonas aeruginosa quorum-sensing circuit. J. Bacteriol. 188:33653370.
93. Lesprit, P.,, F. Faurisson,, O. Join-Lambert,, F. Roudot-Thoraval,, M. Foglino,, C. Vissuzaine,, and C. Carbon. 2003. Role of the quorum-sensing system in experimental pneumonia due to Pseudomonas aeruginosa in rats. Am. J. Respir. Crit. Care Med. 167:14781482.
94. Mangan, S., A. Zaslaver, and, U. Alon. 2003. The coherent feedforward loop serves as a sign-sensitive delay element in transcription networks. J. Mol. Biol. 334:197204.
95. McGrath, S.,, D. S. Wade, and, E.C. Pesci. 2004. Dueling quorum sensing systems in Pseudomonas aeruginosa control the production of the Pseudomonas quinolone signal (PQS). FEMS Microbiol. Lett. 230:2734.
96. McIntosh, M., S. Meyer, and, A. Becker. 2009. Novel Sinorhizobium meliloti quorum sensing positive and negative regulatory feedback mechanisms respond to phosphate availability. Mol. Microbiol. 74:12381256.
97. McKnight, S. L., B. H. Iglewski, and, E.C. Pesci. 2000. The Pseudomonas quinolone signal regulates rhl quorum sensing in Pseudomonas aeruginosa. J. Bacteriol. 182:27022708.
98. Medina, G.,, K. Juarez,, R. Diaz, and, G. Soberon-Chavez. 2003a. Transcriptional regulation of Pseudomonas aeruginosa rhlR, encoding a quorum-sensing regulatory protein. Microbiology 149:30733081.
99. Medina, G., K. Juarez, and, G. Soberon-Chavez. 2003b. The Pseudomonas aeruginosa rhlAB operon is not expressed during the logarithmic phase of growth even in the presence of its activator RhlR and the autoinducer N-butyryl-homoserine lactone. J. Bacteriol. 185:377380.
100. Medina, G.,, K. Juarez,, B. Valderrama, and, G. Soberon-Chavez. 2003c. Mechanism of Pseudomonas aeruginosa RhlR transcriptional regulation of the rhlAB promoter. J. Bacteriol. 185:59765983.
101. More, M. I.,, L.D. Finger,, J.L. Stryker,, C. Fuqua,, A. Eberhard, and, S.C. Winans. 1996. Enzymatic synthesis of a quorum-sensing autoinducer through use of defined substrates. Science 272:16551658.
102. Moreau-Marquis, S.,, B. A. Stanton, and, G.A. O’Toole. 2008. Pseudomonas aeruginosa biofilm formation in the cystic fibrosis airway. Pulm. Pharmacol. Ther. 21:595599.
103. Nealson, K. H., and, J.W. Hastings. 1979. Bacterial bioluminescence: its control and ecological significance. Microbiol. Rev. 43:496518.
104. Nealson, K. H.,, T. Platt, and, C. Hastings. 1970. Cellular control of the synthesis and activity of the bacterial luminescent system. J. Bacteriol. 104:313322.
105. Ochsner, U. A.,, A. Fiechter, and, J. Reiser. 1994a. Isolation, characterization, and expression in Escherichia coli of the Pseudomonas aeruginosa rhlAB genes encoding a rhamnosyltransferase involved in rhamnolipid biosurfactant synthesis. J. Biol. Chem. 269:1978719795.
106. Ochsner, U. A.,, A.K. Koch,, A. Fiechter,, and J. Reiser. 1994b. Isolation and characterization of a regulatory gene affecting rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. J. Bacteriol. 176:20442054.
107. Ochsner, U. A., and, J. Reiser. 1995. Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 92:64246428.
108. Ochsner, U. A.,, P.J. Wilderman,, A.I. Vasil, and, M.L. Vasil. 2002. GeneChip expression analysis of the iron starvation response in Pseudomonas aeruginosa: identification of novel pyover-dine biosynthesis genes. Mol. Microbiol. 45:12771287.
109. Oglesby, A. G.,, J.M. Farrow 3rd,, J.H. Lee, A. P., Tomaras, E.P., Greenberg, E., C. Pesci, and, M.L. Vasil. 2008. The influence of iron on Pseudomonas aeruginosa physiology: a regulatory link between iron and quorum sensing. J. Biol. Chem. 283:1555815567.
110. Passador, L.,, J.M. Cook,, M.J. Gambello,, L. Rust, and, B.H. Iglewski. 1993. Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication. Science 260:11271130.
111. Patankar, A. V., and, J.E. Gonzalez. 2009. Orphan LuxR regulators of quorum sensing. FEMS Microbiol. Rev. 33:739756.
112. Pearson, J. P., C. Van Delden, and, B.H. Iglewski. 1999. Active efflux and diffusion are involved in transport of Pseudomonas aeruginosa cell-to-cell signals. J. Bacteriol. 181:12031210.
113. Pearson, J. P.,, K.M. Gray,, L. Passador,, K. D. Tucker,, A. Eberhard,, B. H. Iglewski, and, E.P. Greenberg. 1994. Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes. Proc. Natl. Acad. Sci. USA 91:197201.
114. Pearson, J. P.,, L. Passador,, B. H. Iglewski, and, E.P. Greenberg. 1995. A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 92:14901494.
115. Pearson, J. P.,, M. Feldman,, B.H. Iglewski, and, A. Prince. 2000. Pseudomonas aeruginosa cell-to-cell signaling is required for virulence in a model of acute pulmonary infection. Infect. Immun. 68:43314334.
116. Pesci, E. C.,, J.B. Milbank,, J.P. Pearson, S., McKnight, A.S., Kende, E., P. Greenberg, and, B.H. Iglewski. 1999. Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 96:1122911234.
117. Pesci, E. C.,, J.P. Pearson,, P.C. Seed, and, B.H. Iglewski. 1997. Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J. Bacteriol. 179:31273132.
118. Pessi, G., and, D. Haas. 2000. Transcriptional control of the hydrogen cyanide biosynthetic genes hcnABC by the anaerobic regulator ANR and the quorum-sensing regulators LasR and RhlR in Pseudomonas aeruginosa. J. Bacteriol. 182:69406949.
119. Potrykus, K., and, M. Cashel. 2008. (p)ppGpp:still magical? Annu. Rev. Microbiol. 62:3551.
120. Ray, A., and, H.D. Williams. 1997. The effects of mutation of the anr gene on the aerobic respiratory chain of Pseudomonas aeruginosa. FEMS Microbiol. Lett. 156:227232.
121. Redfield, R. J. 2002. Is quorum sensing a side effect of diffusion sensing? Trends Microbiol. 10:365370.
122. Ruby, E. G., and, M.J. McFall-Ngai. 1992. A squid that glows in the night: development of an animal-bacterial mutualism. J. Bacteriol. 174:48654870.
123. Rumbaugh, K. P., J. A. Griswold, and, A.N. Hamood. 2000. The role of quorum sensing in the in vivo virulence of Pseudomonas aeruginosa. Microbes Infect. 2:17211731.
124. Rumbaugh, K. P.,, J.A. Griswold,, B.H. Iglewski, and, A.N. Hamood. 1999. Contribution of quorum sensing to the virulence of Pseudomonas aeruginosa in burn wound infections. Infect. Immun. 67:58545862.
125. Rumbaugh, K. P.,, S.P. Diggle,, C.M. Watters, A. Ross-Gillespie, A. S. Griffin, and, S.A. West. 2009. Quorum sensing and the social evolution of bacterial virulence. Curr. Biol. 19:341345.
126. Sanchez-Contreras, M.,, W.D. Bauer,, M. Gao, J. B. Robinson, and, J. Allan Downie. 2007. Quorum-sensing regulation in rhizobia and its role in symbiotic interactions with legumes. Philos. Trans. R. Soc. Lond. B 362:11491163.
127. Sandoz, K., S. Mitzimberg, and, M. Schuster. 2007. Social cheating in Pseudomonas aeruginosa quorum sensing. Proc. Natl. Acad. Sci. USA 104:1587615881.
128. Schaefer, A. L.,, E.P. Greenberg,, C.M. Oliver, Y., Oda, J.J., Huang, G., Bittan-Banin, C. M., Peres, S., Schmidt, K., Juhaszova, J., R. Sufrin, and, C.S. Harwood. 2008. A new class of homoserine lactone quorum-sensing signals. Nature 454:595599.
129. Schuster, M.,, A. C. Hawkins,, C. S. Harwood, and, E.P. Greenberg. 2004a. The Pseudomonas aeruginosa RpoS regulon and its relationship to quorum sensing. Mol. Microbiol. 51:973985.
130. Schuster, M., and, E.P. Greenberg. 2006. A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Int. J. Med. Microbiol. 296:7381.
131. Schuster, M., and, E.P. Greenberg. 2007. Early activation of quorum sensing in Pseudomonas aeruginosa reveals the architecture of a complex regulon. BMC Genomics 8:287.
132. Schuster, M.,, C. P. Lohstroh,, T. Ogi, and, E.P. Greenberg. 2003. Identification, timing and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J. Bacteriol. 185:20662079.
133. Schuster, M.,, M. L. Urbanowski, and, E.P. Greenberg. 2004b. Promoter specificity in Pseudomonas aeruginosa quorum sensing revealed by DNA binding of purified LasR. Proc. Natl. Acad. Sci. USA 101:1583315839.
134. Seed, P. C., L. Passador, and, B.H. Iglewski. 1995. Activation of the Pseudomonas aeruginosa lasI gene by LasR and the Pseudomonas autoinducer PAI:an autoinduction regulatory hierarchy. J. Bacteriol. 177:654659.
135. Shompole, S.,, K.T. Henon,, L.E. Liou,, K. Dziewanowska, G. A. Bohach, and, K.W. Bayles. 2003. Biphasic intracellular expression of Staphylococcus aureus virulence factors and evidence for Agrmediated diffusion sensing. Mol. Microbiol. 49:919927.
136. Smith, E. E.,, D.G. Buckley,, Z. Wu,, C. Saenphimmachak,, L.R. Hoffman,, D. A. D’Argenio,, S. I. Miller,, B.W. Ramsey,, D. P, Speert,, S.M. Moskowitz,, J.L. Burns,, R. Kaul, and, M.V. Olson. 2006. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc. Natl. Acad. Sci. USA 103:84878492.
137. Smith, J. N.,, J.L. Dyszel,, J.A. Soares,, C. D. Ellermeier,, C. Altier,, S. D. Lawhon,, L.G. Adams,, V. Konjufca,, R., Curtiss 3rd, J. M., Slauch, and B.M., Ahmer. 2008. SdiA, an N-acylhomoserine lactone receptor, becomes active during the transit of Salmonella enterica through the gastrointestinal tract of turtles. PLoS ONE 3: e2826.
138. Smith, R. S., and, B.H. Iglewski. 2003. P. aeruginosa quorum-sensing systems and virulence. Curr. Opin. Microbiol. 6:5660.
139. Smith, R. S.,, M.C. Wolfgang, and, S. Lory. 2004. An adenylate cyclase-controlled signaling network regulates Pseudomonas aeruginosa virulence in a mouse model of acute pneumonia. Infect. Immun. 72:16771684.
140. Spira, B., N. Silberstein, and, E. Yagil. 1995. Guanosine 3′,5′-bispyrophosphate (ppGpp) synthesis in cells of Escherichia coli starved for Pi. J. Bacteriol. 177:40534058.
141. Stevens, A. M., and, E.P. Greenberg. 1997. Quorum sensing in Vibrio fischeri: essential elements for activation of the luminescence genes. J. Bacteriol. 179:557562.
142. Stover, C. K.,, X.Q. Pham,, A.L. Erwin,, S. D. Mizoguchi,, P. Warrener,, M. J. Hickey,, F.S. Brinkman,, W.O. Hufnagle,, D.J. Kowalik,, M. Lagrou,, R. L. Garber,, L. Goltry,, E. Tolentino,, S. Westbrock-Wadman,, Y. Yuan,, L.L. Brody,, S.N. Coulter,, K.R. Folger,, A. Kas,, K. Larbig,, R. Lim,, K. Smith,, D. Spencer,, G. K. Wong,, Z. Wu, and, I.T. Paulsen. 2000. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406:947948.
143. Subramoni, S., and, V. Venturi. 2009. LuxR-family ‘solos’: bachelor sensors/regulators of signalling molecules. Microbiology 155:13771385.
144. Suh, S. J.,, L. Silo-Suh, D. E. Woods,, D.J. Hassett, S. E. West, and, D.E. Ohman. 1999. Effect of rpoS mutation on the stress response and expression of virulence factors in Pseudomonas aeruginosa. J. Bacteriol. 181:38903897.
145. Tingpej, P.,, L. Smith,, B. Rose,, H. Zhu,, T. Conibear,, K. Al Nassafi,, J. Manos,, M. Elkins,, P. Bye,, M. Willcox,, S. Bell,, C. Wainwright,, and C. Harbour. 2007. Phenotypic characterization of clonal and nonclonal Pseudomonas aeruginosa strains isolated from lungs of adults with cystic fibrosis. J. Clin. Microbiol. 45:16971704.
146. Typas, A., G. Becker, and, R. Hengge. 2007. The molecular basis of selective promoter activation by the sigmaS subunit of RNA polymerase. Mol Microbiol 63:12961306.
147. Urbanowski, M. L., C. P. Lostroh, and, E.P. Greenberg. 2004. Reversible acyl-homoserine lactone binding to purified Vibrio fischeri LuxR protein. J. Bacteriol. 186:631637.
148. van Delden, C.,, E. C. Pesci,, J., P. Pearson, and, B.H. Iglewski. 1998. Starvation selection restores elastase and rhamnolipid production in a Pseudomonas aeruginosa quorum-sensing mutant. Infect. Immun. 66:44994502.
149. van Delden, C., R. Comte, and, A.M. Bally. 2001. Stringent response activates quorum sensing and modulates cell density-dependent gene expression in Pseudomonas aeruginosa. J. Bacteriol. 183:53765384.
150. Vasil, M. L. 2003. DNA microarrays in analysis of quorum sensing: strengths and limitations. J. Bacteriol. 185:20612065.
151. Velicer, G. J., L. Kroos, and, R.E. Lenski. 2000. Developmental cheating in the social bacterium Myxococcus xanthus. Nature 404:598601.
152. Venturi, V. 2006. Regulation of quorum sensing in Pseudomonas. FEMS Microbiol. Rev. 30:274291.
153. Venturi, V.,, A. Friscina,, I. Bertani,, G. Devescovi, and, C. Aguilar. 2004. Quorum sensing in the Burkholderia cepacia complex. Res. Microbiol. 155:238244.
154. Venturi, V., and, S. Subramoni. 2009. Future research trends in the major chemical language of bacteria. HFSP J. 3:105116.
155. Wade, D. S.,, M.W. Calfee,, E.R. Rocha,, E. A. Ling,, E. Engstrom,, J. P. Coleman, and, E.C. Pesci. 2005. Regulation of Pseudomonas quinolone signal synthesis in Pseudomonas aeruginosa. J. Bacteriol. 187:43724380.
156. Wagner, V. E., and, B.H. Iglewski. 2008. P. aeruginosa biofilms in CF infection. Clin. Rev. Allergy Immunol. 35:124134.
157. Wagner, V. E.,, D. Bushnell,, L. Passador,, A.I. Brooks, and, B.H. Iglewski. 2003. Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment. J. Bacteriol. 185:20802095.
158. West, S. A.,, A.S. Griffin,, A. Gardner, and, S.P. Diggle. 2006. Social evolution theory for microorganisms. Nat. Rev. Microbiol. 4:597607.
159. Whitchurch, C. B.,, S.A. Beatson,, J.C. Comolli,, T. Jakobsen,, J.L. Sargent,, J. J., Bertrand,, J. West,, M. Klausen,, L.L. Waite,, P.J. Kang,, T. Tolker-Nielsen,, J. S. Mattick, and, J.N. Engel. 2005. Pseudomonas aeruginosa fimL regulates multiple virulence functions by intersecting with Vfr-modulated pathways. Mol. Microbiol. 55:13571378.
160. White, C. E., and, S.C. Winans. 2007. Cell-cell communication in the plant pathogen Agrobacterium tumefaciens. Philos. Trans. R. Soc. Lond. B Biol. Sci. 362:11351148.
161. Whitehead, N. A.,, A.M. Barnard,, H. Slater, N. J. Simpson, and, G.P. Salmond. 2001. Quorum-sensing in Gram-negative bacteria. FEMS Microbiol. Rev. 25:365404.
162. Whiteley, M.,, K. M. Lee, and, E.P. Greenberg. 1999. Identification of genes controlled by quorum sensing in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 96:1390413909.
163. Wilder, C. N.,, G. Allada, and, M. Schuster. 2009. Instantaneous within-patient diversity of Pseudomonas aeruginosa quorum-sensing populations from cystic fibrosis lung infections. Infect. Immun. 77:56315639.
164. Wilderman, P. J.,, N.A. Sowa,, D.J. FitzGerald,, P. C. FitzGerald,, S. Gottesman,, U. A. Ochsner, and, M.L. Vasil. 2004. Identification of tandem duplicate regulatory small RNAs in Pseudomonas aeruginosa involved in iron homeostasis. Proc. Natl. Acad. Sci. USA 101:97929797.
165. Williams, P.,, K. Winzer,, W.C. Chan, and, M. Camara. 2007. Look who’s talking:communication and quorum sensing in the bacterial world. Philos. Trans. R. Soc. Lond. B Biol. Sci. 362:11191134.
166. Williams, P., and, M. Camara. 2009. Quorum sensing and environmental adaptation in Pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules. Curr. Opin. Microbiol. 12:182191.
167. Winson, M. K.,, M. Camara,, A. Latifi,, M. Foglino,, S. R. Chhabra,, M. Daykin,, M. Bally,, V. Chapon,, G. P. Salmond,, B. W. Bycroft,, A. Lazdunski,, G. S. A. B. Stewart,, and P. Williams. 1995. Multiple N-acyl-L-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 92:94279431.
168. Winzer, K.,, C. Falconer,, N.C. Garber,, S.P. Diggle,, M. Camara,, and P. Williams. 2000. The Pseudomonas aeruginosa lectins PA-IL and PA-IIL are controlled by quorum sensing and by RpoS. J. Bacteriol. 182:64016411.
169. Wolfgang, M. C.,, V.T. Lee,, M.E. Gilmore,, and S. Lory. 2003. Coordinate regulation of bacterial virulence genes by a novel adenylate cyclase-dependent signaling pathway. Dev. Cell 4:253263.
170. Wu, H.,, Z. Song,, M. Givskov,, G. Doring,, D. Worlitzsch,, K. Mathee,, J. Rygaard,, and N. Hoiby. 2001. Pseudomonas aeruginosa mutations in lasI and rhlI quorum sensing systems result in milder chronic lung infection. Microbiology 147:11051113.
171. Xiao, G., E. Deziel,, J. He,, F. Lepine,, B. Lesic, M. H., Castonguay, S., Milot, A. P., Tampakaki, S., E. Stachel, and, L.G. Rahme. 2006. MvfR, a key Pseudomonas aeruginosa pathogenicity LTTR-class regulatory protein, has dual ligands. Mol. Microbiol. 62:16891699.
172. Yarwood, J. M., E. M. Volper, and, E.P. Greenberg. 2005. Delays in Pseudomonas aeruginosa quorum-controlled gene expression are conditional. Proc. Natl. Acad. Sci. USA 102:90089013.
173. Yu, S.,, V. Jensen,, J. Seeliger,, I. Feldmann,, S. Weber,, E. Schleicher,, S. Haussler,, and W. Blankenfeldt. 2009. Structure elucidation and preliminary assessment of hydrolase activity of PqsE, the Pseudomonas quinolone signal (PQS) response protein. Biochemistry 48:1029810307.
174. Zaborin, A.,, K. Romanowski,, S. Gerdes,, C. Holbrook,, F. Lepine,, J. Long,, V. Poroyko,, S. P. Diggle,, A. Wilke,, K. Righetti,, I. Morozova,, T. Babrowski,, D.C. Liu,, O. Zaborina, and, J.C. Alverdy. 2009. Red death in Caenorhabditis elegans caused by Pseudomonas aeruginosa PAO1. Proc. Natl. Acad. Sci. USA 106:63276332.
175. Zhang, L.,, Y. Jia,, L. Wang, and, R. Fang. 2007. A proline iminopeptidase gene upregulated in planta by a LuxR homologue is essential for pathogenicity of Xanthomonas campestris pv. campestris. Mol. Microbiol. 65:121136.
176. Zhu, J., and, S.C. Winans. 1999. Autoinducer binding by the quorum-sensing regulator TraR increases affinity for target promoters in vitro and decreases TraR turnover rates in whole cells. Proc. Natl. Acad. Sci. USA 96:48324837.

Tables

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Table 1.

Examples of signal integration in acyl-HSL QS systems

Citation: Mellbye B, Schuster M. 2011. More than Just a Quorum: Integration of Stress and Other Environmental Cues in Acyl-Homoserine Lactone Signaling, p 349-363. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch20

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