Specificity and complexity in bacterial quorum-sensing systemsa

FEMS Microbiology Reviews

Volumn 40, Issue 5, 2016, Pages 738-752

  Hawver, Lisa A ^a   Jung, Sarah A ^a,b   Ng, Wai Leung ^a,b  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TUFTS UNIVERSITY   (United States)

Author keywords

Chemical signaling; Gene expression; Group behavior; Intercellular communication; Regulatory network

Indexed keywords

BEHAVIOR; CELL COMMUNICATION; CELL DENSITY; QUORUM SENSING; RECOGNITION; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM; GENE EXPRESSION REGULATION; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

LUXR AUTOINDUCER BINDING PROTEINS; REPRESSOR PROTEIN; TRANSACTIVATOR PROTEIN;

BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; GENE EXPRESSION REGULATION, BACTERIAL; QUORUM SENSING; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS;

EID: 84991030114     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1093/femsre/fuw014     Document Type: Review

References (184)

1. Aggarwal C, Jimenez JC, Nanavati D et al. Multiple length peptide-pheromone variants produced by Streptococcus pyogenes directly bind Rgg proteins to confer transcriptional regulation. J Biol Chem 2014;289:22427-36.
2. Anetzberger C, Schell U, Jung K. Single cell analysis of Vibrio harveyi uncovers functional heterogeneity in response to quorum sensing signals. BMC Microbiology 2012;12:209.
3. Aravind L, Anantharaman V, Balaji S et al. The many faces of the helix-turn-helix domain: transcription regulation and beyond. FEMS Microbiol Rev 2005;29:231-62.
4. August PR, Grossman TH, Minor C et al. Sequence analysis and functional characterization of the violacein biosynthetic pathway from Chromobacterium violaceum. J Mol Microb Biotech 2000;2:513-9.
5. Bae T, Clerc-Bardin S, Dunny GM. Analysis of expression of prgX, a key negative regulator of the transfer of the Enterococcus faecalis pheromone-inducible plasmid pCF10. J Mol Biol 2000;297:861-75.
6. Bannoehr J, Ben Zakour NL, Waller AS et al. Population genetic structure of the Staphylococcus intermedius group: insights into agr diversification and the emergence of methicillinresistant strains. J Bacteriol 2007;189:8685-92.
7. Bassler B, Vogel J. Bacterial regulatory mechanisms: the gene and beyond. Curr Opin Microbiol 2013;16:109-11.
8. Bassler BL, Wright M, Showalter RE et al. Intercellular signalling in Vibrio harveyi: sequence and function of genes regulating expression of luminescence. Mol Microbiol 1993;9: 773-86.
9. Bassler BL, WrightM, Silverman MR.Multiple signalling systems controlling expression of luminescence in Vibrio harveyi: sequence and function of genes encoding a second sensory pathway. Mol Microbiol 1994;13:273-86.
10. Bischofs IB, Hug JA, Liu AWet al. Complexity in bacterial cell-cell communication: quorum signal integration and subpopulation signaling in the Bacillus subtilis phosphorelay. P Natl Acad Sci USA 2009;106:6459-64.
11. Blatch GL, Lassle M. The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. Bioessays 1999;21:932-9.
12. Boettcher KJ, Ruby EG. Detection and quantification of Vibrio fischeri autoinducer from symbiotic squid light organs. J Bacteriol 1995;177:1053-8.
13. Boisset S, Geissmann T, Huntzinger E et al. Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism. Gene Dev 2007;21:1353-66.
14. Bottomley MJ, Muraglia E, Bazzo R et al. Molecular insights into quorum sensing in the human pathogen Pseudomonas aeruginosa fromthe structure of the virulence regulator LasR bound to its autoinducer. J Biol Chem 2007;282:13592-600.
15. Bouillaut L, Perchat S, Arold S et al. Molecular basis for groupspecific activation of the virulence regulator PlcR by PapR heptapeptides. Nucleic Acids Res 2008;36:3791-801.
16. Brachmann AO, Brameyer S, Kresovic D et al. Pyrones as bacterial signaling molecules. Nat Chem Biol 2013;9:573-8.
17. Brameyer S, Heermann R. Specificity of Signal-Binding via Non-AHL LuxR-Type Receptors. PLoS One 2015;10:e0124093.
18. Brint JM, Ohman DE. 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 1995;177:7155-63.
19. Cao JG, Meighen EA. Purification and structural identification of an autoinducer for the luminescence system of Vibrio harveyi. J Biol Chem 1989;264:21670-6.
20. Chang JC, LaSarre B, Jimenez JC et al. Two group A streptococcal peptide pheromones act through opposing Rgg regulators to control biofilm development. PLoS Pathog 2011;7: e1002190.
21. Chen G, Swem LR, Swem DL et al. A strategy for antagonizing quorum sensing. Mol Cell 2011;42:199-209.
22. Chen LC, Tsou LT, Chen FJ. Ligand-receptor recognition for activation of quorum sensing in Staphylococcus aureus. J Microbiol 2009;47:572-81.
23. Chen X, Schauder S, Potier N et al. Structural identification of a bacterial quorum-sensing signal containing boron. Nature 2002;415:545-9.
24. Choi SH, Greenberg EP. The C-terminal region of the Vibrio fischeri LuxR protein contains an inducer-independent lux gene activating domain. P Natl Acad Sci USA 1991;88:11115-9.
25. Choi SH, Greenberg EP. Genetic dissection of DNA binding and luminescence gene activation by the Vibrio fischeri LuxR protein. J Bacteriol 1992;174:4064-9.
26. Christie PJ. Agrobacterium tumefaciens T-complex transport apparatus: a paradigm for a new family of multifunctional transporters in eubacteria. J Bacteriol 1997;179:3085-94.
27. Chugani SA, Whiteley M, Lee KM et al. QscR, a modulator of quorum-sensing signal synthesis and virulence in Pseudomonas aeruginosa. P Natl Acad Sci USA 2001;98:2752-7.
28. Collins CH, Arnold FH, Leadbetter JR. Directed evolution of Vibrio fischeri LuxR for increased sensitivity to a broad spectrum of acyl-homoserine lactones. Mol Microbiol 2005;55:712-23.
29. Collins CH, Leadbetter JR, Arnold FH. Dual selection enhances the signaling specificity of a variant of the quorum-sensing transcriptional activator LuxR. Nat Biotechnol 2006;24:708-12.
30. Cook LC, Federle MJ. Peptide pheromone signaling in Streptococcus and Enterococcus. FEMS Microbiol Rev 2014;38:473-92.
31. Cornforth DM, Popat R, McNally L et al. Combinatorial quorum sensing allows bacteria to resolve their social and physical environment. P Natl Acad Sci USA 2014;111:4280-4.
32. Davidson CJ, Surette MG. Individuality in bacteria. Annu Rev Genet 2008;42:253-68.
33. Davis KM, Mohammadi S, Isberg RR. Community behavior and spatial regulation within a bacterialmicrocolony in deep tissue sites serves to protect against host attack. Cell Host Microbe 2015;17:21-31.
34. Declerck N, Bouillaut L, Chaix D et al. Structure of PlcR: insights into virulence regulation and evolution of quorum sensing in Gram-positive bacteria. P Natl Acad Sci USA 2007;104:18490-5.
35. Drees B, Reiger M, Jung K et al. Amodular view of the diversity of cell-density-encoding schemes in bacterial quorum-sensing systems. Biophys J 2014;107:266-77.
36. Dufour D, Levesque CM. Bacterial behaviors associated with the quorum-sensing peptide pheromone ('alarmone') in streptococci. Future Microbiol 2013;8:593-605.
37. Eberhard A, Burlingame AL, Eberhard C et al. Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry 1981;20:2444-9.
38. Engebrecht J, Nealson K, Silverman M. Bacterial bioluminescence: isolation and genetic analysis of functions from Vibrio fischeri. Cell 1983;32:773-81.
39. Engebrecht J, Silverman M. Identification of genes and gene products necessary for bacterial bioluminescence. P Natl Acad Sci USA 1984;81:4154-8.
40. Even-Tov E, Omer Bendori S, Valastyan J et al. Social evolution selects for redundancy in bacterial quorum sensing. PLoS Biol 2016;14:e1002386.
41. Federle MJ, Bassler BL. Interspecies communication in bacteria. Journal of clinical investigation 2003;112:1291-9.
42. Fleuchot B, Gitton C, Guillot A et al. Rgg proteins associated with internalized small hydrophobic peptides: a new quorum-sensing mechanism in streptococci. Mol Microbiol 2011;80:1102-19.
43. Fontaine L, Boutry C, de Frahan MH et al. A novel pheromone quorum-sensing system controls the development of natural competence in Streptococcus thermophilus and Streptococcus salivarius. J Bacteriol 2010;192:1444-54.
44. Freeman JA, Lilley BN, Bassler BL. A genetic analysis of the functions of LuxN: a two-component hybrid sensor kinase that regulates quorum sensing in Vibrio harveyi. Mol Microbiol 2000;35:139-49.
45. Fuqua C, Greenberg EP. Self perception in bacteria: quorum sensing with acylated homoserine lactones. Curr Opin Microbiol 1998;1:183-9.
46. Fuqua C, Greenberg EP. Listening in on bacteria: acylhomoserine lactone signalling. Nat Rev Mol Cell Bio 2002;3:685-95.
47. Fuqua WC, Winans SC. A LuxR-LuxI type regulatory system activates Agrobacterium Ti plasmid conjugal transfer in the presence of a plant tumor metabolite. J Bacteriol 1994;176: 2796-806.
48. Garmyn D, Gal L, Briandet R et al. Evidence of autoinduction heterogeneity via expression of the Agr system of Listeria monocytogenes at the single-cell level. Appl Environ Microb 2011;77:6286-9.
49. Geisinger E, Adhikari RP, Jin R et al. Inhibition of rot translation by RNAIII, a key feature of agr function. Mol Microbiol 2006;61:1038-48.
50. Geisinger E, George EA, Chen J et al. Identification of ligand specificity determinants in AgrC, the Staphylococcus aureus quorum-sensing receptor. J Biol Chem 2008;283:8930-8.
51. Geisinger E, Muir TW, Novick RP. Agr receptor mutants reveal distinct modes of inhibition by Staphylococcal autoinducing peptides. P Natl Acad Sci USA 2009;106:1216-21.
52. Gilbert KB, Kim TH, Gupta R et al. Global position analysis of the Pseudomonas aeruginosa quorum-sensing transcription factor LasR. Mol Microbiol 2009;73:1072-85.
53. Gohar M, Faegri K, Perchat S et al. The PlcR virulence regulon of Bacillus cereus. PLoS One 2008;3:e2793.
54. Gominet M, Slamti L, Gilois N et al. Oligopeptide permease is required for expression of the Bacillus thuringiensis plcR regulon and for virulence. Mol Microbiol 2001;40:963-75.
55. Grenha R, Slamti L, Nicaise M et al. Structural basis for the activation mechanism of the PlcR virulence regulator by the quorum-sensing signal peptide PapR. P Natl Acad Sci USA 2013;110:1047-52.
56. Gupta RK, Luong TT, Lee CY. RNAIII of the Staphylococcus aureus agr system activates global regulatorMgrA by stabilizing mRNA. P Natl Acad Sci USA 2015;112:14036-41.
57. Hanzelka BL, Greenberg EP. Evidence that the N-terminal region of the Vibrio fischeri LuxR protein constitutes an autoinducerbinding domain. J Bacteriol 1995;177:815-7.
58. Hanzelka BL, Parsek MR, Val DL et al. Acylhomoserine lactone synthase activity of the Vibrio fischeri AinS protein. J Bacteriol 1999;181:5766-70.
59. Havarstein LS, Coomaraswamy G, Morrison DA. An unmodified heptadecapeptide pheromone induces competence for genetic transformation in Streptococcus pneumoniae. P Natl Acad Sci USA 1995;92:11140-4.
60. Hawkins AC, Arnold FH, Stuermer R et al. Directed evolution of Vibrio fischeri LuxR for improved response to butanoyl-homoserine lactone. Appl Environ Microb 2007;73: 5775-81.
61. Henke JM, Bassler BL. Three parallel quorum-sensing systems regulate gene expression in Vibrio harveyi. J Bacteriol 2004;186:6902-14.
62. Higgins DA, Pomianek ME, Kraml CM et al. The major Vibrio cholerae autoinducer and its role in virulence factor production. Nature 2007;450:883-6.
63. Hoch J, Silhavy T. Two-Component Signal Transduction. Washington, DC: ASM Press, 1995.
64. Hwang I, Li PL, Zhang L et al. TraI, a LuxI homologue, is responsible for production of conjugation factor, the Ti plasmid N-acylhomoserine lactone autoinducer. P Natl Acad Sci USA 1994;91:4639-43.
65. Ibrahim M, Guillot A, Wessner F et al. Control of the transcription of a short gene encoding a cyclic peptide in Streptococcus thermophilus: a new quorum-sensing system? J Bacteriol 2007a;189:8844-54.
66. Ibrahim M, Nicolas P, Bessieres P et al. A genome-wide survey of short coding sequences in streptococci. Microbiology 2007b;153:3631-44.
67. InouyeM, Dutta R. Histidine Kinases in Signal Transduction. London: Academic, 2003.
68. Jarraud S, Lyon GJ, Figueiredo AM et al. Exfoliatin-producing strains define a fourth agr specificity group in Staphylococcus aureus. J Bacteriol 2000;182:6517-22.
69. Jarraud S, Mougel C, Thioulouse J et al. Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect Immun 2002;70:631-41.
70. Jensen RO, Winzer K, Clarke SR et al. Differential recognition of Staphylococcus aureus quorum-sensing signals depends on both extracellular loops 1 and 2 of the transmembrane sensor AgrC. J Mol Biol 2008;381:300-9.
71. Ji G, Beavis R, Novick RP. Bacterial interference caused by autoinducing peptide variants. Science 1997;276:2027-30.
72. Ji G, Beavis RC, Novick RP. Cell density control of staphylococcal virulence mediated by an octapeptide pheromone. P Natl Acad Sci USA 1995;92:12055-9.
73. Jimenez JC, Federle MJ. Quorum sensing in group A Streptococcus. Front Cell Infect Microbiol 2014;4:127.
74. Jung SA, Chapman CA, Ng WL. Quadruple quorum-sensing inputs control Vibrio cholerae virulence and maintain system robustness. PLoS Pathog 2015;11:e1004837.
75. Ke X, Miller LC, Bassler BL. Determinants governing ligand specificity of the Vibrio harveyi LuxN quorum-sensing receptor. Mol Microbiol 2015;95:127-42.
76. Kelly RC, Bolitho ME, Higgins DA et al. The Vibrio cholerae quorumsensing autoinducer CAI-1: analysis of the biosynthetic enzyme CqsA. Nat Chem Biol 2009;5:891-5.
77. Kleerebezem M, Quadri LE, Kuipers OP et al. Quorum sensing by peptide pheromones and two-component signaltransduction systems in Gram-positive bacteria. Mol Microbiol 1997;24:895-904.
78. Kuo A, Callahan SM, Dunlap PV. Modulation of luminescence operon expression by N-octanoyl-L-homoserine lactone in ainS mutants of Vibrio fischeri. J Bacteriol 1996;178:971-6.
79. Lasarre B, Aggarwal C, Federle MJ. Antagonistic Rgg regulators mediate quorum sensing via competitive DNA binding in Streptococcus pyogenes. MBio 2013;3:e00333-12.
80. LaSarre B, Chang JC, Federle MJ. Redundant group a streptococcus signaling peptides exhibit unique activation potentials. J Bacteriol 2013;195:4310-8.
81. Latifi A, Foglino M, Tanaka K et al. A hierarchical quorumsensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhIR (VsmR) to expression of the stationary-phase sigma factor RpoS. Mol Microbiol 1996;21:1137-46.
82. Le KY, Otto M. Quorum-sensing regulation in staphylococci-an overview. Front Microbiol 2015;6:1174.
83. Ledgham F, Ventre I, Soscia C et al. Interactions of the quorum sensing regulator QscR: interaction with itself and the other regulators of Pseudomonas aeruginosa LasR and RhlR. Mol Microbiol 2003;48:199-210.
84. Lee JH, Lequette Y, Greenberg EP. Activity of purified QscR, a Pseudomonas aeruginosa orphan quorum-sensing transcription factor. Mol Microbiol 2006;59:602-9.
85. Lenz DH, Mok KC, Lilley BN et al. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 2004;118:69-82.
86. Lequette Y, Lee JH, Ledgham F et al. A distinct QscR regulon in the Pseudomonas aeruginosa quorum-sensing circuit. J Bacteriol 2006;188:3365-70.
87. Lereclus D, Agaisse H, Gominet M et al. Identification of a Bacillus thuringiensis gene that positively regulates transcription of the phosphatidylinositol-specific phospholipase C gene at the onset of the stationary phase. J Bacteriol 1996;178: 2749-56.
88. Lina G, Jarraud S, Ji G et al. Transmembrane topology and histidine protein kinase activity of AgrC, the agr signal receptor in Staphylococcus aureus. Mol Microbiol 1998;28:655-62.
89. Long T, Tu KC, Wang Y et al. Quantifying the integration of quorum-sensing signals with single-cell resolution. PLoS Biol 2009;7:e68.
90. Lupp C, Urbanowski M, Greenberg EP et al. The Vibrio fischeri quorum-sensing systems ain and lux sequentially induce luminescence gene expression and are important for persistence in the squid host. Mol Microbiol 2003;50: 319-31.
91. Lyon GJ, Novick RP. Peptide signaling in Staphylococcus aureus and other Gram-positive bacteria. Peptides 2004;25:1389-403.
92. Lyon GJ, Wright JS, Muir TW et al. Key determinants of receptor activation in the agr autoinducing peptides of Staphylococcus aureus. Biochemistry 2002;41:10095-104.
93. McClean KH,Winson MK, Fish L et al. Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 1997;143 (Pt 12):3703-11.
94. Magnuson R, Solomon J, Grossman AD. Biochemical and genetic characterization of a competence pheromone from B. subtilis. Cell 1994;77:207-16.
95. Mashburn-Warren L, Morrison DA, Federle MJ. A novel doubletryptophan peptide pheromone controls competence in Streptococcus spp. via an Rgg regulator. Mol Microbiol 2010;78:589-606.
96. Mashburn-Warren L, Morrison DA, Federle MJ. The cryptic competence pathway in Streptococcus pyogenes is controlled by a peptide pheromone. J Bacteriol 2012;194:4589-600.
97. Mattmann ME, Blackwell HE. Small molecules that modulate quorum sensing and control virulence in Pseudomonas aeruginosa. J Org Chem2010;75:6737-46.
98. Mayville P, Ji G, Beavis R et al. Structure-activity analysis of synthetic autoinducing thiolactone peptides from Staphylococcus aureus responsible for virulence. P Natl Acad Sci USA 1999;96:1218-23.
99. Medina G, Juarez K, Diaz R et al. Transcriptional regulation of Pseudomonas aeruginosa rhlR, encoding a quorum-sensing regulatory protein. Microbiology 2003a;149:3073-81.
100. Medina G, Juarez K, Valderrama B et al. Mechanism of Pseudomonas aeruginosa RhlR transcriptional regulation of the rhlAB promoter. J Bacteriol 2003b;185:5976-83.
101. Mehta P, Goyal S, Long T et al. Information processing and signal integration in bacterial quorum sensing. Mol Syst Biol 2009;5:325.
102. Miller MB, Bassler BL. Quorum sensing in bacteria. Annu Rev Microbiol 2001;55:165-99.
103. Miller MB, Skorupski K, Lenz DH et al. Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell 2002;110:303-14.
104. Mok KC,Wingreen NS, Bassler BL. Vibrio harveyi quorum sensing: a coincidence detector for two autoinducers controls gene expression. EMBO J 2003;22:870-81.
105. Monnet V, Juillard V, Gardan R. Peptide conversations in Gram-positive bacteria. Crit Rev Microbiol 2014, DOI: 10.3109/1040841X.2014.948804.
106. Nealson KH, Hastings JW. Bacterial bioluminescence: its control and ecological significance. Microbiol Rev 1979;43:496-518.
107. Nealson KH, Platt T, Hastings JW. Cellular control of the synthesis and activity of the bacterial luminescent system. J Bacteriol 1970;104:313-22.
108. Neiditch MB, Federle MJ, Miller ST et al. Regulation of LuxPQ receptor activity by the quorum-sensing signal autoinducer-2. Mol Cell 2005;18:507-18.
109. Neiditch MB, Federle MJ, Pompeani AJ et al. Ligand-induced asymmetry in histidine sensor kinase complex regulates quorum sensing. Cell 2006;126:1095-108.
110. Ng WL, Bassler BL. Bacterial quorum-sensing network architectures. Annu Rev Genet 2009;43:197-222.
111. Ng WL, Perez L, Cong J et al. Broad spectrum pro-quorum-sensing molecules as inhibitors of virulence in vibrios. PLoS Pathog 2012;8:e1002767.
112. Ng WL, Perez LJ, Wei Y et al. Signal production and detection specificity in Vibrio CqsA/CqsS quorum-sensing systems. Mol Microbiol 2011;79:1407-17.
113. Ng WL, Wei Y, Perez LJ et al. Probing bacterial transmembrane histidine kinase receptor-ligand interactions with natural and synthetic molecules. P Natl Acad Sci USA 2010;107: 5575-80.
114. Nguyen Y, NguyenNX, Rogers JL et al. Structural and mechanistic roles of novel chemical ligands on the SdiA quorum-sensing transcription regulator. MBio 2015;6:02429-14.
115. Novick RP, Geisinger E. Quorum sensing in staphylococci. Annu Rev Genet 2008;42:541-64.
116. Novick RP, Projan SJ, Kornblum J et al. The agr P2 operon: an autocatalytic sensory transduction system in Staphylococcus aureus. Mol Gen Genet 1995;248:446-58.
117. Ochsner UA, Koch AK, Fiechter A et al. Isolation and characterization of a regulatory gene affecting rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. J Bacteriol 1994;176:2044-54.
118. Ochsner UA, Reiser J. Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. P Natl Acad Sci USA 1995;92:6424-8.
119. Olson ME, Todd DA, Schaeffer CR et al. Staphylococcus epidermidis agr quorum-sensing system: signal identification, cross talk, and importance in colonization. J Bacteriol 2014;196:3482-93.
120. Otto M, Echner H, Voelter W et al. Pheromone cross-inhibition between Staphylococcus aureus and Staphylococcus epidermidis. Infect Immun 2001;69:1957-60.
121. Otto M, Sussmuth R, Vuong C et al. Inhibition of virulence factor expression in Staphylococcus aureus by the Staphylococcus epidermidis agr pheromone and derivatives. FEBS Lett 1999;450:257-62.
122. Pappas KM, Weingart CL, Winans SC. Chemical communication in proteobacteria: biochemical and structural studies of signal synthases and receptors required for intercellular signalling. Mol Microbiol 2004;53:755-69.
123. Parashar V, Mirouze N, Dubnau DA et al. Structural basis of response regulator dephosphorylation by Rap phosphatases. PLoS Biol 2011;9:e1000589.
124. Parsek MR, Greenberg EP. Sociomicrobiology: the connections between quorum sensing and biofilms. Trends Microbiol 2005;13:27-33.
125. Passador L, Cook JM, Gambello MJ et al. Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication. Science 1993;260:1127-30.
126. Pearson JP, Gray KM, Passador L et al. Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes. P Natl Acad Sci USA 1994;91:197-201.
127. Pearson JP, Passador L, Iglewski BH et al. A second Nacylhomoserine lactone signal produced by Pseudomonas aeruginosa. P Natl Acad Sci USA 1995;92:1490-4.
128. Peng HL, Novick RP, Kreiswirth B et al. Cloning, characterization, and sequencing of an accessory gene regulator (agr) in Staphylococcus aureus. J Bacteriol 1988;170:4365-72.
129. Perego M. A peptide export-import control circuit modulating bacterial development regulates protein phosphatases of the phosphorelay. P Natl Acad Sci USA 1997;94:8612-7.
130. Pereira CS, Thompson JA, Xavier KB. AI-2-mediated signalling in bacteria. FEMS Microbiol Rev 2013;37:156-81.
131. Pesci EC, Pearson JP, Seed PC et al. Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 1997;179:3127-32.
132. Pestova EV, Havarstein LS, Morrison DA. Regulation of competence for genetic transformation in Streptococcus pneumoniae by an auto-induced peptide pheromone and a twocomponent regulatory system. Mol Microbiol 1996;21:853-62.
133. Piper KR, Beck von Bodman S, Farrand SK. Conjugation factor of Agrobacterium tumefaciens regulates Ti plasmid transfer by autoinduction. Nature 1993;362:448-50.
134. Plener L, Lorenz N, Reiger M et al. The phosphorylation flow of the Vibrio harveyi quorum-sensing cascade determines levels of phenotypic heterogeneity in the population. J Bacteriol 2015;197:1747-56.
135. Popat R, Crusz SA, Messina M et al. Quorum-sensing and cheating in bacterial biofilms. Proc Biol Sci 2012;279:4765-71.
136. Pottathil M, Lazazzera BA. The extracellular Phr peptide-Rap phosphatase signaling circuit of Bacillus subtilis. Front Biosci 2003;8:d32-45.
137. Rocha-Estrada J, Aceves-Diez AE, Guarneros G et al. The RNPP family of quorum-sensing proteins in Gram-positive bacteria. Appl Microbiol Biot 2010;87:913-23.
138. Ryan RP, An SQ, Allan JH et al. The DSF Family of Cell-Cell Signals: an expanding class of bacterial virulence regulators. PLoS Pathog 2015;11:e1004986.
139. Sakoulas G, Eliopoulos GM, Moellering RC, Jr et al. Accessory gene regulator (agr) locus in geographically diverse Staphylococcus aureus isolates with reduced susceptibility to vancomycin. Antimicrob Agents Ch 2002;46:1492-502.
140. Sappington KJ, Dandekar AA, Oinuma K et al. Reversible signal binding by the Pseudomonas aeruginosa quorum-sensing signal receptor LasR. MBio 2011;2:e00011-11.
141. Schaefer AL, Hanzelka BL, Eberhard A et al. Quorum sensing in Vibrio fischeri: probing autoinducer-LuxR interactions with autoinducer analogs. J Bacteriol 1996a;178:2897-901.
142. Schaefer AL, Val DL, Hanzelka BL et al. Generation of cell-tocell signals in quorum sensing: acyl homoserine lactone synthase activity of a purified Vibrio fischeri LuxI protein. P Natl Acad Sci USA 1996b;93:9505-9.
143. Schuster M, Lostroh CP, Ogi T et al. Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J Bacteriol 2003;185:2066-79.
144. Schuster M, Urbanowski ML, Greenberg EP. Promoter specificity in Pseudomonas aeruginosa quorum sensing revealed by DNA binding of purified LasR. P Natl Acad Sci USA 2004;101: 15833-9.
145. Shadel GS, Young R, Baldwin TO. Use of regulated cell lysis in a lethal genetic selection in Escherichia coli: identification of the autoinducer-binding region of the LuxR protein from Vibrio fischeri ATCC 7744. J Bacteriol 1990;172:3980-7.
146. Shi K, BrownCK, GuZYet al. Structure of peptide sex pheromone receptor PrgX and PrgX/pheromone complexes and regulation of conjugation in Enterococcus faecalis. P Natl Acad Sci USA 2005;102:18596-601.
147. SimonM, Crane B, Crane A. Two-Component Signaling Systems. San Diego: Academic, 2007.
148. Slamti L, Lereclus D. A cell-cell signaling peptide activates the PlcR virulence regulon in bacteria of the Bacillus cereus group. EMBO J 2002;21:4550-9.
149. Slamti L, Lereclus D. Specificity and polymorphism of the PlcRPapR quorum-sensing system in the Bacillus cereus group. J Bacteriol 2005;187:1182-7.
150. Slock J, VanRiet D, Kolibachuk D et al. Critical regions of the Vibrio fischeri LuxR protein defined by mutational analysis. J Bacteriol 1990;172:3974-9.
151. Smith RS, Iglewski BH. Pseudomonas aeruginosa quorum sensing as a potential antimicrobial target. J Clinical Invest 2003;112:1460-5.
152. Stauff DL, Bassler BL. Quorum sensing in Chromobacterium violaceum: DNA recognition and gene regulation by the CviR receptor. J Bacteriol 2011;193:3871-8.
153. Stevens AM, Dolan KM, Greenberg EP. Synergistic binding of the Vibrio fischeri LuxR transcriptional activator domain and RNA polymerase to the lux promoter region. P Natl Acad Sci USA 1994;91:12619-23.
154. Stevens AM, Fujita N, Ishihama A et al. Involvement of the RNA polymerase alpha-subunit C-terminal domain in LuxRdependent activation of the Vibrio fischeri luminescence genes. J Bacteriol 1999;181:4704-7.
155. Stevens AM, Greenberg EP. Quorum sensing in Vibrio fischeri: essential elements for activation of the luminescence genes. J Bacteriol 1997;179:557-62.
156. Surette MG, Miller MB, Bassler BL. Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: a new family of genes responsible for autoinducer production. P Natl Acad Sci USA 1999;96:1639-44.
157. Swem LR, Swem DL, O'Loughlin CT et al. A quorum-sensing antagonist targets both membrane-bound and cytoplasmic receptors and controls bacterial pathogenicity. Mol Cell 2009;35:143-53.
158. Swem LR, Swem DL, Wingreen NS et al. Deducing receptor signaling parameters from in vivo analysis: LuxN/AI-1 quorum sensing in Vibrio harveyi. Cell 2008;134:461-73.
159. Tiaden A, Spirig T, Hilbi H. Bacterial gene regulation by alphahydroxyketone signaling. Trends Microbiol 2010;18:288-97.
160. Tomasz A. 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 1965;208:155-9.
161. Travisano M, Velicer GJ. Strategies of microbial cheater control. Trends Microbiol 2004;12:72-8.
162. Urbanowski ML, Lostroh CP, Greenberg EP. Reversible acylhomoserine lactone binding to purified Vibrio fischeri LuxR protein. J Bacteriol 2004;186:631-7.
163. Vannini A, Volpari C, Gargioli C et al. The crystal structure of the quorum sensing protein TraR bound to its autoinducer and target DNA. EMBO J 2002;21:4393-401.
164. Venturi V. Regulation of quorum sensing in Pseudomonas. FEMS Microbiol Rev 2006;30:274-91.
165. Vlamakis H, Aguilar C, Losick R et al. Control of cell fate by the formation of an architecturally complex bacterial community. Gene Dev 2008;22:945-53.
166. Wagner VE, Gillis RJ, Iglewski BH. Transcriptome analysis of quorum-sensing regulation and virulence factor expression in Pseudomonas aeruginosa. Vaccine 2004;22 (Suppl 1):S15-20.
167. Waters CM, Bassler BL. Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev B 2005;21:319-46.
168. Wei Q, Ma LZ. Biofilm matrix and its regulation in Pseudomonas aeruginosa. Int J Mol Sci 2013;14:20983-1005.
169. Wei Y, Perez LJ, Ng WL et al. Mechanism of Vibrio cholerae autoinducer-1 biosynthesis. ACS Chem Biol 2011;6:356-65.
170. Welsh MA, Blackwell HE. Chemical genetics reveals environment-specific roles for quorum sensing circuits in Pseudomonas aeruginosa. Cell Chem Biol 2016;23:361-9.
171. West SA, Griffin AS, Gardner A et al. Social evolution theory for microorganisms. Nat Rev Microbiol 2006;4:597-607.
172. Whitehead NA, Barnard AM, Slater H et al. Quorum-sensing in Gram-negative bacteria. FEMS Microbiol Rev 2001;25:365-404.
173. Williams P, Camara M. Quorum sensing and environmental adaptation in Pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules. Curr Opin Microbiol 2009;12:182-91.
174. Williams P, Camara M, Hardman A et al. Quorum sensing and the population-dependent control of virulence. Philos T Roy Soc B 2000;355:667-80.
175. Wintjens R, Rooman M. Structural classification of HTH DNAbinding domains and protein-DNA interaction modes. J Mol Biol 1996;262:294-313.
176. Wright JS, III, Lyon GJ, George EA et al. Hydrophobic interactions drive ligand-receptor recognition for activation and inhibition of staphylococcal quorum sensing. P Natl Acad Sci USA 2004;101:16168-73.
177. Zhang L, Ji G. Identification of a staphylococcal AgrB segment(s) responsible for group-specific processing of AgrD by gene swapping. J Bacteriol 2004;186:6706-13.
178. Zhang RG, Pappas KM, Brace JL et al. Structure of a bacterial quorum-sensing transcription factor complexed with pheromone and DNA. Nature 2002;417:971-4.
179. Zhu J, Beaber JW, More MI et al. Analogs of the autoinducer 3-oxooctanoyl-homoserine lactone strongly inhibit activity of the TraR protein of Agrobacterium tumefaciens. J Bacteriol 1998;180:5398-405.
180. Zhu J, Miller MB, Vance RE et al. Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. P Natl Acad Sci USA 2002;99:3129-34.
181. Zhu J, Winans SC. Autoinducer binding by the quorum-sensing regulator TraR increases affinity for target promoters in vitro and decreases TraR turnover rates in whole cells. P Natl Acad Sci USA 1999;96:4832-7.
182. Zhu J,Winans SC. The quorum-sensing transcriptional regulator TraR requires its cognate signaling ligand for protein folding, protease resistance, and dimerization. P Natl Acad Sci USA 2001;98:1507-12.
183. Zou Y, Nair SK. Molecular basis for the recognition of structurally distinct autoinducer mimics by the Pseudomonas aeruginosa LasR quorum-sensing signaling receptor. Chem Biol 2009;16:961-70.
184. Zouhir S, Perchat S, Nicaise M et al. Peptide-binding dependent conformational changes regulate the transcriptional activity of the quorum-sensor NprR. Nucleic Acids Res 2013;41: 7920-33.