Negative regulation of bacterial quorum sensing tunes public goods cooperation

ISME Journal

Volumn 7, Issue 11, 2013, Pages 2159-2168

  Gupta, Rashmi ^a   Schuster, Martin ^a  

^a OREGON STATE UNIVERSITY   (United States)

Author keywords

bet hedging; cooperation; negative regulation; Pseudomonas aeruginosa; public goods; quorum sensing

Indexed keywords

BACTERIAL PROTEIN;

BET-HEDGING; FITNESS; NUTRIENT; PATHOGEN; POPULATION GROWTH; PUBLIC GOODS; VIRULENCE;

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

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

BACTERIA (MICROORGANISMS); PROTEOBACTERIA; PSEUDOMONAS AERUGINOSA;

EID: 84886716926     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2013.109     Document Type: Article

References (61)

1. Anetzberger C, Pirch T, Jung K. (2009). Heterogeneity in quorum sensing-regulated bioluminescence of Vibrio harveyi. Mol Microbiol 73: 267-277.
2. Becher A, Schweizer HP. (2000). Integration-proficient Pseudomonas aeruginosa vectors for isolation of single-copy chromosomal lacZ and lux gene fusions. Biotechniques 29: 948-950. 952.
3. Brown SP, Cornforth DM, Mideo N. (2012). Evolution of virulence in opportunistic pathogens: generalism, plasticity, and control. Trends Microbiol 20: 336-342.
4. Chugani SA, Whiteley M, Lee KM, D'Argenio D, Manoil C, Greenberg EP. (2001). QscR, a modulator of quorum-sensing signal synthesis and virulence in Pseudomo-nas aeruginosa. Proc Natl Acad Sci USA 98: 2752-2757.
5. Cormack BP, Valdivia RH, Falkow S. (1996). FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173: 33-38.
6. Cremer J, Melbinger A, Frey E. (2012). Growth dynamics and the evolution of cooperation in microbial populations. Sci Rep 2: 281.
7. Czaran T, Hoekstra RF. (2009). Microbial communication, cooperation and cheating: quorum sensing drives the evolution of cooperation in bacteria. PloS One 4: e6655.
8. Darch SE, West SA, Winzer K, Diggle SP. (2012). Density-dependent fitness benefits in quorum-sensing bacterial populations. Proc Natl Acad Sci USA 109: 8259-8263.
9. Dekimpe V, Deziel E. (2009). Revisiting the quorum-sensing hierarchy in Pseudomonas aeruginosa: the transcriptional regulator RhlR regulates LasR-specific factors. Microbiology 155: 712-723.
10. Diggle SP, Griffin AS, Campbell GS, West SA. (2007). Cooperation and conflict in quorum-sensing bacterial populations. Nature 450: 411-414.
11. Foster KR, Shaulsky G, Strassmann JE, Queller DC, Thompson CRL. (2004). Pleiotropy as a mechanism to stabilize cooperation. Nature 431: 693-696.
12. Fuqua C, Burbea M, Winans SC. (1995). Activity of the Agrobacterium Ti plasmid conjugal transfer regulator TraR is inhibited by the product of the traM gene. J Bacteriol 177: 1367-1373.
13. Fuqua C, Greenberg EP. (2002). Listening in on bacteria: acyl-homoserine lactone signalling. Nat Rev Mol Cell Biol 3: 685-695.
14. Galloway DR. (1991). Pseudomonas aeruginosa elastase and elastolysis revisited: recent developments. Mol Microbiol 5: 2315-2321.
15. Garmyn D, Gal L, Briandet R, Guilbaud M, Lemaitre JP, Hartmann A et al. (2011). Evidence of autoinduction heterogeneity via expression of the Agr system of Listeria monocytogenes at the single-cell level. Appl Environ Microbiol 77: 6286-6289.
16. 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: 1072-1085.
17. Hamilton WD. (1964). The genetical evolution of social behaviour, I & II. J Theor Biol 7: 1-52.
18. Hentzer M, Wu H, Andersen JB, Riedel K, Rasmussen TB, Bagge N et al. (2003). Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J 22: 3803-3815.
19. Hibbing ME, Fuqua C, Parsek MR, Peterson SB. (2010). Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol 8: 15-25.
20. Hoang TT, Kutchma AJ, Becher A, Schweizer HP. (2000). Integration-proficient plasmids for Pseudomonas aeruginosa: Site-specific integration and use for engineering of reporter and expression strains. Plasmid 43: 59-72.
21. Iglewski BH, Van Delden C. (1998). Cell-to-cell signaling and Pseudomonas aeruginosa infections. Emerg Infect Dis 4: 551-560.
22. Jacobs MA, Alwood A, Thaipisuttikul I, Spencer D, Haugen E, Ernst S et al. (2003). Comprehensive transposon mutant library of Pseudomonas aerugi-nosa. Proc Natl Acad Sci USA 100: 14339-14344.
23. Juhas M, Eberl L, Tummler B. (2005). Quorum sensing: the power of cooperation in the world of Pseudomonas. Environ Microbiol 7: 459-471.
24. Keller L, Surette MG. (2006). Communication in bacteria: an ecological and evolutionary perspective. Nat Rev Microbiol 4: 249-258.
25. Kohler T, Buckling A, van Delden C. (2009). Cooperation and virulence of clinical Pseudomonas aeruginosa populations. Proc Natl Acad Sci USA 106: 6339-6344.
26. Kummerli R, Brown SP. (2010). Molecular and regulatory properties of a public good shape the evolution of cooperation. Proc Natl Acad Sci USA 107: 18921-18926.
27. Latifi A, Foglino M, Tanaka K, Williams P, Lazdunski A. (1996). A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhIR (VsmR) to expression of the stationary-phase sigma factor RpoS. Mol Microbiol 21: 1137-1146.
28. Ledgham F, Ventre I, Soscia C, Foglino M, Sturgis JN, Lazdunski A. (2003). Interactions of the quorum sensing regulator QscR: interaction with itself and the other regulators of Pseudomonas aeruginosa LasR and RhlR. Mol Microbiol 48: 199-210.
29. Lee JH, Lequette Y, Greenberg EP. (2006). Activity of purified QscR, a Pseudomonas aeruginosa orphan quorum-sensing transcription factor. Mol Microbiol 59: 602-609.
30. Lenski RE, Rose MR, Simpson SC, Tadler SC. (1991). Long-term experimental evolution in Escherichia coli. I. adaptation and divergence during 2, 000 generations. Am Nat 138: 1315-1341.
31. Lequette Y, Lee JH, Ledgham F, Lazdunski A, Greenberg EP. (2006). A distinct QscR regulon in the Pseudomo-nas aeruginosa quorum-sensing circuit. J Bacteriol 188: 3365-3370.
32. Liang H, Duan J, Sibley CD, Surette MG, Duan K. (2011). Identification of mutants with altered phenazine production in Pseudomonas aeruginosa. J Med Micro-biol 60: 22-34.
33. Medina G, Juarez K, Diaz R, Soberon-Chavez G (2003). Transcriptional regulation of Pseudomonas aeruginosa rhlR, encoding a quorum-sensing regulatory protein. Microbiology 149: 3073-3081.
34. Mellbye B, Schuster M. (2011). More than just a quorum: Integration of stress and other environmental cues in acyl-homoserine lactone signaling. In: Storz G, Hengge R (eds) Bacterial stress responses. ASM Press: Washington, DC.
35. Miller MB, Bassler BL. (2001). Quorum sensing in bacteria. Annu Rev Microbiol 55: 165-199.
36. Miller WG, Leveau JH, Lindow SE. (2000). Improved gfp and inaZ broad-host-range promoter-probe vectors. Mol Plant Microbe Interact 13: 1243-1250.
37. Pai A, Tanouchi Y, You L. (2012). Optimality and robustness in quorum sensing-mediated regulation of a costly public good enzyme. Proc Natl Acad Sci USA 109: 19810-19815.
38. Pai A, You L. (2009). Optimal tuning of bacterial sensing potential. Mol Syst Biol 5: 286.
39. Pearson JP, Pesci EC, Iglewski BH. (1997). Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. J Bacteriol 179: 5756-5767.
40. Perez PD, Hagen SJ. (2010). Heterogeneous response to a quorum-sensing signal in the luminescence of individual Vibrio fischeri. PloS One 5: e15473.
41. Pesci EC, Pearson JP, Seed PC, Iglewski BH. (1997). Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 179: 3127-3132.
42. Piper KR, Farrand SK. (2000). Quorum sensing but not autoinduction of Ti plasmid conjugal transfer requires control by the opine regulon and the antiactivator TraM. J Bacteriol 182: 1080-1088.
43. Rampioni G, Bertani I, Zennaro E, Polticelli F, Venturi V, Leoni L. (2006). The quorum-sensing negative regulator RsaL of Pseudomonas aeruginosa binds to the lasI promoter. J Bacteriol 188: 815-819.
44. Rampioni G, Schuster M, Greenberg EP, Bertani I, Grasso M, Venturi V et al. (2007). RsaL provides quorum sensing homeostasis and functions as a global regulator of gene expression in Pseudomonas aeruginosa. Mol Microbiol 66: 1557-1565.
45. Ross-Gillespie A, Gardner A, Buckling A, West SA, Griffin AS. (2009). Density dependence and cooperation: theory and a test with bacteria. Evolution 63: 2315-2325.
46. Rumbaugh KP, Diggle SP, Watters CM, Ross-Gillespie A, Griffin AS, West SA. (2009). Quorum sensing and the social evolution of bacterial virulence. Curr Biol 19: 341-345.
47. Sandoz KM, Mitzimberg SM, Schuster M. (2007). Social cheating in Pseudomonas aeruginosa quorum sensing. Proc Natl Acad Sci USA 104: 15876-15881.
48. Schuster M, Greenberg EP. (2006). A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Int J Med Microbiol 296: 73-81.
49. Schuster M, Lohstroh CP, Ogi T, Greenberg EP. (2003). Identification, timing and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J Bacteriol 185: 2066-2079.
50. Schweizer HP. (1991). Escherichia-Pseudomonas shuttle vectors derived from pUC18/19. Gene 97: 109-121.
51. Siehnel R, Traxler B, An DD, Parsek MR, Schaefer AL, Singh PK. (2010). A unique regulator controls the activation threshold of quorum-regulated genes in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 107: 7916-7921.
52. Simon R, Priefer U, Pühler A. (1983). A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram-negative bacteria. Nature Biotechnology 1: 784-791.
53. 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: 5376-5384.
54. Veening JW, Smits WK, Kuipers OP. (2008). Bistability, epigenetics, and bet-hedging in bacteria. Annu Rev Microbiol 62: 193-210.
55. Wagner VE, Bushnell D, Passador L, Brooks AI, Iglewski BH. (2003). Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment. J Bacteriol 185: 2080-2095.
56. West SA, Diggle SP, Buckling A, Gardner A, Griffins AS. (2007a). The social lives of microbes. Annu Rev Ecol Evol S 38: 53-77.
57. West SA, Griffin AS, Gardner A. (2007b). Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection. J Evol Biol 20: 415-432.
58. 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: 1332-1343.
59. Williams P, Winzer K, Chan WC, Camara M. (2007). Look who's talking: communication and quorum sensing in the bacterial world. Philos Trans R Soc Lond B Biol Sci 362: 1119-1134.
60. Xavier JB, Foster KR. (2007). Cooperation and conflict in microbial biofilms. Proc Natl Acad Sci USA 104: 876-881.
61. Zaslaver A, Bren A, Ronen M, Itzkovitz S, Kikoin I, Shavit S et al. (2006). A comprehensive library of fluorescent transcriptional reporters for Escherichia coli. Nat Methods 3: 623-628.