Acyl-homoserine lactone-dependent eavesdropping promotes competition in a laboratory co-culture model

ISME Journal

Volumn 6, Issue 12, 2012, Pages 2219-2228

  Chandler, Josephine R ^a   Heilmann, Silja ^b   Mittler, John E ^a   Greenberg, E Peter ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; BACTOBOLIN; BENZOPYRAN DERIVATIVE; GAMMA BUTYROLACTONE DERIVATIVE; INDOLE DERIVATIVE; VIOLACEIN;

ANTIBIOTICS; ANTIMICROBIAL ACTIVITY; BACTERIUM; CELL ORGANELLE; COMPETITION (ECOLOGY); ECOLOGICAL MODELING; HABITAT TYPE; INHIBITION; INTERSPECIFIC COMPETITION; MICROBIAL COMMUNITY; NICHE;

ANTIBIOSIS; ARTICLE; BURKHOLDERIA; CHROMOBACTERIUM; COCULTURE; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; PHYSIOLOGY; QUORUM SENSING; SIGNAL TRANSDUCTION;

ACYL-BUTYROLACTONES; ANTI-BACTERIAL AGENTS; ANTIBIOSIS; BENZOPYRANS; BURKHOLDERIA; CHROMOBACTERIUM; COCULTURE TECHNIQUES; INDOLES; MICROBIAL SENSITIVITY TESTS; QUORUM SENSING; SIGNAL TRANSDUCTION; SOIL MICROBIOLOGY;

BACTERIA (MICROORGANISMS); BURKHOLDERIA THAILANDENSIS; CHROMOBACTERIUM VIOLACEUM; PROTEOBACTERIA;

EID: 84871294609     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2012.69     Document Type: Article

References (51)

1. Ahlgren NA, Harwood CS, Schaefer AL, Giraud E, Greenberg EP. (2011). Aryl-homoserine lactone quorum sensing in stem-nodulating photosynthetic bradyrhizobia. Proc Natl Acad Sci USA 108: 7183-7188.
2. An D, Danhorn T, Fuqua C, Parsek MR. (2006). Quorum sensing and motility mediate interactions between Pseudomonas aeruginosa and Agrobacterium tumefaciens in biofilm cocultures. Proc Natl Acad Sci USA 103: 3828-3833.
3. Bainton NJ, Bycroft BW, Chhabra SR, Stead P, Gledhill L, Hill PJ et al. (1992). A general role for the lux autoinducer in bacterial cell signalling: control of antibiotic biosynthesis in Erwinia. Gene 116: 87-91.
4. Bassler BL. (2002). Small talk. Cell-to-cell communication in bacteria. Cell 109: 421-424.
5. Brazilian National Genome Project Consortium (2003). The complete genome sequence of Chromobacterium violaceum reveals remarkable and exploitable bacterial adaptability. Proc Natl Acad Sci USA 100: 11660-11665.
6. Carr G, Seyedsayamdost MR, Chandler JR, Greenberg EP, Clardy J. (2011). Sources of diversity in bactobolin biosynthesis by Burkholderia thailandensis E264. Org Lett 13: 3048-3051.
7. Chandler JR, Duerkop BA, Hinz A, West TE, Herman JP, Churchill ME et al. (2009). Mutational analysis of Burkholderia thailandensis quorum sensing and self-aggregation. J Bacteriol 191: 5901-5909.
8. Chen G, Swem LR, Swem DL, Stauff DL, O'Loughlin CT, Jeffrey PD et al. (2011). A strategy for antagonizing quorum sensing. Mol Cell 42: 199-209.
9. Collins CH, Arnold FH, Leadbetter JR. (2005). Directed evolution of Vibrio fischeri LuxR for increased sensitivity to a broad spectrum of acyl-homoserine lactones. Mol Microbiol 55: 712-723.
10. Cui Y, Chatterjee A, Hasegawa H, Chatterjee AK. (2006). Erwinia carotovora subspecies produce duplicate variants of ExpR, LuxR homologs that activate rsmA transcription but differ in their interactions with N-acylhomoserine lactone signals. J Bacteriol 188: 4715-4726.
11. Davies J, Spiegelman GB, Yim G. (2006). The world of subinhibitory antibiotic concentrations. Curr Opin Microbiol 9: 445-453.
12. Duerkop BA, Varga J, Chandler JR, Peterson SB, Herman JP, Churchill ME et al. (2009). Quorumsensing control of antibiotic synthesis in Burkholderia thailandensis. J Bacteriol 191: 3909-3918.
13. Dulla GF, Lindow SE. (2009). Acyl-homoserine lactonemediated cross talk among epiphytic bacteria modulates behavior of Pseudomonas syringae on leaves. ISME J 3: 825-834.
14. Engebrecht J, Nealson K, Silverman M. (1983). Bacterial bioluminescence: isolation and genetic analysis of functions from Vibrio fischeri. Cell 32: 773-781.
15. Fuqua C. (2006). The QscR quorum-sensing regulon of Pseudomonas aeruginosa: an orphan claims its identity. J Bacteriol 188: 3169-3171.
16. Fuqua C, Parsek MR, Greenberg EP. (2001). Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu Rev Genet 35: 439-468.
17. Fuqua WC, Winans SC, Greenberg EP. (1994). Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176: 269-275.
18. Gallagher LA, Manoil C. (2001). Pseudomonas aeruginosa PAO1 kills Caenorhabditis elegans by cyanide poisoning. J Bacteriol 183: 6207-6214.
19. Hawkins AC, Arnold FH, Stuermer R, Hauer B, Leadbetter JR. (2007). Directed evolution of Vibrio fischeri LuxR for improved response to butanoyl-homoserine lactone. Appl Environ Microbiol 73: 5775-5781.
20. Hibbing ME, Fuqua C, Parsek MR, Peterson SB. (2010). Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol 8: 15-25.
21. Hosni T, Moretti C, Devescovi G, Suarez-Moreno ZR, Fatmi MB, Guarnaccia C et al. (2011). Sharing of quorum-sensing signals and role of interspecies communities in a bacterial plant disease. ISME J 5: 1857-1870.
22. Keller L, Surette MG. (2006). Communication in bacteria: an ecological and evolutionary perspective. Nat Rev Microbiol 4: 249-258.
23. Kownatzki R, Tummler B, Doring G. (1987). Rhamnolipid of Pseudomonas aeruginosa in sputum of cystic fibrosis patients. Lancet 1: 1026-1027.
24. 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.
25. Latifi A, Winson MK, Foglino M, Bycroft BW, Stewart GS, Lazdunski A et al. (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: 333-343.
26. Lee JH, Lequette Y, Greenberg EP. (2006). Activity of purified QscR, a Pseudomonas aeruginosa orphan quorum-sensing transcription factor. Mol Microbiol 59: 602-609.
27. Lindemann A, Pessi G, Schaefer AL, Mattmann ME, Christensen QH, Kessler A et al. (2011). Isovalerylhomoserine lactone, an unusual branched-chain quorum-sensing signal from the soybean symbiont Bradyrhizobium japonicum. Proc Natl Acad Sci USA 108: 16765-16770.
28. Lintz MJ, Oinuma K, Wysoczynski CL, Greenberg EP, Churchill ME. (2011). Crystal structure of QscR, a Pseudomonas aeruginosa quorum sensing signal receptor. Proc Natl Acad Sci USA 108: 15763-15768.
29. Mazzola M, Cook RJ, Thomashow LS, Weller DM, Pierson LS III. (1992). Contribution of phenazine antibiotic biosynthesis to the ecological competence of fluorescent pseudomonads in soil habitats. Appl Environ Microbiol 58: 2616-2624.
30. McClean KH, Winson MK, Fish L, Taylor A, Chhabra SR, Camara M et al. (1997). Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 143 (Part 12) 3703-11.
31. Moons P, Van Houdt R, Aertsen A, Vanoirbeek K, Engelborghs Y, Michiels CW. (2006). Role of quorum sensing and antimicrobial component production by Serratia plymuthica in formation of biofilms, including mixed biofilms with Escherichia coli. Appl Environ Microbiol 72: 7294-7300.
32. Moons P, Van Houdt R, Aertsen A, Vanoirbeek K, Michiels CW. (2005). Quorum sensing dependent production of antimicrobial component influences establishment of E. coli in dual species biofilms with Serratia plymuthica. Commun Agric Appl Biol Sci 70: 195-198.
33. Pierson EA, Wood DW, Cannon JA, Blachere FM, Pierson LS 3rd. (1998). Interpopulation signaling via N-acyl-homoserine lactones among bacteria in the wheat rhizosphere. Mol Plant Microbe Interact 11: 1078-1084.
34. Ran H, Hassett DJ, Lau GW. (2003). Human targets of Pseudomonas aeruginosa pyocyanin. Proc Natl Acad Sci USA 100: 14315-14320.
35. Riedel K, Hentzer M, Geisenberger O, Huber B, Steidle A, Wu H et al. (2001). N-acylhomoserine-lactonemediated communication between Pseudomonas aeruginosa and Burkholderia cepacia in mixed biofilms. Microbiology 147: 3249-3262.
36. Schuster M, Greenberg EP. (2006). A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Int J Med Microbiol 296: 273-81.
37. Seed PC, Passador L, Iglewski BH. (1995). Activation of the Pseudomonas aeruginosa lasI gene by LasR and the Pseudomonas autoinducer PAI: an autoinduction regulatory hierarchy. J Bacteriol 177: 654-659.
38. Seyedsayamdost MR, Chandler JR, Blodgett JA, Lima PS, Duerkop BA, Oinuma K et al. (2010). Quorum-sensingregulated bactobolin production by Burkholderia thailandensis E264. Org Lett 12: 716-719.
39. Sjoblom S, Brader G, Koch G, Palva ET. (2006). Cooperation of two distinct ExpR regulators controls quorum sensing specificity and virulence in the plant pathogen Erwinia carotovora. Mol Microbiol 60: 1474-1489.
40. Stauff DL, Bassler BL. (2011). Quorum sensing in Chromobacterium violaceum: DNA recognition and gene regulation by the CviR receptor. J Bacteriol 193: 3871-3878.
41. Steidle A, Sigl K, Schuhegger R, Ihring A, Schmid M, Gantner S et al. (2001). Visualization of N-acylhomoserine lactone-mediated cell-cell communication between bacteria colonizing the tomato rhizosphere. Appl Environ Microbiol 67: 5761-5770.
42. Strong FM. (1944). Isolation of violacein. Science 100: 287.
43. Swem LR, Swem DL, O'Loughlin CT, Gatmaitan R, Zhao B, Ulrich SM et al. (2009). A quorum-sensing antagonist targets both membrane-bound and cytoplasmic receptors and controls bacterial pathogenicity. Mol Cell 35: 143-153.
44. Tobie WC. (1935). The pigment of Bacillus violaceus: I. The production, extraction, and purification of violacein. J Bacteriol 29: 223-227.
45. Venturi V, Friscina A, Bertani I, Devescovi G, Aguilar C. (2004). Quorum sensing in the Burkholderia cepacia complex. Res Microbiol 155: 238-244.
46. Visick KL, Ruby EG. (1999). The emergent properties of quorum sensing: consequences to bacteria of autoinducer signaling in their natural environment. In: Winans GMDaSC (ed.) Cell-Cell Signaling in Bacteria. ASM Press: Washington, DC, pp 333-352.
47. Visick KL, McFall-Ngai MJ. (2000). An exclusive contract: specificity in the Vibrio fischeri-Euprymna scolopes partnership. J Bacteriol 182: 1779-1787.
48. Waters CM, Bassler BL. (2005). Quorum sensing: cellto-cell communication in bacteria. Annu Rev Cell Dev Biol 21: 319-346.
49. Wu H, Huang Y, Dykes C, Liu D, Ma J, Perelson AS et al. (2006). Modeling and estimation of replication fitness of human immunodeficiency virus type 1 in vitro experiments by using a growth competition assay. J Virol 80: 2380-2389.
50. Xavier JB, Kim W, Foster KR. (2011). A molecular mechanism that stabilizes cooperative secretions in Pseudomonas aeruginosa. Mol Microbiol 79: 166-179.
51. Yim G, Wang HH, Davies J. (2007). Antibiotics as signalling molecules. Philos Trans R Soc Lond Ser B 362: 1195-1200.