Non-native acylated homoserine lactones reveal that LuxIR quorum sensing promotes symbiont stability

Environmental Microbiology

Volumn 16, Issue 8, 2014, Pages 2623-2634

  Studer, Sarah V ^a,b   Schwartzman, Julia A ^a   Ho, Jessica S ^a,c   Geske, Grant D ^a,d   Blackwell, Helen E ^a   Ruby, Edward G ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b Office of Energy Efficiency and Renewable Energy   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

^d Cushing Academy   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; BACTERIA (MICROORGANISMS); CEPHALOPODA; EUPRYMNA SCOLOPES; NEGIBACTERIA; PROTEOBACTERIA; VIBRIO FISCHERI;

AINS PROTEIN, VIBRIO FISCHERI; BACTERIAL PROTEIN; DRUG DERIVATIVE; GAMMA BUTYROLACTONE; HOMOSERINE LACTONE; LUXI PROTEIN, BACTERIA; LUXR AUTOINDUCER BINDING PROTEINS; REPRESSOR PROTEIN; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR;

ALIIVIBRIO FISCHERI; ANIMAL; ARTICLE; CEPHALOPOD; GENE EXPRESSION REGULATION; GENETICS; LUMINESCENCE; METABOLISM; MICROBIOLOGY; QUORUM SENSING; SYMBIOSIS; TIME;

4-BUTYROLACTONE; ALIIVIBRIO FISCHERI; ANIMALS; BACTERIAL PROTEINS; DECAPODIFORMES; GENE EXPRESSION REGULATION, BACTERIAL; LUMINESCENCE; QUORUM SENSING; REPRESSOR PROTEINS; SYMBIOSIS; TIME FACTORS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

EID: 84905366131     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12322     Document Type: Article

References (53)

1. Amara, N., Krom, B.P., Kaufmann, G.F., and Meijler, M.M. (2011) Macromolecular inhibition of quorum sensing: enzymes, antibodies, and beyond. Chem Rev 111: 195-208.
2. Antunes, L.C., Schaefer, A.L., Ferreira, R.B., Qin, N., Stevens, A.M., Ruby, E.G., and Greenberg, E.P. (2007) Transcriptome analysis of the Vibrio fischeri LuxR-LuxI regulon. J Bacteriol 189: 8387-8391.
3. Bjarnsholt, T., and Givskov, M. (2007) Quorum-sensing blockade as a strategy for enhancing host defences against bacterial pathogens. Phil Trans R Soc B 362: 1213-1222.
4. von Bodman, S.B., Bauer, W.D., and Coplin, D.L. (2003) Quorum sensing in plant-pathogenic bacteria. Annu Rev Phytopathol 41: 455-482.
5. Boettcher, K.J., and Ruby, E.G. (1990) Depressed light emission by symbiotic Vibrio fischeri of the sepiolid squid Euprymna scolopes. J Bacteriol 172: 3701-3706.
6. Bose, J.L., Rosenberg, C.S., and Stabb, E.V. (2008) Effects of luxCDABEG induction in Vibrio fischeri: enhancement of symbiotic colonization and conditional attenuation of growth in culture. Arch Microbiol 190: 169-183.
7. Chun, C.K., Troll, J.V., Koroleva, I., Brown, B., Manzella, L., Snir, E., etal. (2008) Effects of colonization, luminescence, and autoinducer on host transcription during development of the squid-vibrio association. Proc Natl Acad Sci U S A 105: 11323-11328.
8. Churchill, M.E., and Chen, L. (2010) Structural basis of acyl-homoserine lactone-dependent signaling. Chem Rev 111: 68-85.
9. D'agostino, R.B., Belanger, A., and D'Agostino, R.B., Jr (1990) A suggestion for using powerful and informative tests of normality. Am Stat 44: 316-321.
10. Dunlap, P.V. (1999) Quorum regulation of luminescence in Vibrio fischeri. J Mol Microbiol Biotechnol 1: 5-12.
11. Galloway, W.R., Hodgkinson, J.T., Bowden, S., Welch, M., and Spring, D.R. (2012) Applications of small molecule activators and inhibitors of quorum sensing in Gram-negative bacteria. Trends Microbiol 20: 449-458.
12. Galloway, W.R.J.D., Hodgkinson, J.T., Bowden, S.D., Welch, M., and Spring, D.R. (2011) Quorum sensing in Gram-negative bacteria: small-molecule modulation of AHL and Al-2 quorum sensing pathways. Chem Rev 111: 28-67.
13. Geske, G.D., O'Neill, J.C., and Blackwell, H.E. (2007a) N-phenylacetanoyl-L-homoserine lactones can strongly antagonize or superagonize quorum sensing in Vibrio fischeri. ACS Chem Biol 2: 315-319.
14. Geske, G.D., O'Neill, J.C., Miller, D.M., Mattmann, M.E., and Blackwell, H.E. (2007b) Modulation of bacterial quorum sensing with synthetic ligands: systematic evaluation of N-acylated homoserine lactones in multiple species and new insights into their mechanisms of action. J Am Chem Soc 129: 13613-13625.
15. Geske, G.D., O'Neill, J.C., Miller, D.M., Wezeman, R.J., Mattmann, M.E., Lin, Q., and Blackwell, H.E. (2008) Comparative analyses of N-acylated homoserine lactones reveal unique structural features that dictate their ability to activate or inhibit quorum sensing. Chembiochem 9: 389-400.
16. Gilson, L., Kuo, A., and Dunlap, P.V. (1995) AinS and a new family of autoinducer synthesis proteins. J Bacteriol 177: 6946-6951.
17. González, J.E., and Marketon, M.M. (2003) Quorum sensing in nitrogen-fixing rhizobia. Microbiol Mol Biol Rev 67: 574-592.
18. González, J.F., and Venturi, V. (2012) A novel widespread interkingdom signaling circuit. Trends Plant Sci 18: 167-174.
19. Graf, J., Dunlap, P.V., and Ruby, E.G. (1994) Effect of transposon-induced motility mutations on colonization of the host light organ by Vibrio fischeri. J Bacteriol 176: 6986-6991.
20. Heath-Heckman, E.A., Peyer, S.M., Whistler, C.A., Apicella, M.A., Goldman, W.E., and McFall-Ngai, M.J. (2013) Bacterial bioluminescence regulates expression of a host cryptochrome gene in the squid-vibrio symbiosis. mBio 4: e00167-13.
21. Hentzer, M., Wu, H., Andersen, J.B., Riedel, K., Rasmussen, T.B., Bagge, N., etal. (2003) Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J 22: 3803-3815.
22. Kimbrough, J.H., and Stabb, E.V. (2013) Substrate specificity and function of the pheromone receptor AinR in Vibrio fischeri ES114. J Bacteriol [Epub ahead of print].
23. Koch, E.J., Miyashiro, T., McFall-Ngai, M.J., and Ruby, E.G. (2013) Features governing symbiont persistence in the squid-vibrio association. Mol Ecol doi:10.1111/mec.12474.
24. Liu, Z., Miyashiro, T., Tsou, A., Hsiao, A., Goulian, M., and Zhu, J. (2008) Mucosal penetration primes Vibrio cholerae for host colonization by repressing quorum sensing. Sci Signal 105: 9769-9774.
25. Lowery, C.A., Salzameda, N.T., Sawada, D., Kaufmann, G.F., and Janda, K.D. (2010) Medicinal chemistry as a conduit for the modulation of quorum sensing. J Medical Chem 53: 7467-7489.
26. Lupp, C., and Ruby, E.G. (2004) Vibrio fischeri LuxS and AinS: comparative study of two signal synthases. J Bacteriol 186: 3873-3881.
27. Lupp, C., and Ruby, E.G. (2005) Vibrio fischeri uses two quorum-sensing systems for the regulation of early and late colonization factors. J Bacteriol 187: 3620-3629.
28. Lupp, C., Urbanowski, M., Greenberg, E.P., and Ruby, E.G. (2003) 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 50: 319-331.
29. Mandel, M.J. (2010) Models and approaches to dissect host-symbiont specificity. Trends Microbiol 18: 504-511.
30. Miyashiro, T., and Ruby, E.G. (2012) Shedding light on bioluminescence regulation in Vibrio fischeri. Mol Microbiol 84: 795-806.
31. Neiditch, M.B., Federle, M.J., Pompeani, A.J., Kelly, R.C., Swem, D.L., Jeffrey, P.D., etal. (2006) Ligand-induced asymmetry in histidine sensor kinase complex regulates quorum sensing. Cell 126: 1095-1108.
32. Njoroge, J., and Sperandio, V. (2009) Jamming bacterial communication: new approaches for the treatment of infectious diseases. EMBO Mol Medical 1: 201-210.
33. Nyholm, S.V., and McFall-Ngai, M.J. (2004) The winnowing: establishing the squid-vibrio symbiosis. Nat Rev Microbiol 2: 632-642.
34. O' Connor, C.J., Laraia, L., and Spring, D.R. (2011) Chemical genetics. Chem Soc Rev 40: 4332-4345.
35. O'Loughlin, C.T., Miller, L.C., Siryaporn, A., Drescher, K., Semmelhack, M.F., and Bassler, B.L. (2013) A quorum-sensing inhibitor blocks Pseudomonas aeruginosa virulence and biofilm formation. Proc Natl Acad Sci USA 110: 17981-17986.
36. Palmer, A.G., Streng, E., and Blackwell, H.E. (2011a) Attenuation of virulence in pathogenic bacteria using synthetic quorum-sensing modulators under native conditions on plant hosts. ACS Chem Biol 6: 1348-1356.
37. Palmer, A.G., Streng, E., Jewell, K.A., and Blackwell, H.E. (2011b) Quorum sensing in bacterial species that use degenerate autoinducers can be tuned by using structurally identical non-native ligands. Chembiochem 12: 138-147.
38. Parsek, M.R., and Greenberg, E.P. (2000) Acyl-homoserine lactone quorum sensing in gram-negative bacteria: a signaling mechanism involved in associations with higher organisms. Proc Natl Acad Sci U S A 97: 8789-8793.
39. Praneenararat, T., Palmer, A.G., and Blackwell, H.E. (2012) Chemical methods to interrogate bacterial quorum sensing pathways. Org Biomol Chem 10: 8189-8199.
40. Rasmussen, T.B., and Givskov, M. (2006) Quorum sensing inhibitors: a bargain of effects. Microbiology 152: 895-904.
41. Ruby, E.G. (1996) Lessons from a cooperative, bacterial-animal association: the Vibrio fischeri-Euprymna scolopes light organ symbiosis. Annu Rev Microbiol 50: 591-624.
42. Rumbaugh, K.P., and Kaufmann, G.F. (2012) Exploitation of host signaling pathways by microbial quorum sensing signals. Curr Opp Microbiol 15: 162-168.
43. Sambrook, J.F., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning. Cold Spring Harbor, New York, NY, USA: Cold Spring Harbor Press.
44. Schaefer, A.L., Hanzelka, B.L., Eberhard, A., and Greenberg, E.P. (1996) Quorum sensing in Vibrio fischeri: probing autoinducer-LuxR interactions with autoinducer analogs. J Bacteriol 178: 2897-2901.
45. Slauch, J.M., and Silhavy, T.J. (1991) cis-acting ompF mutations that result in OmpR-dependent constitutive expression. J Bacteriol 173: 4039-4048.
46. Stabb, E.V., and Visick, K.L. (2013) Vibrio fischeri: a bioluminescent light-organ symbiont of the bobtail squid Euprymna scolopes. In The Prokaryotes. Rosenberg, E., DeLong, E.F., Lory, S., Stackebrandt, E., and Thompson, F. (eds). Berlin, Germany: Springer-Verlag, pp. 497-532.
47. Stabb, E.V., Schaefer, A., Bose, J.L., and Ruby, E.G. (2007) Quorum signaling and symbiosis in the marine luminous bacterium Vibrio fischeri. In Cell-cell signaling in bacteria. Winans, S., and Bassler, B. (eds). Washington, DC, USA: ASM Press, pp. 233-250.
48. Studer, S.V., Mandel, M.J., and Ruby, E.G. (2008) AinS quorum sensing regulates the Vibrio fischeri acetate switch. J Bacteriol 190: 5915-5923.
49. Swem, L.R., Swem, D.L., O'Loughlin, C.T., Gatmaitan, R., Zhao, B., Ulrich, S.M., and Bassler, B.L. (2009) A quorum-sensing antagonist targets both membrane-bound and cytoplasmic receptors and controls bacterial pathogenicity. Mol Cell 35: 143-153.
50. Teplitski, M., Mathesius, U., and Rumbaugh, K.P. (2011) Perception and degradation of N-acyl homoserine lactone quorum sensing signals by mammalian and plant cells. Chem Rev 111: 100-116.
51. Tong, D., Rozas, N.S., Oakley, T.H., Mitchell, J., Colley, N.J., and McFall-Ngai, M.J. (2009) Evidence for light perception in a bioluminescent organ. Proc Natl Acad Sci U S A 106: 9836-9841.
52. Visick, K.L., Foster, J., Doino, J., McFall-Ngai, M., and Ruby, E.G. (2000) Vibrio fischeri lux genes play an important role in colonization and development of the host light organ. J Bacteriol 182: 4578-4586.
53. Wu, H., Song, Z., Hentzer, M., Andersen, J.B., Molin, S., Givskov, M., and Høiby, N. (2004) Synthetic furanones inhibit quorum-sensing and enhance bacterial clearance in Pseudomonas aeruginosa lung infection in mice. J Antimicrob Chemother 53: 1054-1061.