A LuxR-type repressor of Burkholderia cenocepacia inhibits transcription via antiactivation and is inactivated by its cognate acylhomoserine lactone

Molecular Microbiology

Volumn 87, Issue 1, 2013, Pages 94-111

  Ryan, Gina T ^a   Wei, Yuping ^a   Winans, Stephen C ^a  

^a Cornell University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARAC PROTEIN; BETA GALACTOSIDASE; COGNATE ACYLHOMOSERINE LACTONE; DEOXYRIBONUCLEASE I; LACTONE; PROTEIN CEPR2; PROTEIN CEPS; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR LUXR; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BINDING SITE; BIOSYNTHESIS; BURKHOLDERIA CENOCEPACIA; CEPR2 GENE; CEPS GENE; CONTROLLED STUDY; DNA FOOTPRINTING; GENE CONTROL; GENE EXPRESSION; GENE INTERACTION; GENETIC LINKAGE; LACZ GENE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION REGULATION; UPREGULATION;

ACYL-BUTYROLACTONES; ARAC TRANSCRIPTION FACTOR; BACTERIAL PROTEINS; BASE SEQUENCE; BINDING SITES; BURKHOLDERIA CENOCEPACIA; DNA FOOTPRINTING; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; QUORUM SENSING; REPRESSOR PROTEINS; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION, GENETIC;

BURKHOLDERIA CENOCEPACIA;

EID: 84871453730     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12085     Document Type: Article

References (59)

1. Aguilar, C., Friscina, A., Devescovi, G., Kojic, M., and Venturi, V. (2003) Identification of quorum-sensing-regulated genes of Burkholderia cepacia. J Bacteriol 185: 6456-6462.
2. Barrett, A.R., Kang, Y., Inamasu, K.S., Son, M.S., Vukovich, J.M., and Hoang, T.T. (2008) Genetic tools for allelic replacement in Burkholderia species. Appl Environ Microbiol 74: 4498-4508.
3. Bontemps, C., Elliott, G.N., Simon, M.F., Dos Reis Junior, F.B., Gross, E., Lawton, R.C., etal. (2010) Burkholderia species are ancient symbionts of legumes. Mol Ecol 19: 44-52.
4. Cangelosi, G.A., Best, E.A., Martinetti, G., and Nester, E.W. (1991) Genetic analysis of Agrobacterium. Methods Enzymol 204: 384-397.
5. Castang, S., Reverchon, S., Gouet, P., and Nasser, W. (2006) Direct evidence for the modulation of the activity of the Erwinia chrysanthemi quorum-sensing regulator ExpR by acylhomoserine lactone pheromone. J Biol Chem 281: 29972-29987.
6. Chai, Y., and Winans, S.C. (2009) The chaperone GroESL enhances the accumulation of soluble, active TraR protein, a quorum-sensing transcription factor from Agrobacterium tumefaciens. J Bacteriol 191: 3706-3711.
7. Chen, W.M., Moulin, L., Bontemps, C., Vandamme, P., Bena, G., and Boivin-Masson, C. (2003) Legume symbiotic nitrogen fixation by beta-proteobacteria is widespread in nature. J Bacteriol 185: 7266-7272.
8. Cho, H., and Winans, S.C. (2005) VirA and VirG activate the Ti plasmid repABC operon, elevating plasmid copy number in response to wound-released chemical signals. Proc Natl Acad Sci USA 102: 14843-14848.
9. Churchill, M.E., and Chen, L. (2011) Structural basis of acyl-homoserine lactone-dependent signaling. Chem Rev 111: 68-85.
10. Cui, Y., Chatterjee, A., Hasegawa, H., Dixit, V., Leigh, N., and Chatterjee, A.K. (2005) ExpR, a LuxR homolog of Erwinia carotovora subsp. carotovora, activates transcription of rsmA, which specifies a global regulatory RNA-binding protein. J Bacteriol 187: 4792-4803.
11. Delrue, R.M., Deschamps, C., Leonard, S., Nijskens, C., Danese, I., Schaus, J.M., etal. (2005) A quorum-sensing regulator controls expression of both the type IV secretion system and the flagellar apparatus of Brucella melitensis. Cell Microbiol 7: 1151-1161.
12. DeShazer, D., and Woods, D.E. (1996) Broad-host-range cloning and cassette vectors based on the R388 trimethoprim resistance gene. Biotechniques 20: 762-764.
13. Dolan, K.M., and Greenberg, E.P. (1992) Evidence that GroEL, not sigma 32, is involved in transcriptional regulation of the Vibrio fischeri luminescence genes in Escherichia coli. J Bacteriol 174: 5132-5135.
14. Fineran, P.C., Slater, H., Everson, L., Hughes, K., and Salmond, G.P. (2005) Biosynthesis of tripyrrole and beta-lactam secondary metabolites in Serratia: integration of quorum sensing with multiple new regulatory components in the control of prodigiosin and carbapenem antibiotic production. Mol Microbiol 56: 1495-1517.
15. Galloway, W.R., 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 AI-2 quorum sensing pathways. Chem Rev 111: 28-67.
16. Godoy, D., Randle, G., Simpson, A.J., Aanensen, D.M., Pitt, T.L., Kinoshita, R., and Spratt, B.G. (2003) Multilocus sequence typing and evolutionary relationships among the causative agents of melioidosis and glanders, Burkholderia pseudomallei and Burkholderia mallei. J Clin Microbiol 41: 2068-2079.
17. Gotschlich, A., Huber, B., Geisenberger, O., Togl, A., Steidle, A., Riedel, K., etal. (2001) Synthesis of multiple N-acylhomoserine lactones is wide-spread among the members of the Burkholderia cepacia complex. Syst Appl Microbiol 24: 1-14.
18. Hegde, P., Qi, R., Abernathy, K., Gay, C., Dharap, S., Gaspard, R., etal. (2000) A concise guide to cDNA microarray analysis. Biotechniques 29: 548-562.
19. Holden, M.T., Seth-Smith, H.M., Crossman, L.C., Sebaihia, M., Bentley, S.D., Cerdeno-Tarraga, A.M., etal. (2009) The genome of Burkholderia cenocepacia J2315, an epidemic pathogen of cystic fibrosis patients. J Bacteriol 191: 261-277.
20. Huber, B., Riedel, K., Hentzer, M., Heydorn, A., Gotschlich, A., Givskov, M., etal. (2001) The cep quorum-sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility. Microbiology 147: 2517-2528.
21. Jones, A.M., and Webb, A.K. (2003) Recent advances in cross-infection in cystic fibrosis: Burkholderia cepacia complex, Pseudomonas aeruginosa, MRSA and Pandoraea spp. J R Soc Med 96: 66-72.
22. Khan, S.R., Gaines, J., Roop, R.M., 2nd, and Farrand, S.K. (2008) Broad-host-range expression vectors with tightly regulated promoters and their use to examine the influence of TraR and TraM expression on Ti plasmid quorum sensing. Appl Environ Microbiol 74: 5053-5062.
23. Kooi, C., Subsin, B., Chen, R., Pohorelic, B., and Sokol, P.A. (2006) Burkholderia cenocepacia ZmpB is a broad-specificity zinc metalloprotease involved in virulence. Infect Immun 74: 4083-4093.
24. Kothe, M., Antl, M., Huber, B., Stoecker, K., Ebrecht, D., Steinmetz, I., and Eberl, L. (2003) Killing of Caenorhabditis elegans by Burkholderia cepacia is controlled by the cep quorum-sensing system. Cell Microbiol 5: 343-351.
25. Lewenza, S., and Sokol, P.A. (2001) Regulation of ornibactin biosynthesis and N-acyl-L-homoserine lactone production by CepR in Burkholderia cepacia. J Bacteriol 183: 2212-2218.
26. Lewenza, S., Conway, B., Greenberg, E.P., and Sokol, P.A. (1999) Quorum sensing in Burkholderia cepacia: identification of the LuxRI homologs CepRI. J Bacteriol 181: 748-756.
27. Mahenthiralingam, E., Urban, T.A., and Goldberg, J.B. (2005) The multifarious, multireplicon Burkholderia cepacia complex. Nat Rev Microbiol 3: 144-156.
28. Malott, R.J., Baldwin, A., Mahenthiralingam, E., and Sokol, P.A. (2005) Characterization of the cciIR quorum-sensing system in Burkholderia cenocepacia. Infect Immun 73: 4982-4992.
29. Malott, R.J., O'Grady, E.P., Toller, J., Inhulsen, S., Eberl, L., and Sokol, P.A. (2009) A Burkholderia cenocepacia orphan LuxR homolog is involved in quorum-sensing regulation. J Bacteriol 191: 2447-2460.
30. Minogue, T.D., Wehland-von Trebra, M., Bernhard, F., and von Bodman, S.B. (2002) The autoregulatory role of EsaR, a quorum-sensing regulator in Pantoea stewartii ssp. stewartii: evidence for a repressor function. Mol Microbiol 44: 1625-1635.
31. Minogue, T.D., Carlier, A.L., Koutsoudis, M.D., and von Bodman, S.B. (2005) The cell density-dependent expression of stewartan exopolysaccharide in Pantoea stewartii ssp. stewartii is a function of EsaR-mediated repression of the rcsA gene. Mol Microbiol 56: 189-203.
32. Ng, W.L., and Bassler, B.L. (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43: 197-222.
33. Nzula, S., Vandamme, P., and Govan, J.R. (2002) Influence of taxonomic status on the in vitro antimicrobial susceptibility of the Burkholderia cepacia complex. J Antimicrob Chemother 50: 265-269.
34. O'Grady, E.P., Viteri, D.F., Malott, R.J., and Sokol, P.A. (2009) Reciprocal regulation by the CepIR and CciIR quorum sensing systems in Burkholderia cenocepacia. BMC Genomics 10: 441.
35. Parke, J.L., and Gurian-Sherman, D. (2001) Diversity of the Burkholderia cepacia complex and implications for risk assessment of biological control strains. Annu Rev Phytopathol 39: 225-258.
36. Perez-Rueda, E., Gralla, J.D., and Collado-Vides, J. (1998) Genomic position analyses and the transcription machinery. J Mol Biol 275: 165-170.
37. Sambrook, J., and Russell, D.W. (2001) Molecular Cloning, 3rd edn. Cold Spring Harbor: Cold Spring Harbor Laboratory.
38. Schu, D.J., Ramachandran, R., Geissinger, J.S., and Stevens, A.M. (2011) Probing the impact of ligand binding on the acyl-homoserine lactone-hindered transcription factor EsaR of Pantoea stewartii subsp. stewartii. J Bacteriol 193: 6315-6322.
39. Schuster, M., Urbanowski, M.L., and Greenberg, E.P. (2004) Promoter specificity in Pseudomonas aeruginosa quorum sensing revealed by DNA binding of purified LasR. Proc Natl Acad Sci USA 101: 15833-15839.
40. Shin, M., Kang, S., Hyun, S.J., Fujita, N., Ishihama, A., Valentin-Hansen, P., and Choy, H.E. (2001) Repression of deoP2 in Escherichia coli by CytR: conversion of a transcription activator into a repressor. EMBO J 20: 5392-5399.
41. Sjoblom, S., Brader, G., Koch, G., and Palva, E.T. (2006) Cooperation of two distinct ExpR regulators controls quorum sensing specificity and virulence in the plant pathogen Erwinia carotovora. Mol Microbiol 60: 1474-1489.
42. Sokol, P.A., Sajjan, U., Visser, M.B., Gingues, S., Forstner, J., and Kooi, C. (2003) The CepIR quorum-sensing system contributes to the virulence of Burkholderia cenocepacia respiratory infections. Microbiology 149: 3649-3658.
43. Stevens, A.M., Schuster, M., and Rumbaugh, K.P. (2012) Working together for the common good: cell-cell communication in bacteria. J Bacteriol 194: 2131-2141.
44. Tretyachenko-Ladokhina, V., Cocco, M.J., and Senear, D.F. (2006) Flexibility and adaptability in binding of E.coli cytidine repressor to different operators suggests a role in differential gene regulation. J Mol Biol 362: 271-286.
45. Tsai, C.S., and Winans, S.C. (2010) LuxR-type quorum-sensing regulators that are detached from common scents. Mol Microbiol 77: 1072-1082.
46. Tsai, C.S., and Winans, S.C. (2011) The quorum-hindered transcription factor YenR of Yersinia enterocolitica inhibits pheromone production and promotes motility via a small non-coding RNA. Mol Microbiol 80: 556-571.
47. Urbanowski, M.L., Lostroh, C.P., and Greenberg, E.P. (2004) Reversible acyl-homoserine lactone binding to purified Vibrio fischeri LuxR protein. J Bacteriol 186: 631-637.
48. Valentin-Hansen, P., Sogaard-Andersen, L., and Pedersen, H. (1996) A flexible partnership: the CytR anti-activator and the cAMP-CRP activator protein, comrades in transcription control. Mol Microbiol 20: 461-466.
49. Vandamme, P., Holmes, B., Vancanneyt, M., Coenye, T., Hoste, B., Coopman, R., etal. (1997) Occurrence of multiple genomovars of Burkholderia cepacia in cystic fibrosis patients and proposal of Burkholderia multivorans sp. nov. Int J Syst Bacteriol 47: 1188-1200.
50. Vandamme, P., Holmes, B., Coenye, T., Goris, J., Mahenthiralingam, E., LiPuma, J.J., and Govan, J.R. (2003) Burkholderia cenocepacia sp. nov. - a new twist to an old story. Res Microbiol 154: 91-96.
51. Vanlaere, E., Lipuma, J.J., Baldwin, A., Henry, D., De Brandt, E., Mahenthiralingam, E., etal. (2008) Burkholderia latens sp. nov., Burkholderia diffusa sp. nov., Burkholderia arboris sp. nov., Burkholderia seminalis sp. nov. and Burkholderia metallica sp. nov., novel species within the Burkholderia cepacia complex. Int J Syst Evol Microbiol 58: 1580-1590.
52. Vanlaere, E., Baldwin, A., Gevers, D., Henry, D., De Brandt, E., LiPuma, J.J., etal. (2009) Taxon K, a complex within the Burkholderia cepacia complex, comprises at least two novel species, Burkholderia contaminans sp. nov. and Burkholderia lata sp. nov. Int J Syst Evol Microbiol 59: 102-111.
53. Venturi, V., Friscina, A., Bertani, I., Devescovi, G., and Aguilar, C. (2004) Quorum sensing in the Burkholderia cepacia complex. Res Microbiol 155: 238-244.
54. Wei, Y., Ryan, G.T., Flores-Mireles, A.L., Costa, E.D., Schneider, D.J., and Winans, S.C. (2011) Saturation mutagenesis of a CepR binding site as a means to identify new quorum-regulated promoters in Burkholderia cenocepacia. Mol Microbiol 79: 616-632.
55. Weingart, C.L., White, C.E., Liu, S., Chai, Y., Cho, H., Tsai, C.S., etal. (2005) Direct binding of the quorum sensing regulator CepR of Burkholderia cenocepacia to two target promoters in vitro. Mol Microbiol 57: 452-467.
56. Wheelis, M. (1998) First shots fired in biological warfare. Nature 395: 213.
57. Zhu, J., and Winans, S.C. (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: 4832-4837.
58. Zhu, J., and Winans, S.C. (2001) The quorum-sensing transcriptional regulator TraR requires its cognate signaling ligand for protein folding, protease resistance, and dimerization. Proc Natl Acad Sci USA 98: 1507-1512.
59. Zhu, J., Beaber, J.W., More, M.I., Fuqua, C., Eberhard, A., and Winans, S.C. (1998) Analogs of the autoinducer 3-oxooctanoyl-homoserine lactone strongly inhibit activity of the TraR protein of Agrobacterium tumefaciens. J Bacteriol 180: 5398-5405.