The Burkholderia cenocepacia LysR-Type transcriptional regulator ShvR influences expression of quorum-sensing, protease, type II secretion, and afc genes

Journal of Bacteriology

Volumn 193, Issue 1, 2011, Pages 163-176

  O'Grady, Eoin P ^a   Nguyen, David T ^a   Weisskopf, Laure ^b   Eberl, Leo ^b   Sokol, Pamela A ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

AFC PROTEIN; ANTIFUNGAL AGENT; BACTERIAL PROTEIN; CCIIR PROTEIN; CEPIR PROTEIN; METALLOPROTEINASE; PROTEINASE; SHVR PROTEIN; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG; ZINC METALLOPROTEASE A; ZINC METALLOPROTEASE B;

ANTIFUNGAL ACTIVITY; ARTICLE; BACTERIAL GENE; BACTERIAL PHENOMENA AND FUNCTIONS; BURKHOLDERIA CENOCEPACIA; CONTROLLED STUDY; ENZYME ACTIVATION; GENE CONTROL; GENE EXPRESSION; GENE FUSION; GENETIC TRANSCRIPTION; GENOMICS; HYPHOMYCETES; MICROARRAY ANALYSIS; NONHUMAN; OPERON; PRIORITY JOURNAL; PROMOTER REGION; QUORUM SENSING; RHIZOCTONIA SOLANI; TYPE II SECRETION SYSTEM; WILD TYPE;

BACTERIAL PROTEINS; BIOFILMS; BURKHOLDERIA CENOCEPACIA; CULTURE MEDIA; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; MUTATION; OPERON; PEPTIDE HYDROLASES; PHENOTYPE; PROMOTER REGIONS, GENETIC; PROTEIN ARRAY ANALYSIS; QUORUM SENSING; TEMPERATURE; TIME FACTORS;

ANIMALIA; BURKHOLDERIA CENOCEPACIA; THANATEPHORUS CUCUMERIS;

EID: 78650078038     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00852-10     Document Type: Article

References (63)

1. Ausubel, F., R. Brent, R. Kingston, D. Moore, J. Seidman, J. Smith, and K. Struhl. 1989. Current protocols in molecular biology, vol. 1. John Wiley & Sons, Inc., New York, NY.
2. Baldwin, A., P. A. Sokol, J. Parkhill, and E. Mahenthiralingam. 2004. The Burkholderia cepacia epidemic strain marker is part of a novel genomic island encoding both virulence and metabolism-associated genes in Burkholderia cenocepacia. Infect. Immun. 72:1537-1547.
3. Bernier, S. P., A. L. Beeston, and P. A. Sokol. 2008. Detection of N-acyl homoserine lactones using a traI-luxCDABE-based biosensor as a highthroughput screening tool. BMC Biotechnol. 8:59.
4. Bernier, S. P., D. T. Nguyen, and P. A. Sokol. 2008. A LysR-type transcriptional regulator in Burkholderia cenocepacia influences colony morphology and virulence. Infect. Immun. 76:38-47.
5. Bernier, S. P., and P. A. Sokol. 2005. Use of suppression-subtractive hybridization to identify genes in the Burkholderia cepacia complex that are unique to Burkholderia cenocepacia. J. Bacteriol. 187:5278-5291.
6. Bjarnason, J., C. M. Southward, and M. G. Surette. 2003. Genomic profiling of iron-responsive genes in Salmonella enterica serovar Typhimurium by high-throughput screening of a random promoter library. J. Bacteriol. 185:4973-4982.
7. Boon, C., Y. Deng, L. H. Wang, Y. He, J. L. Xu, Y. Fan, S. Q. Pan, and L. H. Zhang. 2008. A novel DSF-like signal from Burkholderia cenocepacia interferes with Candida albicans morphological transition. ISME J. 2:27-36.
8. Chambers, C. E., E. I. Lutter, M. B. Visser, P. P. Law, and P. A. Sokol. 2006. Identification of potential CepR regulated genes using a cep box motif-based search of the Burkholderia cenocepacia genome. BMC Microbiol. 6:104.
9. Chapon-Herve, V., M. Akrim, A. Latifi, P. Williams, A. Lazdunski, and M. Bally. 1997. Regulation of the xcp secretion pathway by multiple quorum-sensing modulons in Pseudomonas aeruginosa. Mol. Microbiol. 24:1169-1178.
10. Corbett, C. R., M. N. Burtnick, C. Kooi, D. E. Woods, and P. A. Sokol. 2003. An extracellular zinc metalloprotease gene of Burkholderia cepacia. Microbiology 149:2263-2271.
11. Deng, Y., C. Boon, L. Eberl, and L. H. Zhang. 2009. Differential modulation of Burkholderia cenocepacia virulence and energy metabolism by the quorum-sensing signal BDSF and its synthase. J. Bacteriol. 191:7270-7278.
12. Dennis, J. J., and P. A. Sokol. 1995. Electrotransformation of Pseudomonas. Methods Mol. Biol. 47:125-133.
13. Duan, K., C. Dammel, J. Stein, H. Rabin, and M. G. Surette. 2003. Modulation of Pseudomonas aeruginosa gene expression by host microflora through interspecies communication. Mol. Microbiol. 50:1477-1491.
14. Fehlner-Gardiner, C. C., T. M. Hopkins, and M. A. Valvano. 2002. Identification of a general secretory pathway in a human isolate of Burkholderia vietnamiensis (formerly B. cepacia complex genomovar V) that is required for the secretion of hemolysin and phospholipase C activities. Microb. Pathog. 32:249-254.
15. Figurski, D. H., and D. R. Helinski. 1979. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc. Natl. Acad. Sci. U. S. A. 76:1648-1652.
16. Flannagan, R. S., T. Linn, and M. A. Valvano. 2008. A system for the construction of targeted unmarked gene deletions in the genus Burkholderia. Environ. Microbiol. 10:1652-1660.
17. Gingues, S., C. Kooi, M. B. Visser, B. Subsin, and P. A. Sokol. 2005. Distribution and expression of the ZmpA metalloprotease in the Burkholderia cepacia complex. J. Bacteriol. 187:8247-8255.
18. Goo, E., Y. Kang, H. Kim, and I. Hwang. 2010. Proteomic analysis of quorum sensing-dependent proteins in Burkholderia glumae. J. Proteome Res. 9:3184-3199.
19. Gotschlich, A., B. Huber, O. Geisenberger, A. Togl, A. Steidle, K. Riedel, P. Hill, B. Tummler, P. Vandamme, B. Middleton, M. Camara, P. Williams, A. Hardman, and L. Eberl. 2001. Synthesis of multiple N-acylhomoserine lactones is widespread among the members of the Burkholderia cepacia complex. Syst. Appl. Microbiol. 24:1-14.
20. Hoang, T. T., R. R. Karkhoff-Schweizer, A. J. Kutchma, and H. P. Schweizer. 1998. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212:77-86.
21. Holden, M. T., H. M. Seth-Smith, L. C. Crossman, M. Sebaihia, S. D. Bentley, A. M. Cerdeno-Tarraga, N. R. Thomson, N. Bason, M. A. Quail, S. Sharp, I. Cherevach, C. Churcher, I. Goodhead, H. Hauser, N. Holroyd, K. Mungall, P. Scott, D. Walker, B. White, H. Rose, P. Iversen, D. Mil-Homens, E. P. Rocha, A. M. Fialho, A. Baldwin, C. Dowson, B. G. Barrell, J. R. Govan, P. Vandamme, C. A. Hart, E. Mahenthiralingam, and J. Parkhill. 2009. The genome of Burkholderia cenocepacia J2315, an epidemic pathogen of cystic fibrosis patients. J. Bacteriol. 191:261-277.
22. Huber, B., F. Feldmann, M. Kothe, P. Vandamme, J. Wopperer, K. Riedel, and L. Eberl. 2004. Identification of a novel virulence factor in Burkholderia cenocepacia H111 required for efficient slow killing of Caenorhabditis elegans. Infect. Immun. 72:7220-7230.
23. Huber, B., K. Riedel, M. Hentzer, A. Heydorn, A. Gotschlich, M. Givskov, S. Molin, and L. Eberl. 2001. The cep quorum-sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility. Microbiology 147:2517-2528.
24. Isles, A., I. Maclusky, M. Corey, R. Gold, C. Prober, P. Fleming, and H. Levison. 1984. Pseudomonas cepacia infection in cystic fibrosis: an emerging problem. J. Pediatr. 104:206-210.
25. Kang, Y., R. Carlson, W. Tharpe, and M. A. Schell. 1998. Characterization of genes involved in biosynthesis of a novel antibiotic from Burkholderia cepacia BC11 and their role in biological control of Rhizoctonia solani. Appl. Environ. Microbiol. 64:3939-3947.
26. Kooi, C., B. Subsin, R. Chen, B. Pohorelic, and P. A. Sokol. 2006. Burkholderia cenocepacia ZmpB is a broad-specificity zinc metalloprotease involved in virulence. Infect. Immun. 74:4083-4093.
27. Kothe, M., M. Antl, B. Huber, K. Stoecker, D. Ebrecht, I. Steinmetz, and L. Eberl. 2003. Killing of Caenorhabditis elegans by Burkholderia cepacia is controlled by the cep quorum-sensing system. Cell. Microbiol. 5:343-351.
28. Leiske, D. L., A. Karimpour-Fard, P. S. Hume, B. D. Fairbanks, and R. T. Gill. 2006. A comparison of alternative 60-mer probe designs in an in situ-synthesized oligonucleotide microarray. BMC Genomics 7:72.
29. Lewenza, S., B. Conway, E. P. Greenberg, and P. A. Sokol. 1999. Quorum sensing in Burkholderia cepacia: identification of the LuxRI homologs CepRI. J. Bacteriol. 181:748-756.
30. Lewenza, S., and P. A. Sokol. 2001. Regulation of ornibactin biosynthesis and N-acyl-L-homoserine lactone production by CepR in Burkholderia cepacia. J. Bacteriol. 183:2212-2218.
31. Loutet, S. A., and M. A. Valvano. 2010. A decade of Burkholderia cenocepacia virulence determinant research. Infect. Immun. 78:4088-4100.
32. Lutter, E., S. Lewenza, J. J. Dennis, M. B. Visser, and P. A. Sokol. 2001. Distribution of quorum-sensing genes in the Burkholderia cepacia complex. Infect. Immun. 69:4661-4666.
33. Maddocks, S. E., and P. C. Oyston. 2008. Structure and function of the LysR-type transcriptional regulator (LTTR) family proteins. Microbiology 154:3609-3623.
34. Mahenthiralingam, E., T. Coenye, J. W. Chung, D. P. Speert, J. R. Govan, P. Taylor, and P. Vandamme. 2000. Diagnostically and experimentally useful panel of strains from the Burkholderia cepacia complex. J. Clin. Microbiol. 38:910-913.
35. Mahenthiralingam, E., T. A. Urban, and J. B. Goldberg. 2005. The multifarious, multireplicon Burkholderia cepacia complex. Nat. Rev. Microbiol. 3:144-156.
36. Malott, R. J., A. Baldwin, E. Mahenthiralingam, and P. A. Sokol. 2005. Characterization of the cciIR quorum-sensing system in Burkholderia cenocepacia. Infect. Immun. 73:4982-4992.
37. Malott, R. J., E. P. O'Grady, J. Toller, S. Inhulsen, L. Eberl, and P. A. Sokol. 2009. A Burkholderia cenocepacia orphan LuxR homolog is involved in quorum-sensing regulation. J. Bacteriol. 191:2447-2460.
38. McCarthy, Y., L. Yang, K. B. Twomey, A. Sass, T. Tolker-Nielsen, E. Mahenthiralingam, J. M. Dow, and R. P. Ryan. 2010. A sensor kinase recognizing the cell-cell signal BDSF (cis-2-dodecenoic acid) regulates virulence in Burkholderia cenocepacia. Mol. Microbiol.77:1220-1236.
39. Miller, V. L., and J. J. Mekalanos. 1988. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J. Bacteriol. 170:2575-2583.
40. Ng, W. L., and B. L. Bassler. 2009. Bacterial quorum-sensing network architectures. Annu. Rev. Genet. 43:197-222.
41. O'Grady, E. P., D. F. Viteri, R. J. Malott, and P. A. Sokol. 2009. Reciprocal regulation by the CepIR and CciIR quorum sensing systems in Burkholderia cenocepacia. BMC Genomics 10:441.
42. Rozen, S., and H. Skaletsky. 2000. Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132:365-386.
43. Ryan, R. P., Y. McCarthy, S. A. Watt, K. Niehaus, and J. M. Dow. 2009. Intraspecies signaling involving the diffusible signal factor BDSF (cis-2-dodecenoic acid) influences virulence in Burkholderia cenocepacia. J. Bacteriol. 191:5013-5019.
44. Saiman, L., and J. Siegel. 2004. Infection control in cystic fibrosis. Clin. Microbiol. Rev. 17:57-71.
45. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
46. Schmidt, S., J. F. Blom, J. Pernthaler, G. Berg, A. Baldwin, E. Mahenthiralingam, and L. Eberl. 2009. Production of the antifungal compound pyrrolnitrin is quorum sensing-regulated in members of the Burkholderia cepacia complex. Environ. Microbiol. 11:1422-1437.
47. Schweizer, H. P., and T. T. Hoang. 1995. An improved system for gene replacement and xylE fusion analysis in Pseudomonas aeruginosa. Gene 158:15-22.
48. Schweizer, H. P., T. Klassen, and T. T. Hoang. 1996. Improved methods for gene analysis and expression in Pseudomonas spp., 1995/05/26 ed. ASM Press, Washington, DC.
49. Sokol, P. A., R. J. Malott, K. Riedel, and L. Eberl. 2007. Communication systems in the genus Burkholderia: global regulators and targets for novel antipathogenic drugs. Future Microbiol. 2:555-563.
50. Sokol, P. A., D. E. Ohman, and B. H. Iglewski. 1979. A more sensitive plate assay for detection of protease production by Pseudomonas aeruginosa. J. Clin. Microbiol. 9:538-540.
51. Sokol, P. A., U. Sajjan, M. B. Visser, S. Gingues, J. Forstner, and C. Kooi. 2003. The CepIR quorum-sensing system contributes to the virulence of Burkholderia cenocepacia respiratory infections. Microbiology 149:3649-3658.
52. Somvanshi, V. S., P. Viswanathan, J. L. Jacobs, M. H. Mulks, G. W. Sundin, and T. A. Ciche. 2010. The type 2 secretion pseudopilin, gspJ, is required for multihost pathogenicity of Burkholderia cenocepacia AU1054. Infect. Immun. 78:4110-4121.
53. Subsin, B., C. E. Chambers, M. B. Visser, and P. A. Sokol. 2007. Identification of genes regulated by the cepIR quorum-sensing system in Burkholderia cenocepacia by high-throughput screening of a random promoter library. J. Bacteriol. 189:968-979.
54. Tomlin, K. L., R. J. Malott, G. Ramage, D. G. Storey, P. A. Sokol, and H. Ceri. 2005. Quorum-sensing mutations affect attachment and stability of Burkholderia cenocepacia biofilms. Appl. Environ. Microbiol. 71:5208-5218.
55. Uehlinger, S., S. Schwager, S. P. Bernier, K. Riedel, D. T. Nguyen, P. A. Sokol, and L. Eberl. 2009. Identification of specific and universal virulence factors in Burkholderia cenocepacia strains by using multiple infection hosts. Infect. Immun. 77:4102-4110.
56. Vandamme, P., D. Henry, T. Coenye, S. Nzula, M. Vancanneyt, J. J. LiPuma, D. P. Speert, J. R. Govan, and E. Mahenthiralingam. 2002. Burkholderia anthina sp. nov. and Burkholderia pyrrocinia, two additional Burkholderia cepacia complex bacteria, may confound results of new molecular diagnostic tools. FEMS Immunol. Med. Microbiol. 33:143-149.
57. Venturi, V., A. Friscina, I. Bertani, G. Devescovi, and C. Aguilar. 2004. Quorum sensing in the Burkholderia cepacia complex. Res. Microbiol. 155:238-244.
58. Vergunst, A. C., A. H. Meijer, S. A. Renshaw, and D. O'Callaghan. 2010. Burkholderia cenocepacia creates an intramacrophage replication niche in zebrafish embryos, followed by bacterial dissemination and establishment of systemic infection. Infect. Immun. 78:1495-1508.
59. Weingart, C. L., C. E. White, S. Liu, Y. Chai, H. Cho, C. S. Tsai, Y. Wei, N. R. Delay, M. R. Gronquist, A. Eberhard, and S. C. Winans. 2005. Direct binding of the quorum sensing regulator CepR of Burkholderia cenocepacia to two target promoters in vitro. Mol. Microbiol. 57:452-467.
60. Winsor, G. L., B. Khaira, T. Van Rossum, R. Lo, M. D. Whiteside, and F. S. Brinkman. 2008. The Burkholderia Genome Database: facilitating flexible queries and comparative analyses. Bioinformatics 24:2803-2804.
61. Yoder-Himes, D. R., P. S. Chain, Y. Zhu, O. Wurtzel, E. M. Rubin, J. M. Tiedje, and R. Sorek. 2009. Mapping the Burkholderia cenocepacia niche response via high-throughput sequencing. Proc. Natl. Acad. Sci. U. S. A. 106:3976-3981.
62. Yoder-Himes, D. R., K. T. Konstantinidis, and J. M. Tiedje. 2010. Identification of potential therapeutic targets for Burkholderia cenocepacia by comparative transcriptomics. PLoS One 5:e8724.
63. Zhu, J., J. W. Beaber, M. I. More, C. Fuqua, A. Eberhard, and S. C. Winans. 1998. Analogs of the autoinducer 3-oxooctanoyl-homoserine lactone strongly inhibit activity of the TraR protein of Agrobacterium tumefaciens. J. Bacteriol. 180:5398-5405.