A unique regulator contributes to quorum sensing and virulence in Burkholderia cenocepacia

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  O'Grady, Eoin P ^a   Viteri, Duber F ^a   Sokol, Pamela A ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

FLAGELLIN; LACTONE; METALLOPROTEINASE; N ACYLHOMOSERINE LACTONE; N OCTANOYL L HOMOSERINE LACTONE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CEPR PROTEIN, BURKHOLDERIA; DRUG DERIVATIVE; GAMMA BUTYROLACTONE; HOMOSERINE LACTONE; LIGASE; N ACYLHOMOSERINE LACTONE SYNTHASE; N-ACYLHOMOSERINE LACTONE SYNTHASE; PRIMER DNA; ZMPA PROTEIN, BURKHOLDERIA CENOCEPACIA;

AIDA GENE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; BCAM1871 GENE; BURKHOLDERIA CENOCEPACIA; CAENORHABDITIS ELEGANS; CCIIR GENE; CEPI GENE; CEPR GENE; CONTROLLED STUDY; FLIC GENE; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSCRIPTION; MALE; NONHUMAN; OPEN READING FRAME; PARASITE SURVIVAL; QUORUM SENSING; RAT; RESPIRATORY TRACT INFECTION; ZMPA GENE; ZMPB GENE; ANIMAL; GENE EXPRESSION REGULATION; GENE LOCUS; GENETICS; KAPLAN MEIER METHOD; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT;

BURKHOLDERIA; BURKHOLDERIA CENOCEPACIA; INVERTEBRATA; RATTUS; VERTEBRATA;

4-BUTYROLACTONE; ANIMALS; BACTERIAL PROTEINS; BURKHOLDERIA CENOCEPACIA; CAENORHABDITIS ELEGANS; DNA PRIMERS; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC LOCI; KAPLAN-MEIER ESTIMATE; LIGASES; METALLOENDOPEPTIDASES; OPEN READING FRAMES; QUORUM SENSING; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; RESPIRATORY TRACT INFECTIONS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84862090238     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037611     Document Type: Article

References (71)

1. Ng WL, Bassler BL, (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43: 197-222.
2. Ryan RP, Dow JM, (2008) Diffusible signals and interspecies communication in bacteria. Microbiology 154: 1845-1858.
3. Subramoni S, Venturi V, (2009) LuxR-family 'solos': bachelor sensors/regulators of signalling molecules. Microbiology 155: 1377-1385.
4. Loutet SA, Valvano MA, (2010) A decade of Burkholderia cenocepacia virulence determinant research. Infect Immun 78: 4088-4100.
5. Mahenthiralingam E, Urban TA, Goldberg JB, (2005) The multifarious, multireplicon Burkholderia cepacia complex. Nat Rev Microbiol 3: 144-156.
6. Eberl L, Tummler B, (2004) Pseudomonas aeruginosa and Burkholderia cepacia in cystic fibrosis: genome evolution, interactions and adaptation. Int J Med Microbiol 294: 123-131.
7. Speert DP, (2002) Advances in Burkholderia cepacia complex. Paediatr Respir Rev 3: 230-235.
8. Jones AM, Dodd ME, Govan JR, Barcus V, Doherty CJ, et al. (2004) Burkholderia cenocepacia and Burkholderia multivorans: influence on survival in cystic fibrosis. Thorax 59: 948-951.
9. Isles A, Maclusky I, Corey M, Gold R, Prober C, et al. (1984) Pseudomonas cepacia infection in cystic fibrosis: an emerging problem. J Pediatr 104: 206-210.
10. Magalhaes M, Doherty C, Govan JR, Vandamme P, (2003) Polyclonal outbreak of Burkholderia cepacia complex bacteraemia in haemodialysis patients. J Hosp Infect 54: 120-123.
11. Lewenza S, Conway B, Greenberg EP, Sokol PA, (1999) Quorum sensing in Burkholderia cepacia: identification of the LuxRI homologs CepRI. J Bacteriol 181: 748-756.
12. Malott RJ, Baldwin A, Mahenthiralingam E, Sokol PA, (2005) Characterization of the cciIR Quorum-Sensing System in Burkholderia cenocepacia. Infect Immun 73: 4982-4992.
13. Malott RJ, O'Grady EP, Toller J, Inhulsen S, Eberl L, et al. (2009) A Burkholderia cenocepacia orphan LuxR homolog is involved in quorum-sensing regulation. J Bacteriol 191: 2447-2460.
14. Gotschlich A, Huber B, Geisenberger O, Togl A, Steidle A, et al. (2001) Synthesis of multiple N-acylhomoserine lactones is wide-spread among the members of the Burkholderia cepacia complex. Syst Appl Microbiol 24: 1-14.
15. Baldwin A, Sokol PA, Parkhill J, Mahenthiralingam E, (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.
16. Lewenza S, Sokol PA, (2001) Regulation of ornibactin biosynthesis and N-acyl-L-homoserine lactone production by CepR in Burkholderia cepacia. J Bacteriol 183: 2212-2218.
17. McKeon SA, Nguyen DT, Viteri DF, Zlosnik JE, Sokol PA, (2011) Functional quorum sensing systems are maintained during chronic Burkholderia cepacia complex infections in patients with cystic fibrosis. J Infect Dis 203: 383-392.
18. Weingart CL, White CE, Liu S, Chai Y, Cho H, et al. (2005) Direct binding of the quorum sensing regulator CepR of Burkholderia cenocepacia to two target promoters in vitro. Mol Microbiol 57: 452-467.
19. O'Grady EP, Viteri DF, Malott RJ, Sokol PA, (2009) Reciprocal regulation by the CepIR and CciIR quorum sensing systems in Burkholderia cenocepacia. BMC Genomics 10: 441.
20. Chambers CE, Lutter EI, Visser MB, Law PP, Sokol PA, (2006) Identification of potential CepR regulated genes using a cep box motif-based search of the Burkholderia cenocepacia genome. BMC Microbiol 6: 104.
21. Huber B, Riedel K, Hentzer M, Heydorn A, Gotschlich A, et al. (2001) The cep quorum-sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility. Microbiology 147: 2517-2528.
22. Kooi C, Subsin B, Chen R, Pohorelic B, Sokol PA, (2006) Burkholderia cenocepacia ZmpB is a broad-specificity zinc metalloprotease involved in virulence. Infect Immun 74: 4083-4093.
23. Sokol PA, Sajjan U, Visser MB, Gingues S, Forstner J, et al. (2003) The CepIR quorum-sensing system contributes to the virulence of Burkholderia cenocepacia respiratory infections. Microbiology 149: 3649-3658.
24. Subsin B, Chambers CE, Visser MB, Sokol PA, (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.
25. Tomlin KL, Malott RJ, Ramage G, Storey DG, Sokol PA, et al. (2005) Quorum-sensing mutations affect attachment and stability of Burkholderia cenocepacia biofilms. Appl Environ Microbiol 71: 5208-5218.
26. Kothe M, Antl M, Huber B, Stoecker K, Ebrecht D, et al. (2003) Killing of Caenorhabditis elegans by Burkholderia cepacia is controlled by the cep quorum-sensing system. Cell Microbiol 5: 343-351.
27. Uehlinger S, Schwager S, Bernier SP, Riedel K, Nguyen DT, et al. (2009) Identification of specific and universal virulence factors in Burkholderia cenocepacia strains by using multiple infection hosts. Infect Immun 77: 4102-4110.
28. Vergunst AC, Meijer AH, Renshaw SA, O'Callaghan D, (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.
29. Huber B, Riedel K, Kothe M, Givskov M, Molin S, et al. (2002) Genetic analysis of functions involved in the late stages of biofilm development in Burkholderia cepacia H111. Mol Microbiol 46: 411-426.
30. O'Grady EP, Nguyen DT, Weisskopf L, Eberl L, Sokol PA, (2011) The Burkholderia cenocepacia LysR-type transcriptional regulator ShvR influences expression of quorum-sensing, protease, type II secretion, and afc genes. J Bacteriol 193: 163-176.
31. Dehal PS, Joachimiak MP, Price MN, Bates JT, Baumohl JK, et al. (2009) MicrobesOnline: an integrated portal for comparative and functional genomics. Nucleic Acids Res 38: D396-400.
32. Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, et al. (2011) CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39: D225-229.
33. Corbett CR, Burtnick MN, Kooi C, Woods DE, Sokol PA, (2003) An extracellular zinc metalloprotease gene of Burkholderia cepacia. Microbiology 149: 2263-2271.
34. Bernier SP, Nguyen DT, Sokol PA, (2008) A LysR-type transcriptional regulator in Burkholderia cenocepacia influences colony morphology and virulence. Infect Immun 76: 38-47.
35. Subramoni S, Nguyen DT, Sokol PA, (2011) Burkholderia cenocepacia ShvR-Regulated Genes That Influence Colony Morphology, Biofilm Formation, and Virulence. Infect Immun 79: 2984-2997.
36. Huber B, Feldmann F, Kothe M, Vandamme P, Wopperer J, et al. (2004) Identification of a novel virulence factor in Burkholderia cenocepacia H111 required for efficient slow killing of Caenorhabditis elegans. Infect Immun 72: 7220-7230.
37. Aguilar C, Friscina A, Devescovi G, Kojic M, Venturi V, (2003) Identification of quorum-sensing-regulated genes of Burkholderia cepacia. J Bacteriol 185: 6456-6462.
38. Riedel K, Arevalo-Ferro C, Reil G, Gorg A, Lottspeich F, et al. (2003) Analysis of the quorum-sensing regulon of the opportunistic pathogen Burkholderia cepacia H111 by proteomics. Electrophoresis 24: 740-750.
39. Hedl M, Tabernero L, Stauffacher CV, Rodwell VW, (2004) Class II 3-hydroxy-3-methylglutaryl coenzyme A reductases. J Bacteriol 186: 1927-1932.
40. Kim J, Kang Y, Choi O, Jeong Y, Jeong JE, et al. (2007) Regulation of polar flagellum genes is mediated by quorum sensing and FlhDC in Burkholderia glumae. Mol Microbiol 64: 165-179.
41. Wei Y, Ryan GT, Flores-Mireles AL, Costa ED, Schneider DJ, et al. (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.
42. Lamothe J, Huynh KK, Grinstein S, Valvano MA, (2007) Intracellular survival of Burkholderia cenocepacia in macrophages is associated with a delay in the maturation of bacteria-containing vacuoles. Cell Microbiol 9: 40-53.
43. Edwards A, Frederix M, Wisniewski-Dye F, Jones J, Zorreguieta A, et al. (2009) The cin and rai quorum-sensing regulatory systems in Rhizobium leguminosarum are coordinated by ExpR and CinS, a small regulatory protein coexpressed with CinI. J Bacteriol 191: 3059-3067.
44. Daniels R, Reynaert S, Hoekstra H, Verreth C, Janssens J, et al. (2006) Quorum signal molecules as biosurfactants affecting swarming in Rhizobium etli. Proc Natl Acad Sci U S A 103: 14965-14970.
45. Frederix M, Edwards A, McAnulla C, Downie JA, (2011) Co-ordination of quorum-sensing regulation in Rhizobium leguminosarum by induction of an anti-repressor. Mol Microbiol 81: 994-1007.
46. Williams P, Camara M, (2009) Quorum sensing and environmental adaptation in Pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules. Curr Opin Microbiol 12: 182-191.
47. Patankar AV, Gonzalez JE, (2009) Orphan LuxR regulators of quorum sensing. FEMS Microbiol Rev 33: 739-756.
48. Venturi V, Rampioni G, Pongor S, Leoni L, (2011) The virtue of temperance: built-in negative regulators of quorum sensing in Pseudomonas. Mol Microbiol 82: 1060-1070.
49. Coggan KA, Wolfgang MC, (2012) Global regulatory pathways and cross-talk control Pseudomonas aeruginosa environmental lifestyle and virulence phenotype. Curr Issues Mol Biol 14: 47-70.
50. Bernier SP, Beeston AL, Sokol PA, (2008) Detection of N-acyl homoserine lactones using a traI-luxCDABE-based biosensor as a high-throughput screening tool. BMC Biotechnol 8: 59.
51. Bernier SP, Silo-Suh L, Woods DE, Ohman DE, Sokol PA, (2003) Comparative analysis of plant and animal models for characterization of Burkholderia cepacia virulence. Infect Immun 71: 5306-5313.
52. Sokol PA, Ohman DE, Iglewski BH, (1979) A more sensitive plate assay for detection of protease production by Pseudomanas aeruginosa. J Clin Microbiol 9: 538-540.
53. Sambrook J, Fritsch EF, Maniatis T, (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor NY.
54. Ausubel F, Brent R, Kingston R, Moore D, Seidman J, et al. (1989) Current protocols in molecular biology: John Wiley & Sons, Inc., New York.
55. Rozen S, Skaletsky H, (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 365-386.
56. Dennis JJ, Sokol PA, (1995) Electrotransformation of Pseudomonas. Methods Mol Biol 47: 125-133.
57. Flannagan RS, Linn T, Valvano MA, (2008) A system for the construction of targeted unmarked gene deletions in the genus Burkholderia. Environ Microbiol 10: 1652-1660.
58. Schmittgen TD, Livak KJ, (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101-1108.
59. Cash HA, Woods DE, McCullough B, Johanson WG Jr, Bass JA, (1979) A rat model of chronic respiratory infection with Pseudomonas aeruginosa. Am Rev Respir Dis 119: 453-459.
60. Tan MW, Mahajan-Miklos S, Ausubel FM, (1999) Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis. Proc Natl Acad Sci U S A 96: 715-720.
61. Brenner S, (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
62. Miller VL, Mekalanos JJ, (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.
63. Mahenthiralingam E, Coenye T, Chung JW, Speert DP, Govan JR, et al. (2000) Diagnostically and experimentally useful panel of strains from the Burkholderia cepacia complex. J Clin Microbiol 38: 910-913.
64. Holloway BW, Romling U, Tummler B, (1994) Genomic mapping of Pseudomonas aeruginosa PAO. Microbiology 140 (Pt 11): 2907-2929.
65. Zhu J, Beaber JW, More MI, Fuqua C, Eberhard A, et al. (1998) Analogs of the autoinducer 3-oxooctanoyl-homoserine lactone strongly inhibit activity of the TraR protein of Agrobacterium tumefaciens. J Bacteriol 180: 5398-5405.
66. Figurski DH, Helinski DR, (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.
67. Schweizer HP, Klassen T, Hoang TT, (1996) Improved methods for gene analysis and expression in Pseudomonas spp. In: T. Nakazawa KF, Hass D, Silver S, editors. Washington, D.C. ASM Press pp. 229-237.
68. Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, et al. (1995) Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166: 175-176.
69. Lewenza S, Visser MB, Sokol PA, (2002) Interspecies communication between Burkholderia cepacia and Pseudomonas aeruginosa. Can J Microbiol 48: 707-716.
70. Duan K, Dammel C, Stein J, Rabin H, Surette MG, (2003) Modulation of Pseudomonas aeruginosa gene expression by host microflora through interspecies communication. Mol Microbiol 50: 1477-1491.
71. Sibley CD, Duan K, Fischer C, Parkins MD, Storey DG, et al. (2008) Discerning the complexity of community interactions using a Drosophila model of polymicrobial infections. PLoS Pathog 4: e1000184.