Exposing the third chromosome of Burkholderia cepacia complex strains as a virulence plasmid

Molecular Microbiology

Volumn 83, Issue 2, 2012, Pages 362-378

  Agnoli, K ^a   Schwager, S ^a   Uehlinger, S ^a   Vergunst, A ^b,c   Viteri, D F ^d   Nguyen, D T ^d   Sokol, P A ^d   Carlier, A ^a   Eberl, L ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b CHU Nîmes   (France)

^c UNIV MONTPELLIER   (France)

^d UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EXOPOLYSACCHARIDE; FATTY ACID; PYRIMIDINE; XYLOSE;

ANIMAL TISSUE; ANTIFUNGAL ACTIVITY; ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATION; BACTERIUM MUTANT; BURKHOLDERIA CEPACIA COMPLEX; CAENORHABDITIS ELEGANS; CHROMOSOME 3; CHROMOSOME LOSS; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; MALE; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PLASMID; PRIORITY JOURNAL; PROTEIN DEGRADATION; RAT; REPLICON; SPECIES DIFFERENCE; STRAIN DIFFERENCE; TRANSPOSON; ZEBRA FISH;

ANIMALS; BURKHOLDERIA CEPACIA COMPLEX; BURKHOLDERIA INFECTIONS; CAENORHABDITIS ELEGANS; CHROMOSOMES, BACTERIAL; DISEASE MODELS, ANIMAL; DNA TRANSPOSABLE ELEMENTS; DROSOPHILA MELANOGASTER; LEPIDOPTERA; METABOLIC NETWORKS AND PATHWAYS; MUTAGENESIS, INSERTIONAL; MUTATION; PLASMIDS; RATS; SEQUENCE DELETION; SURVIVAL ANALYSIS; VIRULENCE FACTORS; ZEBRAFISH;

BACTERIA (MICROORGANISMS); BURKHOLDERIA CEPACIA COMPLEX; CAENORHABDITIS ELEGANS; DANIO RERIO; DROSOPHILA MELANOGASTER; GALLERIA MELLONELLA; RATTUS;

EID: 84855760653     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07937.x     Document Type: Article

References (61)

1. Bartholdson, S.J., Brown, A.R., Mewburn, B.R., Clarke, D.J., Fry, S.C., Campopiano, D.J., and Govan, J.R. (2008) Plant host and sugar alcohol induced exopolysaccharide biosynthesis in the Burkholderia cepacia complex. Microbiology 154: 2513-2521.
2. Bentley, S.D., and Parkhill, J. (2004) Comparative genomic structure of prokaryotes. Annu Rev Genet 38: 771-792.
3. Bernier, S.P., Silo-Suh, L., Woods, D.E., Ohman, D.E., and Sokol, P.A. (2003) Comparative analysis of plant and animal models for characterization of Burkholderia cepacia virulence. Infect Immun 71: 5306-5313.
4. Bernier, S.P., Nguyen, D.T., and Sokol, P.A. (2008) A LysR-type transcriptional regulator in Burkholderia cenocepacia influences colony morphology and virulence. Infect Immun 76: 38-47.
5. Cardona, S.T., Wopperer, J., Eberl, L., and Valvano, M.A. (2005) Diverse pathogenicity of Burkholderia cepacia complex strains in the Caenorhabditis elegans host model. FEMS Microbiol Lett 250: 97-104.
6. Carver, T., Berriman, M., Tivey, A., Patel, C., Böhme, U., Barrell, B.G., etal. (2008) Artemis and ACT: viewing, annotating and comparing sequences stored in a relational database. Bioinformatics 24: 2672-2676.
7. Casadaban, M.J., and Cohen, S.N. (1980) Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J Mol Biol 138: 179-207.
8. Cash, H.A., Woods, D.E., McCullough, B., Johanson, W.G., Jr, and Bass, J.A. (1979) A rat model of chronic respiratory infection with Pseudomonas aeruginosa. Am Rev Respir Dis 119: 453-459.
9. Clark, D.J., and Maaloe, O. (1967) DNA replication and division cycle in Escherichia coli. J Mol Biol 23: 99-112.
10. Clowes, R.C., and Hayes, W. (1968) Experiments in microbial genetics. Gene 142: 49-54.
11. Coenye, T., and Vandamme, P. (2003) Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ Microbiol 5: 719-729.
12. Coenye, T., Vandamme, P., Govan, J.R., and LiPuma, J.J. (2001) Taxonomy and identification of the Burkholderia cepacia complex. J Clin Microbiol 39: 3427-3436.
13. Corbett, C.R., Burtnick, M.N., Kooi, C., Woods, D.E., and Sokol, P.A. (2003) An extracellular zinc metalloprotease gene of Burkholderia cepacia. Microbiology 149: 2263-2271.
14. Darling, A.E., Mau, B., and Perna, N.T. (2010) progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 5: e11147.
15. Drevinek, P., and Mahenthiralingam, E. (2010) Burkholderia cenocepacia in cystic fibrosis: epidemiology and molecular mechanisms of virulence. Clin Microbiol Infect 16: 821-830.
16. Drevinek, P., Baldwin, A., Dowson, C.G., and Mahenthiralingam, E. (2008a) Diversity of the parB and repA genes of the Burkholderia cepacia complex and their utility for rapid identification of Burkholderia cenocepacia. BMC Microbiol 8: 44.
17. Drevinek, P., Holden, M.T., Ge, Z., Jones, A.M., Ketchell, I., Gill, R.T., and Mahenthiralingam, E. (2008b) Gene expression changes linked to antimicrobial resistance, oxidative stress, iron depletion and retained motility are observed when Burkholderia cenocepacia grows in cystic fibrosis sputum. BMC Infect Dis 8: 121.
18. Dubarry, N., Pasta, F., and Lane, D. (2006) ParABS systems of the four replicons of Burkholderia cenocepacia: new chromosome centromeres confer partition specificity. J Bacteriol 188: 1489-1496.
19. Egan, E.S., Fogel, M.A., and Waldor, M.K. (2005) Divided genomes: negotiating the cell cycle in prokaryotes with multiple chromosomes. Mol Microbiol 56: 1129-1138.
20. Geisenberger, O., Givskov, M., Riedel, K., Hoiby, N., Tummler, B., and Eberl, L. (2000) Production of N-acyl-L-homoserine lactones by P. aeruginosa isolates from chronic lung infections associated with cystic fibrosis. FEMS Microbiol Lett 184: 273-278.
21. Hanahan, D. (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166: 557-580.
22. Herrero, M., de Lorenzo, V., and Timmis, K.N. (1990) Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J Bacteriol 172: 6557-6567.
23. Herschleb, J., Ananiev, G., and Schwartz, D.C. (2007) Pulsed-field gel electrophoresis. Nat Protoc 2: 677-684.
24. Hoang, T.T., Karkhoff-Schweizer, R.R., Kutchma, A.J., and Schweizer, H.P. (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.
25. 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.
26. Huber, B., Feldmann, F., Kothe, M., Vandamme, P., Wopperer, J., Riedel, K., and Eberl, L. (2004) Identification of a novel virulence factor in Burkholderia cenocepacia H111 required for efficient slow killing of Caenorhabditis elegans. Infect Immun 72: 7220-7230.
27. Hynes, M.F., Quandt, J., Oconnell, M.P., and Puhler, A. (1989) Direct selection for curing and deletion of rhizobium plasmids using transposons carrying the Bacillus subtilis sacB gene. Gene 78: 111-120.
28. Jander, G., Rahme, L.G., and Ausubel, F.M. (2000) Positive correlation between virulence of Pseudomonas aeruginosa mutants in mice and insects. J Bacteriol 182: 3843-3845.
29. Kang, Y., Carlson, R., Tharpe, W., and Schell, M.A. (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.
30. Komatsu, H., Imura, Y., Ohori, A., Nagata, Y., and Tsuda, M. (2003) Distribution and organization of auxotrophic genes on the multichromosomal genome of Burkholderia multivorans ATCC 17616. J Bacteriol 185: 3333-3343.
31. 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.
32. 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.
33. Kovach, M.E., Elzer, P.H., Hill, D.S., Robertson, G.T., Farris, M.A., Roop, R.M., 2nd, and Peterson, K.M. (1995) Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166: 175-176.
34. Lessie, T.G., Hendrickson, W., Manning, B.D., and Devereux, R. (1996) Genomic complexity and plasticity of Burkholderia cepacia. FEMS Microbiol Lett 144: 117-128.
35. Li, L., Stoeckert, C.J., and Roos, D.S. (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13: 2178-2189.
36. Lu, S.E., Novak, J., Austin, F.W., Gu, G., Ellis, D., Kirk, M., etal. (2009) Occidiofungin, a unique antifungal glycopeptide produced by a strain of Burkholderia contaminans. Biochemistry 48: 8312-8321.
37. Mahenthiralingam, E., Urban, T.A., and Goldberg, J.B. (2005) The multifarious, multireplicon Burkholderia cepacia complex. Nat Rev Microbiol 3: 144-156.
38. Mahenthiralingam, E., Song, L.J., Sass, A., White, J., Wilmot, C., Marchbank, A., etal. (2011) Enacyloxins are products of an unusual hybrid modular polyketide synthase encoded by a cryptic Burkholderia ambifaria genomic island. Chem Biol 18: 665-677.
39. Meijer, A.H., and Spaink, H.P. (2011) Host-pathogen interactions made transparent with the zebrafish model. Curr Drug Targets 12: 1000-1017.
40. Moon, S.S., Kang, P.M., Park, K.S., and Kim, C.H. (1996) Plant growth promoting and fungicidal 4-quinolinones from Pseudomonas cepacia. Phytochemistry 42: 365-368.
41. Ni, B., Du, Z., Guo, Z., Zhang, Y., and Yang, R. (2008) Curing of four different plasmids in Yersinia pestis using plasmid incompatibility. Lett Appl Microbiol 47: 235-240.
42. Nishiyama, E., Ohtsubo, Y., Nagata, Y., and Tsuda, M. (2010) Identification of Burkholderia multivorans ATCC 17616 genes induced in soil environment by in vivo expression technology. Environ Microbiol 12: 2539-2558.
43. 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.
44. O'Grady, E.P., Nguyen, D.T., Weisskopf, L., Eberl, L., and Sokol, P.A. (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.
45. Riedel, K., and Eberl, L. (2007) Social behavior of members of the genus Burkholderia: quorum sensing and Biofilms. In Burkholderia, Molecular Microbiology and Genomics. Coenye, T., and Vandamme, P. (eds). Norfolk: Horizon Bioscience, pp. 251-282.
46. Rodley, P.D., Romling, U., and Tummler, B. (1995) A physical genome map of the Burkholderia cepacia type strain. Mol Microbiol 17: 57-67.
47. Romling, U., Fiedler, B., Bosshammer, J., Grothues, D., Greipel, J., von der Hardt, H., and Tummler, B. (1994) Epidemiology of chronic Pseudomonas aeruginosa infections in cystic fibrosis. J Infect Dis 170: 1616-1621.
48. Salanoubat, M., Genin, S., Artiguenave, F., Gouzy, J., Mangenot, S., Arlat, M., etal. (2002) Genome sequence of the plant pathogen Ralstonia solanacearum. Nature 415: 497-502.
49. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
50. Schmidt, S., Blom, J.F., Pernthaler, J., Berg, G., Baldwin, A., Mahenthiralingam, E., and Eberl, L. (2009) Production of the antifungal compound pyrrolnitrin is quorum sensing-regulated in members of the Burkholderia cepacia complex. Environ Microbiol 11: 1422-1437.
51. Seed, K.D., and Dennis, J.J. (2008) Development of Galleria mellonella as an alternative infection model for the Burkholderia cepacia complex. Infect Immun 76: 1267-1275.
52. Uehlinger, S., Schwager, S., Bernier, S.P., Riedel, K., Nguyen, D.T., Sokol, P.A., and Eberl, L. (2009) Identification of specific and universal virulence factors in Burkholderia cenocepacia strains by using multiple infection hosts. Infect Immun 77: 4102-4110.
53. Uraji, M., Suzuki, K., and Yoshida, K. (2002) A novel plasmid curing method using incompatibility of plant pathogenic Ti plasmids in Agrobacterium tumefaciens. Genes Genet Syst 77: 1-9.
54. Vandamme, P., and Dawyndt, P. (2011) Classification and identification of the Burkholderia cepacia complex: past, present and future. Syst Appl Microbiol 34: 87-95.
55. 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.
56. 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.
57. Vergunst, A.C., Meijer, A.H., Renshaw, S.A., and 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.
58. Vial, L., Lepine, F., Milot, S., Groleau, M.C., Dekimpe, V., Woods, D.E., and Deziel, E. (2008) Burkholderia pseudomallei, B. thailandensis, and B. ambifaria produce 4-hydroxy-2-alkylquinoline analogues with a methyl group at the 3 position that is required for quorum-sensing regulation. J Bacteriol 190: 5339-5352.
59. Wang, H.G., Liu, X.K., Feng, E.L., Zhu, L., Wang, D.S., Liao, X.R., and Wang, H.L. (2011) Curing the plasmid pXO2 from Bacillus anthracis A16 using plasmid incompatibility. Curr Microbiol 62: 703-709.
60. Yoder-Himes, D.R., Chain, P.S., Zhu, Y., Wurtzel, O., Rubin, E.M., Tiedje, J.M., and Sorek, R. (2009) Mapping the Burkholderia cenocepacia niche response via high-throughput sequencing. Proc Natl Acad Sci USA 106: 3976-3981.
61. Zlosnik, J.E., Hird, T.J., Fraenkel, M.C., Moreira, L.M., Henry, D.A., and Speert, D.P. (2008) Differential mucoid exopolysaccharide production by members of the Burkholderia cepacia complex. J Clin Microbiol 46: 1470-1473.