Involvement of a plasmid-encoded type IV secretion system in the plant tissue watersoaking phenotype of Burkholderia cenocepacia

Journal of Bacteriology

Volumn 186, Issue 18, 2004, Pages 6015-6024

  Engledow, Amanda S ^a   Medrano, Enrique G ^a,d   Mahenthiralingam, Eshwar ^b   LiPuma, John J ^c   Gonzalez, Carlos F ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOTOXIC FACTOR; PROTEIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; VIRB PROTEIN; VIRD4 PROTEIN;

ARTICLE; BACTERIAL STRAIN; BURKHOLDERIA CENOCEPACIA; BURKHOLDERIA CEPACIA; GENE; GENE CLUSTER; GENE SEQUENCE; GENETIC COMPLEMENTATION; GENETIC TRAIT; MUTAGENESIS; NONHUMAN; ONION; PHENOTYPE; PLANT DISEASE; PLANT TISSUE; PLASMID; PLASMOLYSIS; PRIORITY JOURNAL; PROTOPLAST; PTWB10 GENE; PTWB4 GENE; PTWC GENE; PTWD4 GENE; RNA TRANSLATION; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS;

BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; BURKHOLDERIA CEPACIA COMPLEX; BURKHOLDERIA INFECTIONS; CONJUGATION, GENETIC; CYTOTOXINS; DNA, BACTERIAL; GENE ORDER; GENES, BACTERIAL; GENETIC COMPLEMENTATION TEST; MULTIGENE FAMILY; MUTAGENESIS, INSERTIONAL; MUTAGENESIS, SITE-DIRECTED; ONIONS; PLANT DISEASES; PLASMIDS; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY; VIRULENCE FACTORS;

ALLIUM CEPA; BACTERIA (MICROORGANISMS); BURKHOLDERIA; BURKHOLDERIA CENOCEPACIA; BURKHOLDERIA CEPACIA; BURKHOLDERIA CEPACIA COMPLEX; NEGIBACTERIA;

EID: 4444280161     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.186.18.6015-6024.2004     Document Type: Article

References (74)

1. Bacon, D. J., R. A. Alm, D. H. Burr, L. Hu, D. J. Kopecko, D. P. Ewing, T. J. Trust, and P. Guerry. 2000. Involvement of a plasmid in virulence of Campylobacter jejuni 81-176. Infect. Immun. 68:4384-4390.
2. Baron, C., D. O'Callaghan, and E. Lanka. 2002. Bacterial secrets of secretion: Euro conference on the biology of type IV secretion processes. Mol. Microbiol. 43:1359-1365.
3. Bates, S., A. M. Cashmore, and B. M. Wilkins. 1998. IncP plasmids are unusually effective in mediating conjugation of Escherichia coli and Saccharomyces cerevisiae. J. Bacteriol. 180:6538-6543.
4. Blank, R. D., and D. B. Wilson. 1982. Isolation and characterization of a 2000-bp derivative of pBR322. Plasmid 7:278-289.
5. Bogdanove, A. J., J. F. Kim, Z. Wei, P. Kolchinsky, A. O. Charakowski, A. K. Conlin, A. Collmer, and S. V. Beer. 1998. Homology and functional similarity of an hrp-linked pathogenicity locus, dspEF, of Erwinia amylovora and the avirulence locus avrE of Pseudomonas syringae pathovar tomato. Proc. Natl. Acad. Sci. USA 95:1325-1330.
6. Boyer, H., and D. Roulland-Dussoix. 1969. A complementation analysis of the restriction and modification DNA in Escherichia coli. J. Mol. Biol. 41:115-117.
7. Burns, D. L. 2003. Type IV transporters of pathogenic bacteria. Curr. Opin. Microbiol. 6:29-34.
8. Chen, J. S., K. A. Witzmann, T. Spiker, R. J. Fink, and J. J. LiPuma. 2001. Endemicity and inter-city spread of Burkholderia cepacia genomovar III in cystic fibrosis. J. Pediatr. 139:643-649.
9. Christie, P. J., and J. P. Vogel. 2000. Bacterial type IV secretion: conjugation systems adapted to deliver effector molecules to host cells. Trends Microbiol. 8:354-360.
10. Christie, P. J. 2001. Type IV secretion: intercellular transfer of macromolecules by systems ancestrally related to conjugation machines. Mol. Microbiol. 40:294-305.
11. Coenye, T., P. Vandamme, J. R. W. Govan, and J. J. LiPuma. 2001. Taxonomy and identification of the Burkholderia cepacia complex. J. Clin. Microbiol. 39:3427-3436.
12. Coenye, T., and J. J. LiPuma. 2002. Multilocus restriction typing: a novel tool for studying global epidemiology of Burkholderia cepacia complex infection in cystic fibrosis. J. Infect. Dis. 185:1454-1462.
13. Datta, N., and R. W. Hedges. 1972. Trimethoprim resistance conferred by W plasmids in Enterobacteriaceae. J. Gen. Microbiol. 72:349-355.
14. DeFeyter, R., C. I. Kado, and D. W. Gabriel. 1990. Small, stable shuttle vectors for use in Xanthomonas. Gene 88:65-72.
15. Dennis, J. J., and G. J. Zylstra. 1998. Plasposons: modular self-cloning minitransposon derivatives for rapid genetic analysis of gram-negative bacterial genomes. Appl. Environ. Microbiol. 64:2710-2715.
16. Dhar, S. K., R. K. Soni, B. K. Das, and G. Mukhopadhyay. 2003. Molecular mechanism of action of major Helicobacterpylori virulence factors. Mol. Cell. Biochem. 253:207-215.
17. Dillard, J. P., and H. S. Seifert. 2001. A variable genetic island specific for Neisseria gonorrhoeae is involved in providing DNA for natural transformation and is found more often in disseminated infection isolates. Mol. Microbiol. 41:263-277.
18. Ding, Z., K. Atmakuri, and P. J. Christie. 2003. The outs and ins of bacterial type IV secretion substrates. Trends Microbiol. 11:527-535.
19. Fekete, R. A., and L. S. Frost. 2000. Mobilization of chimeric oriT plasmids by F and R100-1: role of relaxosome formation in defining plasmid specificity. J. Bacteriol. 182:4022-4027.
20. Figurski, D., 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. USA 76:1648-1652.
21. Fischer, W., J. Puls, R. Buhrdorf, B. Gebert, S. Odenbreit, and R. Hass. 2001. Systemic mutagenesis of the Helicobacter pylori cag pathogenicity island: essential genes for CagA translocation in host cells and induction of interleukin-8. Mol. Microbiol. 42:1337-1348.
22. Frederick, R. D., M. Ahmad, D. R. Majerczak, A. S. Arroyo-Rodriguez, S. Manulis, and D. L. Coplin. 2001. Genetic organization of the Pantoea stewartii subsp. stewartii hrp gene cluster and sequence analysis of the hrpA, hrpC, hrpN, and wtsE operons. Mol. Plant-Microbe Interact. 14:1213-1222.
23. Gonzalez, C. F., and A. K. Vidaver. 1979. Bacteriocin, plasmid, and pectolytic diversity in Pseudomonas cepacia of clinical and plant origin. J. Gen. Microbiol. 110:161-170.
24. Gonzalez, C. F., E. A. Pettit, V. A. Valadez, and E. Provin. 1997. Mobilization, cloning, and sequence determination of a plasmid-encoded polygalacturonase from a phytopathogenic Burkholderia (Pseudomonas) cepacia. Mol. Plant-Microbe Interact. 10:840-851.
25. Grohmann, E., G. Muth, and M. Espinosa. 2003. Conjugative plasmid transfer in gram-positive bacteria. Microbiol. Mol. Biol. Rev. 67:277-301.
26. Hamilton, H. I., K. J. Schwartz, and J. P. Dillard. 2001. Insertion-duplication mutagenesis of Neisseria: use in characterization of DNA transfer genes in the gonococcal genetic island. J. Bacteriol. 186:4718-4726.
27. Herrero, M., V. de Lorenzo, and K. N. Timmis. 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.
28. Hodgman, T. C. 1988. A new superfamily of replicative proteins. Nature 333:22-23.
29. Hofreuter, D., S. Odenbreit, and R. Haas. 2001. Natural transformation competence in Helicobacter pylori is mediated by the basic components of a type IV secretion system. Mol. Microbiol. 41:379-391.
30. Hutchison M. L., I. R. Poxton, and J. R. W. Govan. 1998. Burkholderia cepacia produces a hemolysin that is capable of inducing apoptosis and degranulation of mammalian phagocytes. Infect. Immun. 66:2033-2039.
31. Jakubowski, S. J., V. Krishnamoorthy, and P. J. Christie. 2003. Agrobacterium tumefaciens VirB6 protein participates in formation of VirB7 and VirB9 complexes required for type IV secretion. J. Bacteriol. 185:2867-2878.
32. Johnson, W. M., S. D. Tyler, and K. R. Rozee. 1994. Linkage analysis of geographic and clinical clusters in Pseudomonas cepacia infections by multilocus enzyme electrophoresis and ribotyping. J. Clin. Microbiol. 32:924-930.
33. Jones, R. W., A. O. Jackson, and T. H. Morris. 1990. Defective- interfering RNAs and elevated temperatures inhibit replication of tomato bushy stunt virus in inoculated protoplasts. Virology 176:539-545.
34. Karlin, S. 2001. Detecting anomalous gene clusters and pathogenicity islands in diverse bacterial genomes. Trends Microbiol. 9:335-343.
35. Kersulyte, D., B. Velapatino, A. K. Mukhopadhyay, L. Cahuayne, A. Bussalleu, J. Combe, R. H. Gilman, and D. E. Berg. 2003. Cluster of type IV secretion genes in Helicobacter pylori's plasticity zone. J. Bacteriol. 185:3764-3772.
36. Koch, A., and S. Putnam. 1971. Sensitive biuret method for determination of protein in an impure system such as whole bacteria. Anal. Biochem. 44:239-245.
37. Kumar, R. B., and A. Das. 2002. Polar location and functional domains of the Agrobacterium tumefaciens DNA transfer protein VirD4. Mol. Microbiol. 43:1523-1532.
38. Lawley, T. D., W. A. Klimke, M. J. Gubbins, and L. S. Frost. 2003. F factor conjugation is a true type IV secretion system. FEMS Microbiol. Lett. 224:1-15.
39. Ledson, M. J., M. J. Gallagher, M. Jackson, C. A. Hart, and M. J. Walshaw. 2002. Outcome of Burkholderia cepacia colonization in an adult cystic fibrosis centre. Thorax 57:142-145.
40. 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.
41. LiPuma, J. J. 1998. Burkholderia cepacia-management issues and new insights. Clin. Chest Med. 19:473-486.
42. LiPuma, J. J., T. Spilker, L. Gill, P. W. Campbell, L. Liu, and E. Mahenthiralingam. 2001. Disproportionate distribution of Burkholderia cepacia complex species and transmissibility factors in cystic fibrosis. Am. J. Resp. Crit. Care Med. 164:92-96.
43. LiPuma, J. J. 2003. Burkholderia cepacia complex as human pathogens. J. Nematol. 35:212-217.
44. Llosa, M., S. Bolland, and F. de la Cruz. 1994. Genetic organization of the conjugal DNA processing region of the IncW plasmid R388. J. Mol. Biol. 233:448-464.
45. Llosa, M., S. Zunzunegui, and F. de la Cruz. 2003. Conjugative coupling proteins interact with cognate and heterologous VirB10-like proteins while exhibiting specificity for cognate relaxosomes. Proc. Natl. Acad. Sci. USA 100:10465-10470.
46. Macnab, R. M. 1999. The bacterial flagellum: reversible rotary propeller and type III export apparatus. J. Bacteriol. 181:7149-7153.
47. Mahenthiralingam, E., T. Coenye, J. W. Chung, D. P. Speert, J. R. W. 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.
48. Matson, S. W., W. C. Nelson, and B. S. Morton. 1993. Characterization of the reaction product of the ortT nicking reaction catalyzed by Escherichia coli DNA helicase I. J. Bacteriol. 175:2599-2606.
49. Matson, S. W., J. K. Sampson, and D. R. N. Byrd. 2001. F plasmid conjugative DNA transfer. J. Biol. Chem. 276:2372-2379.
50. Medrano, E. G. 2002. Ph.D. thesis. Texas A&M University, College Station, Tex.
51. Moncalián, G., E. CabeŸon, I. Alkorta, M. Valle, F. Moro, J. M. Valpuesta, F. M. Goñi, and F. de la Cruz. 1999. Characterization of ATP and DNA binding activities of TrwB, the coupling protein essential in plasmid R388 conjugation. J. Biol. Chem. 274:36117-36124.
52. Nagai, H., and C. R. Roy. 2003. Show me the substrates: modulation of host cell function by type IV secretion systems. Cell. Microbiol. 5:373-383.
53. Planet, P. J., S. C. Kachlany, R. DeSalle, and D. H. Figurski. 2001. Phylogeny of genes for secretion NTPases: identification of the widespread tadA subfamily and development of a diagnostic key for gene classification. Proc. Natl. Acad. Sci. USA 98:2503-2508.
54. Plano, G. V., J. B. Day, and F. Ferracci. 2001. Type III export: new uses for an old pathway. Mol. Microbiol. 40:284-293.
55. Quandt, J., and M. F. Hynes. 1993. Versatile suicide vectors which allow direct selection for gene replacement in gram-negative bacteria. Gene 127:15-21.
56. Sajjan, U. S., F. A. Sylvester, and J. Forstner. 2000. Cable-piliated Burkholderia cepacia binds to cytokeratin 13 of epithelial cells. Infect. Immun. 68:1787.
57. Sajjan, U. S., Y. Wu, G. Kent, and J. Forstner. 2000. Preferential adherence of cable-piliated Burkholderia cepacia to respiratory epithelia of CF knockout mice and human CF lung explants. J. Med. Microbiol. 49:875-882.
58. Salmond, G. P. C. 1994. Secretion of extracellular virulence factors by plant pathogenic bacteria. Annu. Rev. Phytopathol. 32:181-200.
59. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
60. Schröder, G., S. Krause, E. L. Zechner, B. Traxler, H. Yeo, R. Lurz, G. Waksman, and E. Lanka. 2002. TraG-like proteins of DNA transfer systems and of the Helicobacter pylori type IV secretion system: inner membrane gate for exported substrates? J. Bacteriol. 184:2767-2779.
61. Schröder, G., and E. Lanka. 2003. TraG-like proteins of type IV secretion systems: functional dissection of the multiple activities of TraG (RP4) and TrwB (R388). J. Bacteriol. 185:4371-4381.
62. 5-Oxygenase. Infect. Immun. 67:443-445.
63. Swarup, S., R. DeFeyter, R. H. Brlansky, and D. W. Gabriel. 1991. A pathogenicity locus from Xanthomonas citri enables strains from several pathovars of Xanthomonas campestris to elicit cankerlike lesions on citrus. Phytopathology 81:802-809.
64. Tomasek, P. H., B. Frantz, U. M. Sangodkar, R. A. Haugland, and A. M. Chakrabarty. 1989. Characterization and nucleotide sequence determination of a repeat element isolated from a 2, 4, 5-T degrading strain of Pseudomonas cepacia. Gene 76:227-238.
65. Vandamme, P., D. Henry, T. Coenye, S. Nzula, M. Vancanneyt, J. J. LiPuma, D. P. Speert, J. R. W. Govan, and E. Mahenthiralingam. 2002. Burkholderia anthina sp. nov and Burkholderia pyrrocinia, two additional Burkholderia cepacia complex bacteria, may confound test results of new molecular diagnostic tools. FEMS Immunol. Med. Microbiol. 33:143-149.
66. Vandamme, P., B. Holmes, T. Coenye, E. Mahenthiralingam, J. J. LiPuma, and J. R. W. Govan. 2003. Burkholderia cenocepacia sp. nov., a new twist on an old story. Res. Microbiol. 154:91-96.
67. Vasil, M. L., D. P. Krieg, J. S. Kuhns, J. W. Ogle, V. D. Shortridge, R. M. Ostroff, and A. I. Vasil. 1990. Molecular analysis of hemolytic and phospholipase activities of Pseudomonas cepacia. Infect. Immun. 58:4020-4029.
68. Vermis, K., T. Coenye, J. J. LiPuma, E. Mahenthiralingam, H. J. Nelis, and P. Vandamme. 2004. Identification of Burkholderia dolosa sp. nov. (formerly Burkholderia cepacia genomovar VI). Int. J. Syst. Evol. Microbiol. 54:689-691.
69. Vogel, H. J., and D. M. Bonner. 1965. Acetylornithinase of Escherichia coli partial purification and some properties. J. Biol. Chem. 281:97-106.
70. Walker, J. E., M. Saraste, M. J. Runswick, and N. J. Gay. 1982. Distantly related sequence in the alpha- and beta-subunits of ATP sythase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1:945-951.
71. Ward, D. V., and P. C. Zambryski. 2001. The six functions of Agrobacterium VirE. Proc. Natl. Acad. Sci. USA 98:385-386.
72. Waters, V. L. 2001. Conjugation between bacterial and mammalian cells. Nat. Genet. 29:375-376.
73. Wilkins, B. M., and A. T. Thomas. 2000. DNA-independent transport of plasmid primase protein between bacteria by the I1 conjugation system. Mol. Microbiol. 38:650-657.
74. Yeo, H., and G. Waksman. 2004. Unveiling molecular scaffolds of the type IV secretion system. J. Bacteriol. 186:1919-1926.