1887

Abstract

Two large tetracycline resistance (Tc) plasmids have been completely sequenced, the pTet plasmid (45·2 kb) from strain 81-176 and a plasmid pCC31 (44·7 kb) from strain CC31 that was isolated from a human case of severe gastroenteritis in the UK. Both plasmids are mosaic in structure, having homologues of genes found in a variety of different commensal and pathogenic bacteria, but nevertheless, showed striking similarities in DNA sequence and overall gene organization. Several predicted proteins encoded by genes involved in conjugation showed highest homology to proteins found in , a periodontal pathogen. In addition to replication- and conjugation-associated genes, both plasmids carried a (O) gene encoding tetracycline resistance, a 6 kb ORF encoding a putative methylase and a number of genes of unknown function. The pTet plasmid co-exists in strain 81-176 with a smaller, previously characterized, non-conjugative plasmid pVir that also encodes a type IV secretion system (T4SS) that may affect virulence. In contrast, the T4SS encoded by pTet and pCC31 are shown to mediate bacterial conjugation between . The possible origin and evolution of pCC31 and pTet is discussed.

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2004-10-01
2019-10-17
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References

  1. Alm, R. A. & Trust, T. J. ( 1999; ). Analysis of the genetic diversity of Helicobacter pylori: the tale of two genomes. J Mol Med 77, 834–846.[CrossRef]
    [Google Scholar]
  2. Alm, R. A., Guerry, P. & Trust, T. J. ( 1993; ). Distribution and polymorphism of the flagellin genes from isolates of Campylobacter coli and Campylobacter jejuni. J Bacteriol 175, 3051–3057.
    [Google Scholar]
  3. Alm, R. A., Ling, L. S., Moir, D. T. & 20 other authors ( 1999; ). Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397, 176–180.[CrossRef]
    [Google Scholar]
  4. Alonso, J. C., Weise, F. & Rojo, F. ( 1995; ). The Bacillus subtilis histone-like protein Hbsu is required for DNA resolution and DNA inversion mediated by the β recombinase of plasmid pSM19035. J Biol Chem 270, 2938–2945.[CrossRef]
    [Google Scholar]
  5. Anderson, L. B., Hertzel, A. V. & Das, A. ( 1996; ). Agrobacterium tumefaciens VirB7 and VirB9 form a disulfide-linked protein complex. Proc Natl Acad Sci U S A 93, 8889–8894.[CrossRef]
    [Google Scholar]
  6. Bacon, D. J., Alm, R. A., Burr, D. H., Hu, L., Kopecko, D. J., Ewing, C. P., Trust, T. J. & Guerry, P. ( 2000; ). Involvement of a plasmid in virulence of Campylobacter jejuni 81-176. Infect Immun 68, 4384–4390.[CrossRef]
    [Google Scholar]
  7. Bacon, D. J., Alm, R. A., Hu, L., Hickey, T. E., Ewing, C. P., Batchelor, R. A., Trust, T. J. & Guerry, P. ( 2002; ). DNA sequence and mutational analyses of the pVir plasmid of Campylobacter jejuni 81-176. Infect Immun 70, 6242–6250.[CrossRef]
    [Google Scholar]
  8. Balzer, D., Pansegrau, W. & Lanka, E. ( 1994; ). Essential motifs of relaxase (TraI) and TraG proteins involved in conjugative transfer of plasmid RP4. J Bacteriol 176, 4285–4295.
    [Google Scholar]
  9. Beaupre, C. E., Bohne, J., Dale, E. M. & Binns, A. N. ( 1997; ). Interactions between VirB9 and VirB10 membrane proteins involved in movement of DNA from Agrobacterium tumefaciens into plant cells. J Bacteriol 179, 78–89.
    [Google Scholar]
  10. Black, R. E., Levine, M. M., Clements, M. L., Hughes, T. P. & Blaser, M. J. ( 1988; ). Experimental Campylobacter jejuni infection in humans. J Infect Dis 157, 472–479.[CrossRef]
    [Google Scholar]
  11. Bruand, C., Ehrlich, S. D. & Janniere, L. ( 1995; ). Primosome assembly site in Bacillus subtilis. EMBO J 14, 2642–2650.
    [Google Scholar]
  12. Cabezon, E., Lanka, E. & de la Cruz, F. ( 1994; ). Requirements for mobilization of plasmids RSF1010 and ColE1 by the IncW plasmid R388: trwB and RP4 traG are interchangeable. J Bacteriol 176, 4455–4458.
    [Google Scholar]
  13. Cao, T. B. & Saier, M. H., Jr ( 2001; ). Conjugal type IV macromolecular transfer systems of Gram-negative bacteria: organismal distribution, structural constraints and evolutionary conclusions. Microbiology 147, 3201–3214.
    [Google Scholar]
  14. Censini, S., Lange, C., Xiang, Z., Crabtree, J. E., Ghiara, P., Borodovsky, M., Rappuoli, R. & Covacci, A. ( 1996; ). cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc Natl Acad Sci U S A 93, 14648–14653.[CrossRef]
    [Google Scholar]
  15. Chauhan, S. & Kuramitsu, H. K. ( 2004; ). Sequence analysis of plasmid pTS1 isolated from oral spirochetes. Plasmid 51, 61–65.[CrossRef]
    [Google Scholar]
  16. Christie, P. J. & Vogel, J. P. ( 2000; ). Bacterial type IV secretion: conjugation systems adapted to deliver effector molecules to host cells. Trends Microbiol 8, 354–360.[CrossRef]
    [Google Scholar]
  17. Christie, P. J., Ward, J. E., Winans, S. C. & Nester, E. W. ( 1988; ). The Agrobacterium tumefaciens virE2 gene product is a single-stranded-DNA-binding protein that associates with T-DNA. J Bacteriol 170, 2659–2667.
    [Google Scholar]
  18. Covacci, A., Telford, J. L., Del Giudice, G., Parsonnet, J. & Rappuoli, R. ( 1999; ). Helicobacter pylori virulence and genetic geography. Science 284, 1328–1333.[CrossRef]
    [Google Scholar]
  19. Eisenbrandt, R., Kalkum, M., Lurz, R. & Lanka, E. ( 2000; ). Maturation of IncP pilin precursors resembles the catalytic Dyad-like mechanism of leader peptidases. J Bacteriol 182, 6751–6761.[CrossRef]
    [Google Scholar]
  20. Fliegerova, K., Benada, O. & Flint, H. J. ( 1998; ). Large plasmids in ruminal strains of Selenomonas ruminantium. Lett Appl Microbiol 26, 243–247.[CrossRef]
    [Google Scholar]
  21. Galli, D. M., Chen, J., Novak, K. F. & Leblanc, D. J. ( 2001; ). Nucleotide sequence and analysis of conjugative plasmid pVT745. J Bacteriol 183, 1585–1594.[CrossRef]
    [Google Scholar]
  22. Gaynor, E. C., Ghori, N. & Falkow, S. ( 2001; ). Bile-induced ‘pili’ in Campylobacter jejuni are bacteria-independent artifacts of the culture medium. Mol Microbiol 39, 1546–1549.[CrossRef]
    [Google Scholar]
  23. Guerry, P., Pope, P. M., Burr, D. H., Leifer, J., Joseph, S. W. & Bourgeois, A. L. ( 1994; ). Development and characterization of recA mutants of Campylobacter jejuni for inclusion in attenuated vaccines. Infect Immun 62, 426–432.
    [Google Scholar]
  24. Guerry, P., Ewing, C. P., Hickey, T. E., Prendergast, M. M. & Moran, A. P. ( 2000; ). Sialylation of lipooligosaccharide cores affects immunogenicity and serum resistance of Campylobacter jejuni. Infect Immun 68, 6656–6662.[CrossRef]
    [Google Scholar]
  25. Janniere, L., Gruss, A. & Ehrlich, S. D. ( 1993; ). Plasmids, Bacillus subtilis and other gram-positive bacteria. In Plasmids, pp. 625–644. Edited by A. L. Sonenshein, J. A. Hoch & R. Losick. Washington, DC: American Society for Microbiology.
  26. Kersulyte, D., Velapatino, B., Mukhopadhyay, A. K., Cahuayme, L., Bussalleu, A., Combe, J., Gilman, R. H. & Berg, D. E. ( 2003; ). Cluster of type IV secretion genes in Helicobacter pylori's plasticity zone. J Bacteriol 185, 3764–3772.[CrossRef]
    [Google Scholar]
  27. Konieczny, I. ( 2003; ). Strategies for helicase recruitment and loading in bacteria. EMBO Rep 4, 37–41.[CrossRef]
    [Google Scholar]
  28. Korlath, J. A., Osterholm, M. T., Judy, L. A., Forfang, J. C. & Robinson, R. A. ( 1985; ). A point-source outbreak of campylobacteriosis associated with consumption of raw milk. J Infect Dis 152, 592–596.[CrossRef]
    [Google Scholar]
  29. Krause, S., Barcena, M., Pansegrau, W., Lurz, R., Carazo, J. M. & Lanka, E. ( 2000; ). Sequence-related protein export NTPases encoded by the conjugative transfer region of RP4 and by the cag pathogenicity island of Helicobacter pylori share similar hexameric ring structures. Proc Natl Acad Sci U S A 97, 3067–3072.[CrossRef]
    [Google Scholar]
  30. Kuipers, E. J., Israel, D. A., Kusters, J. G. & Blaser, M. J. ( 1998; ). Evidence for a conjugation-like mechanism of DNA transfer in Helicobacter pylori. J Bacteriol 180, 2901–2905.
    [Google Scholar]
  31. Lee, C. Y., Tai, C. L., Lin, S. C. & Chen, Y. T. ( 1994; ). Occurrence of plasmids and tetracycline resistance among Campylobacter jejuni and Campylobacter coli isolated from whole market chickens and clinical samples. Int J Food Microbiol 24, 161–170.[CrossRef]
    [Google Scholar]
  32. Lessl, M., Balzer, D., Pansegrau, W. & Lanka, E. ( 1992; ). Sequence similarities between the RP4 Tra2 and the Ti VirB region strongly support the conjugation model for T-DNA transfer. J Biol Chem 267, 20471–20480.
    [Google Scholar]
  33. Moncalian, G., Cabezon, E., Alkorta, I., Valle, M., Moro, F., Valpuesta, J. M., Goni, F. M. & de la Cruz, F. ( 1999; ). Characterization of ATP and DNA binding activities of TrwB, the coupling protein essential in plasmid R388 conjugation. J Biol Chem 274, 36117–36124.[CrossRef]
    [Google Scholar]
  34. Nachamkin, I., Allos, B. M. & Ho, T. ( 1998; ). Campylobacter species and Guillain–Barré syndrome. Clin Microbiol Rev 11, 555–567.
    [Google Scholar]
  35. Oberhelman, R. A. & Taylor, D. E. ( 2000; ). Campylobacter infections in developing countries. In Campylobacter, pp. 139–153. Edited by I. Nachamkin & M. J. Blaser. Washington, DC: American Society for Microbiology.
  36. Pansegrau, W. & Lanka, E. ( 1996; ). Enzymology of DNA transfer by conjugative mechanisms. Prog Nucleic Acid Res Mol Biol 54, 197–251.
    [Google Scholar]
  37. Parkhill, J., Wren, B. W., Mungall, K. & 18 other authors ( 2000; ). The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403, 665–668.[CrossRef]
    [Google Scholar]
  38. Schmidt-Eisenlohr, H., Domke, N., Angerer, C., Wanner, G., Zambryski, P. C. & Baron, C. ( 1999; ). Vir proteins stabilize VirB5 and mediate its association with the T pilus of Agrobacterium tumefaciens. J Bacteriol 181, 7485–7492.
    [Google Scholar]
  39. Schmidt-Ott, R., Pohl, S., Burghard, S., Weig, M. & Groß, U. ( 2004; ). Identification and characterization of a major subgroup of conjugative Campylobacter jejuni plasmids. J Infect (in press).
    [Google Scholar]
  40. Schneiker, S., Keller, M., Droge, M., Lanka, E., Puhler, A. & Selbitschka, W. ( 2001; ). The genetic organization and evolution of the broad host range mercury resistance plasmid pSB102 isolated from a microbial population residing in the rhizosphere of alfalfa. Nucleic Acids Res 29, 5169–5181.[CrossRef]
    [Google Scholar]
  41. Spudich, G. M., Fernandez, D., Zhou, X. R. & Christie, P. J. ( 1996; ). Intermolecular disulfide bonds stabilize VirB7 homodimers and VirB7/VirB9 heterodimers during biogenesis of the Agrobacterium tumefaciens T-complex transport apparatus. Proc Natl Acad Sci U S A 93, 7512–7517.[CrossRef]
    [Google Scholar]
  42. Strack, B., Lessl, M., Calendar, R. & Lanka, E. ( 1992; ). A common sequence motif, -E-G-Y-A-T-A-, identified within the primase domains of plasmid-encoded I- and P-type DNA primases and the α protein of the Escherichia coli satellite phage P4. J Biol Chem 267, 13062–13072.
    [Google Scholar]
  43. Takai, S., Hines, S. A., Sekizaki, T. & 10 other authors ( 2000; ). DNA sequence and comparison of virulence plasmids from Rhodococcus equi ATCC 33701 and 103. Infect Immun 68, 6840–6847.[CrossRef]
    [Google Scholar]
  44. Tauch, A., Schneiker, S., Selbitschka, W. & 13 other authors ( 2002; ). The complete nucleotide sequence and environmental distribution of the cryptic, conjugative, broad-host-range plasmid pIPO2 isolated from bacteria of the wheat rhizosphere. Microbiology 148, 1637–1653.
    [Google Scholar]
  45. Taylor, D. E. ( 1986; ). Plasmid-mediated tetracycline resistance in Campylobacter jejuni: expression in Escherichia coli and identification of homology with streptococcal class M determinant. J Bacteriol 165, 1037–1039.
    [Google Scholar]
  46. Taylor, D. E., De Grandis, S. A., Karmali, M. A. & Fleming, P. C. ( 1981; ). Transmissible plasmids from Campylobacter jejuni. Antimicrob Agents Chemother 19, 831–835.[CrossRef]
    [Google Scholar]
  47. Taylor, D. E., Chang, N., Garner, R. S., Sherburne, R. & Mueller, L. ( 1986; ). Incidence of antibiotic resistance and characterization of plasmids in Campylobacter jejuni strains isolated from clinical sources in Alberta, Canada. Can J Microbiol 32, 28–32.[CrossRef]
    [Google Scholar]
  48. Tenover, F. C., Williams, S., Gordon, K. P., Nolan, C. & Plorde, J. J. ( 1985; ). Survey of plasmids and resistance factors in Campylobacter jejuni and Campylobacter coli. Antimicrob Agents Chemother 27, 37–41.[CrossRef]
    [Google Scholar]
  49. Thorstenson, Y. R., Kuldau, G. A. & Zambryski, P. C. ( 1993; ). Subcellular localization of seven VirB proteins of Agrobacterium tumefaciens: implications for the formation of a T-DNA transport structure. J Bacteriol 175, 5233–5241.
    [Google Scholar]
  50. Tomb, J. F., White, O., Kerlavage, A. R. & 39 other authors ( 1997; ). The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388, 539–547.[CrossRef]
    [Google Scholar]
  51. Vergunst, A. C., Schrammeijer, B., den Dulk-Ras, A., de Vlaam, C. M., Regensburg-Tuink, T. J. & Hooykaas, P. J. ( 2000; ). VirB/D4-dependent protein translocation from Agrobacterium into plant cells. Science 290, 979–982.[CrossRef]
    [Google Scholar]
  52. Wassenaar, T. M. & Blaser, M. J. ( 1999; ). Pathophysiology of Campylobacter jejuni infections of humans. Microbes Infect 1, 1023–1033.[CrossRef]
    [Google Scholar]
  53. Yao, R., Alm, R. A., Trust, T. J. & Guerry, P. ( 1993; ). Construction of new Campylobacter cloning vectors and a new mutational cat cassette. Gene 130, 127–130.[CrossRef]
    [Google Scholar]
  54. Zechner, E. L., de la Cruz, F., Eisenbrandt, R. & 8 other authors ( 2000; ). Conjugative-DNA transfer processes. In The Horizontal Gene Pool – Bacterial Plasmids and Gene Spread, pp. 87–174. Edited by C. M. Thomas. Amsterdam: Harwood Academic.
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