1887

Abstract

A novel filamentous bacteriophage, designated VEJ, was isolated from strain MO45 of of the O139 serogroup. A molecular characterization of the phage was carried out, which included sequencing of its whole genome, study of the genomic structure, identification of the phage receptor, and determination of the function of some of the genes, such as those encoding the major capsid protein and the single-stranded DNA-binding protein. The genome nucleotide sequence of VEJ, which consists of 6842 bp, revealed that it is organized in modules of functionally related genes in an array that is characteristic of the genus (filamentous phages). VEJ is closely related to other previously described filamentous phages of including VGJ, VSK and fs1. Like these phages, VEJ uses as a cellular receptor the type IV fimbria called the mannose-sensitive haemagglutinin (MSHA). It was also demonstrated that VEJ, like phage VGJ, is able to transmit the genome of phage CTX, and therefore the genes encoding the cholera toxin (CT), horizontally among populations of expressing the MSHA receptor fimbria. This suggests that the variety of phages implicated in the horizontal transmission of the CT genes could be more diverse than formerly thought.

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2010-01-01
2020-01-17
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References

  1. Campos, J., Martinez, E., Marrero, K., Silva, Y., Rodriguez, B. L., Suzarte, E., Ledon, T. & Fando, R. ( 2003a; ). Novel type of specialized transduction for CTXφ or its satellite phage RS1 mediated by filamentous phage VGJφ in Vibrio cholerae. J Bacteriol 185, 7231–7240.[CrossRef]
    [Google Scholar]
  2. Campos, J., Martinez, E., Suzarte, E., Rodriguez, B. L., Marrero, K., Silva, Y., Ledon, T., del Sol, R. & Fando, R. ( 2003b; ). VGJφ, a novel filamentous phage of Vibrio cholerae, integrates into the same chromosomal site as CTXφ. J Bacteriol 185, 5685–5696.[CrossRef]
    [Google Scholar]
  3. Davis, B. M. & Waldor, M. K. ( 2003; ). Filamentous phages linked to virulence of Vibrio cholerae. Curr Opin Microbiol 6, 35–42.[CrossRef]
    [Google Scholar]
  4. Davis, B. M., Lawson, E. H., Sandkvist, M., Ali, A., Sozhamannan, S. & Waldor, M. K. ( 2000; ). Convergence of the secretory pathways for cholera toxin and the filamentous phage, CTXφ. Science 288, 333–335.[CrossRef]
    [Google Scholar]
  5. Ehara, M., Shimodori, S., Kojima, F., Ichinose, Y., Hirayama, T., Albert, M. J., Supawat, K., Honma, Y., Iwanaga, M. & Amako, K. ( 1997; ). Characterization of filamentous phages of Vibrio cholerae O139 and O1. FEMS Microbiol Lett 154, 293–301.[CrossRef]
    [Google Scholar]
  6. Falero, A., Caballero, A., Ferrán, B., Izquierdo, Y., Fando, R. & Campos, J. ( 2009; ). DNA binding proteins of the filamentous phages CTXφ and VGJφ of Vibrio cholerae. J Bacteriol 191, 5873–5876.[CrossRef]
    [Google Scholar]
  7. Faruque, S. M., Asadulghani, Kamruzzaman, M., Nandi, R. K., Ghosh, A. N., Nair, G. B., Mekalanos, J. J. & Sack, D. A. ( 2002; ). RS1 element of Vibrio cholerae can propagate horizontally as a filamentous phage exploiting the morphogenesis genes of CTXφ. Infect Immun 70, 163–170.[CrossRef]
    [Google Scholar]
  8. Faruque, S. M., Zhu, J., Asadulghani, Kamruzzaman, M. & Mekalanos, J. J. ( 2003; ). Examination of diverse toxin-coregulated pilus-positive Vibrio cholerae strains fails to demonstrate evidence for Vibrio pathogenicity island phage. Infect Immun 71, 2993–2999.[CrossRef]
    [Google Scholar]
  9. Faruque, S. M., Bin Naser, I., Fujihara, K., Diraphat, P., Chowdhury, N., Kamruzzaman, M., Qadri, F., Yamasaki, S., Ghosh, A. N. & Mekalanos, J. J. ( 2005; ). Genomic sequence and receptor for the Vibrio cholerae phage KSF-1φ: evolutionary divergence among filamentous vibriophages mediating lateral gene transfer. J Bacteriol 187, 4095–4103.[CrossRef]
    [Google Scholar]
  10. Huber, K. E. & Waldor, M. K. ( 2002; ). Filamentous phage integration requires the host recombinases XerC and XerD. Nature 417, 656–659.[CrossRef]
    [Google Scholar]
  11. Jouravleva, E. A., McDonald, G. A., Garon, C. F., Boesman-Finkelstein, M. & Finkelstein, R. A. ( 1998; ). Characterization and possible functions of a new filamentous bacteriophage from Vibrio cholerae O139. Microbiology 144, 315–324.[CrossRef]
    [Google Scholar]
  12. Kar, S., Ghosh, R. K., Ghosh, A. N. & Ghosh, A. ( 1996; ). Integration of the DNA of a novel filamentous bacteriophage VSK from Vibrio cholerae 0139 into the host chromosomal DNA. FEMS Microbiol Lett 145, 17–22.[CrossRef]
    [Google Scholar]
  13. Karaolis, D. K. & Kaper, J. B. ( 1999; ). Vibrio cholerae TCP: a trifunctional virulence factor? Response. Trends Microbiol 7, 393 [CrossRef]
    [Google Scholar]
  14. Karaolis, D. K., Johnson, J. A., Bailey, C. C., Boedeker, E. C., Kaper, J. B. & Reeves, P. R. ( 1998; ). A Vibrio cholerae pathogenicity island associated with epidemic and pandemic strains. Proc Natl Acad Sci U S A 95, 3134–3139.[CrossRef]
    [Google Scholar]
  15. Kiefer, D. & Kuhn, A. ( 1999; ). Hydrophobic forces drive spontaneous membrane insertion of the bacteriophage Pf3 coat protein without topological control. EMBO J 18, 6299–6306.[CrossRef]
    [Google Scholar]
  16. Kiefer, D., Hu, X., Dalbey, R. & Kuhn, A. ( 1997; ). Negatively charged amino acid residues play an active role in orienting the Sec-independent Pf3 coat protein in the Escherichia coli inner membrane. EMBO J 16, 2197–2204.[CrossRef]
    [Google Scholar]
  17. Kimsey, H. H. & Waldor, M. K. ( 1998; ). CTXφ immunity: application in the development of cholera vaccines. Proc Natl Acad Sci U S A 95, 7035–7039.[CrossRef]
    [Google Scholar]
  18. Kostrikis, L. G., Reisberg, S. A., Kim, H. Y., Shin, S. & Day, L. A. ( 1995; ). C2, and unusual filamentous bacterial virus: protein sequence and conformation, DNA size and conformation, and nucleotide/subunit ratio. Biochemistry 34, 4077–4087.[CrossRef]
    [Google Scholar]
  19. Lee, C. A. ( 1999; ). Vibrio cholerae TCP: a trifunctional virulence factor? Trends Microbiol 7, 391–392.[CrossRef]
    [Google Scholar]
  20. Marciano, D. K., Russel, M. & Simon, S. M. ( 1999; ). An aqueous channel for filamentous phage export. Science 284, 1516–1519.[CrossRef]
    [Google Scholar]
  21. Marvin, D. A. ( 1998; ). Filamentous phage structure, infection and assembly. Curr Opin Struct Biol 8, 150–158.[CrossRef]
    [Google Scholar]
  22. McMaster, G. K. & Carmichael, G. G. ( 1977; ). Analysis of single- and double-stranded nucleic acids on polyacrylamide and agarose gels by using glyoxal and acridine orange. Proc Natl Acad Sci U S A 74, 4835–4838.[CrossRef]
    [Google Scholar]
  23. Mendez, C. & Chater, K. F. ( 1987; ). Cloning of whiG, a gene critical for sporulation of Streptomyces coelicolor A3(2). J Bacteriol 169, 5715–5720.
    [Google Scholar]
  24. Nakasone, N., Honma, Y., Toma, C., Yamashiro, T. & Iwanaga, M. ( 1998; ). Filamentous phage fs1 of Vibrio cholerae O139. Microbiol Immunol 42, 237–239.[CrossRef]
    [Google Scholar]
  25. Rajanna, C., Wang, J., Zhang, D., Xu, Z., Ali, A., Hou, Y. M. & Karaolis, D. K. ( 2003; ). The vibrio pathogenicity island of epidemic Vibrio cholerae forms precise extrachromosomal circular excision products. J Bacteriol 185, 6893–6901.[CrossRef]
    [Google Scholar]
  26. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  27. Serek, J., Bauer-Manz, G., Struhalla, G., van den Berg, L., Kiefer, D., Dalbey, R. & Kuhn, A. ( 2004; ). Escherichia coli YidC is a membrane insertase for Sec-independent proteins. EMBO J 23, 294–301.[CrossRef]
    [Google Scholar]
  28. Thelin, K. H. & Taylor, R. K. ( 1996; ). Toxin-coregulated pilus, but not mannose-sensitive hemagglutinin, is required for colonization by Vibrio cholerae O1 El Tor biotype and O139 strains. Infect Immun 64, 2853–2856.
    [Google Scholar]
  29. Val, M. E., Bouvier, M., Campos, J., Sherratt, D., Cornet, F., Mazel, D. & Barre, F. X. ( 2005; ). The single-stranded genome of phage CTX is the form used for integration into the genome of Vibrio cholerae. Mol Cell 19, 559–566.[CrossRef]
    [Google Scholar]
  30. Waldor, M. K. & Mekalanos, J. J. ( 1996; ). Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272, 1910–1914.[CrossRef]
    [Google Scholar]
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