1887

Abstract

The mechanism by which becomes invasive is not well understood. Comparative genomics identified the presence of an 8 kb island in strains belonging to invasive clonal complexes. This island was designated MDA for meningococcal disease associated. MDA is highly conserved among meningococcal isolates and its analysis revealed a genomic organization similar to that of a filamentous prophage such as CTXΦ of . Subsequent molecular investigations showed that the MDA island has indeed the characteristics of a filamentous prophage, which can enter into a productive cycle and is secreted using the type IV pilus (tfp) secretin PilQ. At least three genes of the prophage are necessary for the formation of the replicative cytoplasmic form (, and ). Immunolabelling of the phage with antibodies against the major capsid protein, ORF4, confirmed that filamentous particles, about 1200 nm long, covered with ORF4 are present at the bacterial surface forming bundles in some places and interacting with pili. The MDA bacteriophage is able to infect different strains, using the type IV pili as a receptor via an interaction with the adsorption protein ORF6. Altogether, these data demonstrate that the MDA island encodes a functional prophage able to produce infectious filamentous phage particles.

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2016-02-01
2020-04-04
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References

  1. Achtman M., Neibert M., Crowe B. A., Strittmatter W., Kusecek B., Weyse E., Walsh M. J., Slawig B., Morelli G., other authors. 1988; Purification and characterization of eight class 5 outer membrane protein variants from a clone of Neisseria meningitidis serogroup A. J Exp Med168:507–525 [CrossRef][PubMed]
    [Google Scholar]
  2. Bille E., Zahar J. R., Perrin A., Morelle S., Kriz P., Jolley K. A., Maiden M. C., Dervin C., Nassif X., Tinsley C. R.. 2005; A chromosomally integrated bacteriophage in invasive meningococci. J Exp Med201:1905–1913 [CrossRef][PubMed]
    [Google Scholar]
  3. Bille E., Ure R., Gray S. J., Kaczmarski E. B., McCarthy N. D., Nassif X., Maiden M. C., Tinsley C. R.. 2008; Association of a bacteriophage with meningococcal disease in young adults. PLoS One3:e3885 [CrossRef][PubMed]
    [Google Scholar]
  4. Bradley D. E.. 1965; Staining of bacteriophage nucleic acids with acridine orange. Nature205:1230 [CrossRef]
    [Google Scholar]
  5. Campos J., Martínez E., Suzarte E., Rodríguez B. L., Marrero K., Silva Y., Ledón T., del Sol R., Fando R.. 2003; VGJ phi, a novel filamentous phage of Vibrio cholerae, integrates into the same chromosomal site as CTX phi. J Bacteriol185:5685–5696 [CrossRef][PubMed]
    [Google Scholar]
  6. Carbonnelle E., Hélaine S., Prouvensier L., Nassif X., Pelicic V.. 2005; Type IV pilus biogenesis in Neisseria meningitidis: PilW is involved in a step occurring after pilus assembly, essential for fibre stability and function. Mol Microbiol55:54–64 [CrossRef][PubMed]
    [Google Scholar]
  7. Cary S. G., Hunter D. H.. 1967; Isolation of bacteriophages active against Neisseria meningitidis . J Virol1:538–542[PubMed]
    [Google Scholar]
  8. Coureuil M., Bourdoulous S., Marullo S., Nassif X.. 2014; Invasive meningococcal disease: a disease of the endothelial cells. Trends Mol Med20:571–578 [CrossRef][PubMed]
    [Google Scholar]
  9. Davis B. M., Waldor M. K.. 2003; Filamentous phages linked to virulence of Vibrio cholerae . Curr Opin Microbiol6:35–42 [CrossRef][PubMed]
    [Google Scholar]
  10. Endemann H., Model P.. 1995; Location of filamentous phage minor coat proteins in phage and in infected cells. J Mol Biol250:496–506 [CrossRef][PubMed]
    [Google Scholar]
  11. Geoffroy M. C., Floquet S., Métais A., Nassif X., Pelicic V.. 2003; Large-scale analysis of the meningococcus genome by gene disruption: resistance to complement-mediated lysis. Genome Res13:391–398 [CrossRef][PubMed]
    [Google Scholar]
  12. Hélaine S., Carbonnelle E., Prouvensier L., Beretti J. L., Nassif X., Pelicic V.. 2005; PilX, a pilus-associated protein essential for bacterial aggregation, is a key to pilus-facilitated attachment of Neisseria meningitidis to human cells. Mol Microbiol55:65–77 [CrossRef][PubMed]
    [Google Scholar]
  13. Hill D. J., Griffiths N. J., Borodina E., Virji M.. 2010; Cellular and molecular biology of Neisseria meningitidis colonization and invasive disease. Clin Sci (Lond)118:547–564 [CrossRef][PubMed]
    [Google Scholar]
  14. Karaolis D. K., Somara S., Maneval D. R. Jr, Johnson J. A., Kaper J. B.. 1999; A bacteriophage encoding a pathogenicity island, a type-IV pilus and a phage receptor in cholera bacteria. Nature399:375–379 [CrossRef][PubMed]
    [Google Scholar]
  15. Kawai M., Uchiyama I., Kobayashi I.. 2005; Genome comparison in silico in Neisseria suggests integration of filamentous bacteriophages by their own transposase. DNA Res12:389–401[CrossRef]
    [Google Scholar]
  16. Kellogg D. S. Jr, Cohen I. R., Norins L. C., Schroeter A. L., Reising G.. 1968; Neisseria gonorrhoeae. II. Colonial variation and pathogenicity during 35 months in vitro. J Bacteriol96:596–605[PubMed]
    [Google Scholar]
  17. Klee S. R., Nassif X., Kusecek B., Merker P., Beretti J. L., Achtman M., Tinsley C. R.. 2000; Molecular and biological analysis of eight genetic islands that distinguish Neisseria meningitidis from the closely related pathogen Neisseria gonorrhoeae . Infect Immun68:2082–2095 [CrossRef][PubMed]
    [Google Scholar]
  18. Lopez J., Webster R. E.. 1983; Morphogenesis of filamentous bacteriophage f1: orientation of extrusion and production of polyphage. Virology127:177–193 [CrossRef][PubMed]
    [Google Scholar]
  19. Maiden M. C., Bygraves J. A., Feil E., Morelli G., Russell J. E., Urwin R., Zhang Q., Zhou J., Zurth K., other authors. 1998; Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci U S A95:3140–3145 [CrossRef][PubMed]
    [Google Scholar]
  20. Marvin D. A.. 1998; Filamentous phage structure, infection and assembly. Curr Opin Struct Biol8:150–158 [CrossRef][PubMed]
    [Google Scholar]
  21. Marvin D. A., Hohn B.. 1969; Filamentous bacterial viruses. Bacteriol Rev33:172–209[PubMed]
    [Google Scholar]
  22. Mehr I. J., Long C. D., Serkin C. D., Seifert H. S.. 2000; A homologue of the recombination-dependent growth gene, rdgC, is involved in gonococcal pilin antigenic variation. Genetics154:523–532[PubMed]
    [Google Scholar]
  23. Nassif X., Lowy J., Stenberg P., O'Gaora P., Ganji A., So M.. 1993; Antigenic variation of pilin regulates adhesion of Neisseria meningitidis to human epithelial cells. Mol Microbiol8:719–725 [CrossRef][PubMed]
    [Google Scholar]
  24. Omer H., Rose G., Jolley K. A., Frapy E., Zahar J. R., Maiden M. C., Bentley S. D., Tinsley C. R., Nassif X., Bille E.. 2011; Genotypic and phenotypic modifications of Neisseria meningitidis after an accidental human passage. PLoS One6:e17145 [CrossRef][PubMed]
    [Google Scholar]
  25. Parkhill J., Achtman M., James K. D., Bentley S. D., Churcher C., Klee S. R., Morelli G., Basham D., Brown D., other authors. 2000; Complete DNA sequence of a serogroup A strain of Neisseria meningitidis Z2491. Nature404:502–506 [CrossRef][PubMed]
    [Google Scholar]
  26. Perkins-Balding D., Ratliff-Griffin M., Stojiljkovic I.. 2004; Iron transport systems in Neisseria meningitidis . Microbiol Mol Biol Rev68:154–171 [CrossRef][PubMed]
    [Google Scholar]
  27. Piekarowicz A., Majchrzak M., Kłyz A., Adamczyk-Popławska M.. 2006; Analysis of the filamentous bacteriophage genomes integrated into Neisseria gonorrhoeae FA1090 chromosome. Pol J Microbiol55:251–260[PubMed][CrossRef]
    [Google Scholar]
  28. Piekarowicz A., Kłyz A., Majchrzak M., Adamczyk-Popławska M., Maugel T. K., Stein D. C.. 2007; Characterization of the dsDNA prophage sequences in the genome of Neisseria gonorrhoeae and visualization of productive bacteriophage. BMC Microbiol7:66 [CrossRef][PubMed]
    [Google Scholar]
  29. Piekarowicz A., Kłyz˙ A., Majchrzak M., Szczêsna E., Piechucki M., Kwiatek A., Maugel T. K., Stein D. C.. 2014; Neisseria gonorrhoeae filamentous phage NgoΦ6 is capable of infecting a variety of Gram-negative bacteria. J Virol88:1002–1010 [CrossRef][PubMed]
    [Google Scholar]
  30. Pujol C., Eugène E., de Saint Martin L., Nassif X.. 1997; Interaction of Neisseria meningitidis with a polarized monolayer of epithelial cells. Infect Immun65:4836–4842[PubMed]
    [Google Scholar]
  31. Pujol C., Eugène E., Marceau M., Nassif X.. 1999; The meningococcal PilT protein is required for induction of intimate attachment to epithelial cells following pilus-mediated adhesion. Proc Natl Acad Sci U S A96:4017–4022 [CrossRef][PubMed]
    [Google Scholar]
  32. Rosenstein N. E., Perkins B. A., Stephens D. S., Popovic T., Hughes J. M.. 2001; Meningococcal disease. N Engl J Med344:1378–1388 [CrossRef][PubMed]
    [Google Scholar]
  33. Sambrook J., Fritsch E. F., Maniatis T.. 1989; Purification of bacteriophage lambda. In Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  34. Sarkari J., Pandit N., Moxon E. R., Achtman M.. 1994; Variable expression of the Opc outer membrane protein in Neisseria meningitidis is caused by size variation of a promoter containing poly-cytidine. Mol Microbiol13:207–217 [CrossRef][PubMed]
    [Google Scholar]
  35. Stephens D. S., Greenwood B., Brandtzaeg P.. 2007; Epidemic meningitis, meningococcaemia, and Neisseria meningitidis . Lancet369:2196–2210 [CrossRef][PubMed]
    [Google Scholar]
  36. Waldor M. K., Rubin E. J., Pearson G. D., Kimsey H., Mekalanos J. J.. 1997; Regulation, replication, and integration functions of the Vibrio cholerae CTXphi are encoded by region RS2. Mol Microbiol24:917–926 [CrossRef][PubMed]
    [Google Scholar]
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