1887

Abstract

Bacteriophage R1-37 was isolated based on its ability to infect strain YeO3-R1, a virulence-plasmid-cured O antigen-negative derivative of serotype O : 3. In this study, the phage receptor was found to be a structure in the outer core hexasaccharide of O : 3 LPS. The phage receptor was present in the outer core of strains of many other serotypes, but also in some strains. Surprisingly, the receptor structure resided in the O antigen of O : 9. Electron microscopy demonstrated that R1-37 particles have an icosahedral head of 88 nm, a short neck of 10 nm, a long contractile tail of 236 nm, and tail fibres of at least 86 nm. This implies that the phage belongs to the order and the family in the ICTV (International Committee for Taxonomy of Viruses) classification. R1-37 was found to have a lytic life cycle, with eclipse and latent periods of 40 and 50 min, respectively, and a burst size of ∼80 p.f.u. per infected cell. Restriction digestions and PFGE showed that the R1-37 genome was dsDNA and ∼270 kb in size. Enzymically hydrolysed DNA was subjected to HPLC-MS/MS analysis, which demonstrated that the R1-37 genome is composed of DNA in which thymidine (T) is >99 % replaced by deoxyuridine (dU). The only organisms known to have similar DNA are the -specific bacteriophages PBS1 and PBS2. N-terminal amino acid sequences of four major structural proteins did not show any similarity to (viral) protein sequences in databases, indicating that close relatives of R1-37 have not yet been characterized. Genes for two of the structural proteins, p24 and p46, were identified from the partially sequenced R1-37 genome.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.28265-0
2005-12-01
2020-04-01
Loading full text...

Full text loading...

/deliver/fulltext/micro/151/12/4093.html?itemId=/content/journal/micro/10.1099/mic.0.28265-0&mimeType=html&fmt=ahah

References

  1. Acharya N., Kumar P., Varshney U. 2003; Complexes of the uracil-DNA glycosylase inhibitor protein, Ugi, with Mycobacterium smegmatis and Mycobacterium tuberculosis uracil-DNA glycosylases. Microbiology149:1647–1658[CrossRef]
    [Google Scholar]
  2. Ackermann H. W. 2003; Bacteriophage observations and evolution. Res Microbiol154:245–251[CrossRef]
    [Google Scholar]
  3. Al-Hendy A., Toivanen P., Skurnik M. 1991; Expression cloning of the Yersinia enterocolitica O : 3 rfb gene cluster in Escherichia coli K12. Microb Pathog10:47–59[CrossRef]
    [Google Scholar]
  4. Al-Hendy A., Toivanen P., Skurnik M. 1992; Lipopolysaccharide O side chain of Yersinia enterocolitica O : 3 is an essential virulence factor in an orally infected murine model. Infect Immun60:870–875
    [Google Scholar]
  5. Appleyard R. K. 1954; Segregation of new lysogenic types during growth of doubly lysogenic strain derived from Escherichia coli K12. Genetics39:440–452
    [Google Scholar]
  6. Ausubel F. M., Brent R., Kingston R. E., Moore D. D., Seidman J. G., Smith J. A., Struhl K. 1987; Current Protocols in Molecular Biology New York: Wiley;
    [Google Scholar]
  7. Baker P. M., Farmer J. J. III. 1982; New bacteriophage typing system for Yersinia enterocolitica, Yersinia kristensenii, Yersinia frederiksenii , and Yersinia intermedia : correlation with serotyping, biotyping and antibiotic susceptibility. J Clin Microbiol15:491–502
    [Google Scholar]
  8. Ben-Gurion R., Hertman I. 1958; Bacteriocin-like material produced by Pasteurella pestis . J Gen Microbiol19:289–297[CrossRef]
    [Google Scholar]
  9. Bennett S. E., Schimerlik M. I., Mosbaugh D. W. 1993; Kinetics of the uracil-DNA glycosylase/inhibitor protein association. Ung interaction with Ugi, nucleic acids, and uracil compounds. J Biol Chem268:26879–26885
    [Google Scholar]
  10. Biedzka-Sarek M., Venho R., Skurnik M. 2005; Role of YadA, Ail, and lipopolysaccharide in serum resistance of Yersinia enterocolitica serotype O : 3. Infect Immun73:2232–2244[CrossRef]
    [Google Scholar]
  11. Birge E. A. 1988; Bacterial and Bacteriophage Genetics: an Introduction , 2nd edn. New York: Springer;
    [Google Scholar]
  12. Bölin I., Norlander L., Wolf-Watz H. 1982; Temperature-inducible outer membrane protein of Yersinia pseudotuberculosis and Yersinia enterocolitica is associated with the virulence plasmid. Infect Immun37:506–512
    [Google Scholar]
  13. Bölin I., Portnoy D. A., Wolf-Watz H. 1985; Expression of the temperature-inducible outer membrane proteins of Yersiniae . Infect Immun48:234–240
    [Google Scholar]
  14. Bolivar F., Rodriguez R. L., Greene P. J., Betlach M. C., Heyneker H. L., Boyer H. W. 1977; Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. Gene2:95–113[CrossRef]
    [Google Scholar]
  15. Bottone E. J. 1997; Yersinia enterocolitica : the charisma continues. Clin Microbiol Rev10:257–276
    [Google Scholar]
  16. Boyer H. W., Roulland-Dussoix D. 1969; A complementation analysis of the restriction and modification of DNA in Escherichia coli . J Mol Biol41:459–472[CrossRef]
    [Google Scholar]
  17. Bradley D. E. 1967; Ultrastructure of bacteriophage and bacteriocins. Bacteriol Rev31:230–314
    [Google Scholar]
  18. Condron B. G., Atkins J. F., Gesteland R. F. 1991; Frameshifting in gene 10 of bacteriophage T7. J Bacteriol173:6998–7003
    [Google Scholar]
  19. Crain P. F. 1990; Preparation and enzymatic hydrolysis of DNA and RNA for mass spectrometry. Methods Enzymol193:782–790
    [Google Scholar]
  20. Ditta G., Stanfield S., Corbin D., Helinski D. R. 1980; Broad host range DNA cloning system for Gram-negative bacteria: construction of a gene bank of Rhizobium meliloti . Proc Natl Acad Sci U S A77:7347–7351[CrossRef]
    [Google Scholar]
  21. Duncan B. K., Warner H. R. 1977; Metabolism of uracil-containing DNA: degradation of bacteriophage PBS2 DNA in Bacillus subtilis . J Virol22:835–838
    [Google Scholar]
  22. El Tahir J., Skurnik M. 2001; YadA, the multifaceted Yersinia adhesin. Int J Med Microbiol291:209–218[CrossRef]
    [Google Scholar]
  23. Garcia E., Nedialkov Y. A., Elliott J., Motin V. L., Brubaker R. R. 1999; Molecular characterization of KatY (antigen 5), a thermoregulated chromosomally encoded catalase-peroxidase of Yersinia pestis . J Bacteriol181:3114–3122
    [Google Scholar]
  24. Garcia E., Elliott J. M., Ramanculov E., Chain P. S., Chu M. C., Molineux I. J. 2003a; The genome sequence of Yersinia pestis bacteriophage ϕ A1122 reveals an intimate history with the coliphage T3 and T7 genomes. J Bacteriol185:5248–5262[CrossRef]
    [Google Scholar]
  25. Garcia P., Ladero V., Suarez J. E. 2003b; Analysis of the morphogenetic cluster and genome of the temperate Lactobacillus casei bacteriophage A2. Arch Virol148:1051–1070[CrossRef]
    [Google Scholar]
  26. Gerhardt P., Murray R. G. E., Wood W. A., Krieg N. R. 1984; Methods for General and Molecular Bacteriology Washington, DC: American Society for Microbiology;
    [Google Scholar]
  27. Hendrix R. W. 2002; Bacteriophages: evolution of the majority. Theor Popul Biol61:471–480[CrossRef]
    [Google Scholar]
  28. Hertwig S., Klein I., Lurz R., Lanka E., Appel B. 2003a; PY54, a linear plasmid prophage of Yersinia enterocolitica with covalently closed ends. Mol Microbiol48:989–1003[CrossRef]
    [Google Scholar]
  29. Hertwig S., Klein I., Schmidt V., Beck S., Hammerl J. A., Appel B. 2003b; Sequence analysis of the genome of the temperate Yersinia enterocolitica phage PY54. J Mol Biol331:605–622[CrossRef]
    [Google Scholar]
  30. Kukkonen M., Suomalainen M., Kyllönen P., Lähteenmäki K., Lång H., Virkola R., Helander I. M., Holst O., Korhonen T. K. 2004; Lack of O-antigen is essential for plasminogen activation by Yersinia pestis and Salmonella enterica . Mol Microbiol51:215–225
    [Google Scholar]
  31. Kutter E., Gachechiladze K., Poglazov A., Marusich E., Shneider M., Aronsson P., Napuli A., Porter D., Mesyanzhinov V. 1995; Evolution of T4-related phages. Virus Genes11:285–297[CrossRef]
    [Google Scholar]
  32. Lindahl T. 1993; Instability and decay of the primary structure of DNA. Nature362:709–715[CrossRef]
    [Google Scholar]
  33. Lindahl T., Ljungquist S., Siegert W., Nyberg B., Sperens B. 1977; DNA N-glycosidases: properties of uracil-DNA glycosidase from Escherichia coli . J Biol Chem252:3286–3294
    [Google Scholar]
  34. Lundquist A. J., Beger R. D., Bennett S. E., Bolton P. H., Mosbaugh D. W. 1997; Site-directed mutagenesis and characterization of uracil-DNA glycosylase inhibitor protein. Role of specific carboxylic amino acids in complex formation with Escherichia coli uracil-DNA glycosylase. J Biol Chem272:21408–21419[CrossRef]
    [Google Scholar]
  35. Maniloff J., Ackermann H. W. 1998; Taxonomy of bacterial viruses: establishment of tailed virus genera and the order Caudovirales . Arch Virol143:2051–2063[CrossRef]
    [Google Scholar]
  36. Mathews C. K., Kutter E., Mosig G., Berget P. B. 1983; Bacteriophage T4 Washington, DC: American Society for Microbiology;
    [Google Scholar]
  37. Mesyanzhinov V. V., Robben J., Grymonprez B., Kostyuchenko V. A., Bourkaltseva M. V., Sykilinda N. N., Krylov V. N., Volckaert G. 2002; The genome of bacteriophage ϕ KZ of Pseudomonas aeruginosa . J Mol Biol317:1–19[CrossRef]
    [Google Scholar]
  38. Michiels T., Cornelis G. R. 1991; Secretion of hybrid proteins by the Yersinia Yop export system. J Bacteriol173:1677–1685
    [Google Scholar]
  39. Miller E. S., Kutter E., Mosig G., Arisaka F., Kunisawa T., Ruger W. 2003; Bacteriophage T4 genome. Microbiol Mol Biol Rev67:86–156[CrossRef]
    [Google Scholar]
  40. Olsen L. C., Aasland R., Wittwer C. U., Krokan H. E., Helland D. E. 1989; Molecular cloning of human uracil-DNA glycosylase, a highly conserved DNA repair enzyme. EMBO J8:3121–3125
    [Google Scholar]
  41. Olsen L. C., Aasland R., Krokan H. E., Helland D. E. 1991; Human uracil-DNA glycosylase complements E. coli ung mutants. Nucleic Acids Res19:4473–4478[CrossRef]
    [Google Scholar]
  42. Pajunen M., Kiljunen S., Skurnik M. 2000; Bacteriophage ϕ YeO3-12 specific for Yersinia enterocolitica serotype O : 3 is related to coliphages T3 and T7. J Bacteriol182:5114–5120[CrossRef]
    [Google Scholar]
  43. Pajunen M. I., Kiljunen S. J., Söderholm M. E.-L., Skurnik M. 2001; Complete genomic sequence of the lytic bacteriophage ϕ YeO3-12 of Yersinia enterocolitica serotype O : 3. J Bacteriol183:1928–1937[CrossRef]
    [Google Scholar]
  44. Pedulla M. L., Ford M. E., Houtz J. M.. 17 other authors 2003; Origins of highly mosaic mycobacteriophage genomes. Cell113:171–182[CrossRef]
    [Google Scholar]
  45. Poole A., Penny D., Sjoberg B. M. 2001; Confounded cytosine! Tinkering and the evolution of DNA. Nat Rev Mol Cell Biol2:147–151
    [Google Scholar]
  46. Popp A., Hertwig S., Lurz R., Appel B. 2000; Comparative study of temperate bacteriophages isolated from Yersinia . Syst Appl Microbiol23:469–478[CrossRef]
    [Google Scholar]
  47. Porat R., McCabe W. R., Brubaker R. R. 1995; Lipopolysaccharide-associated resistance to killing of Yersiniae by complement. J Endotoxin Res2:91–97
    [Google Scholar]
  48. Portnoy D. A., Falkow S. 1981; Virulence-associated plasmids from Yersinia enterocolitica and Yersinia pestis . J Bacteriol148:877–883
    [Google Scholar]
  49. Portnoy D. A., Moseley S. L., Falkow S. 1981; Characterization of plasmids and plasmid-associated determinants of Yersinia enterocolitica pathogenesis. Infect Immun31:775–782
    [Google Scholar]
  50. Radany E. H., Dornfeld K. J., Sanderson R. J., Savage M. K., Majumdar A., Seidman M. M., Mosbaugh D. W. 2000; Increased spontaneous mutation frequency in human cells expressing the phage PBS2-encoded inhibitor of uracil-DNA glycosylase. Mutat Res461:41–58[CrossRef]
    [Google Scholar]
  51. Radziejewska-Lebrecht J., Skurnik M., Shashkov A. S., Brade L., Rozalski A., Bartodziejska B., Mayer H. 1998; Immunochemical studies on R mutants of Yersinia enterocolitica O : 3. Acta Biochim Pol45:1011–1019
    [Google Scholar]
  52. Sambrook J., Russell D. 2001; Molecular Cloning: a Laboratory Manual , 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  53. Skurnik M. 1984; Lack of correlation between the presence of plasmids and fimbriae in Yersinia enterocolitica and Yersinia pseudotuberculosis . J Appl Bacteriol56:355–363[CrossRef]
    [Google Scholar]
  54. Skurnik M. 1985; Studies on the virulence plasmids of Yersinia species PhD thesis, University of Oulu;
    [Google Scholar]
  55. Skurnik M., Toivanen P. 1991; Intervening sequences (IVSs) in the 23S ribosomal RNA genes of pathogenic Yersinia enterocolitica strains. The IVSs in Y. enterocolitica and Salmonella typhimurium have a common origin. Mol Microbiol5:585–593[CrossRef]
    [Google Scholar]
  56. Skurnik M., Venho R., Toivanen P., Al-Hendy A. 1995; A novel locus of Yersinia enterocolitica serotype O : 3 involved in lipopolysaccharide outer core biosynthesis. Mol Microbiol17:575–594[CrossRef]
    [Google Scholar]
  57. Stevenson R., Airdrie D. 1984; Isolation of Yersinia ruckeri bacteriophages. Appl Environ Microbiol47:1201–1205
    [Google Scholar]
  58. Sung J. S., Mosbaugh D. W. 2003; Escherichia coli uracil- and ethenocytosine-initiated base excision DNA repair: rate-limiting step and patch size distribution. Biochemistry42:4613–4625[CrossRef]
    [Google Scholar]
  59. Sutcliffe J. G. 1979; Complete nucleotide sequence of the Escherichia coli plasmid pBR322. Cold Spring Harb Symp Quant Biol43:77–90[CrossRef]
    [Google Scholar]
  60. Takahashi I., Marmur J. 1963; Replacement of thymidylic acid by deoxyuridylic acid in the deoxyribonucleic acid of a transducing phage for Bacillus subtilis . Nature197:794–795[CrossRef]
    [Google Scholar]
  61. Taylor A. F., Weiss B. 1982; Role of exonuclease III in the base excision repair of uracil-containing DNA. J Bacteriol151:351–357
    [Google Scholar]
  62. Tsubokura M., Aleksic S. 1995; A simplified antigenic scheme for serotyping of Yersinia pseudotuberculosis : phenotypic characterization of reference strains and preparation of O and H factor sera. Contrib Microbiol Immunol13:99–105
    [Google Scholar]
  63. Tye B. K., Chien J., Lehman I. R., Duncan B. K., Warner H. R. 1978; Uracil incorporation: a source of pulse-labeled DNA fragments in the replication of the Escherichia coli chromosome. Proc Natl Acad Sci U S A75:233–237[CrossRef]
    [Google Scholar]
  64. Wang Z., Mosbaugh D. W. 1988; Uracil-DNA glycosylase inhibitor of bacteriophage PBS2: cloning and effects of expression of the inhibitor gene in Escherichia coli . J Bacteriol170:1082–1091
    [Google Scholar]
  65. Wauters G., Aleksic S., Charlier J., Schulze G. 1991; Somatic and flagellar antigens of Yersinia enterocolitica and related species. Contrib Microbiol Immunol12:239–243
    [Google Scholar]
  66. Zhang L., Radziejewska-Lebrecht J., Krajewska-Pietrasik D., Toivanen P., Skurnik M. 1997; Molecular and chemical characterization of the lipopolysaccharide O-antigen and its role in the virulence of Yersinia enterocolitica serotype O : 8. Mol Microbiol23:63–76[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.28265-0
Loading
/content/journal/micro/10.1099/mic.0.28265-0
Loading

Data & Media loading...

Most cited this month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error