1887

Abstract

In , generalized transduction mediated by temperate bacteriophages represents a highly efficient way of transferring antibiotic resistance genes between strains. In the present study, we identified and characterized in detail a new efficiently transducing bacteriophage of the family , designated ϕJB, which resides as a prophage in the meticillin-resistant (MRSA) strain Jevons B. Whole-genome sequencing followed by detailed analysis uncovered a linear dsDNA genome consisting of 43 012 bp and comprising 70 ORFs, of which ∼40 encoded proteins with unknown function. A global genome alignment of ϕJB and other efficiently transducing phages ϕ11, ϕ53, ϕ80, ϕ80α and ϕNM4 showed a high degree of homology with ϕNM4 and substantial differences with regard to other phages. Using a model transduction system with a well-defined donor and recipient, ϕJB transferred the tetracycline resistance plasmid pT181 and a penicillinase plasmid with outstanding frequencies, beating most of the above-mentioned phages by an order of magnitude. Moreover, ϕJB demonstrated high frequencies of transferring antibiotic resistance plasmids even upon induction from a lysogenic donor strain. Considering such transducing potential, ϕJB and related bacteriophages may serve as a suitable tool for elucidating the nature of transduction and its contribution to the spread of antibiotic resistance genes in naturally occurring MRSA populations.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000329
2016-01-01
2019-10-23
Loading full text...

Full text loading...

/deliver/fulltext/jgv/97/1/258.html?itemId=/content/journal/jgv/10.1099/jgv.0.000329&mimeType=html&fmt=ahah

References

  1. Altschul S. F. , Gish W. , Miller W. , Myers E. W. , Lipman D. J. . ( 1990;). Basic local alignment search tool. J Mol Biol 215: 403–410 [CrossRef] [PubMed].
    [Google Scholar]
  2. Asheshov E. H. . ( 1969;). The genetics of penicillinase production in Staphylococcus aureus strain PS80. J Gen Microbiol 59: 289–301 [CrossRef] [PubMed].
    [Google Scholar]
  3. Bae T. , Baba T. , Hiramatsu K. , Schneewind O. . ( 2006;). Prophages of Staphylococcus aureus Newman and their contribution to virulence. Mol Microbiol 62: 1035–1047 [CrossRef] [PubMed].
    [Google Scholar]
  4. Blouse L. E. , Mauney C. U. , Marraro R. V. , Dupuy H. J. . ( 1972;). Apparent spontaneous induction of Staphylococcus aureus isolated from clinical sources. Appl Microbiol 23: 1023–1024 [PubMed].
    [Google Scholar]
  5. Bradley R. K. , Roberts A. , Smoot M. , Juvekar S. , Do J. , Dewey C. , Holmes I. , Pachter L. . ( 2009;). Fast statistical alignment. PLOS Comput Biol 5: e1000392 [CrossRef] [PubMed].
    [Google Scholar]
  6. Brown D. T. , Brown N. C. , Burlingham B. T. . ( 1972;). Morphology and physical properties of Staphylococcus bacteriophage P11-M15. J Virol 9: 664–671 [PubMed].
    [Google Scholar]
  7. Brudno M. , Do C. B. , Cooper G. M. , Kim M. F. , Davydov E. , Green E. D. , Sidow A. , Batzoglou S. , NISC Comparative Sequencing Program . ( 2003;). lagan and Multi-lagan: efficient tools for large-scale multiple alignment of genomic DNA. Genome Res 13: 721–731 [CrossRef] [PubMed].
    [Google Scholar]
  8. Canchaya C. , Proux C. , Fournous G. , Bruttin A. , Brüssow H. . ( 2003;). Prophage genomics. Microbiol Mol Biol Rev 67: 238–276 [CrossRef] [PubMed].
    [Google Scholar]
  9. Casjens S. R. , Gilcrease E. B. . ( 2009;). Determining DNA packaging strategy by analysis of the termini of the chromosomes in tailed-bacteriophage virions. Methods Mol Biol 502: 91–111 [CrossRef] [PubMed].
    [Google Scholar]
  10. Chen J. , Novick R. P. . ( 2009;). Phage-mediated intergeneric transfer of toxin genes. Science 323: 139–141 [CrossRef] [PubMed].
    [Google Scholar]
  11. Cohen S. , Sweeney H. M. . ( 1970;). Transduction of methicillin resistance in Staphylococcus aureus dependent on an unusual specificity of the recipient strain. J Bacteriol 104: 1158–1167 [PubMed].
    [Google Scholar]
  12. Deghorain M. , Bobay L. M. , Smeesters P. R. , Bousbata S. , Vermeersch M. , Perez-Morga D. , Drèze P. A. , Rocha E. P. , Touchon M. , Van Melderen L. . ( 2012;). Characterization of novel phages isolated in coagulase-negative staphylococci reveals evolutionary relationships with Staphylococcus aureus phages. J Bacteriol 194: 5829–5839 [CrossRef] [PubMed].
    [Google Scholar]
  13. Doškarˇ J. , Pallová P. , Pantu˚ček R. , Rosypal S. , Ru˚žičková V. , Pantu˚čková P. , Kailerová J. , Klepárník K. , Malá Z. , Boček P. . ( 2000;). Genomic relatedness of Staphylococcus aureus phages of the International Typing Set and detection of serogroup A, B, and F prophages in lysogenic strains. Can J Microbiol 46: 1066–1076 [CrossRef] [PubMed].
    [Google Scholar]
  14. Dowell C. E. , Rosenblum E. D. . ( 1962;). Serology and transduction in staphylococcal phage. J Bacteriol 84: 1071–1075 [PubMed].
    [Google Scholar]
  15. Ferrer M. D. , Quiles-Puchalt N. , Harwich M. D. , Tormo-Más M. A. , Campoy S. , Barbé J. , Lasa I. , Novick R. P. , Christie G. E. , Penadés J. R. . ( 2011;). RinA controls phage-mediated packaging and transfer of virulence genes in Gram-positive bacteria. Nucleic Acids Res 39: 5866–5878 [CrossRef] [PubMed].
    [Google Scholar]
  16. Frazer K. A. , Pachter L. , Poliakov A. , Rubin E. M. , Dubchak I. . ( 2004;). vista: computational tools for comparative genomics. Nucleic Acids Res 32: (Web Server), W273–W239 [CrossRef] [PubMed].
    [Google Scholar]
  17. Goerke C. , Pantu˚ček R. , Holtfreter S. , Schulte B. , Zink M. , Grumann D. , Bröker B. M. , Doškarˇ J. , Wolz C. . ( 2009;). Diversity of prophages in dominant Staphylococcus aureus clonal lineages. J Bacteriol 191: 3462–3468 [CrossRef] [PubMed].
    [Google Scholar]
  18. Goujon M. , McWilliam H. , Li W. , Valentin F. , Squizzato S. , Paern J. , Lopez R. . ( 2010;). A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res 38: (Web Server), W695–W699 [CrossRef] [PubMed].
    [Google Scholar]
  19. Iandolo J. J. , Worrell V. , Groicher K. H. , Qian Y. , Tian R. , Kenton S. , Dorman A. , Ji H. , Lin S. , other authors . ( 2002;). Comparative analysis of the genomes of the temperate bacteriophages φ11, φ12 and φ13 of Staphylococcus aureus 8325. Gene 289: 109–118 [CrossRef] [PubMed].
    [Google Scholar]
  20. Isidro A. , Henriques A. O. , Tavares P. . ( 2004;). The portal protein plays essential roles at different steps of the SPP1 DNA packaging process. Virology 322: 253–263 [CrossRef] [PubMed].
    [Google Scholar]
  21. Jevons M. P. . ( 1961;). “Celbenin”-resistant staphylococci. Br Med J 1: 124–125 [CrossRef].
    [Google Scholar]
  22. Kahánková J. , Pantu˚ček R. , Goerke C. , Ru˚žičková V. , Holochová P. , Doškarˇ J. . ( 2010;). Multilocus PCR typing strategy for differentiation of Staphylococcus aureus siphoviruses reflecting their modular genome structure. Environ Microbiol 12: 2527–2538 [CrossRef] [PubMed].
    [Google Scholar]
  23. Kayser F. H. , Wüst J. , Corrodi P. . ( 1972;). Transduction and elimination of resistance determinants in methicillin-resistant Staphylococcus aureus . Antimicrob Agents Chemother 2: 217–223 [CrossRef] [PubMed].
    [Google Scholar]
  24. Keary R. , McAuliffe O. , Ross R. P. , Hill C. , O'Mahony J. , Coffey A. . ( 2014;). Genome analysis of the staphylococcal temperate phage DW2 and functional studies on the endolysin and tail hydrolase. Bacteriophage 4: e28451 [CrossRef] [PubMed].
    [Google Scholar]
  25. Krausz K. L. , Bose J. L. . ( 2016;). Bacteriophage transduction in Staphylococcus aureus: broth-based method. Methods Mol Biol 1373: 63–68 [PubMed].[CrossRef]
    [Google Scholar]
  26. Kreiswirth B. N. , Löfdahl S. , Betley M. J. , O'Reilly M. , Schlievert P. M. , Bergdoll M. S. , Novick R. P. . ( 1983;). The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305: 709–712 [CrossRef] [PubMed].
    [Google Scholar]
  27. Kuntová L. , Pantu˚ček R. , Rájová J. , Ru˚žičková V. , Petráš P. , Mašlanˇová I. , Doškarˇ J. . ( 2012;). Characteristics and distribution of plasmids in a clonally diverse set of methicillin-resistant Staphylococcus aureus strains. Arch Microbiol 194: 607–614 [CrossRef] [PubMed].
    [Google Scholar]
  28. Kwan T. , Liu J. , DuBow M. , Gros P. , Pelletier J. . ( 2005;). The complete genomes and proteomes of 27 Staphylococcus aureus bacteriophages. Proc Natl Acad Sci U S A 102: 5174–5179 [CrossRef] [PubMed].
    [Google Scholar]
  29. Lee C. Y. , Iandolo J. J. . ( 1986;). Integration of staphylococcal phage L54a occurs by site-specific recombination: structural analysis of the attachment sites. Proc Natl Acad Sci U S A 83: 5474–5478 [CrossRef] [PubMed].
    [Google Scholar]
  30. Lesnik E. A. , Sampath R. , Levene H. B. , Henderson T. J. , McNeil J. A. , Ecker D. J. . ( 2001;). Prediction of rho-independent transcriptional terminators in Escherichia coli . Nucleic Acids Res 29: 3583–3594 [CrossRef] [PubMed].
    [Google Scholar]
  31. Lindsay J. A. . ( 2008;). S. aureus evolution: lineages and mobile genetic elements. . In Staphylococcus: Molecular Genetics , pp. 46–69. Edited by Lindsay J. A. . Norwich: Caister Academic Press;.
    [Google Scholar]
  32. Lukashin A. V. , Borodovsky M. . ( 1998;). GeneMark.hmm: new solutions for gene finding. Nucleic Acids Res 26: 1107–1115 [CrossRef] [PubMed].
    [Google Scholar]
  33. Maiques E. , Ubeda C. , Tormo M. A. , Ferrer M. D. , Lasa I. , Novick R. P. , Penadés J. R. . ( 2007;). Role of staphylococcal phage and SaPI integrase in intra- and interspecies SaPI transfer. J Bacteriol 189: 5608–5616 [CrossRef] [PubMed].
    [Google Scholar]
  34. Martineau F. , Picard F. J. , Grenier L. , Roy P. H. , Ouellette M. , Bergeron M. G. . ( 2000;). Multiplex PCR assays for the detection of clinically relevant antibiotic resistance genes in staphylococci isolated from patients infected after cardiac surgery. The ESPRIT Trial. J Antimicrob Chemother 46: 527–534 [CrossRef] [PubMed].
    [Google Scholar]
  35. Mašlanˇová I. , Doškarˇ J. , Varga M. , Kuntová L. , Mužík J. , Malúšková D. , Ru˚žičková V. , Pantu˚ček R. . ( 2013;). Bacteriophages of Staphylococcus aureus efficiently package various bacterial genes and mobile genetic elements including SCCmec with different frequencies. Environ Microbiol Rep 5: 66–73 [CrossRef] [PubMed].
    [Google Scholar]
  36. Morse M. L. , Labelle J. W. . ( 1962;). Characteristics of a staphylococcal phage capable of transduction. J Bacteriol 83: 775–780 [PubMed].
    [Google Scholar]
  37. Ng L. K. , Martin I. , Alfa M. , Mulvey M. . ( 2001;). Multiplex PCR for the detection of tetracycline resistant genes. Mol Cell Probes 15: 209–215 [CrossRef] [PubMed].
    [Google Scholar]
  38. Novick R. . ( 1967;). Properties of a cryptic high-frequency transducing phage in Staphylococcus aureus . Virology 33: 155–166 [CrossRef] [PubMed].
    [Google Scholar]
  39. Oliveira L. , Tavares P. , Alonso J. C. . ( 2013;). Headful DNA packaging: bacteriophage SPP1 as a model system. Virus Res 173: 247–259 [CrossRef] [PubMed].
    [Google Scholar]
  40. Pantu˚ček R. , Doškarˇ J. , Ru˚žičková V. , Kašpárek P. , Oráčová E. , Kvardová V. , Rosypal S. . ( 2004;). Identification of bacteriophage types and their carriage in Staphylococcus aureus . Arch Virol 149: 1689–1703 [CrossRef] [PubMed].
    [Google Scholar]
  41. Penadés J. R. , Chen J. , Quiles-Puchalt N. , Carpena N. , Novick R. P. . ( 2015;). Bacteriophage-mediated spread of bacterial virulence genes. Curr Opin Microbiol 23: 171–178 [CrossRef] [PubMed].
    [Google Scholar]
  42. Price M. N. , Dehal P. S. , Arkin A. P. . ( 2010;). FastTree 2 - approximately maximum-likelihood trees for large alignments. PLoS One 5: e9490 [CrossRef] [PubMed].
    [Google Scholar]
  43. Rao V. B. , Feiss M. . ( 2008;). The bacteriophage DNA packaging motor. Annu Rev Genet 42: 647–681 [CrossRef] [PubMed].
    [Google Scholar]
  44. Resch A. , Fehrenbacher B. , Eisele K. , Schaller M. , Götz F. . ( 2005;). Phage release from biofilm and planktonic Staphylococcus aureus cells. FEMS Microbiol Lett 252: 89–96 [CrossRef] [PubMed].
    [Google Scholar]
  45. Skippington E. , Ragan M. A. . ( 2011;). Lateral genetic transfer and the construction of genetic exchange communities. FEMS Microbiol Rev 35: 707–735 [CrossRef] [PubMed].
    [Google Scholar]
  46. Solovyev V. , Salamov A. . ( 2011;). Automatic annotation of microbial genomes and metagenomic sequences. . In Metagenomics and its Applications in Agriculture, Biomedicine and Environmental Studies, pp. 171–204. Edited by Li R. W. . New York, NY: Nova Science;.
    [Google Scholar]
  47. van der Mee-Marquet N. , Corvaglia A. R. , Valentin A. S. , Hernandez D. , Bertrand X. , Girard M. , Kluytmans J. , Donnio P. Y. , Quentin R. , François P. . ( 2013;). Analysis of prophages harbored by the human-adapted subpopulation of Staphylococcus aureus CC398. Infect Genet Evol 18: 299–308 [CrossRef] [PubMed].
    [Google Scholar]
  48. Varga M. , Kuntová L. , Pantu˚ček R. , Mašlanˇová I. , Ru˚žičková V. , Doškarˇ J. . ( 2012;). Efficient transfer of antibiotic resistance plasmids by transduction within methicillin-resistant Staphylococcus aureus USA300 clone. FEMS Microbiol Lett 332: 146–152 [CrossRef] [PubMed].
    [Google Scholar]
  49. Wiedenbeck J. , Cohan F. M. . ( 2011;). Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches. FEMS Microbiol Rev 35: 957–976 [CrossRef] [PubMed].
    [Google Scholar]
  50. Winstel V. , Kühner P. , Krismer B. , Peschel A. , Rohde H. . ( 2015;). Transfer of plasmid DNA to clinical coagulase-negative staphylococcal pathogens by using a unique bacteriophage. Appl Environ Microbiol 81: 2481–2488 [CrossRef] [PubMed].
    [Google Scholar]
  51. Zhang X. , Xu X. , Yuan W. , Hu Q. , Shang W. , Hu X. , Tong Y. , Rao X. . ( 2014;). Complete genome sequence of Staphylococcus aureus XN108, an ST239-MRSA-SCCmec III strain with intermediate vancomycin resistance isolated in mainland China. Genome Announc 2: e00449–e00414 [CrossRef] [PubMed].
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000329
Loading
/content/journal/jgv/10.1099/jgv.0.000329
Loading

Data & Media loading...

Supplements

Supplementary Data



PDF

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