The complete genomes of Staphylococcus aureus bacteriophages 80 and 80α-Implications for the specificity of SaPI mobilization

Virology

Volumn 407, Issue 2, 2010, Pages 381-390

  Christie, G E ^a   Matthews, A M ^b   King, D G ^a   Lane, K D ^a   Olivarez, N P ^a   Tallent, S M ^a   Gill, S R ^c   Novick, R P ^b  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c J CRAIG VENTER INSTITUTE   (United States)

Author keywords

Derepression; Genome sequence comparison; Helper phage; Horizontal gene transfer; Pathogenicity island; Phage packaging; Staphylococcus aureus; Transduction

Indexed keywords

ARTICLE; CONTROLLED STUDY; GENE SEQUENCE; GENE TRANSFER; GENETIC TRANSDUCTION; GENOME ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENICITY ISLAND; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS PHAGE; STAPHYLOCOCCUS PHAGE 80; STAPHYLOCOCCUS PHAGE 80ALPHA; VIRUS GENOME; VIRUS LIKE AGENT; VIRUS REPLICATION; DNA REPLICATION; DNA SEQUENCE; GENETICS; GENOMIC ISLAND; HELPER VIRUS; LYSOGENIZATION; METABOLISM; MOLECULAR GENETICS; PATHOGENICITY; PHYSIOLOGY; VIROLOGY; VIRUS ASSEMBLY;

ATTACHMENT SITES, MICROBIOLOGICAL; BASE SEQUENCE; DNA REPLICATION; GENOME, VIRAL; GENOMIC ISLANDS; HELPER VIRUSES; INTEGRASES; LYSOGENY; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS PHAGES; TRANSDUCTION, GENETIC; VIRAL STRUCTURAL PROTEINS; VIRUS ASSEMBLY;

STAPHYLOCOCCUS AUREUS;

BACTERIOPHAGE RECEPTOR; INTEGRASE; VIRUS PROTEIN;

EID: 77957677710     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.08.036     Document Type: Article

References (56)

1. Bae T., Baba T., Hiramatsu K., Schneewind O. Prophages of Staphylococcus aureus Newman and their contribution to virulence. Mol. Microbiol. 2006, 62:1035-1047.
2. Betley M.J., Mekalanos J.J. Staphylococcal enterotoxin A is encoded by phage. Science 1985, 229:185-187.
3. Chen J., Novick R.P. Phage-mediated intergeneric transfer of toxin genes. Science 2009, 323:139-141.
4. Christie G.E., Temple L.M., Bartlett B.A., Goodwin T.S. Programmed translational frameshift in the bacteriophage P2 FETUD tail gene operon. J. Bacteriol. 2002, 184:6522-6531.
5. Christie G.E., Kropinski A.M., Kuzio J., ŁoŚ M., McConnell M.R., Wȩgrzyn G. Lysogenic conversion in bacteria of importance to the food industry. Bacteriophage in the Detection and Control of Foodborne Pathogens 2010, 157-198. ASM Press, Washington, D.C. M.P. Sabour, M. Griffiths (Eds.).
6. de Azavedo J.C., Foster T.J., Hartigan P.J., Arbuthnott J.P., O'Reilly M., Kreiswirth B.N., et al. Expression of the cloned toxic shock syndrome toxin 1 gene (tst) in vivo with a rabbit uterine model. Infect. Immun. 1985, 50:304-309.
7. Delcher A.L., Bratke K.A., Powers E.C., Salzberg S.L. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 2007, 23:673-679.
8. Dempsey R.M., Carroll D., Kong H., Higgins L., Keane C.T., Coleman D.C. Sau42I, a BcgI-like restriction-modification system encoded by the Staphylococcus aureus quadruple-converting phage Phi42. Microbiology 2005, 151:1301-1311.
9. Dokland T., Isaksen M.L., Fuller S.D., Lindqvist B.H. Capsid localization of the bacteriophage P4 psu protein. Virology 1993, 194:682-687.
10. Gill S.R., Fouts D.E., Archer G.L., Mongodin E.F., Deboy R.T., et al. Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain. J. Bacteriol. 2005, 187:2426-2438.
11. Goerke C., Pantucek R., Holtfreter S., Schulte B., Zink M., Grumann D., et al. Diversity of prophages in dominant Staphylococcus aureus clonal lineages. J. Bacteriol. 2009, 191:3462-3468.
12. Grindley N.D., Whiteson K.L., Rice P.A. Mechanisms of site-specific recombination. Annu. Rev. Biochem. 2006, 75:567-605.
13. Groth A.C., Calos M.P. Phage integrases: Biology and applications. J. Mol. Biol. 2004, 335:667-678.
14. Hansen E.B. Structure and regulation of the lytic replicon of phage P1. J. Mol. Biol. 1989, 207:135-149.
15. Huson D.H., Reinert K., Kravitz S.A., Remington K.A., Delcher A.L., et al. Design of a compartmentalized shotgun assembler for the human genome. Bioinformatics 2001, 17(Suppl 1):S132-139.
16. Iandolo J.J., Worrell V., Groicher K.H., Qian Y., Tian R., Kenton S., et al. Comparative analysis of the genomes of the temperate bacteriophages phi 11, phi 12 and phi 13 of Staphylococcus aureus 8325. Gene 2002, 289:109-118.
17. Iyer L.M., Koonin E.V., Aravind L. Extensive domain shuffling in transcription regulators of DNA viruses and implications for the origin of fungal APSES transcription factors. Genome Biol. 2002, 3. RESEARCH0012.
18. Kwan T., Liu J., DuBow M., Gros P., Pelletier J. The complete genomes and proteomes of 27 Staphylococcus aureus bacteriophages. Proc. Natl Acad. Sci. USA 2005, 102:5174-5179.
19. Levin M.E., Hendrix R.W., Casjens S.R. A programmed translational frameshift is required for the synthesis of a bacteriophage lambda tail assembly protein. J. Mol. Biol. 1993, 234:124-139.
20. Lewis J.A., Hatfull G.F. Control of directionality in integrase-mediated recombination: examination of recombination directionality factors (RDFs) including xis and cox proteins. Nucleic Acids Res. 2001, 29:2205-2216.
21. Lindqvist B.H., Deho G., Calendar R. Mechanisms of genome propagation and helper exploitation by satellite phage P4. Microbiol. Rev. 1993, 57:683-702.
22. Lindsay J.A., Ruzin A., Ross H.F., Kurepina N., Novick R.P. The gene for toxic shock toxin is carried by a family of mobile pathogenicity islands in Staphylococcus aureus. Mol. Microbiol. 1998, 29:527-543.
23. Liu J., Dehbi M., Moeck G., Arhin F., Bauda P., Bergeron D., et al. Antimicrobial drug discovery through bacteriophage genomics. Nat. Biotechnol. 2004, 22:185-191.
24. Lucchini S., Desiere F., Brussow H. Similarly organized lysogeny modules in temperate siphoviridae from low GC content gram-positive bacteria. Virology 1999, 263:427-435.
25. Maiques E., Ubeda C., Campoy S., Salvador N., Lasa I., Novick R.P., et al. Beta-lactam antibiotics induce the SOS response and horizontal transfer of virulence factors in Staphylococcus aureus. J. Bacteriol. 2006, 188:2726-2729.
26. Maiques E., Ubeda C., Tormo M.A., Ferrer M.D., Lasa I., Novick R.P., et al. Role of staphylococcal phage and SaPI integrase in intra- and interspecies SaPI transfer. J. Bacteriol. 2007, 189:5608-5616.
27. Mumm J.P., Landy A., Gelles J. Viewing single lambda site-specific recombination events from start to finish. EMBO J. 2006, 25:4586-4595.
28. Narita S., Kaneko J., Chiba J., Piemont Y., Jarraud S., Etienne J., et al. Phage conversion of panton-valentine leukocidin in Staphylococcus aureus: molecular analysis of a PVL-converting phage, phiSLT. Gene 2001, 268:195-206.
29. Novick R.P. Analysis by transduction of mutations affecting penicillinase formation in Staphylococcus aureus. J. Gen. Microbiol. 1963, 33:121-136.
30. Novick R. Properties of a cryptic high-frequency transducing phage in Staphylococcus aureus. Virology 1967, 33:155-166.
31. Novick R.P. Genetic systems in staphylococci. Methods Enzymol. 1991, 204:587-636.
32. Novick R.P. Mobile genetic elements and bacterial toxinoses: the superantigen-encoding pathogenicity islands of Staphylococcus aureus. Plasmid 2003, 49:93-105.
33. Novick R.P., Christie G.E., Penadés J.R. The phage-related chromosomal islands of Gram-positive bacteria. Nat. Rev. Microbiol. 2010, 8:541-551.
34. Pani B., Banerjee S., Chalissery J., Muralimohan A., Loganathan R.M., Suganthan R.B., et al. Mechanism of inhibition of rho-dependent transcription termination by bacteriophage P4 protein psu. J. Biol. Chem. 2006, 281:26491-26500.
35. Pantucek R., Doskar J., Ruzickova V., Kasparek P., Oracova E., Kvardova V., et al. Identification of bacteriophage types and their carriage in Staphylococcus aureus. Arch. Virol. 2004, 149:1689-1703.
36. Poliakov A., Chang J.R., Spilman M.S., Damle P.K., Christie G.E., Mobley J., et al. Capsid size determination by Staphylococcus aureus pathogenicity island SaPI1 involves specific incorporation of SaPI1 proteins into procapsids. J. Mol. Biol. 2008, 380:465-475.
37. Rashel M., Uchiyama J., Takemura I., Hoshiba H., Ujihara T., Takatsuji H., et al. Tail-associated structural protein gp61 of Staphylococcus aureus phage phi MR11 has bifunctional lytic activity. FEMS Microbiol. Lett. 2008, 284:9-16.
38. Riedel H.D., Heinrich J., Heisig A., Choli T., Schuster H. The antirepressor of phage P1. isolation and interaction with the C1 repressor of P1 and P7. FEBS Lett. 1993, 334:165-169.
39. Ruzin A., Lindsay J., Novick R.P. Molecular genetics of SaPI1-a mobile pathogenicity island in Staphylococcus aureus. Mol. Microbiol. 2001, 41:365-377.
40. Shearwin K.E., Brumby A.M., Egan J.B. The tum protein of coliphage 186 is an antirepressor. J. Biol. Chem. 1998, 273:5708-5715.
41. Sumby P., Waldor M.K. Transcription of the toxin genes present within the staphylococcal phage phiSa3ms is intimately linked with the phage's life cycle. J. Bacteriol. 2003, 185:6841-6851.
42. Tallent S.M., Langston T.B., Moran R.G., Christie G.E. Transducing particles of Staphylococcus aureus pathogenicity island SaPI1 are comprised of helper phage-encoded proteins. J. Bacteriol. 2007, 189:7520-7524.
43. Tormo M.Á., Ferrer M.D., Maiques E., Ubeda C., Selva L., Lasa Í., et al. Staphylococcus aureus pathogenicity island DNA is packaged in particles composed of phage proteins. J. Bacteriol. 2008, 190:2434-2440.
44. Tormo-Más M.Á., Mir I., Shrestha A., Tallent S.M., Campoy S., Lasa Í., Barbé J., Novick R.P., Christie G.E., Penadés J.R. Moonlighting phage proteins de-repress staphylococcal pathogenicity islands. Nature 2010, 465:779-782.
45. Ubeda C., Barry P., Penades J.R., Novick R.P. A pathogenicity island replicon in Staphylococcus aureus replicates as an unstable plasmid. Proc. Natl Acad. Sci. USA 2007, 104:14182-14188.
46. Ubeda C., Maiques E., Tormo M., Campoy S., Lasa I., Barbe J., et al. SaPI operon I is required for SaPI packaging and is controlled by LexA. Mol. Microbiol. 2007, 65:41-50.
47. Ubeda C., Maiques E., Barry P., Matthews A., Tormo M.A., Lasa I., et al. SaPI mutations affecting replication and transfer and enabling autonomous replication in the absence of helper phage. Mol. Microbiol. 2008, 67:493-503.
48. Ubeda C., Olivarez N.P., Barry P., Wang H., Kong X., Matthews A., et al. Specificity of staphylococcal phage and SaPI DNA packaging as revealed by integrase and terminase mutations. Mol. Microbiol. 2009, 72:98-108.
49. van Wamel W.J., Rooijakkers S.H., Ruyken M., van Kessel K.P., van Strijp J.A. The innate immune modulators staphylococcal complement inhibitor and chemotaxis inhibitory protein of Staphylococcus aureus are located on beta-hemolysin-converting bacteriophages. J. Bacteriol. 2006, 188:1310-1315.
50. Vinga I., Droge A., Stiege A.C., Lurz R., Santos M.A., Daugelavicius R., et al. The minor capsid protein gp7 of bacteriophage SPP1 is required for efficient infection of Bacillus subtilis. Mol. Microbiol. 2006, 61:1609-1621.
51. Winkler K.C., de Waart J., Grootsen C. Lysogenic conversion of staphylococci to loss of beta-toxin. J. Gen. Microbiol. 1965, 39:321-333.
52. Xu J., Hendrix R.W., Duda R.L. Conserved translational frameshift in dsDNA bacteriophage tail assembly genes. Mol. Cell 2004, 16:11-21.
53. Yamaguchi T., Hayashi T., Takami H., Nakasone K., Ohnishi M., Nakayama K., et al. Phage conversion of exfoliative toxin A production in Staphylococcus aureus. Mol. Microbiol. 2000, 38:694-705.
54. Ye Z.H., Lee C.Y. Nucleotide sequence and genetic characterization of staphylococcal bacteriophage L54a int and xis genes. J. Bacteriol. 1989, 171:4146-4153.
55. Ye Z.H., Lee C.Y. Cloning, sequencing, and genetic characterization of regulatory genes, rinA and rinB, required for the activation of staphylococcal phage phi11 int expression. J. Bacteriol. 1993, 175:1095-1102.
56. Ye Z.H., Buranen S.L., Lee C.Y. Sequence analysis and comparison of int and xis genes from staphylococcal bacteriophages L54a and phi 11. J. Bacteriol. 1990, 172:2568-2575.