Phages of Staphylococcus aureus and their impact on host evolution

Infection, Genetics and Evolution

Volumn 21, Issue , 2014, Pages 593-601

  Xia, Guoqing ^a,b   Wolz, Christiane ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b German Center for Research in Infectious Disease (DZIF)   (Germany)

Author keywords

Adaptation; Classification; Genomics; Phage; Staphylococcus aureus; Virulence factor

Indexed keywords

ADSORPTION; ANIMAL; CLASSIFICATION; EVOLUTION; GENETICS; HORIZONTAL GENE TRANSFER; HUMAN; PHYLOGENY; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS PHAGE; VIROLOGY; VIRUS GENOME;

ADSORPTION; ANIMALS; BIOLOGICAL EVOLUTION; GENE TRANSFER, HORIZONTAL; GENOME, VIRAL; HUMANS; PHYLOGENY; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS PHAGES;

EID: 84893811675     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2013.04.022     Document Type: Article

References (101)

1. Ackermann H.W. Classification of the bacteriophages of Gram-positive cocci: Micrococcus, Staphylococcus, and Streptococcus. Pathol. Biol. (Paris) 1975, 23:247-253.
2. Bae T., Baba T., Hiramatsu K., Schneewind O. Prophages of Staphylococcus aureus Newman and their contribution to virulence. Mol. Microbiol. 2006, 62:1035-1047.
3. Baptista C., Santos M.A., Sao-Jose C. Phage SPP1 reversible adsorption to Bacillus subtilis cell wall teichoic acids accelerates virus recognition of membrane receptor YueB. J. Bacteriol. 2008, 190:4989-4996.
4. Belley A., Callejo M., Arhin F., Dehbi M., Fadhil I., Liu J., McKay G., Srikumar R., Bauda P., Bergeron D., Ha N., Dubow M., Gros P., Pelletier J., Moeck G. Competition of bacteriophage polypeptides with native replicase proteins for binding to the DNA sliding clamp reveals a novel mechanism for DNA replication arrest in Staphylococcus aureus. Mol. Microbiol. 2006, 62:1132-1143.
5. Boakes E., Kearns A.M., Ganner M., Perry C., Hill R.L., Ellington M.J. Distinct bacteriophages encoding Panton-Valentine leukocidin (PVL) among international methicillin-resistant Staphylococcus aureus clones harboring PVL. J. Clin. Microbiol. 2011, 49:684-692.
6. Boyle-Vavra S., Jones M., Gourley B.L., Holmes M., Ruf R., Balsam A.R., Boulware D.R., Kline S., Jawahir S., Devries A., Peterson S.N., Daum R.S. Comparative genome sequencing of an isogenic pair of USA800 clinical methicillin-resistant Staphylococcus aureus isolates obtained before and after daptomycin treatment failure. Antimicrob. Agents Chemother. 2011, 55:2018-2025.
7. Brandis H., Lenz W. Staphylokokken-Bakteriophagen. Staphylokokken und Staphylokokken-Erkrankungen 1984, 186-214. VEB Gustav Fischer Verlag, Jena. W. Meyer (Ed.).
8. Bronner S., Stoessel P., Gravet A., Monteil H., Prevost G. Variable expressions of Staphylococcus aureus bicomponent leucotoxins semiquantified by competitive reverse transcription-PCR. Appl Environ Microbiol 2000, 66:3931-3938.
9. Broudy T.B., Pancholi V., Fischetti V.A. The in vitro interaction of Streptococcus pyogenes with human pharyngeal cells induces a phage-encoded extracellular DNase. Infect Immun. 2002, 70:2805-2811.
10. Brussow H., Desiere F. Comparative phage genomics and the evolution of Siphoviridae: insights from dairy phages. Mol. Microbiol. 2001, 39:213-222.
11. Canchaya C., Proux C., Fournous G., Bruttin A., Brussow H. Prophage genomics. Microbiol. Mol. Biol. Rev. 2003, 67:238-276. table of contents.
12. Carroll J.D., Cafferkey M.T., Coleman D.C. Serotype F double- and triple-converting phage insertionally inactivate the Staphylococcus aureus beta-toxin determinant by a common molecular mechanism. FEMS Microbiol. Lett. 1993, 106:147-155.
13. Chen J., Novick R.P. Phage-mediated intergeneric transfer of toxin genes. Science 2009, 323:139-141.
14. Chen L., Shopsin B., Zhao Y., Smyth D., Wasserman G.A., Fang C., Liu L., Kreiswirth B.N. Real-time nucleic acid sequence-based amplification assay for rapid detection and quantification of agr functionality in clinical Staphylococcus aureus isolates. J. Clin. Microbiol. 2012, 50:657-661.
15. Christie G.E., Dokland T. Pirates of the caudovirales. Virology 2012, 434:210-221.
16. Deghorain M., Van Melderen L. The Staphylococci phages family: an overview. Viruses 2012, 4:3316-3335.
17. Deghorain M., Bobay L.M., Smeesters P.R., Bousbata S., Vermeersch M., Perez-Morga D., Dreze P.A., Rocha E.P., Touchon M., Van Melderen L. Characterization of novel phages isolated in coagulase-negative staphylococci reveals evolutionary relationships with Staphylococcus aureus phages. J. Bacteriol. 2012, 194:5829-5839.
18. Dehbi M., Moeck G., Arhin F.F., Bauda P., Bergeron D., Kwan T., Liu J., McCarty J., Dubow M., Pelletier J. Inhibition of transcription in Staphylococcus aureus by a primary sigma factor-binding polypeptide from phage G1. J. Bacteriol. 2009, 191:3763-3771.
19. 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.
20. Dokland T., Isaksen M.L., Fuller S.D., Lindqvist B.H. Capsid localization of the bacteriophage P4 Psu protein. Virology 1993, 194:682-687.
21. Dumitrescu O., Choudhury P., Boisset S., Badiou C., Bes M., Benito Y., Wolz C., Vandenesch F., Etienne J., Cheung A.L., Bowden M.G., Lina G. Beta-lactams interfering with PBP1 induce Panton-Valentine leukocidin expression by triggering sarA and rot global regulators of Staphylococcus aureus. Antimicrob. Agents Chemother. 2011, 55:3261-3271.
22. Feil E.J., Cooper J.E., Grundmann H., Robinson D.A., Enright M.C., Berendt T., Peacock S.J., Smith J.M., Murphy M., Spratt B.G., Moore C.E., Day N.P. How clonal is Staphylococcus aureus?. J. Bacteriol. 2003, 185:3307-3316.
23. Ferrer M.D., Quiles-Puchalt N., Harwich M.D., Tormo-Mas M.A., Campoy S., Barbe J., Lasa I., Novick R.P., Christie G.E., Penades J.R. RinA controls phage-mediated packaging and transfer of virulence genes in Gram-positive bacteria. Nucleic Acids Res. 2011, 39:5866-5878.
24. Ganguly T., Das M., Bandhu A., Chanda P.K., Jana B., Mondal R., Sau S. Physicochemical properties and distinct DNA binding capacity of the repressor of temperate Staphylococcus aureus phage phi11. FEBS J. 2009, 276:1975-1985.
25. Goerke C., Matias y Papenberg S., Dasbach S., Dietz K., Ziebach R., Kahl B.C., Wolz C. Increased frequency of genomic alterations in Staphylococcus aureus during chronic infection is in part due to phage mobilization. J. Infect. Dis. 2004, 189:724-734.
26. Goerke C., Koller J., Wolz C. Ciprofloxacin and trimethoprim cause phage induction and virulence modulation in Staphylococcus aureus. Antimicrob. Agents Chemother. 2006, 50:171-177.
27. Goerke C., Wirtz C., Fluckiger U., Wolz C. Extensive phage dynamics in Staphylococcus aureus contributes to adaptation to the human host during infection. Mol. Microbiol. 2006, 61:1673-1685.
28. Goerke C., Pantucek R., Holtfreter S., Schulte B., Zink M., Grumann D., Broker B.M., Doskar J., Wolz C. Diversity of prophages in dominant Staphylococcus aureus clonal lineages. J. Bacteriol. 2009, 191:3462-3468.
29. Guinane C.M., Penades J.R., Fitzgerald J.R. The role of horizontal gene transfer in Staphylococcus aureus host adaptation. Virulence 2011, 2:241-243.
30. Hatfull G.F., Hendrix R.W. Bacteriophages and their genomes. Curr. Opin. Virol. 2011, 1:298-303.
31. Holden M.T., Lindsay J.A., Corton C., Quail M.A., Cockfield J.D., Pathak S., Batra R., Parkhill J., Bentley S.D., Edgeworth J.D. Genome sequence of a recently emerged, highly transmissible, multi-antibiotic- and antiseptic-resistant variant of methicillin-resistant Staphylococcus aureus, sequence type 239 (TW). J. Bacteriol. 2010, 192:888-892.
32. Holochova P., Ruzickova V., Dostalova L., Pantucek R., Petras P., Doskar J. Rapid detection and differentiation of the exfoliative toxin A-producing Staphylococcus aureus strains based on phiETA prophage polymorphisms. Diagn. Microbiol. Infect. Dis. 2010, 66:248-252.
33. Iandolo J.J., Worrell V., Groicher K.H., Qian Y., Tian R., Kenton S., Dorman A., Ji H., Lin S., Loh P., Qi S., Zhu H., Roe B.A. 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.
34. Jin T., Bokarewa M., McIntyre L., Tarkowski A., Corey G.R., Reller L.B., Fowler V.G. Fatal outcome of bacteraemic patients caused by infection with staphylokinase-deficient Staphylococcus aureus strains. J. Med. Microbiol. 2003, 52:919-923.
35. Kahankova J., Pantucek R., Goerke C., Ruzickova V., Holochova P., Doskar J. Multilocus PCR typing strategy for differentiation of Staphylococcus aureus siphoviruses reflecting their modular genome structure. Environ. Microbiol. 2010, 12:2527-2538.
36. Kaneko J., Kimura T., Narita S., Tomita T., Kamio Y. Complete nucleotide sequence and molecular characterization of the temperate staphylococcal bacteriophage phiPVL carrying Panton-Valentine leukocidin genes. Gene 1998, 215:57-67.
37. Kaneko J., Narita-Yamada S., Wakabayashi Y., Kamio Y. Identification of ORF636 in phage phiSLT carrying Panton-Valentine leukocidin genes, acting as an adhesion protein for a poly(glycerophosphate) chain of lipoteichoic acid on the cell surface of Staphylococcus aureus. J. Bacteriol. 2009, 191:4674-4680.
38. Kato F., Kadomoto N., Iwamoto Y., Bunai K., Komatsuzawa H., Sugai M. Regulatory mechanism for exfoliative toxin production in Staphylococcus aureus. Infect. Immun. 2011, 79:1660-1670.
39. Kurt K., Rasigade J.P., Laurent F., Goering R.V., Zemlickova H., Machova I., Struelens M.J., Zautner A.E., Holtfreter S., Broker B., Ritchie S., Reaksmey S., Limmathurotsakul D., Peacock S.J., Cuny C., Layer F., Witte W., Nubel U. Subpopulations of Staphylococcus aureus clonal complex 121 are associated with distinct clinical entities. PLoS One 2013, 8:e58155.
40. 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.
41. Lee C.Y., Iandolo J.J. Lysogenic conversion of staphylococcal lipase is caused by insertion of the bacteriophage L54a genome into the lipase structural gene. J. Bacteriol. 1986, 166:385-391.
42. Li M., Du X., Villaruz A.E., Diep B.A., Wang D., Song Y., Tian Y., Hu J., Yu F., Lu Y., Otto M. MRSA epidemic linked to a quickly spreading colonization and virulence determinant. Nat. Med. 2012, 18:816-819.
43. Lindsay J.A. Genomic variation and evolution of Staphylococcus aureus. Int. J. Med. Microbiol. 2010, 300:98-103.
44. Lindsay J.A., Holden M.T. Staphylococcus aureus: superbug, super genome?. Trends Microbiol. 2004, 12:378-385.
45. Liu J., Dehbi M., Moeck G., Arhin F., Bauda P., Bergeron D., Callejo M., Ferretti V., Ha N., Kwan T., McCarty J., Srikumar R., Williams D., Wu J.J., Gros P., Pelletier J., DuBow M. Antimicrobial drug discovery through bacteriophage genomics. Nat. Biotechnol. 2004, 22:185-191.
46. Lobocka M., Hejnowicz M.S., Dabrowski K., Gozdek A., Kosakowski J., Witkowska M., Ulatowska M.I., Weber-Dabrowska B., Kwiatek M., Parasion S., Gawor J., Kosowska H., Glowacka A. Genomics of staphylococcal Twort-like phages-potential therapeutics of the post-antibiotic era. Adv. Virus Res. 2012, 83:143-216.
47. Loessner M.J., Gaeng S., Wendlinger G., Maier S.K., Scherer S. The two-component lysis system of Staphylococcus aureus bacteriophage Twort: a large TTG-start holin and an associated amidase endolysin. FEMS Microbiol. Lett. 1998, 162:265-274.
48. Ma X.X., Ito T., Kondo Y., Cho M., Yoshizawa Y., Kaneko J., Katai A., Higashiide M., Li S., Hiramatsu K. Two different Panton-Valentine leukocidin phage lineages predominate in Japan. J. Clin. Microbiol. 2008, 46:3246-3258.
49. Maiques E., Ubeda C., Campoy S., Salvador N., Lasa I., Novick R.P., Barbé J., Penadés J.R. Beta-lactam antibiotics induce the SOS response and horizontal transfer of virulence factors in Staphylococcus aureus. J. Bacteriol. 2006, 188:2726-2729.
50. Matthews A.M., Novick R.P. Staphylococcal phages. Phages. Their Role in Bacterial Pathogenesis and Biotechnology 2005, 297-318. American Society for Microbiology Press, Washington, DC. M.K. Waldor, D.I. Friedman, S.L. Adhya (Eds.).
51. McCarthy A.J., van Wamel W., Vandendriessche S., Larsen J., Denis O., Garcia-Graells C., Uhlemann A.C., Lowy F.D., Skov R., Lindsay J.A. Staphylococcus aureus CC398 clade associated with human-to-human transmission. Appl. Environ. Microbiol. 2012, 78:8845-8848.
52. McCarthy A.J., Witney A.A., Lindsay J.A. Staphylococcus aureus temperate bacteriophage: carriage and horizontal gene transfer is lineage associated. Front. Cell. Infect. Microbiol. 2012, 2:6.
53. Melles D.C., Gorkink R.F., Boelens H.A., Snijders S.V., Peeters J.K., Moorhouse M.J., van der Spek P.J., van Leeuwen W.B., Simons G., Verbrugh H.A., van Belkum A. Natural population dynamics and expansion of pathogenic clones of Staphylococcus aureus. J. Clin. Invest. 2004, 114:1732-1740.
54. Morikawa K., Takemura A.J., Inose Y., Tsai M., Nguyen Thi li T., Ohta T., Msadek T. Expression of a cryptic secondary sigma factor gene unveils natural competence for DNA transformation in Staphylococcus aureus. PLoS Pathog. 2012, 8:e1003003.
55. Narita S., Kaneko J., Chiba J., Piemont Y., Jarraud S., Etienne J., Kamio Y. Phage conversion of Panton-Valentine leukocidin in Staphylococcus aureus: molecular analysis of a PVL-converting phage, phiSLT. Gene 2001, 268:195-206.
56. Navarre W.W., Ton-That H., Faull K.F., Schneewind O. Multiple enzymatic activities of the murein hydrolase from staphylococcal phage phi11. Identification of a d-alanyl-glycine endopeptidase activity. J. Biol. Chem. 1999, 274:15847-15856.
57. Nelson D. Phage taxonomy: we agree to disagree. J. Bacteriol. 2004, 186:7029-7031.
58. Novick R.P., Christie G.E., Penades J.R. The phage-related chromosomal islands of Gram-positive bacteria. Nat. Rev. Microbiol. 2010, 8:541-551.
59. Nubel U., Roumagnac P., Feldkamp M., Song J.H., Ko K.S., Huang Y.C., Coombs G., Ip M., Westh H., Skov R., Struelens M.J., Goering R.V., Strommenger B., Weller A., Witte W., Achtman M. Frequent emergence and limited geographic dispersal of methicillin-resistant Staphylococcus aureus. Proc. Natl. Acad. Sci. USA 2008, 105:14130-14135.
60. Nubel U., Dordel J., Kurt K., Strommenger B., Westh H., Shukla S.K., Zemlickova H., Leblois R., Wirth T., Jombart T., Balloux F., Witte W. A timescale for evolution, population expansion, and spatial spread of an emerging clone of methicillin-resistant Staphylococcus aureus. PLoS Pathog. 2010, 6:e1000855.
61. Osmundson J., Montero-Diez C., Westblade L.F., Hochschild A., Darst S.A. Promoter-specific transcription inhibition in Staphylococcus aureus by a phage protein. Cell 2012, 151:1005-1016.
62. Otter J.A., Kearns A.M., French G.L., Ellington M.J. Panton-Valentine leukocidin-encoding bacteriophage and gene sequence variation in community-associated methicillin-resistant Staphylococcus aureus. Clin. Microbiol. Infect. 2010, 16:68-73.
63. Otto M. Coagulase-negative staphylococci as reservoirs of genes facilitating MRSA infection: staphylococcal commensal species such as Staphylococcus epidermidis are being recognized as important sources of genes promoting MRSA colonization and virulence. Bioessays 2013, 35:4-11.
64. Pani B., Banerjee S., Chalissery J., Muralimohan A., Loganathan R.M., Suganthan R.B., Sen R. Mechanism of inhibition of Rho-dependent transcription termination by bacteriophage P4 protein Psu. J. Biol. Chem. 2006, 281:26491-26500.
65. Peacock S.J., Moore C.E., Justice A., Kantzanou M., Story L., Mackie K., O'Neill G., Day N.P. Virulent combinations of adhesin and toxin genes in natural populations of Staphylococcus aureus. Infect. Immun. 2002, 70:4987-4996.
66. Poliakov A., Chang J.R., Spilman M.S., Damle P.K., Christie G.E., Mobley J.A., Dokland T. Capsid size determination by Staphylococcus aureus pathogenicity island SaPI1 involves specific incorporation of SaPI1 proteins into procapsids. J. Mol. Biol. 2008, 380:465-475.
67. Price L.B., Stegger M., Hasman H., Aziz M., Larsen J., Andersen P.S., Pearson T., Waters A.E., Foster J.T., Schupp J., Gillece J., Driebe E., Liu C.M., Springer B., Zdovc I., Battisti A., Franco A., Zmudzki J., Schwarz S., Butaye P., Jouy E., Pomba C., Porrero M.C., Ruimy R., Smith T.C., Robinson D.A., Weese J.S., Arriola C.S., Yu F., Laurent F., Keim P., Skov R., Aarestrup F.M. Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. MBio 2012, 3:e00305-e00311.
68. Resch G., Francois P., Morisset D., Stojanov M., Bonetti E.J., Schrenzel J., Sakwinska O., Moreillon P. Human-to-bovine jump of Staphylococcus aureus CC8 is associated with the loss of a beta-hemolysin converting prophage and the acquisition of a new staphylococcal cassette chromosome. PLoS One 2013, 8:e58187.
69. Rippon J.E. A new serological division of Staphylococcus aureus bacteriophages: group G. Nature 1952, 170:287.
70. Rippon J.E. The classification of bacteriophages lysing staphylococci. J. Hyg. (Lond.) 1956, 54:213-226.
71. Rodriguez L., Martinez B., Zhou Y., Rodriguez A., Donovan D.M., Garcia P. Lytic activity of the virion-associated peptidoglycan hydrolase HydH5 of Staphylococcus aureus bacteriophage vB_SauS-phiIPLA88. BMC Microbiol. 2011, 11:138.
72. Rooijakkers S.H., Ruyken M., van Roon J., van Kessel K.P., van Strijp J.A., van Wamel W.J. Early expression of SCIN and CHIPS drives instant immune evasion by Staphylococcus aureus. Cell. Microbiol. 2006, 8:1282-1293.
73. Rountree P.M. The serological differentiation of staphylococcal bacteriophages. J. Gen. Microbiol. 1949, 3:164-173.
74. Ruzickova V., Pantucek R., Petras P., Machova I., Kostylkova K., Doskar J. Major clonal lineages in impetigo Staphylococcus aureus strains isolated in Czech and Slovak maternity hospitals. Int. J. Med. Microbiol. 2012, 302:237-241.
75. Schulte B., Bierbaum G., Pohl K., Goerke C., Wolz C. Diversification of clonal complex 5 MRSA strains (Rhine-Hesse clone) within Germany. J. Clin. Microbiol. 2013, 51:212-216.
76. Shallcross L.J., Fragaszy E., Johnson A.M., Hayward A.C. The role of the Panton-Valentine leucocidin toxin in staphylococcal disease: a systematic review and meta-analysis. Lancet Infect. Dis. 2013, 13:43-54.
77. Shi D., Higuchi W., Takano T., Saito K., Ozaki K., Takano M., Nitahara Y., Yamamoto T. Bullous impetigo in children infected with methicillin-resistant Staphylococcus aureus alone or in combination with methicillin-susceptible S. aureus: analysis of genetic characteristics, including assessment of exfoliative toxin gene carriage. J. Clin. Microbiol. 2011, 49:1972-1974.
78. Spilman M.S., Damle P.K., Dearborn A.D., Rodenburg C.M., Chang J.R., Wall E.A., Christie G.E., Dokland T. Assembly of bacteriophage 80alpha capsids in a Staphylococcus aureus expression system. Virology 2012, 434:242-250.
79. 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.
80. Takac M., Witte A., Blasi U. Functional analysis of the lysis genes of Staphylococcus aureus phage P68 in Escherichia coli. Microbiology 2005, 151:2331-2342.
81. 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.
82. Tao L., Wu X., Sun B. Alternative sigma factor sigmaH modulates prophage integration and excision in Staphylococcus aureus. PLoS Pathog. 2010, 6:e1000888.
83. Tattevin P., Schwartz B.S., Graber C.J., Volinski J., Bhukhen A., Mai T.T., Vo N.H., Dang D.N., Phan T.H., Basuino L., Perdreau-Remington F., Chambers H.F., Diep B.A. Concurrent epidemics of skin and soft tissue infection and bloodstream infection due to community-associated methicillin-resistant Staphylococcus aureus. Clin. Infect. Dis. 2012, 55:781-788.
84. Tormo M.A., Ferrer M.D., Maiques E., Ubeda C., Selva L., Lasa I., Calvete J.J., Novick R.P., Penades J.R. Staphylococcus aureus Pathogenicity Island DNA is packaged in particles composed of phage proteins. J. Bacteriol. 2008, 190:2434-2440.
85. Tormo-Mas M.A., Mir I., Shrestha A., Tallent S.M., Campoy S., Lasa I., Barbe J., Novick R.P., Christie G.E., Penades J.R. Moonlighting bacteriophage proteins derepress staphylococcal pathogenicity islands. Nature 2010, 465:779-782.
86. Uchikawa K., Sekikawa I., Azuma I. Structural studies on teichoic acids in cell walls of several serotypes of Listeria monocytogenes. J. Biochem. 1986, 99:315-327.
87. 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.
88. Vandenesch F., Naimi T., Enright M.C., Lina G., Nimmo G.R., Heffernan H., Liassine N., Bes M., Greenland T., Reverdy M.E., Etienne J. Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: worldwide emergence. Emerg. Infect. Dis. 2003, 9:978-984.
89. Verkaik N.J., Benard M., Boelens H.A., de Vogel C.P., Nouwen J.L., Verbrugh H.A., Melles D.C., van Belkum A., van Wamel W.J. Immune evasion cluster-positive bacteriophages are highly prevalent among human Staphylococcus aureus strains, but they are not essential in the first stages of nasal colonization. Clin. Microbiol. Infect. 2011, 17:343-348.
90. Vinga I., Baptista C., Auzat I., Petipas I., Lurz R., Tavares P., Santos M.A., Sao-Jose C. Role of bacteriophage SPP1 tail spike protein gp21 on host cell receptor binding and trigger of phage DNA ejection. Mol. Microbiol. 2012, 83:289-303.
91. Wagner P.L., Waldor M.K. Bacteriophage control of bacterial virulence. Infect. Immun. 2002, 70:3985-3993.
92. Waldron D.E., Lindsay J.A. Sau1: a novel lineage-specific type I restriction-modification system that blocks horizontal gene transfer into Staphylococcus aureus and between S. aureus isolates of different lineages. J. Bacteriol. 2006, 188:5578-5585.
93. Weidenmaier C., Peschel A. Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions. Nat. Rev. Microbiol. 2008, 6:276-287.
94. Wielders C.L., Vriens M.R., Brisse S., de Graaf-Miltenburg L.A., Troelstra A., Fleer A., Schmitz F.J., Verhoef J., Fluit A.C. In-vivo transfer of mecA DNA to Staphylococcus aureus [corrected]. Lancet 2001, 357:1674-1675.
95. Wirtz C., Witte W., Wolz C., Goerke C. Transcription of the phage-encoded Panton-Valentine leukocidin of Staphylococcus aureus is dependent on the phage life-cycle and on the host background. Microbiology 2009, 155:3491-3499.
96. Xia G., Kohler T., Peschel A. The wall teichoic acid and lipoteichoic acid polymers of Staphylococcus aureus. Int. J. Med. Microbiol. 2010, 300:148-154.
97. Xia G., Corrigan R.M., Winstel V., Goerke C., Grundling A., Peschel A. Wall teichoic acid-dependent adsorption of staphylococcal siphovirus and myovirus. J. Bacteriol. 2011, 193:4006-4009.
98. Yamaguchi T., Hayashi T., Takami H., Ohnishi M., Murata T., Nakayama K., Asakawa K., Ohara M., Komatsuzawa H., Sugai M. Complete nucleotide sequence of a Staphylococcus aureus exfoliative toxin B plasmid and identification of a novel ADP-ribosyltransferase, EDIN-C. Infect. Immun. 2001, 69:7760-7771.
99. Yamaguchi T., Nishifuji K., Sasaki M., Fudaba Y., Aepfelbacher M., Takata T., Ohara M., Komatsuzawa H., Amagai M., Sugai M. Identification of the Staphylococcus aureus etd pathogenicity island which encodes a novel exfoliative toxin, ETD, and EDIN-B. Infect. Immun. 2002, 70:5835-5845.
100. Ye Z.H., Lee C.Y. Cloning, sequencing, and genetic characterization of regulatory genes, rinA and rinB, required for the activation of staphylococcal phage phi 11 int expression. J. Bacteriol. 1993, 175:1095-1102.
101. Zanger P., Nurjadi D., Schleucher R., Scherbaum H., Wolz C., Kremsner P.G., Schulte B. Import and spread of Panton-Valentine leukocidin-positive Staphylococcus aureus through nasal carriage and skin infections in travelers returning from the tropics and subtropics. Clin. Infect. Dis. 2012, 54:483-492.