Isolation and characterization of a new Staphylococcus epidermidis broad-spectrum bacteriophage

Journal of General Virology

Volumn 95, Issue PART 2, 2014, Pages 506-515

  Melo, Luís D R ^a   Sillankorva, Sanna ^a   Ackermann, Hans Wolfgang ^b   Kropinski, Andrew M ^c,d   Azeredo, Joana ^a   Cerca, Nuno ^a  

^a UNIVERSITY OF MINHO   (Portugal)

^b UNIVERSITÉ LAVAL   (Canada)

^c PUBLIC HEALTH AGENCY OF CANADA   (Canada)

^d UNIVERSITY OF GUELPH   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIOPHAGE; BACTERIUM EXAMINATION; BACTERIUM ISOLATION; CONTROLLED STUDY; DNA SEQUENCE; GENE SEQUENCE; GENOMICS; MORPHOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEOMICS; STAPHYLOCOCCUS EPIDERMIDIS; TWORTLIKEVIRUS; VIRUS; VIRUS IDENTIFICATION;

DNA, VIRAL; GENOME, VIRAL; HOST SPECIFICITY; HUMANS; MOLECULAR SEQUENCE DATA; MYOVIRIDAE; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY; STAPHYLOCOCCUS EPIDERMIDIS; STAPHYLOCOCCUS PHAGES; SYNTENY;

EID: 84892567534     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.060590-0     Document Type: Article

References (73)

1. Ackermann, H. W. (2009). Basic phage electron microscopy. Methods Mol Biol 501, 113-126.
2. Ackermann, H. W. & Kropinski, A. M. (2007). Curated list of prokaryote viruses with fully sequenced genomes. Res Microbiol 158, 555-566.
3. 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.
4. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25, 3389-3402.
5. Aswani, V. H. & Shukla, S. K. (2011). Prevalence of Staphylococcus aureus and lack of its lytic bacteriophages in the anterior nares of patients and healthcare workers at a rural clinic. Clin Med Res 9, 75-81.
6. Aziz, R. K., Bartels, D., Best, A. A., DeJongh, M., Disz, T., Edwards, R. A., Formsma, K., Gerdes, S., Glass, E. M. & other authors (2008). The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9, 75.
7. Bae, T., Baba, T., Hiramatsu, K. & Schneewind, O. (2006). Prophages of Staphylococcus aureus Newman and their contribution to virulence. Mol Microbiol 62, 1035-1047.
8. Bailey, T. L., Boden, M., Buske, F. A., Frith, M., Grant, C. E., Clementi, L., Ren, J., Li, W. W. & Noble, W. S. (2009). MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37 (Web Server issue), W202-W208.
9. Barabas, O., Ronning, D. R., Guynet, C., Hickman, A. B., Ton-Hoang, B., Chandler, M. & Dyda, F. (2008). Mechanism of IS200/IS605 family DNA transposases: activation and transposon-directed target site selection. Cell 132, 208-220.
10. 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.
11. Cerca, N., Martins, S., Cerca, F., Jefferson, K. K., Pier, G. B., Oliveira, R. & Azeredo, J. (2005). Comparative assessment of antibiotic susceptibility of coagulase-negative staphylococci in biofilm versus planktonic culture as assessed by bacterial enumeration or rapid XTT colorimetry. J Antimicrob Chemother 56, 331-336.
12. Cerca, N., Jefferson, K. K., Oliveira, R., Pier, G. B. & Azeredo, J. (2006). Comparative antibody-mediated phagocytosis of Staphylococcus epidermidis cells grown in a biofilm or in the planktonic state. Infect Immun 74, 4849-4855.
13. Cerca, N., Oliveira, R. & Azeredo, J. (2007). Susceptibility of Staphylococcus epidermidis planktonic cells and biofilms to the lytic action of staphylococcus bacteriophage K. Lett Appl Microbiol 45, 313-317.
14. Cerca, N., Gomes, F., Bento, J. C., França, A., Rolo, J., Miragaia, M., Teixeira, P. & Oliveira, R. (2013). Farnesol induces cell detachment from established S. epidermidis biofilms. J Antibiot (Tokyo) 66, 255-258.
15. Cui, Z., Song, Z., Wang, Y., Zeng, L., Shen, W., Wang, Z., Li, Q., He, P., Qin, J. & Guo, X. (2012). Complete genome sequence of wide-hostrange Staphylococcus aureus phage JD007. J Virol 86, 13880-13881.
16. Daly, C., Fitzgerald, G. F. & Davis, R. (1996). Biotechnology of lactic acid bacteria with special reference to bacteriophage resistance. Antonie van Leeuwenhoek 70, 99-110.
17. Daniel, A., Bonnen, P. E. & Fischetti, V. A. (2007). First complete genome sequence of two Staphylococcus epidermidis bacteriophages. J Bacteriol 189, 2086-2100.
18. Darling, A. E., Mau, B. & Perna, N. T. (2010). progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 5, e11147.
19. Eyer, L., Pantůcek, R., Zdráhal, Z., Konecná, H., Kaspárek, P., Růzicková, V., Hernychová, L., Preisler, J. & Doskar, J. (2007). Structural protein analysis of the polyvalent staphylococcal bacteriophage 812. Proteomics 7, 64-72.
20. Feng, Y., Chen, C. J., Su, L. H., Hu, S., Yu, J. & Chiu, C. H. (2008). Evolution and pathogenesis of Staphylococcus aureus: lessons learned from genotyping and comparative genomics. FEMS Microbiol Rev 32, 23-37.
21. Gill, J. J. & Hyman, P. (2010). Phage choice, isolation, and preparation for phage therapy. Curr Pharm Biotechnol 11, 2-14.
22. Gu, J., Liu, X., Lu, R., Li, Y., Song, J., Lei, L., Sun, C., Feng, X., Du, C. & other authors (2012). Complete genome sequence of Staphylococcus aureus bacteriophage GH15. J Virol 86, 8914-8915.
23. Gupta, R. & Prasad, Y. (2011). Efficacy of polyvalent bacteriophage P-27/HP to control multidrug resistant Staphylococcus aureus associated with human infections. Curr Microbiol 62, 255-260.
24. Gustafsson, I., Cars, O. & Andersson, D. I. (2003). Fitness of antibiotic resistant Staphylococcus epidermidis assessed by competition on the skin of human volunteers. J Antimicrob Chemother 52, 258-263.
25. Gutiérrez, D., Martínez, B., Rodríguez, A. & García, P. (2010). Isolation and characterization of bacteriophages infecting Staphylococcus epidermidis. Curr Microbiol 61, 601-608.
26. Gutiérrez, D., Martínez, B., Rodríguez, A. & García, P. (2012). Genomic characterization of two Staphylococcus epidermidis bacteriophages with anti-biofilm potential. BMC Genomics 13, 228.
27. Hoshiba, H., Uchiyama, J., Kato, S., Ujihara, T., Muraoka, A., Daibata, M., Wakiguchi, H. & Matsuzaki, S. (2010). Isolation and characterization of a novel Staphylococcus aureus bacteriophage, phiMR25, and its therapeutic potential. Arch Virol 155, 545-552.
28. 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 phi 11, phi 12 and phi 13 of Staphylococcus aureus 8325. Gene 289, 109-118.
29. Jabbouri, S. & Sadovskaya, I. (2010). Characteristics of the biofilm matrix and its role as a possible target for the detection and eradication of Staphylococcus epidermidis associated with medical implant infections. FEMS Immunol Med Microbiol 59, 280-291.
30. Käll, L. & Sonnhammer, E. L. (2002). Reliability of transmembrane predictions in whole-genome data. FEBS Lett 532, 415-418.
31. Käll, L., Krogh, A. & Sonnhammer, E. L. (2004). A combined transmembrane topology and signal peptide prediction method. J Mol Biol 338, 1027-1036.
32. Kaneko, J., Kimura, T., Narita, S., Tomita, T. & Kamio, Y. (1998). Complete nucleotide sequence and molecular characterization of the temperate staphylococcal bacteriophage phiPVL carrying Panton-Valentine leukocidin genes. Gene 215, 57-67.
33. Kelly, D., McAuliffe, O., Ross, R. P. & Coffey, A. (2012). Prevention of Staphylococcus aureus biofilm formation and reduction in established biofilm density using a combination of phage K and modified derivatives. Lett Appl Microbiol 54, 286-291.
34. Klumpp, J., Dorscht, J., Lurz, R., Bielmann, R., Wieland, M., Zimmer, M., Calendar, R. & Loessner, M. J. (2008). The terminally redundant, nonpermuted genome of Listeria bacteriophage A511: a model for the SPO1-like myoviruses of Gram-positive bacteria. J Bacteriol 190, 5753-5765.
35. Klumpp, J., Lavigne, R., Loessner, M. J. & Ackermann, H. W. (2010). The SPO1-related bacteriophages. Arch Virol 155, 1547-1561.
36. Kropinski, A. M., Sulakvelidze, A., Konczy, P. & Poppe, C. (2007). Salmonella phages and prophages-genomics and practical aspects. Methods Mol Biol 394, 133-175.
37. Kutateladze, M. & Adamia, R. (2010). Bacteriophages as potential new therapeutics to replace or supplement antibiotics. Trends Biotechnol 28, 591-595.
38. Kvachadze, L., Balarjishvili, N., Meskhi, T., Tevdoradze, E., Skhirtladze, N., Pataridze, T., Adamia, R., Topuria, T., Kutter, E. & other authors (2011). Evaluation of lytic activity of staphylococcal bacteriophage Sb-1 against freshly isolated clinical pathogens. Microb Biotechnol 4, 643-650.
39. 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.
40. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
41. Laslett, D. & Canback, B. (2004). ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res 32, 11-16.
42. Lavigne, R., Seto, D., Mahadevan, P., Ackermann, H. W. & Kropinski, A. M. (2008). Unifying classical and molecular taxonomic classification: analysis of the Podoviridae using BLASTP-based tools. Res Microbiol 159, 406-414.
43. Lavigne, R., Darius, P., Summer, E. J., Seto, D., Mahadevan, P., Nilsson, A. S., Ackermann, H. W. & Kropinski, A. M. (2009). Classification of Myoviridae bacteriophages using protein sequence similarity. BMC Microbiol 9, 224.
44. Lindqvist, R. (2006). Estimation of Staphylococcus aureus growth parameters from turbidity data: characterization of strain variation and comparison of methods. Appl Environ Microbiol 72, 4862-4870.
45. Łobocka, M. B., Rose, D. J., Plunkett, G., III, Rusin, M., Samojedny, A., Lehnherr, H., Yarmolinsky, M. B. & Blattner, F. R. (2004). Genome of bacteriophage P1. J Bacteriol 186, 7032-7068.
46. Łobocka, M., Hejnowicz, M. S., Dabrowski, K., Gozdek, A., Kosakowski, J., Witkowska, M., Ulatowska, M. I., Weber-Dabrowska, B., Kwiatek, M. & other authors (2012). Genomics of staphylococcal Twort-like phages-potential therapeutics of the postantibiotic era. Adv Virus Res 83, 143-216.
47. Loc-Carrillo, C. & Abedon, S. T. (2011). Pros and cons of phage therapy. Bacteriophage 1, 111-114.
48. Madhusoodanan, J., Seo, K. S., Remortel, B., Park, J. Y., Hwang, S. Y., Fox, L. K., Park, Y. H., Deobald, C. F., Wang, D. & other authors (2011). An enterotoxin-bearing pathogenicity island in Staphylococcus epidermidis. J Bacteriol 193, 1854-1862.
49. Mahadevan, P., King, J. F. & Seto, D. (2009). Data mining pathogen genomes using GeneOrder and CoreGenes and CGUG: gene order, synteny and in silico proteomes. Int J Comput Biol Drug Des 2, 100-114.
50. Marchler-Bauer, A., Lu, S., Anderson, J. B., Chitsaz, F., Derbyshire, M. K., DeWeese-Scott, C., Fong, J. H., Geer, L. Y., Geer, R. C. & other authors (2011). CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res 39 (Database issue), D225-D229.
51. Myers, E. W. & Miller, W. (1988). Optimal alignments in linear space. Comput Appl Biosci 4, 11-17.
52. Naville, M., Ghuillot-Gaudeffroy, A., Marchais, A. & Gautheret, D. (2011). ARNold: a web tool for the prediction of Rho-independent transcription terminators. RNA Biol 8, 11-13.
53. NNIS System (2004). National Nosocomial Infections Surveillance (NNIS) System Report, data summary from January 1992 through June 2004, issued October 2004. Am J Infect Control 32, 470-485.
54. O'Flaherty, S., Coffey, A., Edwards, R., Meaney, W., Fitzgerald, G. F. & Ross, R. P. (2004). Genome of staphylococcal phage K: a new lineage of Myoviridae infecting Gram-positive bacteria with a low G+C content. J Bacteriol 186, 2862-2871.
55. O'Flaherty, S., Ross, R. P., Meaney, W., Fitzgerald, G. F., Elbreki, M. F. & Coffey, A. (2005). Potential of the polyvalent anti-Staphylococcus bacteriophage K for control of antibiotic-resistant staphylococci from hospitals. Appl Environ Microbiol 71, 1836-1842.
56. Otto, M. (2009). Staphylococcus epidermidis-the 'accidental' pathogen. Nat Rev Microbiol 7, 555-567.
57. Otto, M. (2010). Basis of virulence in community-associated methicillin-resistant Staphylococcus aureus. Annu Rev Microbiol 64, 143-162.
58. Pantůček, R., Rosypalová, A., Doškar, J., Kailerová, J., Růžičková, V., Borecká, P., Snopková, S., Horváth, R., Götz, F. & Rosypal, S. (1998). The polyvalent staphylococcal phage phi 812: its host-range mutants and related phages. Virology 246, 241-252.
59. Pires, D., Sillankorva, S., Faustino, A. & Azeredo, J. (2011). Use of newly isolated phages for control of Pseudomonas aeruginosa PAO1 and ATCC 10145 biofilms. Res Microbiol 162, 798-806.
60. Rees, P. J. & Fry, B. A. (1981). The morphology of staphylococcal bacteriophage K and DNA metabolism in infected Staphylococcus aureus. J Gen Virol 53, 293-307.
61. Rice, P., Longden, I. & Bleasby, A. (2000). EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16, 276-277.
62. Rohwer, F. & Edwards, R. (2002). The Phage Proteomic Tree: a genome-based taxonomy for phage. J Bacteriol 184, 4529-4535.
63. Schattner, P., Brooks, A. N. & Lowe, T. M. (2005). The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 33 (Web Server issue), W686-W689.
64. Sillankorva, S., Neubauer, P. & Azeredo, J. (2008). Isolation and characterization of a T7-like lytic phage for Pseudomonas fluorescens. BMC Biotechnol 8, 80.
65. Sillankorva, S., Neubauer, P. & Azeredo, J. (2010). Phage control of dual species biofilms of Pseudomonas fluorescens and Staphylococcus lentus. Biofouling 26, 567-575.
66. Son, J. S., Lee, S. J., Jun, S. Y., Yoon, S. J., Kang, S. H., Paik, H. R., Kang, J. O. & Choi, Y. J. (2010). Antibacterial and biofilm removal activity of a Podoviridae Staphylococcus aureus bacteriophage SAP-2 and a derived recombinant cell-wall-degrading enzyme. Appl Microbiol Biotechnol 86, 1439-1449.
67. Stothard, P. & Wishart, D. S. (2005). Circular genome visualization and exploration using CGView. Bioinformatics 21, 537-539.
68. Sulakvelidze, A., Alavidze, Z. & Morris, J. G., Jr (2001). Bacteriophage therapy. Antimicrob Agents Chemother 45, 649-659.
69. Van Twest, R. & Kropinski, A. M. (2009). Bacteriophage enrichment from water and soil. Methods Mol Biol 501, 15-21.
70. Vandersteegen, K., Mattheus, W., Ceyssens, P. J., Bilocq, F., De Vos, D., Pirnay, J. P., Noben, J. P., Merabishvili, M., Lipinska, U. & other authors (2011). Microbiological and molecular assessment of bacteriophage ISP for the control of Staphylococcus aureus. PLoS ONE 6, e24418.
71. Vandersteegen, K., Kropinski, A. M., Nash, J. H., Noben, J. P., Hermans, K. & Lavigne, R. (2013). Romulus and Remus, two phage isolates representing a distinct clade within the Twortlikevirus genus, display suitable properties for phage therapy applications. J Virol 87, 3237-3247.
72. Vuong, C. & Otto, M. (2002). Staphylococcus epidermidis infections. Microbes Infect 4, 481-489.
73. Zuker, M. (2003). Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31, 3406-3415.