Genome analysis of Cronobacter phage vB_CsaP_Ss1 reveals an endolysin with potential for biocontrol of Gram-negative bacterial pathogens

Journal of General Virology

Volumn 96, Issue 2, 2015, Pages 463-477

  Endersen, Lorraine ^a   Guinane, Caitriona M ^b   Johnston, Christopher ^a   Neve, Horst ^c   Coffey, Aidan ^a   Paul Ross, R ^b   McAuliffe, Olivia ^b   O’Mahony, Jim ^a  

^a Department of Chemistry   (Ireland)

^b TEAGASC FOOD RESEARCH CENTRE   (Ireland)

^c FEDERAL RESEARCH INSTITUTE OF NUTRITION AND FOOD   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; HYDROLASE; PEPTIDOGLYCAN; ENDOLYSIN; PROTEINASE; VIRUS DNA;

ARTICLE; BACTERIOPHAGE; CLONING; CRONOBACTER; DATA BASE; GENE EXPRESSION; GENE SEQUENCE; GENOME ANALYSIS; GRAM NEGATIVE BACTERIUM; HYDROLYSIS; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; ZYMOGRAPHY; BIOLOGICAL PEST CONTROL; CELL WALL; CHEMISTRY; DNA BASE COMPOSITION; DNA SEQUENCE; DRUG EFFECTS; GENETICS; METABOLISM; MOLECULAR GENETICS; PROCEDURES; VIROLOGY; VIRUS GENOME;

BACTERIA (MICROORGANISMS); NEGIBACTERIA;

BACTERIOPHAGES; BASE COMPOSITION; CELL WALL; CRONOBACTER; DNA, VIRAL; ENDOPEPTIDASES; GENOME, VIRAL; GRAM-NEGATIVE BACTERIA; HYDROLYSIS; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; PEPTIDOGLYCAN; PEST CONTROL, BIOLOGICAL; SEQUENCE ANALYSIS, DNA;

EID: 84921751840     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.068494-0     Document Type: Article

References (103)

1. Al-Holy, M. A., Lin, M., Al-Qadiri, H. M. & Rasco, B. A. (2008). A comparative study between overlay methods and selective-differential media for recovery of stressed Enterobacter sakazakii from infant formula. J Food Microbiol 25, 22-28.
2. Anany, H., Chen, W., Pelton, R. & Griffiths, M. W. (2011). Biocontrol of Listeria monocytogenes and Escherichia coli O157: H7 in meat by using phages immobilized on modified cellulose membranes. Appl Environ Microbiol 77, 6379-6387.
3. Aravind, L. & Koonin, E. V. (1998). Phosphoesterase domains associated with DNA polymerases of diverse origins. Nucleic Acids Res 26, 3746-3752.
4. Bar-Oz, B., Preminger, A., Peleg, O., Block, C. & Arad, I. (2001). Enterobacter sakazakii infection in the newborn. Acta Paediatr 90, 356-358.
5. Bardina, C., Spricigo, D. A., Cortés, P. & Llagostera, M. (2012). Significance of the bacteriophage treatment schedule in reducing Salmonella colonization of poultry. Appl Environ Microbiol 78, 6600-6607.
6. Barrett, A. J., Woessner, J. F. & Rawlings, N. D. (2004). Chapter 68, Catalytic mechanisms for metallopeptidases, pp. 268-287. In Handbook of Proteolytic Enzymes, vol. 1. Amsterdam: Elsevier.
7. Barron, J. C. & Forsythe, S. J. (2007). Dry stress and survival time of Enterobacter sakazakii and other Enterobacteriaceae in dehydrated powdered infant formula. J Food Prot 70, 2111-2117.
8. Berchieri, A., Jr, Lovell, M. A. & Barrow, P. A. (1991). The activity in the chicken alimentary tract of bacteriophages lytic for Salmonella typhimurium. Res Microbiol 142, 541-549.
9. Bigot, B., Lee, W. J., McIntyre, L., Wilson, T., Hudson, J. A., Billington, C. & Heinemann, J. A. (2011). Control of Listeria monocytogenes growth in a ready-to-eat poultry product using a bacteriophage. Food Microbiol 28, 1448-1452.
10. Black, L. W. (1989). DNA packaging in dsDNA bacteriophages. Annu Rev Microbiol 43, 267-292.
11. Borie, C., Albala, I., Sánchez, P., Sánchez, M. L., Ramírez, S., Navarro, C., Morales, M. A., Retamales, A. J. & Robeson, J. (2008). Bacteriophage treatment reduces Salmonella colonization of infected chickens. Avian Dis 52, 64-67.
12. Botsaris, G., Liapi, M., Kakogiannis, C., Dodd, C. E. & Rees, C. E. (2013). Detection of Mycobacterium avium subsp. paratuberculosis in bulk tank milk by combined phage-PCR assay: evidence that plaque number is a good predictor of MAP. Int J Food Microbiol 164, 76-80.
13. Botstein, D. (1980). A theory of modular evolution for bacteriophages. Ann N Y Acad Sci 354, 484-491.
14. Briers, Y., Volckaert, G., Cornelissen, A., Lagaert, S., Michiels, C. W., Hertveldt, K. & Lavigne, R. (2007). Muralytic activity and modular structure of the endolysins of Pseudomonas aeruginosa bacteriophages wKZ and EL. Mol Microbiol 65, 1334-1344.
15. Briers, Y., Walmagh, M. & Lavigne, R. (2011). Use of bacteriophage endolysin EL188 and outer membrane permeabilizers against Pseudomonas aeruginosa. J Appl Microbiol 110, 778-785.
16. Briers, Y., Walmagh, M., Van Puyenbroeck, V., Cornelissen, A., Cenens, W., Aertsen, A., Oliveira, H., Azeredo, J., Verween, G. & other authors (2014). Engineered endolysin-based "Artilysins" to combat multidrug-resistant Gram-negative pathogens. MBio 5, e01379-14.
17. Brüssow, H. & Desiere, F. (2001). Comparative phage genomics and the evolution of Siphoviridae: insights from dairy phages. Mol Microbiol 39, 213-223.
18. Brüssow, H., Canchaya, C. & Hardt, W. D. (2004). Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 68, 560-602.
19. Bullman, S., Lucid, A., Corcoran, D., Sleator, R. D. & Lucey, B. (2013). Genomic investigation into strain heterogeneity and pathogenic potential of the emerging gastrointestinal pathogen Campylobacter ureolyticus. PLoS One 8, e71515.
20. Carver, T., Berriman, M., Tivey, A., Patel, C., Böhme, U., Barrell, B. G., Parkhill, J. & Rajandream, M. A. (2008). Artemis and ACT: viewing, annotating and comparing sequences stored in a relational database. Bioinformatics 24, 2672-2676.
21. Casjens, S. & Hendrix, R. (1998). Control mechanisms in dsDNA bacteriophage assembly, pp. 15-75. In The Bacteriophages, Vol. 1. Edited by R. L. Calendar. New York: Plenum.
22. Chang, C. H., Chiang, M. L. & Chou, C. C. (2010). The effect of heat shock on the response of Cronobacter sakazakii to subsequent lethal stresses. Foodborne Pathog Dis 7, 71-76.
23. Chikova, A. K. & Schaaper, R. M. (2005). The bacteriophage P1 hot gene product can substitute for the Escherichia coli DNA polymerase III h subunit. J Bacteriol 187, 5528-5536.
24. Coffey, B., Rivas, L., Duffy, G., Coffey, A., Ross, R. P. & McAuliffe, O. (2011). Assessment of Escherichia coli O157: H7-specific bacteriophages e11/2 and e4/1c in model broth and hide environments. Int J Food Microbiol 147, 188-194.
25. Darzentas, N. (2010). Circoletto: visualizing sequence similarity with Circos. Bioinformatics 26, 2620-2621.
26. Delcher, A. L., Harmon, D., Kasif, S., White, O. & Salzberg, S. L. (1999). Improved microbial gene identification with GLIMMER. Nucleic Acids Res 27, 4636-4641.
27. DeRose, E. F., Li, D., Darden, T., Harvey, S., Perrino, F. W., Schaaper, R. M. & London, R. E. (2002). Model for the catalytic domain of the proofreading epsilon subunit of Escherichia coli DNA polymerase III based on NMR structural data. Biochemistry 41, 94-110.
28. Desiere, F., Mahanivong, C., Hillier, A. J., Chandry, P. S., Davidson, B. E. & Brüssow, H. (2001). Comparative genomics of lactococcal phages: insight from the complete genome sequence of Lactococcus lactis phage BK5-T. Virology 283, 240-252.
29. Doehn, J. M., Fischer, K., Reppe, K., Gutbier, B., Tschernig, T., Hocke, A. C., Fischetti, V. A., Löffler, J., Suttorp, N. & other authors (2013). Delivery of the endolysin Cpl-1 by inhalation rescues mice with fatal pneumococcal pneumonia. J Antimicrob Chemother 68, 2111-2117.
30. Donovan, D. M., Lardeo, M. & Foster-Frey, J. (2006). Lysis of staphylococcal mastitis pathogens by bacteriophage w11 endolysin. FEMS Microbiol Lett 265, 133-139.
31. Dube, P., Tavares, P., Lurz, R. & van Heel, M. (1993). The portal protein of bacteriophage SPP1: a DNA pump with 13-fold symmetry. EMBO J 12, 1303-1309.
32. El-Arabi, T. F., Griffiths, M. W., She, Y. M., Villegas, A., Lingohr, E. J. & Kropinski, A. M. (2013). Genome sequence and analysis of a broadhost range lytic bacteriophage that infects the Bacillus cereus group. Virol J 10, 48.
33. El-Shibiny, A., Scott, A., Timms, A., Metawea, Y., Connerton, P. & Connerton, I. (2009). Application of a group II Campylobacter bacteriophage to reduce strains of Campylobacter jejuni and Campylobacter coli colonizing broiler chickens. J Food Prot 72, 733-740.
34. Endersen, L., O'Mahony, J., Hill, C., Ross, R. P., McAuliffe, O. & Coffey, A. (2014). Phage therapy in the food industry. Annu Rev Food Sci Technol 5, 327-349.
35. Farmer, J. J., III, Asbury, M. A., Hickman, F. W. & Brenner, D. J. (1980). The enterobacteriaceae study group. Enterobacter sakazakii: a new species of 'Enterobacteriaceae' isolated from clinical specimens. Int J Syst Bacteriol 30, 569-584.
36. Faruque, S. M. & Mekalanos, J. J. (2012). Phage-bacterial interactions in the evolution of toxigenic Vibrio cholerae. Virulence 3, 556-565.
37. Fenton, M., Keary, R., McAuliffe, O., Ross, R. P., O'Mahony, J. & Coffey, A. (2013). Bacteriophage-derived peptidase CHAPK eliminates and prevents staphylococcal biofilms. Int J Microbiol 2013, 625341.
38. Fischetti, V. A. (2010). Bacteriophage endolysins: a novel antiinfective to control Gram-positive pathogens. Int J Med Microbiol 300, 357-362.
39. Frick, D. N. & Richardson, C. C. (2001). DNA primases. Annu Rev Biochem 70, 39-80.
40. Gaeng, S., Scherer, S., Neve, H. & Loessner, M. J. (2000). Gene cloning and expression and secretion of Listeria monocytogenes bacteriophage-lytic enzymes in Lactococcus lactis. Appl Environ Microbiol 66, 2951-2958.
41. Goodridge, L. D. & Bisha, B. (2011). Phage-based biocontrol strategies to reduce foodborne pathogens in foods. Bacteriophage 1, 130-137.
42. Gorbalenya, A. E. (1994). Self-splicing group I and group II introns encode homologous (putative) DNA endonucleases of a new family. Protein Sci 3, 1117-1120.
43. Gordon, D. (2003). Viewing and editing assembled sequences using Consed. In Current Protocols in Bioinformatics, Chapter 11, Unit 11. 2. New York, NY: Wiley.
44. Guasch, A., Pous, J., Ibarra, B., Gomis-Rüth, F. X., Valpuesta, J. M., Sousa, N., Carrascosa, J. L. & Coll, M. (2002). Detailed architecture of a DNA translocating machine: the high-resolution structure of the bacteriophage w29 connector particle. J Mol Biol 315, 663-676.
45. Guenther, S., Huwyler, D., Richard, S. & Loessner, M. J. (2009). Virulent bacteriophage for efficient biocontrol of Listeria monocytogenes in ready-to-eat foods. Appl Environ Microbiol 75, 93-100.
46. Hendrix, R. W., Smith, M. C., Burns, R. N., Ford, M. E. & Hatfull, G. F. (1999). Evolutionary relationships among diverse bacteriophages and prophages: all the world's a phage. Proc Natl Acad Sci U S A 96, 2192-2197.
47. Hobbs, L. J. & Nossal, N. G. (1996). Either bacteriophage T4 RNase H or Escherichia coli DNA polymerase I is essential for phage replication. J Bacteriol 178, 6772-6777.
48. Horgan, M., O'Flynn, G., Garry, J., Cooney, J., Coffey, A., Fitzgerald, G. F., Ross, R. P. & McAuliffe, O. (2009). Phage lysin LysK can be truncated to its CHAP domain and retain lytic activity against live antibiotic-resistant staphylococci. Appl Environ Microbiol 75, 872-874.
49. Hunter, C. J., Petrosyan, M., Ford, H. R. & Prasadarao, N. V. (2008). Enterobacter sakazakii: an emerging pathogen in infants and neonates. Surg Infect (Larchmt) 9, 533-539.
50. Hyatt, D., Chen, G. L., Locascio, P. F., Land, M. L., Larimer, F. W. & Hauser, L. J. (2010). Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11, 119.
51. Kandhai, M. C., Reij, M. W., Gorris, L. G. M., Guillaume-Gentil, O. & van Schothorst, M. (2004). Occurrence of Enterobacter sakazakii in food production environments and households. Lancet 363, 39-40.
52. Kelly, D., O'Sullivan, O., Mills, S., McAuliffe, O., Ross, R. P., Neve, H. & Coffey, A. (2012). Genome sequence of the phage c1P1, which infects the beer spoilage bacterium Pediococcus damnosus. Gene 502, 53-63.
53. Kim, K. P., Klumpp, J. & Loessner, M. J. (2007). Enterobacter sakazakii bacteriophages can prevent bacterial growth in reconstituted infant formula. Int J Food Microbiol 115, 195-203.
54. King, A. M. Q., Adams, M. J., Lefkowitz, E. J. & Carstens, E. B. (editors) (2012). Part II The double stranded DNA viruses, pp. 63-85. In Virus Taxonomy: Classification and Nomenclature of Viruses: Ninth Report of the International Committee on Taxonomy of Viruses, vol. 9. San Diego: Elsevier.
55. Korndörfer, I. P., Kanitz, A., Danzer, J., Zimmer, M., Loessner, M. J. & Skerra, A. (2008). Structural analysis of the L-alanoyl-D-gutamate endopeptidase domain of Listeria bacteriophages endolysin Ply500 reveals a new member of the LAS peptidase family. Acta Crystallogr 64, 644-650.
56. Kropinski, A. M. (2006). Phage therapy-everything old is new again. Can J Infect Dis Med Microbiol 17, 297-306.
57. Kucerova, E., Clifton, S. W., Xia, X. Q., Long, F., Porwollik, S., Fulton, L., Fronick, C., Minx, P., Kyung, K. & other authors (2010). Genome sequence of Cronobacter sakazakii BAA-894 and comparative genomic hybridization analysis with other Cronobacter species. PLoS ONE 5, e9556.
58. Kutter, E. & Sulakvelidze, A. (2005). Bacteriophages-Biology and Applications. Boca Raton, FL: CRC Press.
59. Lai, M. J., Lin, N. T., Hu, A., Soo, P. C., Chen, L. K., Chen, L. H. & Chang, K. C. (2011). Antibacterial activity of Acinetobacter baumannii phage wAB2 endolysin (LysAB2) against both Gram-positive and Gram-negative bacteria. Appl Microbiol Biotechnol 90, 529-539.
60. Laslett, D. & Canback, B. (2004). ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res 32, 11-16.
61. Leverentz, B., Conway, W. S., Camp, M. J., Janisiewicz, W. J., Abuladze, T., Yang, M., Saftner, R. & Sulakvelidze, A. (2003). Biocontrol of Listeria monocytogenes on fresh-cut produce by treatment with lytic bacteriophages and a bacteriocin. Appl Environ Microbiol 69, 4519-4526.
62. Lim, T. H., Kim, M. S., Lee, D. H., Lee, Y. N., Park, J. K., Youn, H. N., Lee, H. J., Yang, S. Y., Cho, Y. W. & other authors (2012). Use of bacteriophage for biological control of Salmonella enteritidis infection in chicken. Res Vet Sci 93, 1173-1178.
63. Lionnet, T., Spiering, M. M., Benkovic, S. J., Bensimon, D. & Croquette, V. (2007). Real-time observation of bacteriophage T4 gp41 helicase reveals an unwinding mechanism. Proc Natl Acad Sci U S A 104, 19790-19795.
64. Loc Carrillo, C., Atterbury, R. J., el-Shibiny, A., Connerton, P. L., Dillon, E., Scott, A. & Connerton, I. F. (2005). Bacteriophage therapy to reduce Campylobacter jejuni colonization of broiler chickens. Appl Environ Microbiol 71, 6554-6563.
65. Loessner, M. J., Wendlinger, G. & Scherer, S. (1995). Heterogeneous endolysins in Listeria monocytogenes bacteriophages: a new class of enzymes and evidence for conserved holin genes within the siphoviral lysis cassettes. Mol Microbiol 16, 1231-1241.
66. Lowe, T. M. & Eddy, S. R. (1997). tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25, 955-964.
67. Martin, J. & Hartl, F. U. (1997). Chaperone-assisted protein folding. Curr Opin Struct Biol 7, 41-52.
68. Mikoulinskaia, G. V., Odinokova, I. V., Zimin, A. A., Lysanskaya, V. Y., Feofanov, S. A. & Stepnaya, O. A. (2009). Identification and characterization of the metal ion-dependent L-alanoyl-Dglutamate peptidase encoded by bacteriophage T5. FEBS J 276, 7329-7342.
69. Moore, S. D. & Prevelige, P. E., Jr (2002). DNA packaging: a new class of molecular motors. Curr Biol 12, R96-R98.
70. Myllykallio, H., Lipowski, G., Leduc, D., Filee, J., Forterre, P. & Liebl, U. (2002). An alternative flavin-dependent mechanism for thymidylate synthesis. Science 297, 105-107.
71. O'Flaherty, S., Coffey, A., Meaney, W. J., Fitzgerald, G. F. & Ross, R. P. (2005). Inhibition of bacteriophage K proliferation on Staphylococcus aureus in raw bovine milk. Lett Appl Microbiol 41, 274-279.
72. O'Flynn, G., Ross, R. P., Fitzgerald, G. F. & Coffey, A. (2004). Evaluation of a cocktail of three bacteriophages for biocontrol of Escherichia coli O157: H7. Appl Environ Microbiol 70, 3417-3424.
73. Obeso, J. M., Martínez, B., Rodríguez, A. & García, P. (2008). Lytic activity of the recombinant staphylococcal bacteriophage wH5 endolysin active against Staphylococcus aureus in milk. Int J Food Microbiol 128, 212-218.
74. Payne, K. M. & Hatfull, G. F. (2012). Mycobacteriophage endolysins: diverse and modular enzymes with multiple catalytic activities. PLoS ONE 7, e34052.
75. Preston, V. G., al-Kobaisi, M. F., McDougall, I. M. & Rixon, F. J. (1994). The herpes simplex virus gene UL26 proteinase in the presence of the UL26. 5 gene product promotes the formation of scaffold-like structures. J Gen Virol 75, 2355-2366.
76. Rao, V. B. & Feiss, M. (2008). The bacteriophage DNA packaging motor. Annu Rev Genet 42, 647-681.
77. Rawlings, N. D. & Barrett, A. J. (1995). Evolutionary families of metallopeptidases. Methods Enzymol 248, 183-228.
78. Rees, C. E. & Dodd, C. E. (2006). Phage for rapid detection and control of bacterial pathogens in food. Adv Appl Microbiol 59, 159-186.
79. Riedel, K. & Lehner, A. (2007). Identification of proteins involved in osmotic stress response in Enterobacter sakazakii by proteomics. Proteomics 7, 1217-1231.
80. Rivas, L., Coffey, B., McAuliffe, O., McDonnell, M. J., Burgess, C. M., Coffey, A., Ross, R. P. & Duffy, G. (2010). In vivo and ex vivo evaluations of bacteriophages e11/2 and e4/1c for use in the control of Escherichia coli O157: H7. Appl Environ Microbiol 76, 7210-7216.
81. Rodríguez-Rubio, L., Martínez, B., Donovan, D. M., García, P. & Rodríguez, A. (2013). Potential of the virion-associated peptidoglycan hydrolase HydH5 and its derivative fusion proteins in milk biopreservation. PLoS ONE 8, e54828.
82. Rossi, R., Montecucco, A., Ciarrocchi, G. & Biamonti, G. (1997). Functional characterization of the T4 DNA ligase: a new insight into the mechanism of action. Nucleic Acids Res 25, 2106-2113.
83. Rozema, E. A., Stephens, T. P., Bach, S. J., Okine, E. K., Johnson, R. P., Stanford, K. & McAllister, T. A. (2009). Oral and rectal administration of bacteriophages for control of Escherichia coli O157: H7 in feedlot cattle. J Food Prot 72, 241-250.
84. Schatz, M. C., Phillippy, A. M., Sommer, D. D., Delcher, A. L., Puiu, D., Narzisi, G., Salzberg, S. L. & Pop, M. (2011). Hawkeye and AMOS: visualizing and assessing the quality of genome assemblies. Brief Bioinform 14, 213-224.
85. Sharples, G. J., Chan, S. N., Mahdi, A. A., Whitby, M. C. & Lloyd, R. G. (1994). Processing of intermediates in recombination and DNA repair: Identification of a new endonuclease that specifically cleaves Holliday junctions. The EMBO journal 13, 6133.
86. Sharples, G. J., Ingleston, S. M. & Lloyd, R. G. (1999). Holliday junction processing in bacteria: insights from the evolutionary conservation of RuvABC, RecG, and RusA. J Bacteriol 181, 5543-5550.
87. Simpson, A. A., Tao, Y., Leiman, P. G., Badasso, M. O., He, Y., Jardine, P. J., Olson, N. H., Morais, M. C., Grimes, S. & other authors (2000). Structure of the bacteriophage w29 DNA packaging motor. Nature 408, 745-750.
88. Singh, A., Poshtiban, S. & Evoy, S. (2013). Recent advances in bacteriophage based biosensors for food-borne pathogen detection. Sensors (Basel) 13, 1763-1786.
89. Spellberg, B., Bartlett, J. G. & Gilbert, D. N. (2013). The future of antibiotics and resistance. N Engl J Med 368, 299-302.
90. Stock, I. & Wiedemann, B. (2002). Natural antibiotic susceptibility of Enterobacter amnigenus, Enterobacter cancerogenus, Enterobacter gergoviae and Enterobacter sakazakii strains. Clin Microbiol Infect 8, 564-578.
91. Viazis, S., Akhtar, M., Feirtag, J. & Diez-Gonzalez, F. (2011). Reduction of Escherichia coli O157: H7 viability on leafy green vegetables by treatment with a bacteriophage mixture and transcinnamaldehyde. Food Microbiol 28, 149-157.
92. Wagenaar, J. A., Van Bergen, M. A. P., Mueller, M. A., Wassenaar, T. M. & Carlton, R. M. (2005). Phage therapy reduces Campylobacter jejuni colonization in broilers. Vet Microbiol 109, 275-283.
93. Wall, S. K., Zhang, J., Rostagno, M. H. & Ebner, P. D. (2010). Phage therapy to reduce preprocessing Salmonella infections in marketweight swine. Appl Environ Microbiol 76, 48-53.
94. Walmagh, M., Briers, Y., dos Santos, S. B., Azeredo, J. & Lavigne, R. (2012). Characterization of modular bacteriophage endolysins from Myoviridae phages OBP, 201Q2-1 and PVP-SE1. PLoS ONE 7, e36991.
95. Walmagh, M., Boczkowska, B., Grymonprez, B., Briers, Y., Drulis-Kawa, Z. & Lavigne, R. (2013). Characterization of five novel endolysins from Gram-negative infecting bacteriophages. Appl Microbiol Biotechnol 97, 4369-4375.
96. White, M. F., Giraud-Panis, M. J. E., Pöhler, J. R. G. & Lilley, D. M. (1997). Recognition and manipulation of branched DNA structure by junction-resolving enzymes. J Mol Biol 269, 647-664.
97. Wittmann, J., Dreiseikelmann, B., Rohde, M., Meier-Kolthoff, J. P., Bunk, B. & Rohde, C. (2014). First genome sequences of Achromobacter phages reveal new members of the N4 family. Virol J 11, 14.
98. Young, R. (1992). Bacteriophage lysis: mechanism and regulation. Microbiol Rev 56, 430-481.
99. Young, R. & Bläsi, U. (1995). Holins: form and function in bacteriophage lysis. FEMS Microbiol Rev 17, 191-205.
100. Zhang, H., Bao, H., Billington, C., Hudson, J. A. & Wang, R. (2012). Isolation and lytic activity of the Listeria bacteriophage endolysin LysZ5 against Listeria monocytogenes in soya milk. Food Microbiol 31, 133-136.
101. Zimmer, M., Vukov, N., Scherer, S. & Loessner, M. J. (2002). The murein hydrolase of the bacteriophage w3626 dual lysis system is active against all tested Clostridium perfringens strains. Appl Environ Microbiol 68, 5311-5317.
102. Zuber, S., Ngom-Bru, C., Barretto, C., Bruttin, A., Brüssow, H. & Denou, E. (2007). Genome analysis of phage JS98 defines a fourth major subgroup of T4-like phages in Escherichia coli. J Bacteriol 189, 8206-8214.
103. Zuber, S., Boissin-Delaporte, C., Michot, L., Iversen, C., Diep, B., Brüssow, H. & Breeuwer, P. (2008). Decreasing Enterobacter sakazakii (Cronobacter spp.) food contamination level with bacteriophages: prospects and problems. Microb Biotechnol 1, 532-543.