Phage resistance mechanisms in lactic acid bacteria

International Dairy Journal

Volumn 8, Issue 3, 1998, Pages 207-226

  Allison, Gwen E ^a   Klaenhammer, Todd R ^b  

^a Environmental Resources Management   (Australia)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Abortive infection; Bacteriophage; Defense; Lactic acid bacteria; Lactococcus; Modification; Resistance; Restriction; Streptococcus thermophilus

Indexed keywords

BACTERIOPHAGE; FERMENTATION; MICROBIAL ACTIVITY; PHAGE DISPLAY; RESISTANCE MANAGEMENT; STARTER CULTURE;

LACTOCOCCUS LACTIS; STREPTOCOCCUS THERMOPHILUS;

EID: 0032029067     PISSN: 09586946     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0958-6946(98)00043-0     Document Type: Article

References (114)

1. Anba, J., Bidnenko, E., Hillier, A., Ehrlich, S. D. and Chopin, M.-C. (1995) Characterization of the lactococcal abiD1 gene coding for phage abortive infection. Journal of Bacteriology 177, 3818-3823.
2. Auvray, F., Coddeville, M., Ritzenthaler, P. and Dupont, L. (1997) Plasmid integration in a wide range of bacteria mediated by the integrase of Lactobacillus delbrueckii bacteriophage mv4. Journal of Bacteriology 179, 1837-1845.
3. Babu, K. S., Spence, W. S., Montville, M. R. and Geller, B. L. (1995) Characterization of a cloned gene (pip) from Lactococcus lactis required for phage infection, p. 569-575. In Genetics of Streptococci, Enterococci and Lactococci, eds J.J. Ferretti, M. S. Gilmore, T. R. Klaenhammer and F. Brown. Karger, Basel, Switzerland.
4. Benbadis, L., Barel, J.-R. and Hartley, D. L. (1991) Purification, properties, and sequence specificity of SslI, a new type II restriction endonuclease from Streptococcus salivarius subsp. thermophilus. Applied and Environmental Microbiology 57, 3677-3678.
5. Bickle, T. A. and Kruger, D. H. (1993) Biology of DNA restriction. Microbiology Reviews 57, 434-450
6. Bidnenko, I., Ehrlich, S. D., and Chopin, M.-C. (1995) Phage operon involved in sensitivity to the Lactococcus lactis abortive infection mechanism AbiD1. Journal of Bacteriology 177, 3824-3829.
7. Botstein, D. (1980) A theory of modular evolution for bacteriophages. Annals of the New York Academy of Science 354, 484-491.
8. Boyce, J. D., Davidson, B. E., and Hillier, A. J. (1995). Identification of prophage genes expressed in lysogens of the Lactococcus lactis temperate bacteriophage BK5-T. Applied and Environmental Microbiology 61, 4099-4104.
9. Chandry, P. S., Moore, S. C., Boyce, J. D., Davidson, B. E. and Hillier, A. J. (1997). Analysis of the DNA sequence, gene expression, origin of replication and modular structure of the Lactococcus lactis lytic bacteriophage sk1. Molecular Microbiology 26, 49-64.
10. Christiansen, B., Brondsted, L., Vogensen, F. K. and Hammer, K. (1996) A resolvase-like protein is required for the site-specific integration of the temperate lactococcal bacteriophage TP901-1. Journal of Bacteriology 178, 5164-5173.
11. Chung, D. K., Chung, S. K., and Batt, C. A. (1992) Antisense RNA directed against the major capsid protein of Lactococcus lactis subsp. cremoris bacteriophage 4-1 confers partial resistance to the host. Journal of Applied Microbiology and Biotechnology 37, 79-83.
12. Cluzel, P.-J., Chopin, A., Ehrlich, S.D. and Chopin, M.-C. (1991) Phage abortive infection mechanism from Lactococcus lactis subsp. lactis, expression of which is mediated by an Iso-ISS1 element. Applied and Environmental Microbiology 57, 3547-3551.
13. Coakley, M., Fitzgerald, G. F. and Ross, R. P. (1997) Application and evaluation of the phage resistance-and bacteriocin-encoding plasmid pMRC01 for the improvement of dairy starter cultures. Applied and Environmental Microbiology 63, 1434-1440.
14. Coffey, A. G., Fitzgerald, G. F. and Daly, C. (1991) Cloning and characterization of the determinant for abortive infection of bacteriophage from lactococcal plasmid pCI829. Journal of General Microbiology 137, 1355-1362.
15. Daly, C., Fitzgerald, G. F. and Davis, R. (1996) Biotechnology of lactic acid bacteria with special reference to bacteriophage resistance. Antonie van Leeuwenhoek 70, 99-110.
16. Davis, R., Lelie, van der Lelie, D., Mercenier, A., Daly, C. and Fitzgerald, G.F. (1993) ScrFI restriction-modification system of Lactococcus lactis subsp. cremoris UC503, cloning and characterization of two ScrFI methylase genes. Applied and Environmental Microbiology 59, 777-785.
17. de los Reyes-Gavilan, C. G., Limsowtin, G. K. Y., Sechaud, L., Veaux, M. and Accolas, J.-P. (1990) Evidence for a plasmid-linked restriction-modification system in Lactobacillus helveticus. Applied and Environmental Microbiology 56, 3412-3419.
18. Deng, Y.-M., Harvey, M. L., Liu, C.-Q. and Dunn, N.W. (1997) A novel plasmid-encoded phage abortive infection system for Lactococcus lactis biovar. diacetylactis. FEMS Microbiology Letters 146, 149-154.
19. de Ruyter, P.G.G.A., Kuipers, O.P., Meijer, W.C., de Vos, W.M. (1997) Food-grade controlled lysis of Lactococcus lactis for accelerated cheese ripening. Nature Biotechnology. 15, 976-979.
20. Desiere, F., Lucchini, S., Bruttin, A., Zwahlen, M.-C. and Brussow, H. (1997) A highly conserved DNA replication module from Streptococcus thermophilus phages is similar in sequence and topology to a module from Lactococcus lactis phages. Virology 234, 372-382.
21. de Vos, W.M. (1989). On the carrier state of bacteriophages in starter lactococci: an elementary explanation involving a bacteriophage resistance plasmid. Netherlands Milk and Dairy Journal 43, 221-227.
22. Dinsmore, P. K. and Klaenhammer, T. R. (1994) Phenotypic consequences of altering the copy number of abiA, a gene responsible for aborting bacteriophage infections in Lactococcus lactis. Applied and Environmental Microbiology 60, 1129-1136.
23. Dinsmore, P. K., and Klaenhammer, T. R. (1995) Bacteriophage resistance in Lactococcus. Molecular Biotechnology. 4, 297-314.
24. Dinsmore, P. K., and Klaenhammer, T. R. (1997) Molecular characterization of a genomic region in a Lactococcus bacteriophage that is involved in its sensitivity to the phage defense mechanism AbiA. Journal of Bacteriology 179, 2949-2957.
25. Dinsmore, P. K., O'Sullivan, D. J. and Klaenhammer, T. R. (1998) A leucine repeat motif in AbiA is required for resistance of Lactococcus lactis to phages representing three species. Gene, (in press).
26. Djordjevic, G. M. and Klaenhammer, T. R. (1996) Positive selection, cloning vectors for Gram-positive bacteria based on a restriction endonuclease cassette. Plasmid 35, 37-45.
27. Djordjevic, G. M., O'Sullivan, D. J., Walker, S. A., Conkling, M. A. and Klaenhammer, T. R. (1997) Triggered-suicide system designed as a defense against bacteriophages. Journal of Bacteriology 179, 6741-6748.
28. Djordjevic, G. M. and Klaenhammer, T. R. (1997) Bacteriophage-triggered defense systems: phage adaptation and design improvements. Applied and Environmental Microbiology 63, 4370-4376
29. Dupont, L., Boizet-Bonhoure, B., Coddevile, M., Auvray, F. and Ritzenhaler, P. (1995) Characterization of genetic elements required for site-specific integration of Lactobacillus delbrueckii subsp. bulgaricus bacteriophage mv4 and construction of an integration-proficient vector for Lactobacillus plantarum. Journal of Bacteriology 177, 586-595.
30. Durmaz, E., Higgins, D. L. and Klaenhammer, T. R. (1992) Molecular characterization of a second abortive phage resistance gene present in Lactococcus lactis subsp. lactis ME2. Journal of Bacteriology 174, 7463-7469.
31. Durmaz, E. D., and Klaenhammer, T. R. (1995) A starter culture rotation strategy incorporating paired restriction/modification and abortive infection bacteriophage defenses in a single Lactococcus lactis strain. Applied and Environmental Microbiology 61, 1266-1273.
32. Durmaz, E., and Klaenhammer, T. R. (1997) Lactococcus lactis NCK203 DNA homologous to the temperate lactococcal phages r1t and BK5-T contributes to the evolution of recombinant variants of the lytic phage φ31. Journal of Dairy Sci. 80 (Supp. 1); 119. (Abstract D87).
33. Emond, E., Holler, B. J., Boucher, P. A., Vandenbergh, P, Vedamuthu, E. R., Kondo, J. K. and Moineau, S. (1997) Phenotypic and genetic characterization of the bacteriophage abortive infection mechanism AbiK from Lactococcus lactis. Applied and Environmental Microbiology 63, 1274-1283.
34. Fremaux, C., de Antoni, G. L., Raya, P. R. and Klaenhammer, T. R. (1993) Genetic organization and sequence of the region encoding integrative functions from Lactobacillus gasseri temperate bacteriophage φadh. Gene 126, 61-66.
35. Garbutt, K. C., Kraus, J. and Geller, B. L. (1997) Bacteriophage resistance in Lactococcus lactis engineered by replacement of a gene for a bacteriophage receptor. Journal of Dairy Science 80, 1512-1519.
36. Garvey, P., Fitzgerald, G. F. and Hill, C. (1995) Cloning and DNA sequence analysis of two abortive infection phage resistance determinants from the lactococcal plasmid pNP40. Applied and Environmental Microbiology 61, 4321-4328.
37. Garvey, P. A., Hill, C. and Fitzgerald, G. F. (1996) The lactococcal plasmid pNP40 encodes a third bacteriophage resistance mechanism, one which affects phage DNA penetration. Applied and Environmental Microbiology 62, 676-679.
38. L in abortive infection. Applied and Environmental Microbiology 63, 1244-1251.
39. Gasson, M. J. (1996) Lytic systems in lactic acid bacteria and their bacteriophages. Antonie van Leeuwenhoek 70, 147-159.
40. Geller, B., Ivey, R. G., Trempy, J. E. and Hettinger-Smith, B. (1993) Cloning of a chromosomal gene required for phage infection of Lactococcus lactis subsp. lactis C2. Journal of Bacteriology 175, 5510-5560.
41. Gerdes, K., Poulsen, L. K., Thisted, T., Nielsen, A. K., Martinussen, J. and Andreasen, P.H. (1990) The hok killer gene family in gram-negative bacteria. New Biology 2, 946-956.
42. Gopal, P. K. and Crow, V. L. (1993) Characterisation of loosely associated material from the cell surface of Lactococcus lactis subsp. cremoris E8 and its phage-resistant variant strain 398. Applied and Environmental Microbiology 59, 3177-3189.
43. Guimont, C., Henry, P. and Linden, G. (1993) Restriction/modification in Streptococcus thermophilus: isolation and characterisation of a type II restriction endonuclease Sth455I. Journal of Applied Microbiology and Biotechnology 39, 216-220.
44. Heap, H. A. and Lawrence, R. C. (1976) The selection of starter strains for cheesemaking. New Zealand Journal of Dairy Science Technology 11, 16-20.
45. Henrich, B., Binishofer, B. and Blasi, U. (1995) Primary structure and functional analysis of the lysis genes of Lactobacillus gasseri bacteriophage φadh. Journal of Bacteriology 177, 723-732.
46. Hill, C., Romero, D. A., McKenney, D. S., Finer, K. R. and Klaenhammer, T. R. (1989) Localisation, cloning, and expression of genetic determinants for bacteriophage resistance (Hsp) from the conjugative plasmid pTR2030. Applied and Environmental Microbiology 55, 1684-1689.
47. Hill, C., Miller, L. A. and Klaenhammer, T. R. (1990a) Cloning, expression, and sequence determination of a bacteriophage fragment encoding bacteriophage resistance in Lactococcus lactis. Journal of Bacteriology 172, 6419-6426.
48. Hill, C., Miller, L. A. and Klaenhammer, T. R. (1990b) Nucleotide sequence and distribution of the pTR2030 resistance determinant (hsp) which aborts bacteriophage infection in lactococci. Applied and Environmental Microbiology 56, 2255-2258.
49. Hill, C., Miller, L. A. and Klaenhammer, T. R. (1991) In vivo genetic exchange of a functional domain from a type II A methylase between lactococcal plasmid pTR2030 and a virulent bacteriophage. Journal of Bacteriology 173, 4363-4370.
50. Hill, C. (1993) Bacteriophage and bacteriophage resistance in lactic acid bacteria. FEMS Microbiology Reviews 12, 87-108.
51. Jarvis, A. W., Fitzgerald, G. F., Mata, M., Mercenier, A., Neve, H., Powell, I. B., Ronda, C., Saxelin, M. and Teuber, M. (1991) Species and type phages of lactococcal bacteriophages. Intervirology 32, 2-9.
52. Kim, S. G., and Batt, C. A. (1991a) Identification of a nucleotide sequence conserved in Lactococcus lactis bacteriophages. Gene 98, 95-100.
53. Kim, S. G. and Batt, C. A. (1991b) Antisense mRNA-mediated bacteriophage resistance in Lactococcus lactis subsp. lactis. Applied and Environmental Microbiology 57, 1109-1113.
54. Klaenhammer, T. R. (1989) Genetic characterization of multiple mechanisms of phage defense from a prototype phage-insensitive strain, Lactococcus lactis ME2. Journal of Dairy Science 72, 3429-3443.
55. Klaenhammer, T. R. (1991) Development of bacteriophage resistant strains of lactic acid bacteria. Biochemical Society Transactions 19, 675-681.
56. Klaenhammer, T. R., Romero, D., Sing, W. and Hill, C. (1991) Molecular analysis of pTR2030 gene systems that confer phage resistance to lactococci. In Genetics and Molecular Biology of Streptococci, Lactococci, and Enterococci, eds G. Dunny, P. Cleary, and L. McKay. American Society for Microbiology, Washington, DC, pp. 124-130.
57. Klaenhammer, T. R. and Fitzgerald, G. F. (1994) Bacteriophage and bacteriophage resistance. In Genetics and Biotechnology of Lactic Acid Bacteria, eds M. J. Gasson and W. M. de Vos. Blackie Academic and Professional, Chapman and Hall, Glasgow, pp. 106-168.
58. Kodaira, K.-I., Oki, M., Kakikawa, M., Watanabe, N., Hirakawa, M., Yamada, K. and Taketo, A. (1997) Genome structure of the Lactobacillus temperate phage φg1e: the whole genome sequence and the putative promoter/repressor system. Gene 187, 45-53.
59. Kulakauskas, S., Lubys, A. and Ehrlich, S. D. (1995) DNA restriction-modification systems mediate plasmid maintenance. Journal of Bacteriology 177, 3451-3454.
60. Kusano, K., Naito, T., Handa, N. and Kobayashi, I. (1995) Restriction-modification systems as genomic parasites in competition for specific sequences. Proceedings of the National Academy of Sciences 92, 11095-11099.
61. Langella, P. and Chopin, A. (1989) Effect of restriction-modification systems on transfer of foreign DNA into Lactococcus lactis subsp. lactis. FEMS Microbiology Letters 59, 301-306.
62. Lillehaug, D., Nes, I.F. and Birkeland, N.-K. (1997) A highly efficient and stable system for site-specific integration of genes and plasmids into the phage φLC3 attachment (attB) of the Lactococcus lactis chromosome. Gene 188, 129-136.
63. Lubbers, M. W., Waterfield, N. R., Beresford, T. P. J., Le Page, R. W. F. and Jarvis, A. W. (1995) Sequencing and analysis of the prolate-headed lactococcal bacteriophage c2 genome and identification of the structural genes. Applied and Environmental Microbiology 61, 4348-4356.
64. Madsen, A. and Josephsen, J. (1996) Cloning and anaylsis of the genes coding for the LlaDII restriction and modification enzymes isolated from Lactococcus lactis subsp. cremoris W39. Abstr. F11. 5th Symposium on lactic acid bacteria. Veldhoven, The Netherlands.
65. Mayo, B., Hardisson, C. and Brana, A. F. (1991) Nucleolytic activities in Lactococcus lactis subsp. lactis NCDO497. FEMS Microbiology Letters 79, 195-198.
66. McLandsborough, L. A., Kolaetis, K. M., Requena, T. and McKay, L. L. (1995) Cloning and characterization of the abortive infection genetic determinant abiD isolated from pBF61 of Lactococcus lactis subsp. lactis KR5. Applied and Environmental Microbiology 61, 2023-2026.
67. Mikkonen, M., Raisanen, L. and Alatossava, T. (1996) The early gene region completes the nucleotide sequence of Lactobacillus delbrueckii subsp. lactis phage LL-H. Gene 175, 49-57.
68. Moineau S., Borkaev, M., Walker, S. A., Vedamuthu, E. R. and Vandenbergh, P. A. (1994a). Novel starter rotation system based on phage species sensitivity. Journal of Dairy Science 77 (Suppl 1), 61.
69. Moineau, S., Pandian, S. and Klaenhammer, T. R. (1994b) Evolution of a lytic bacteriophage via DNA acquisition from the Lactococcus lactis chromosome. Applied and Environmental Microbiology 60, 1832-1814.
70. Moineau, S., Walker, S. A., Vedamuthu, E. R. and Vandenbergh, P. A. (1995a) Cloning and sequencing of LlaII restriction/modification genes from Lactococcus lactis and relatedness of this system to the Streptococcus pneumoniae DpnII System. Journal of Applied and Environmental Microbiology 61, 2193-2202.
71. Moineau, S., Walker, S. A., Holler, B. J., Vedamuthu, E. R. and Vandenbergh, P. A. (1995b) Expression of a Lactococcus lactis phage resistance mechanism by Streptococcus thermophilus. Applied and Environmental Microbiology 61, 2461-2466.
72. Molineux, I.J. (1991) Host-parasite interactions: recent developments in the genetics of abortive phage infections. New Biology 3, 230-236.
73. Nauta, A., van den Burg, B., Karsens, H., Venema, G. and Kok, J. (1997) Design of thermolabile bacteriophage repressor mutants by comparative molecular modeling. Nature Biotechnology 15, 980-983.
74. Nauta, A., van Sinderen, D., Karsens, H., Smit, E., Venema, G. and Kok, J. (1996) Inducible gene expression mediated by a repressor-operator system isolated from Lactococcus lactis bacteriophage r1t. Molecular Microbiology 19, 1331-1341.
75. Neve, H. (1996) Bacteriophage. In Dairy Starter Cultures, eds T. M. Cogan and J.-P. Accolas. VCH Publishers. New York, NY, pp. 157-189.
76. Nyengaard, N. R., Falkenberg-Klok, J. and Josephsen, J. (1996). Cloning and analysis of the restriction-modification system LlaBI, a bacteriophage resistance system from Lactococcus lactis subsp. cremoris W56. Applied and Environmental Microbiology 62, 3494-3498.
77. Nyengaard, N., Vogensen, F. K. and Josephsen, J. (1995) Restriction-modification systems in Lactococcus lactis. Gene 157, 13-18.
78. Nyengaard, N., Vogensen, F. K. and Josephsen, J. (1993) LlaAI and LlaBI, two type-II restriction endonucleases from Lactococcus lactis subp. cremoris W9 and W56 recognizing, respectively, 5'-/GATC-3' and 5'-C/TRYAG-3'. Gene 136, 371-372.
79. O'Connor, L., Coffey, L. A., Daly, C. and Fitzgerald, G. F. (1996) AbiG, a genotypically novel abortive infection mechanism encoded by plasmid pCI750 of Lactococcus lactis subsp. cremoris UC653. Applied and Environmental Microbiology 62, 3075-3082.
80. O'Sullivan, D. J., Hill, C. and Klaenhammer, T. R. (1993) Effect of increasing the copy number of bacteriophage origins of replication, in trans, on incoming-phage proliferation. Applied and Environmental Microbiology 59, 2449-2456.
81. O'Sullivan, D. J. and Klaenhammer, T. R. (1998) Control of expression of LlaI restriction in Lactococcus lactis. Molecular Microbiology 27, (in press).
82. O'Sullivan, D. J., Walker, S. A., West, S. G. and Klaenhammer, T. R. (1996) Development of an expression system using a lytic phage to trigger explosive plasmid amplification and gene expression. Biotechnology 14, 82-87.
83. O'Sullivan, D. J., Zagula, K. and Klaenhammer, T. R (1995) In vivo restriction by LlaI is encoded by three genes, arranged in an operon with llaI M, on the conjugative Lactococcus plasmid pTR2030. Journal of Bacteriology 177, 134-143.
84. Parreira, R., Ehrlich, S. D. and Chopin, M.-C. (1996) Dramatic decay of phage transcripts in lactococcal cells carrying the abortive infection determinant AbiB. Molecular Microbiology 19, 221-230.
85. Payne, J., MacCormick, C. A., Griffin, H. G. and Gasson, M. J. (1996) Exploitation of a chromosomally integrated lactose operon for controlled gene expression in Lactococcus lactis. FEMS Microbiology Letters 136, 19-24.
86. Pecota, D. C. and Wood, T. K. (1996) Exclusion of T4 phage by the hok/sok killer locus from plasmid R1. Journal of Bacteriology 178, 2044-2050.
87. Poch, M. T., Somkuti, G. A. and Solaiman, D. K. Y. (1997) Sth132I, a novel class-IIS restriction endonuclease of Streptococcus thermophilus ST132. Gene 195, 201-206.
88. Polzin, K. M., Collins, L. J., Lubbers, M. W. and Jarvis, A. W. (1996) Effect of various mRNA's on bacteriophage c2 replication. Abstr. F2. 5th Symposium on Lactic Acid Bacteria. Veldhoven, The Netherlands.
89. Prevots, F., Daloyau, M., Bonin, O., Dumont, X. and Tolou, S. (1996) Cloning and sequencing of the novel abortive infection gene abiH of Lactococcus lactis ssp. lactis biovar. diacetylactis S94. FEMS Microbiology Letters 142, 295-299.
90. Raya, R. R., Fremaux, C., de Antoni, G. L., and Klaenhammer, T. R. (1992) Site-specific integration of the temperate bacteriophage φadh into the Lactobacillus gasseri chromosome and molecular characterization of the phage (attP) and bacterial (attB) attachment sites. Journal of Bacteriology 174, 5584-5592.
91. Ryan, M. P., Rea, M. C., Hill, C. and Ross, R. P. (1996) An application in cheddar cheese manufacture for a strain of Lactococcus lactis producing a novel broad-spectrum bacteriocin, lacticin 3147. Applied and Environmental Microbiology 62, 612-619.
92. Salama, M. S., Musafija-Jeknic, T., Sandine, W. E. and Giovannoni, S. J. (1995) An ecological study of lactic acid bacteria: isolation of new strains of Lactococcus including Lactococcus lactis subspecies cremoris. Journal of Dairy Science 78, 1004-1017.
93. Salama, M. S., Sandine, W. E. and Giovannoni, S. J. (1993) Isolation of Lactococcus lactis subsp. cremoris from nature by colony hybridization with rRNA probes. Applied and Environmental Microbiology 59, 3941-3945.
94. Salama, M. S., Sandine, W. E. and Giovannoni, S. J. (1991) Devolopment and application of oligonucleotide probes for identification of Lactococcus lactis subsp. cremoris. Journal of Applied and Environmental Microbiology 57, 1313-1318.
95. Sanders, M. E. and Klaenhammer, T. R. (1980) Restriction and modification in the group N streptococci: the effect of heat on the development of modified lytic bacteriophage. Applied and Environmental Microbiology 40, 500-506.
96. Schouler, C., Ehrlich, S. D. and Chopin, M.-C. (1994) Sequence and organization of the lactococcal prolate-headed bIL67 phage genome. Microbiology 140, 3061-3069.
97. Schouler, C., Clier, F., Lerayer, A. D., Ehrlich, S. D., and Chopin, M-C. (1998) A type IC restriction-modification system in Lactococcus lactis. Journal of Bacteriology 180, 407-411.
98. Shearman, C. A., Jury, K. and Gasson, M. J. (1992) Autolytic Lactococcus lactis expressing a lactococcal bacteriophage gene. Biotechnology 10, 196-199.
99. Shearman, C. A., Underwood, H. M., Jury, K. and Gasson, M. J. (1989) Cloning and DNA sequence anaylsis of a Lactococcus bacteriophage lysin gene. Molecular and General Genetics 218, 214-221.
100. Shub, D. A. (1994) Bacterial altruism? Current Biology 4, 555-556.
101. Sijtsma, L., Wouters, J. T. M., and Hellingwerf, K. J. (1990) Isolation and characterisation of lipoteichoic acid, a cell envelope component involved in preventing phage adsorption from Lactococcus lactis subsp. cremoris SK110. Journal of Bacteriology 172, 7126-7130.
102. Sing, W. D. and Klaenhammer, T. R. (1993) A strategy for rotation of different bacteriophage defenses in a lactococcal single-strain starter culture system. Applied and Environmental Microbiology 59, 365-372.
103. Snyder, L. (1995) Phage-exclusion enzymes: a bonanza of biochemical and cell biology reagents. Molecular Microbiology 15, 415-420.
104. Solaiman, D. K. Y., and Somkuti, G. A. (1991) A type II restriction endonuclease of Streptococcus thermophilus ST117. FEMS Microbiology Letters 80, 75-80.
105. Solaiman, D. K. Y., and Somkuti, G. A. (1990) Isolation and characterization of a type II restriction endonuclease from Streptococcus thermophilus. FEMS Microbiology Letters 67, 261-266.
106. Stanley, E., Fitzgerald, G. F., Le Marrec, C., Fayard, B., and van Sinderen, D. (1997) Sequence analysis and characterization of φ01205, a temperate bacteriophage infecting Streptococcus thermophilus CNRZ1205. Microbiology 143, 3417-3429.
107. Steenson, L. R., and Klaenhammer. (1986) Plasmid heterogeneity in Streptococcus cremoris M12R: effects on proteolytic activity and host-dependent phage replication. Journal of Dairy Science 69, 2227-2236
108. Su, P., Harvey, M. L., Im, H. J. and Dunn, N. W. (1997) Isolation, cloning, and charaterisation of the abiI gene from Lactococcus lactis subsp. lactis M138 encoding abortive phage infection. Journal of Biotechnology 54, 95-104.
109. 5C methyltransferase of Lactococcus lactis. Gene 136, 205-209.
110. Twomey, D. P., Gabillet, N., Daly, C. and Fitzgerald, G. F. (1997) Molecular characterization of the restriction endonuclease gene (scrFIR) associated with the ScrFI restriction/modification system from Lactococcus lactis subsp. cremoris UC503. Microbiology 143, 2277-2286.
111. Tyndall, C., Lehnherr, H., Sandmeier, U., Kulik, E. and Bickle, T.A. (1997) The type IC hsd loci of the enterobacteria are flanked by DNA with high homology to the phage P1 genome: implications for the evolution and spread of DNA restriction systems. Molecular Microbiology 23, 729-736.
112. van Sinderen, D., Karsens, H., Kok, J., Terpstra, P., Ruiters, M. H. J., Venema, G. and Nauta, A. (1996) Sequence analysis and molecular characterization of the temperate lactococcal bacteriophage r1t. Molecular Microbiology 19, 1343-1355.
113. Walker, S. A., and Klaenhammer, T. R. (1998) Molecular characterization of a phage-inducible middle promoter and its transcriptional activator from the lactococcal bacteriophage φ31. Journal of Bacteriology 180, 921-931.
114. Waterfield, N. R., Lubbers, M. W., Polzin, K. M., LePage, R. W. and Jarvis, A. W. (1996) An origin of DNA replication from Lactococcus lactis bacteriophage c2. Journal of Applied and Environmental Microbiology 62, 1452-1453.