Skip to main content
Log in

Bacteriophage resistance inLactococcus

  • Review
  • Published:
Molecular Biotechnology Aims and scope Submit manuscript

Abstract

Lactic acid bacteria are industrial microorganisms used in many food fermentations.Lactococcus species are susceptible to bacteriophage infections that may result in slowed or failed fermentations. A substantial amount of research has focused on characterizing natural mechanisms by which bacterial cells defend themselves against phage. Numerous natural phage defense mechanisms have been identified and studied, and recent efforts have improved phage resistance by using molecular techniques. The study of how phages overcome these resistance mechanisms is also an important objective. New strategies to minimize the presence, virulence, and evolution of phage are being developed and are likely to be applied industrially.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Sanders, M. E. (1987) Bacteriophages of industrial importance, inPhage Ecology (Goyal, S. M., Gerba, C. P., and Bitton, G., eds.), Wiley Interscience, NY, pp. 211–244.

    Google Scholar 

  2. Hill, C. (1993) Bacteriophage and bacteriophage resistance in lactic acid bacteria.FEMS Microbiol. Rev. 12, 87–108.

    Article  CAS  Google Scholar 

  3. Klaenhammer, T. R. and Fitzgerald, G. F. (1994) Bacteriophages and bacteriophage resistance, inApplied Genetics of Lactic Acid Bacteria (Gasson, M. J. and de Vos, W., eds.), Backie and Son, UK, pp. 106–168.

    Google Scholar 

  4. King, W. R., Collins, E. B., and Barrett, E. L. (1983) Frequencies of bacteriophage-resistant and slow acid-producing variants ofStreptococcus cremoris.Appl. Environ. Microbiol. 45, 1481–1485.

    PubMed  CAS  Google Scholar 

  5. Limsowtin, G. K. Y. and Terzaghi, B. E. (1976) Phage resistant mutants: their selection and use in cheese factories.N.Z. J. Dairy Sci. Technol. 11, 251–256.

    Google Scholar 

  6. Marshall, R. J. and Berridge, N. J. (1976) Selection and some properties of phage-resistant starters for cheese-making.J. Dairy Res. 43, 449–458.

    CAS  Google Scholar 

  7. Vlegels P. A. P., Hazeleger, W. C., Helmerhorst, T. H., and Wouters, J. T. M. (1988) Phage resistance ofStreptococcus cremoris due to low adsorption efficiency.Neth. Milk Dairy J. 42, 195–206.

    Google Scholar 

  8. Valyasevi, R., Sandine, W. E., and Geller, B. L. (1990) The bacteriophage kh receptor ofLactococcus lactis subsp.cremoris KH is the rhamnose of the extracellular wall polysaccharide.Appl. Environ. Microbiol. 56, 1882–1889.

    PubMed  CAS  Google Scholar 

  9. Valyasevi, R., Sandine, W. E., and Geller, B. L. (1994)Lactococcus lactis ssp.lactis C2 bacteriophage sk1 receptor involving rhamnose and glucose moieties in the cell wall.J. Dairy Sci. 77, 1–6.

    CAS  Google Scholar 

  10. Schäfer, A., Geis, A., Neve, H., and Teuber, M. (1991) Bacteriophage receptors ofLactococcus lactis subsp. “diacetylactis” F7/2 andLactococcus lactis subsp.cremoris Wg2-1.FEMS Microbiol. Lett. 78, 69–74.

    Article  Google Scholar 

  11. Oram, J. D. and Reiter, B. (1968) The adsorption of phage to group N streptococci. The specificity of adsorption and the location of phage receptor substances in cell-wall and plasma-membrane fractions.J. Gen. Virol. 3, 103–119.

    Article  PubMed  CAS  Google Scholar 

  12. Oram, J. D. (1971) Isolation and properties of a phage receptor substance from the plasma membrane ofStreptococcus lactis ML3.J. Gen. Virol. 13, 59–71.

    PubMed  CAS  Google Scholar 

  13. Valyasevi, R., Sandine, W. E., and Geller, B. L. (1991) A membrane protein is required for bacteriophage c2 infection ofLactococcus lactcis subsp.lactis C2.J. Bacteriol. 173, 6095–6100.

    PubMed  CAS  Google Scholar 

  14. Geller, B. L., Ivey, R. G., Trempy, T. E., and Hettinger-Smith, B. (1993) Cloning of a chromosomal gene required for phage infection ofLactococcus lactis subsp.lactis C2.J. Bacteriol. 175, 5510–5519.

    PubMed  CAS  Google Scholar 

  15. Monteville, M. R., Ardestani, B., and Geller, B. L. (1994) Lactococcal bacteriophages require a host cell wall carbohydrate and a plasma membrane protein for adsorption and ejection of DNA.Appl. Environ. Microbiol. 60, 3204–3211.

    PubMed  CAS  Google Scholar 

  16. Gopal, P. K. and Crow, V. L. (1993) Characterization of loosely associated material from the cell surface ofLactococcus lactis subsp.cremoris E8 and its phageresistant variant strain 398.Appl. Environ. Microbiol. 59, 3177–3182.

    PubMed  CAS  Google Scholar 

  17. Sanders, M. E. and Klaenhammer, T. R. (1983) Characterization of phage-sensitive mutants from a phageinsensitive strain ofStreptococcus lactis: evidence for a plasmid determinant that prevents phage adsorption.Appl. Environ. Microbiol. 46, 1125–1133.

    PubMed  CAS  Google Scholar 

  18. de Vos, W. M., Underwood, H. M., and Davies, F. L. (1984) Plasmid encoded bacteriophage resistance inStreptococcus cremoris SK11.FEMS Microbiol. Lett. 23, 175–178.

    Article  Google Scholar 

  19. Sijtsma, L., Jansen, N., Hazeleger, W. C., Wouters, J. T. M., and Hellingwerf, K. J. (1990) Cell surface characteristics of bacteriophage-resistantLactococcus lactis subsp.cremoris SK110 and its bacteriophage-sensitive variant SK112.Appl. Environ. Microbiol. 56, 3230–3233.

    PubMed  CAS  Google Scholar 

  20. Sijtsma, L., Sterkenburg, A., and Wouters, J. T. M. (1988) Properties of the cell walls ofLactococcus lactis subsp.cremoris SK110 and SK112 and their relation to bacteriophage resistance.Appl. environ. Microbiol. 54, 2808–2811.

    PubMed  CAS  Google Scholar 

  21. Sijtsma, L., Wouters, J. T. M., and Hellingwerf, K. J. (1990) Isolation and characterization of lipoteichoic acid, a cell envelope component involved in preventing phage adsorption, fromLactococcus lactis subsp.cremoris SK110.J. Bacteriol. 172, 7126–7130.

    PubMed  CAS  Google Scholar 

  22. Lucey, M., Daly, C., and Fitzgerald, G. F. (1992) Cell surface characteristics ofLactococcus lactis harbouring pCI528, a 46 kb plasmid encoding inhibition of bacteriophage adsorption.J. Gen. Microbiol. 138, 2137–2143.

    CAS  Google Scholar 

  23. Harrington, A. and Hill, C. (1992) Plasmid involvement in the formation of a spontaneous bacteriophage insensitive mutant ofLactococcus lactis.FEMS Microbiol. Lett. 96, 135–142.

    Article  CAS  Google Scholar 

  24. Watanabe, K., Ishibashi, K., Nadashima, Y., and Sakurai, T. (1984) A phage-resistant mutant ofLactobacillus casei which permits phage adsorption but not genome injection.J. Gen. Virol. 65, 981–986.

    PubMed  Google Scholar 

  25. Boussemaer, J. P., Schrauwen, P. P., Sourrouille, J. L., and Guy, P. (1980) Multiple modification/restriction systems in lactic streptococci and their significance in defining a phage-typing system.J. Dairy Res. 47, 404–409.

    Google Scholar 

  26. Chopin, A., Chopin, M.-C., Moillo-Batt, A., and Langella, P. (1984) Two plasmid-determined restriction and modification systems inStreptococcus lactis.Plasmid 11, 260–263.

    Article  PubMed  CAS  Google Scholar 

  27. Froseth, B. R., Harlander, S. K., and McKay, L. L. (1988) Plasmid-mediated reduced phage sensitivity inStreptococcus lactis KR5.J. Dairy Sci. 71, 275–284.

    PubMed  CAS  Google Scholar 

  28. Gautier, M. and Chopin, M.-C. (1987) Plasmiddetermined systems for restriction and modification activity and abortive infection inStreptococcus cremoris.Appl. Environ. Microbiol. 53, 923–927.

    PubMed  CAS  Google Scholar 

  29. Higgins, D. L., Sanozky-Dawes, R. B., and Klaenhammer, T. R. (1988) Restriction and modification activities fromStreptococcus lactis ME2 are encoded by a self-transmissible plasmid, pTN20, that forms cointegrates during mobilization of lactose-fermenting ability.J. Bacteriol. 170, 3435–3442.

    PubMed  CAS  Google Scholar 

  30. Hill, C., Pierce, K., and Klaenhammer, T. R. (1989). The conjugative plasmid pTR2030 encodes two bacteriophage defense mechanisms in lactococci, restriction/modification (R+/M+) and abortive infection (Hsp+).Appl. Environ. Microbiol. 55, 2416–2419.

    PubMed  CAS  Google Scholar 

  31. Josephsen, J. and Vogensen, F. K. (1989) Identification of three different plasmid-encoded restriction/modification systems inStreptococcus lactis subsp.cremoris W56.FEMS Microbiol. Lett. 59, 161–166.

    Article  CAS  Google Scholar 

  32. McKay, L. L., Bohanon, M. J., Polzin, K. M., Rule, P. L., and Baldwin, K. A. (1989) Localization of separate genetic loci for reduced sensitivity towards small isometric-headed bacteriophage sk1 and prolateheaded bacteriophage c2 on pGBK17 fromLactococcus lactis subsp.lactis KR2.Appl. Environ. Microbiol. 55, 2702–2709.

    PubMed  CAS  Google Scholar 

  33. Pearce, L. E. (1978) The effect of host controlled modification on the replication rate of a lactic streptococcal bacteriophage.N.Z. J. Dairy Sci. Technol. 13, 166–171.

    Google Scholar 

  34. Sanders, M. E. and Klaenhammer, T. R. (1980) Restriction and modification in group N streptococci: Effect of heat on development of modified lytic bacteriophage.Appl. Environ. Microbiol. 40, 500–506.

    PubMed  CAS  Google Scholar 

  35. Sanders, M. E. and Klaenhammer, T. R. (1981) Evidence for plasmid linkage of restriction and modification inStreptococcus cremoris KM.Appl. Environ. Microbiol. 42, 944–950.

    PubMed  CAS  Google Scholar 

  36. Sanders, M. E. and Shultz, J. W. (1990) Cloning of phage resistance genes fromLactococcus lactis ssp.cremoris KH.J. Dairy Sci. 73, 2044–2053.

    CAS  Google Scholar 

  37. Sing, W. D. and Klaenhammer, T. R. (1991) Characterization of restriction-modification plasmids fromLactococcus lactis ssp.cremoris and their effects when combined with pTR2030.J. Dairy Sci. 74, 1133–1144.

    CAS  Google Scholar 

  38. Steenson, L. R. and Klaenhammer, T. R. (1986) Plasmid heterogeneity inStreptococcus cremoris M12R: effects on proteolytic activity and host-dependent phage replication.J. Dairy Sci. 69, 2227–2236.

    PubMed  CAS  Google Scholar 

  39. Fitzgerald, G. F., Daly, C., Broen, L. R., and Gingeras, T. R. (1982)ScrFI: a new sequence specific endonuclease fromStreptococcus cremoris.Nucleic Acids Res. 10, 8171–8179.

    Article  CAS  Google Scholar 

  40. Nyengaard, N., Vogensen, F. K., and Josephsen, J. (1993)LlaAI andLlaBI, two type-II restriction endonucleases fromLactococcus lactis subsp.cremoris W9 and W56 recognizing, respectively, 5′-/GATC-3′ and 5′-C/TRYAG-3′.Gene 136, 371, 372.

    Article  PubMed  CAS  Google Scholar 

  41. Mayo, B., Hardisson, C., and Brana, A. F. (1991) Nucleolytic activities inLactococcus lactis subsp.lactis NCDO 497.FEMS Microbiol. Lett. 79, 195–198.

    Article  CAS  Google Scholar 

  42. Solaiman, D. K. Y. and Somkuti, G. A. (1990) Isolation and characterization of a type II restriction endonuclease fromStreptococcus thermophilus.FEMS Microbiol. Lett. 67, 261–266.

    Article  CAS  Google Scholar 

  43. Solaiman, D. K. Y. and Somkuti, G. A. (1991) A type II restriction endonuclease ofStreptococcus thermophilus ST117.FEMS Microbiol. Lett. 80, 75–80.

    Article  CAS  Google Scholar 

  44. Benbadis, L., Garel, J.-R., and Hartley, D. L. (1991) Purification, properties, and sequence specificity ofSsll, a new type II restriction endonuclease fromStreptococcus salivarius subsp.thermophilus. Appl. Environ.Microbiol. 57, 3677, 3678.

    CAS  Google Scholar 

  45. Davis, R., van der Lelie, D., Mercenier, A., Daly, C., and Fitzgerald, G. F. (1993)ScrFI restriction-modification system ofLactococcus lactis subsp.cremoris UC503: cloning and characterization of twoScrFI methylase genes.Appl. Environ. Microbiol. 59, 777–785.

    PubMed  CAS  Google Scholar 

  46. Klaenhammer, T. R. and Sanozky, R. B. (1985) Conjugal transfer fromStreptococcus lactis ME2 of plasmids encoding phage resistance, nisin resistance, and lactose fermenting ability: evidence for a high-frequency conjugal plasmid responsible for abortive infection of virulent bacteriophage.J. Gen. Microbiol. 131, 1531–1541.

    PubMed  CAS  Google Scholar 

  47. 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.J. Bacteriol. 173, 4363–4370.

    PubMed  CAS  Google Scholar 

  48. O'Sullivan, D. J. and Klaenhammer, T. R. (1995)C-LlaI is a bifunctional regulatory protein of thellaI restriction modification operon fromLactococcus lactis, inGenetics of Streptococci, Enterococci, and Lactococci; Proceedings of the IVth International Conference on Streptococci Genetics (Ferretti, J. J., Gilmore, M., Klaenhammer, T. R., and Brown, F., eds.), Dev. Biol. Stand., Karger, Basel, vol. 85, pp. 591–595.

    Google Scholar 

  49. O'Sullivan, D. J., Zagula, K., and Klaenhammer, T. R. (1995)In vivo restriction byLlaI is encoded by three genes, arranged in an operon withllaIM, on the conjugativeLactococcus plasmid pTR2030.J. Bacteriol. 177, 134–143.

    PubMed  Google Scholar 

  50. Duckworth, D. H., Glenn, J., and McCorquodale, D. J. (1981) Inhibition of bacteriophage replication by extra-chromosomal elements.Microbiol. Rev. 45, 52–71.

    PubMed  CAS  Google Scholar 

  51. Klaenhammer, T. R. (1989) Genetic characterization of multiple mechanisms of phage defense from a prototype phage-insensitive strain,Lactococcus lactis ME2.J. Dairy Sci. 72, 3429–3443.

    CAS  Google Scholar 

  52. Sing, W. D. and Klaenhammer, T. R. (1990) Plasmid-induced abortive infection in lactococci: a review.J. Dairy Sci. 73, 2239–2251.

    CAS  Google Scholar 

  53. Sing, W. D. and Klaenhammer, T. R. (1986) Conjugal transfer of bacteriophage resistance determinants on pTR2030 intoStreptococcus cremoris strains.Appl. Environ. Microbiol.,51, 1264–1271.

    PubMed  CAS  Google Scholar 

  54. Steenson, L. R. and Klaenhammer, T. R. (1985)Streptococcus cremoris M12R transconjugants carrying the conjugal plasmid pTR2030 are insensitive to attack by lytic bacteriophages.Appl. Environ. Microbiol. 50, 851–858.

    PubMed  CAS  Google Scholar 

  55. Jarvis, A. W. and Klaenhammer, T. R. (1986) Bacteriophage resistance conferred on lactic streptococci by the conjugative plasmid pTR2030: effects on small isometric-, large isometric-, and prolate-headed phages,Appl. Environ. Microbiol. 51, 1272–1277.

    PubMed  CAS  Google Scholar 

  56. Jarvis, A. W. and Klaenhammer, T. R. (1987) Bacteriophage resistance plasmid pTR2030 inhibits lytic infection of r1t temperate bacteriophage but not induction of r1t prophage inStreptococcus cremoris R1.Appl. Environ. Microbiol.,53, 385–389.

    PubMed  CAS  Google Scholar 

  57. Hill, C., Romero, D. A., McKenney, D. S., Finer, K. R., and Klaenhammer, T. R. (1989) Localization, cloning, and expression of genetic determinants for bacteriophage resistance (Hsp) from the conjugative plasmid pTR2030.Appl. Environ. Microbiol. 55, 1684–1689.

    PubMed  CAS  Google Scholar 

  58. Hill, C., Miller, L. A., and Klaenhammer, T. R. (1990) Nucleotide sequence and distribution of the pTR2030 resistance determinant (hsp) which aborts bacteriophage infection in lactococci.Appl. Environ. Microbiol. 56, 2255–2258.

    PubMed  CAS  Google Scholar 

  59. 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.J. Gen. Microbiol. 137, 1355–1362.

    PubMed  CAS  Google Scholar 

  60. Dinsmore, P. K. and Klaenhammer, T. R. (1994) Phenotypic consequences of altering the copy number ofabiA, a gene responsible for aborting bacteriophage infections inLactococcus lactis.Appl. Environ. Microbiol. 60, 1129–1136.

    PubMed  CAS  Google Scholar 

  61. Casey, J., Daly, C., and Fitzgerald, G. F. (1992) Controlled integration into theLactococcus chromosome of the pCI829-encoded abortive infection gene fromLactococcus lactis subsp.lactis UC811.Appl. Environ. Microbiol. 58, 3283–3291.

    PubMed  CAS  Google Scholar 

  62. Hill, C., Massey, I. J., and Klaenhammer, T. R. (1991) Rapid method to characterize lactococcal bacteriophage genomes.Appl. Environ. Microbiol. 57, 283–288.

    PubMed  CAS  Google Scholar 

  63. Moineau, S., Durmaz, E., Pandian, S., and Klaenhammer, T. R. (1993) Differentiation of two abortive mechanisms by using monoclonal antibodies directed toward lactococcal bacteriophage capsid proteins.Appl. Environ. Microbiol. 59, 208–212.

    PubMed  CAS  Google Scholar 

  64. Cluzel, P.-J., Chopin, A., Erlich, S. D., and Chopin, M.-C. (1991) Phage abortive infection mechanism fromLactococcus lactis subsp.lactis, expression of which is mediated by an isoISS1 element.Appl. Environ. Microbiol. 57, 3547–3551.

    PubMed  CAS  Google Scholar 

  65. Durmaz, E., Higgins, D. L., and Klaenhammer, T. R. (1992) Molecular characterization of a second abortive phage resistance gene present inLactococcus lactis subsp.lactis ME2.J. Bacteriol. 174, 7463–7469.

    PubMed  CAS  Google Scholar 

  66. Coffey, A., Costello, V., Daly, C., and Fitzgerald, G. (1991) Plasmid encoded bacteriophage insensitivity in members of the genusLactococcus, with special reference to pCI829, inGenetics and Molecular Biology of Streptococci, Lactococci, and Enterococci (Dunny, G. M., Cleary, P. P., and McKay, L. L., eds.), American Society for Microbiology, Washington, DC, pp. 131–135.

    Google Scholar 

  67. Jarvis, A. W. (1992) Analysis of phage resistance mechanisms encoded by lactococcal plasmid pAJ2074.Can. J. Microbiol. 39, 252–258.

    Google Scholar 

  68. Ward, A. C., Davidson, B. E., Hillier, A. J., and Powell, I. B. (1992) Conjugally transferable phage resistance activities fromLactococcus lactis DRC1.J. Dairy Sci. 75, 683–691.

    Google Scholar 

  69. Durmaz, E. and Klaenhammer, T. R. (1995) A starter culture rotation strategy incorporating paired restriction/modification and abortive infection bacteriophage defenses in a singleLactococcus lactis strain.Appl. Environ. Microbiol. 1266–1273.

  70. Josephsen, J. and Klaenhammer, T. R. (1990) Stacking of three different restriction and modification systems inLactococcus lactis by contransformation.Plasmid 23, 71–75.

    Article  PubMed  CAS  Google Scholar 

  71. Sing, W. D. and Klaenhammer, T. R. (1993) A strategy for rotation of different bacteriophage defenses in a lactococcal single-strain starter culture system.Appl. Environ. Microbiol. 59, 365–372.

    PubMed  CAS  Google Scholar 

  72. McKay, L. L. and Baldwin, K. A. (1984) Conjugative 40-megadalton plasmid inStreptococcus lactis subsp.diacetylactis DRC3 is associated with resistance to nisin and bacteriophage.Appl. Environ. Microbiol. 47, 68–74.

    PubMed  CAS  Google Scholar 

  73. Jarvis, A. W. (1988) Conjugal transfer in lactic streptococci of plasmid-encoded insensitivity to prolate-and small isometric-headed bacteriophages.Appl. Environ. Microbiol. 54, 777–783.

    PubMed  CAS  Google Scholar 

  74. Kelly, W., Dobson, J., Jorch-Remberg, D., Fitzgerald, G., and Daly, C. (1990) Introduction of bacteriophage resistance plasmids into commercialLactococcus starter strains.FEMS Microbiol. Rev. 87, 63.

    Google Scholar 

  75. Sanders, M. E., Leonhard, P. J., Sing, W. D., and Klaenhammer, T. R. (1986) Conjugal strategy for construction of fast acid-producing, bacteriophage-resistant lactic streptococci for use in dairy fermentations.Appl. Environ. Microbiol. 52, 1001–1007.

    PubMed  CAS  Google Scholar 

  76. Broadbent, J. R. and Kondo, J. K. (1991) Genetic construction of nisin-producingLactococcus lactis subsp.cremoris and analysis of a rapid method for conjugation.Appl. Environ. Microbiol. 57, 517–524.

    PubMed  CAS  Google Scholar 

  77. Klaenhammer, T. R. (1987) Plasmid-directed mechanisms for bacteriophage defense in lactic streptococci.FEMS Microbiol. Rev. 46, 313–325.

    Article  CAS  Google Scholar 

  78. Romero, D. A. and Klaenhammer, T. R. (1990) Abortive phage infection and restriction/modification activities directed by pTR2030 determinants are enhanced by recombination with conjugal elements in lactococci.J. Gen. Microbiol. 136, 1817–1824.

    CAS  Google Scholar 

  79. Romero, D. A. and Klaenhammer, T. R. (1990) Characterization of Gram-positive insertion sequence IS946, and iso-ISS1 element, isolated from the conjugative lactococcal plasmid pTR2030.J. Bacteriol. 172, 4151–4160.

    PubMed  CAS  Google Scholar 

  80. Romero, D. A. and Klaenhammer, T. R. (1991) Construction of an IS946-based composite transposon inLactococcus lactis subsp.lactis.J. Bacteriol. 173, 7599–7606.

    PubMed  CAS  Google Scholar 

  81. Polzin, K. M. and McKay, L. L. (1991) Identification, DNA sequence, and distribution of IS981, a new, high-copy number insertion sequence in lactococci.Appl. Environ. Microbiol. 57, 734–743.

    PubMed  CAS  Google Scholar 

  82. Kim, J. H. and Batt, C. A. (1991) Identification of a nucleotide sequence conserved inLactococcus lactis bacteriophages.Gene 98, 95–100.

    Article  PubMed  CAS  Google Scholar 

  83. Chung, D. K., Chung, S. K., and Batt, C. A. (1992) Antisense RNA directed against the major capsid protein ofLactococcus lactis subsp.cremoris bacteriophage 4-1 confers partial resistance to the host.Appl. Microbiol. Biotechnol. 37, 79–83.

    Article  PubMed  CAS  Google Scholar 

  84. Jarvis, A. W. Relationships by DNA homology between lactococcal phages 7–9, P335, and New Zealand industrial lactococcal phages.Intl. Dairy J., in press.

  85. Hill, C., Miller, L. A., and Klaenhammer, T. R. (1990) Cloning, expression, and sequence determination of a bacteriophage fragment encoding bacteriophage resistance inLactococcus lactis.J. Bacteriol. 172, 6419–6426.

    PubMed  CAS  Google Scholar 

  86. O'Sullivan, D. J., Hill, C., and Klaenhammer, T. R. (1993) Effect of increasing the copy number of bacteriophage origins of replication, intrans, on incoming-phage proliferation.Appl. Environ. Microbiol. 59, 2449–2456.

    PubMed  Google Scholar 

  87. Moineau, S., Pandian, S., and Klaenhammer, T. R. (1994) Evolution of a lytic bacteriophage via DNA acquisition from theLactococcus lactis chromosome.Appl. Environ. Microbiol. 60, 1832–1841.

    PubMed  CAS  Google Scholar 

  88. Lenski, R. E. (1984) Coevolution of bacteria and phage: are there endless cycles of bacterial defenses and phage counterdefenses?J. Theor. Biol. 108, 319–325.

    PubMed  CAS  Google Scholar 

  89. Kruger, D. H. and Bickle, T. A. (1983) Bacteriophage survival: multiple mechanisms for avoiding the deoxyribonucleic acid restriction systems of their hosts.Microbiol. Rev. 47, 345–360.

    PubMed  CAS  Google Scholar 

  90. Sharpe, P. M. (1986) Molecular evolution of bacteriophages: evidence of selection against the recognition sites of host restriction enzymes.Mol. Biol. Evol. 3, 75–83.

    Google Scholar 

  91. Moineau, S., Pandian, S., and Klaenhammer, T. R. (1993) Restriction/modification systems and restriction endonucleases are more effective on lactococcal bacteriophages that have emerged recently in the dairy industry.Appl. Environ. Microbiol. 59, 197–202.

    PubMed  CAS  Google Scholar 

  92. Braun, V., Hertwig, S., Neve, H., Geis, A., and Teuber, M. (1989) Taxonomic differentiation of bacteriophages ofLactococcus lactis by electron microscopy, DNA-DNA hybridization, and protein profiles.J. Gen. Microbiol. 135, 2551–2560.

    CAS  Google Scholar 

  93. Coveney, F. A., Fitzgerald, G. F., and Daly, C. (1987) Detailed characterization and comparison of four lactic streptococcal bacteriophages based on morphology, restriction mapping, DNA homology, and structural protein analysis.Appl. Environ. Microbiol. 53, 1439–1447.

    PubMed  CAS  Google Scholar 

  94. Jarvis, A. W. and Meyer, J. (1986) Electron microscopic heteroduplex study and restriction endonuclease cleavage analysis of the DNA genomes of three lactic streptococcal bacteriophages.Appl. Environ. Microbiol. 51, 1272–1277.

    PubMed  CAS  Google Scholar 

  95. Kim, J. H. and Batt, C. A. (1991) Molecular characterization ofLactococcus lactis bacteriophage F4-1.Food Microbiol. 8, 15–24.

    Article  CAS  Google Scholar 

  96. Moineau, S., Fortier, F., Ackermann, H. W., and Pandian, S. (1992) Characterization of lactococcal bacteriophages in Quebec cheese plants.Can. J. Microbiol. 38, 875–882.

    CAS  Google Scholar 

  97. Powell, I. A., Arnold, P. M., Hillier, A. J., and Davidson, B. E. (1989) Molecular comparison of prolate- and isometric-headed bacteriophages of lactococci.Can. J. Microbiol. 35, 860–866.

    Article  CAS  Google Scholar 

  98. Powell, I. B. and Davidson, B. E. (1986) Resistance to in vitro restriction of DNA from lactic streptococcal bacteriophage c6A.Appl. Environ. Microbiol. 51, 1358–1360.

    PubMed  CAS  Google Scholar 

  99. Prevots, F., Mata, M., and Ritzenthaler, P. (1990) Taxonomic differentiation of 101 lactococcal bacteriophages and characterization of bacteriophages with unsually large genomes.Appl. Environ. Microbiol. 56, 2180–2185.

    PubMed  CAS  Google Scholar 

  100. Shearman, C. A., Hertwig, S., Teuber, M., and Gasson, M. J. (1991) Characterization of the prolate-headed lactococcal bacteriophage vML3: location of the lysin gene and its DNA homology with other prolate-headed phages.J. Gen. Microbiol. 137, 1285–1291.

    CAS  Google Scholar 

  101. Alatossava, T. and Klaenhammer, T. R. (1991) Molecular characterization of three small isometric-headed bacteriophages which vary in their sensitivity to the lactococcal phage resistance plasmid pTR2030.Appl. Environ. Microbiol. 57, 1346–1353.

    PubMed  CAS  Google Scholar 

  102. D'Amelio, G. (1994) MS thesis. North Carolina State University.

  103. Bidnenko, E., Schouler, C., Ehrlich, S. D., and Chopin, M.-C. (1993) Identification of a phage fragment conferring resistance to abi-105 by complementation or recombination.FEMS Microbiol. Rev. 12, P107.

    Google Scholar 

  104. Bidnenko, E., Valyasevi, R., Cluzel, P. J., Parreira, R., Hillier, A., Gautier, M., Anba, J., Ehrlich, S. D., Chopin, M.-C. (1993) Amélioration de la résistance des lactocoques aux bactériophages.Lait 73, 199–205.

    Article  CAS  Google Scholar 

  105. Parreira, R., Valyasevi, R., Ehrlich, S. D., and Chopin, M.-C. (1993) Identification of a phage DNA fragment conferring resistance to abi-416 by complementation.FEMS Microbiol. Rev. 12, P107.

    Google Scholar 

  106. Lawrence, R. C., Thomas, T. D., and Terzaghi, B. E. (1976) Reviews in the progress of dairy science: cheese starters.J. Dairy Res. 43, 141–193.

    CAS  Google Scholar 

  107. Lodics, T. A. and Steenson, L. R. (1993) Phage-host interactions in commercial mixed-strain dairy starter cultures: practical significance—a review.J. Dairy Sci. 76, 2380–2391.

    Article  Google Scholar 

  108. Sandine, W. E. (1989) Use of bacteriophage-resistant mutants of lactococcal starters in cheesemaking.Neth. Milk Dairy J. 43, 211–219.

    Google Scholar 

  109. Jarvis, A. W. (1977) The serological differentiation of lactic streptococcal bacteriophage.N.Z.J. Dairy Sci. Technol. 12, 176–181.

    Google Scholar 

  110. Klaenhammer, T. R. (1984) Interactions of bacteriophages with lactic streptococci.Adv. Appl. Microbiol. 30, 1–29.

    Article  CAS  Google Scholar 

  111. Graham, D. M., Parmelee, C. E., and Nelson, F. E. (1952) The carrier state of lacticStreptococcus bacteriophage.J. Dairy Sci. 35, 813.

    Google Scholar 

  112. Tesfaigzi, J. and Sussmuth, R. (1989) Proportion of phage-insensitive and phage-sensitive cells within pure strains of lactic streptococci, and the influence of calcium.J. Dairy Res. 56, 151–154.

    PubMed  CAS  Google Scholar 

  113. de Vos, W. M. (1989) On the carrier state of bacteriophages in starter lactococci: an elementary explanation involving a bacteriophage resistance plasmid.Neth. Milk Dairy J. 43, 221–227.

    Google Scholar 

  114. Moineau, S., Borkaev, M., Walker, S. A., Vedamuthu, E. R., and Vandenbergh, P. A. (1994) Novel starter rotation system based on phage species sensitivity.J. Dairy Sci. 77, 18.

    Google Scholar 

  115. Harrington, A. and Hill, C. (1991) Construction of a bacteriophage-resistant derivative ofLactococcus lactis subsp.lactis 425A by using the conjugal plasmid pNP40.Appl. Environ. Microbiol. 57, 3405–3409.

    PubMed  CAS  Google Scholar 

  116. Hughes, B. F. and McKay, L. L. (1992) Deriving phage-insensitive lactococci using a food-grade vector encoding phage and nisin resistance.J. Dairy Sci. 75, 914–923.

    Article  Google Scholar 

  117. Coffey, A. G., Fitzgerald, G. F., and Daly, C. (1989) Identification and characterisation of a plasmid encoding abortive infection fromLactococcus lactis ssp.lactis UC811.Neth. Milk Dairy J. 43, 229–244.

    CAS  Google Scholar 

  118. Murphy, M. C., Steele, J. L., Daly, C., and McKay L. L. (1988) Concomitant conjugal transfer of reduced-bacteriophage-sensitivity mechanisms with lactose- and sucrose-fermenting ability in lactic streptococci.Appl. Environ. Microbiol. 54, 1951–1956.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dinsmore, P.K., Klaenhammer, T.R. Bacteriophage resistance inLactococcus . Mol Biotechnol 4, 297–314 (1995). https://doi.org/10.1007/BF02779022

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02779022

Index Entries

Navigation