Acta Biologica Hungarica

, Volume 57, Issue 3, pp 377–385 | Cite as

Identification of Adsorption Inhibition, Restriction/Modification and Abortive Infection Type Phage Resistance Systems in Lactococcus lactis Strains

  • Çağla Tükel
  • Pinar Şanlibaba
  • Banu Özden
  • M. AkçelikEmail author


98 Lactococcus lactis strains were isolated from traditional fermented milk products in Turkey tested against 60 lactococcal lytic phages to determine their resistance levels. While 82 L. lactis strains were sensitive against lactic phages at different levels, 16 L. lactis strains showed resistance to all phages tested. Types of phage resistance among 16 L. lactis strains were identified as phage adsorption inhibition in eight strains, restriction/modification in six strains and abortive infection (heat sensitive phage resistance) in two strains, using three broad-spectrum phages Φpll 98-32, Φpld 67-42 and Φpld 67-44.


L. lactis phage resistance adsorption restriction/modification abortive infection 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.



This research was supported by the Institute of Biotechnology, Ankara University, under the project entitled “Endüstriyel Açıdan Kullanışlı Lactococcus lactis Suşlarının Tanısıve Laktik Fajların İnaktivasyonu Üzerinde Araştırmalar”.


  1. 1.
    Akçelik, M. (1998) A phage DNA injection-blocking type resistance mechanisms encoded by chromosomal DNA in Lactococcus lactis subsp. lactis PLM18. Milchwissenchaft 53, 619–622.Google Scholar
  2. 2.
    Akçelik, M., Şanlibaba, P., Tükel, Ç. (2000) Phage resistance in Lactococcus lactis subsp. lactis strains isolated from traditional fermented milk products in Turkey. International Journal of Food Science and Technology 35, 473–481.CrossRefGoogle Scholar
  3. 3.
    Allison, G. E., Klaenhammer, T. R., (1998) Phage resistance mechanisms in lactic acid bacteria. Int. Dairy J. 8, 207–226.CrossRefGoogle Scholar
  4. 4.
    Brüssow, H., Desire, F. (2001) Comparative phage genomics and the evolution of Siphoviridae: Insights from dairy phages. Mol. Microbiol. 39, 213–222.CrossRefGoogle Scholar
  5. 5.
    Chopin, M. C., Chopin, A., Bidnenko, E. (2005) Phage abortive infection in lactococci: Variation on a theme. Current Opinion in Microbiology 8, 473–479.CrossRefGoogle Scholar
  6. 6.
    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.CrossRefGoogle Scholar
  7. 7.
    Deng, Y.-M., Harvey, M. L., Lui, C. Q., Dunn, N. W., (1997) A novel plasmid encoded phage abortive infection system from Lactococcus lactis biovar. diacetylactis. FEMS Microbiology Letters 146, 149–154.CrossRefGoogle Scholar
  8. 8.
    Desiere, F., Lucchini, S., Canchaya, C., Ventura, M., Brüssow, H. (2002) Comparative genomics of phages and prophages in lactic acid bacteria. Antonie van Leeuwenhoek 82, 73–91.CrossRefGoogle Scholar
  9. 9.
    Dinsmore, P. K., Klaenhammer, T. R., (1995) Bacteriophage resistance in Lactococcus. Mol. Biotechnology 4, 297–313.CrossRefGoogle Scholar
  10. 10.
    Garvey, P., Hill, C., Fitzgerald, G. F., (1996) The lactococcal plasmid pNP40 encodes a third bacteriophage resistance mechanisms, one which affects phage DNA penetration. Appl. Environ. Microbiol. 62, 676–679.PubMedPubMedCentralGoogle Scholar
  11. 11.
    Higgins, D. L., Sanozky, R. B., Klaenhammer, T. R., (1988) Restriction and modification activities from Streptococcus lactis ME2 are encoded by a self-transmissible plasmid, pTN 20, that forms cointegrates during mobilization of lactose-fermenting ability. J. Bacteriol. 170, 3435–3442.CrossRefGoogle Scholar
  12. 12.
    Hill, C. (1993) Bacteriophage and bacteriophage resistance in lactic acid bacteria. FEMS Microbiology Reviews 12, 87–108.CrossRefGoogle Scholar
  13. 13.
    Hill, C., Massey, I. J., Klaenhammer, T. R., (1991) Rapid method to characterize lactococcal bacteriophage genomes. Appl. Environ. Microbiol. 57, 286–288.Google Scholar
  14. 14.
    Jarvis, A. W., Fitzgerald, G. F., Mata, M., Mercenier, A., Neve, H., Powell, I. B., Rondo, C., Saxelin, M., Teuber, M. (1991) Species and types phages of lactococcal bacteriophages. Intervirology 32, 2–9.CrossRefGoogle Scholar
  15. 15.
    Josephsen, J., Madsen, A. (2001) The LlaG1 restriction and modification system of Lactococcus lactis W10 consists of only one single polypeptide. FEMS Microbiology Letters 200, 91–96.CrossRefGoogle Scholar
  16. 16.
    Lauridsen, B. S., Janzen, T., Schnabl, J., Johansen, E. (2003) Identification of the host determinants of two prolate-headed phages infecting Lactococcus lactis. Virology 309, 10–17.CrossRefGoogle Scholar
  17. 17.
    Lucey, M., Daly, C., Fitzgerald, G. F., (1992) Cell surface characteristics of Lactococcus lactis harboring pCI 528 a 46 kb plasmid encoding inhibition of phage adsorption. J. Gen. Microbiol. 138, 2137–2143.CrossRefGoogle Scholar
  18. 18.
    Madera, C., Garcia, P., Janzen, T., Rodriguez, A., Suárez, E. J. (2003) Characterization of the technologically proficient wild Lactococcus lactis strains resistant to phage infection. International Journal of Food Microbiology 86, 213–222.CrossRefGoogle Scholar
  19. 19.
    McGrath, S., Seegers, J. F., M. L., Fitzgerald, G. F., Van Sinderen, D. (1999) Molecular characterization of a phage encoded resistance system in Lactococcus lactis. Appl. Environ. Microbiol. 65, 1891–1999.PubMedPubMedCentralGoogle Scholar
  20. 20.
    McGrath, S., Fitzgerald, G. F., Van Sinderen, D. (2001) Improvement and optimization of two engineered phage resistance mechanisms in Lactococcus lactis. Appl. Environ. Microbiol. 67, 608–616.CrossRefGoogle Scholar
  21. 21.
    McGrath, S., Fitzgerald, G. F., Van Sinderen, D. (2004) The impact of bacteriophage genomics. Current Opinion in Biotechnology 15, 94–99.CrossRefGoogle Scholar
  22. 22.
    McKay, L. L., Baldwin, K. A., Zottola, E. A., (1972) Loss of lactose metabolism in lactic Streptococci. Appl. Microbiol. 23, 1090–1096.PubMedPubMedCentralGoogle Scholar
  23. 23.
    Moineau, S., Levesque, C. (2005) Control of bacteriophages in industrial fermentations. In: Kutter, E., Sulakvelidze, A. (eds) Bacteriophages: Biology and Applications. CRC Press, Chap. 10, pp. 285–296.Google Scholar
  24. 24.
    O’Sullivan, D., Ross, R. P., Twomey, D. P., Hill, C. (2001) Naturally occurring lactococcal plasmid pAH90 links bacteriophage resistance and mobility function to a food grade selectable marker. Appl. Environ. Microbiol. 67, 929–938.CrossRefGoogle Scholar
  25. 25.
    Sturnio, J. M., Klaenhammer, T. R., (2004) Bacteriophage defense systems and strategies for lactic acid bacteria. Adv. Appl. Microbiol. 56, 331–378.CrossRefGoogle Scholar
  26. 26.
    Terzaghi, B. E., Sandine, W. E., (1975) Improved medium for lactic streptococci and their bacteriophage. Appl. Microbiol. 29, 807–813.PubMedPubMedCentralGoogle Scholar
  27. 27.
    Twomey, D. P., Gabillet, N., Daly, C., Fitzgerald, G. F., (1997) Molecular characterization of the restriction endonuclease gene (ScrFI) associated with the ScrFI restriction/modification system from Lactococcus lactis subsp. cremoris UC503. Microbiology 143, 2277–2286.CrossRefGoogle Scholar

Copyright information

© Akadémiai Kiadó, Budapest 2006

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (, which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  • Çağla Tükel
    • 1
  • Pinar Şanlibaba
    • 2
  • Banu Özden
    • 3
  • M. Akçelik
    • 3
    Email author
  1. 1.Department of Medical Microbiology and Immunology, School of MedicineUniversity of California at DavisDavisUSA
  2. 2.Department of Food Technology, Kalecik High SchoolUniversity of AnkaraKalecik, AnkaraTurkey
  3. 3.Department of Biology, Faculty of ScienceUniversity of AnkaraTandoğan, AnkaraTurkey

Personalised recommendations