Skip to main content
SpringerLink
Log in

Starter culture design to overcome phage infection during yogurt fermentation

  • Research Article
  • Published:
Food Science and Biotechnology Aims and scope Submit manuscript

Abstract

Streptococcus thermophilus phages present hazards for yogurt processing. In order to avoid adverse effects, different component yogurt starters were designed. For 2-component yogurt starters consisting of an S. thermophilus sensitive and a Lactobacillus delbrueckii ssp. bulgaricus strain, phage infection was destructive. Phages resulted in increased fermentation time, unbalanced cocci to rod ratios, decreased viscosity values, and varied sensory properties. For 3-component yogurt starters consisting of S. thermophilus sensitive, S. thermophilus insensitive, and L. bulgaricus strains, phage invasion did not result in the undesirable effects of slow acidification, decreased viscosity values, and unbalanced cocci to rod ratios. The 3-component yogurt starter stabilized fermentation and improved the practical fermentation performance in the presence of phages. Combinations of different S. thermophilus strains in the design and use of yogurt starters should be considered.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Sieuwerts S, de Bok FAM, Hugenholtz J, van Hylckama Vlieg JET. Unraveling microbial interactions in food fermentations: From classical to genomics approaches. Appl. Environ. Microb. 74: 4997–5007 (2008)

    Article  CAS  Google Scholar 

  2. Robitaille G, Tremblay A, Moineau S, St-Gelais D, Vadeboncoeur C, Britten M. Fat-free yogurt made using a galactose-positive expolysaccharide-producing recombinant strain of Streptococcus thermophilus. J. Dairy Sci. 92: 477–482 (2009)

    Article  CAS  Google Scholar 

  3. Soomro AH, Masud T. Selection of yogurt starter culture from indigenous isolates of Streptococcus thermophilus and Lactobacillus delbrueckii subsp. bulgaricus on the basis of technological properties. Ann. Microbiol. 58: 67–71 (2008)

    Article  CAS  Google Scholar 

  4. Skriver A, Stenby E, Folkenberg D, Runge M, Jensen NB. Tools in the development of future starter cultures for fermented milk. pp. 55–61. In: Proceedings of the IDF Seminar on Aroma and Texture of Fermented Milk. Kolding, Denmark. International Dairy Federation, Brussels, Belgium (2003)

    Google Scholar 

  5. Urshev ZL, Pashova-Baltova KN, Dimitrov ZP. Tracing Streptococcus thermophilus strains in three-component yogurt starters. World J. Microb. Biot. 22: 1223–1228 (2006)

    Article  CAS  Google Scholar 

  6. Mills S, Griffin C, O’Sullivan O, Coffey A, McAuliffe OE, Meijer WC, Serrano LM, Ross RP. A new phage on the ‘Mozzarella’ block: Bacteriophage 5093 shares a low level of homology with other Streptococcus thermophilus phages. Int. Dairy J. 21: 963–969 (2011)

    Article  CAS  Google Scholar 

  7. Quiberoni A, Moineau S, Rousseau GM, Reinheimer J, Ackermann H-W. Streptococcus thermophilus bacteriophages. Int. Dairy J. 20: 657–664 (2010)

    Article  CAS  Google Scholar 

  8. Binetti AG, Bailo NB, Reinheimer JA. Spontaneous phage-resistant mutants of Streptococcus thermophilus: Isolation and technological characteristics. Int. Dairy J. 17: 343–349 (2007)

    Article  CAS  Google Scholar 

  9. Garneau JE, Dupuis MÈ, Villion M, Romero DA, Barrangou R, Boyaval P, Fremaux C, Horvath P, Magadán AH, Moineau S. The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468: 67–71 (2010)

    Article  CAS  Google Scholar 

  10. Viscardia M, Capparellib R, Iannelli D. Rapid selection of phage-resistant mutants in Streptococcus thermophilus by immunoselection and cell sorting. Int. J. Food Microbiol. 89: 223–231 (2003)

    Article  Google Scholar 

  11. Mills S, Griffin C, Coffey A, Meijer WC, Hafkamp B, Ross RP. CRISPR analysis of bacteriophage-insensitive mutants (BIMs) of industrial Streptococcus thermophilus-implications for starter design. J. Appl. Microbiol. 108: 945–955 (2010)

    Article  CAS  Google Scholar 

  12. Ma C, Wu Z, Chen Z, Du Z, Sun K, Ma A. Differentiation of Streptococcus thermophilus strains in commercial Direct Vat Set yogurt starter. Food Sci. Biotechnol. 22: 987–991 (2013)

    Article  CAS  Google Scholar 

  13. Ma C, Pan N, Chen Z, Liu Z, Gong G, Ma A. Geographical diversity of Streptococcus thermophilus phages in Chinese yoghurt plants. Int. Dairy J. 35: 32–37 (2014)

    Article  CAS  Google Scholar 

  14. Quiberoni A, Tremblay D, Ackermann HW, Moineau S, Reinheimer JA. Diversity of Streptococcus thermophilus phages in a large-production cheese factory in Argentina. J. Dairy Sci. 89: 3791–3799 (2006)

    Article  CAS  Google Scholar 

  15. Ayhan K, Durlu-Özkaya F, Tunail N. Commercially important characteristics of Turkish origin domestic strains of Streptococcus thermophilus and Lactobacillus delbrueckii ssp. bulgaricus. Int. J. Dairy Technol. 58: 150–157 (2005)

    Article  Google Scholar 

  16. Condurso C, Verzera A, Romeo V, Ziino M, Conte F. Solid-phase microextraction and gas chromatography mass spectrometry analysis of dairy product volatiles for the determination of shelf-life. Int. Dairy J. 18: 819–825 (2008)

    Article  CAS  Google Scholar 

  17. Lucey JA. Cultured dairy products: An overview of their gelation and texture properties. Int. J. Dairy Technol. 57: 77–84 (2004)

    Article  CAS  Google Scholar 

  18. Najgebauer-Lejko D, Sady M, Grega T, Walczycka M. The impact of tea supplementation on microflora, pH, and antioxidant capacity of yoghurt. Int. Dairy J. 21: 568–574 (2011)

    Article  CAS  Google Scholar 

  19. Hui YH. Dairy Science and Technology Handbook. 1st ed. VCH Publishers, New York, NY, USA. pp. 1–56 (1993)

    Google Scholar 

  20. Escobar D, Clark S, Ganesan V, Repiso L, Waller J, Harte F. High-pressure homogenization of raw and pasteurized milk modifies the yield, composition, and texture of queso fresco cheese. J. Dairy Sci. 94: 1201–1210 (2011)

    Article  CAS  Google Scholar 

  21. Ayala-Hernandez I, Goff HD, Corredig M. Interaction between milk proteins and exopolysaccharides produced by Lactococcus lactis observed by scanning electron microscopy. J. Dairy Sci. 91: 2583–2590 (2008)

    Article  CAS  Google Scholar 

  22. Iyer R, Tomar SK, Uma Maheswari T, Singh R. Streptococcus thermophilus strains: Multifunctional lactic acid bacteria. Int. Dairy J. 20: 133–141 (2010)

    Article  CAS  Google Scholar 

  23. Hols P, Hancy F, Fontaine L, Grossiord B, Prozzi D, Leblond-Bourget N, Decaris B, Bolotin A, Delorme C, Dusko Ehrlich S, Guédon E, Monnet V, Renault P, Kleerebezem M. New insights in the molecular biology and physiology of Streptococcus thermophilus revealed by comparative genomics. FEMS Microbiol. Rev. 29: 435–463 (2005)

    CAS  Google Scholar 

  24. Auad L, de Ruiz Holgado AAP, Forsman P, Alatossava T, Raya RR. Isolation and characterization of a new Lactobacillus delbrueckii ssp. bulgaricus temperate bacteriophage. J. Dairy Sci. 80: 2706–2712 (1997)

    Article  CAS  Google Scholar 

  25. Binetti AG, Suárez VB, Tailliez P, Reinheimer JA. Characterization of spontaneous phage-resistant variants of Streptococcus thermophilus by randomly amplified polymorphic DNA analysis and identification of phage-resistance mechanisms. Int. Dairy J. 17: 1115–1122 (2007)

    Article  CAS  Google Scholar 

  26. Labrie SJ, Samson JE, Moineau S. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8: 317–327 (2010)

    Article  CAS  Google Scholar 

  27. Bondy-Denomy J, Pawluk A, Maxwell KL, Davidson AR. Bacteriophage genes that inactivate the CRISPR/Cas bacterial immune system. Nature 493: 429–432 (2013)

    Article  CAS  Google Scholar 

  28. Marrec CL, van Sinderen D, Walsh L, Stanley E, Vlegels E, Moineau S, Heinze P, Fitzgerald G, Fayard B. Two groups of bacteriophages infecting Streptococcus thermophilus can be distinguished on the basis of mode of packaging and genetic determinants for major structural proteins. Appl. Environ. Microb. 63: 3246–3253 (1997)

    Google Scholar 

  29. Lévesque C, Duplessis M, Labonté J, Labrie S, Fremaux C, Tremblay D, Moineau S. Genomic organization and molecular analysis of virulent bacteriophage 2972 infecting an exopolysaccharide-producing Streptococcus thermophilus strain. Appl. Environ. Microb. 71: 4057–4068 (2005)

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. State Key Laboratory of Dairy Biotechnology, Technology Center of Bright Dairy & Food Co., Ltd., Shanghai, 200436, China

    Chengjie Ma, Guangyu Gong & Sha Li

  2. State Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, Hubei, 430070, China

    Zhengjun Chen

  3. College of Food Science and Technology, Huazhong Agricultural University, Wuhan, Hubei, 430070, China

    Lifen Huang & Aimin Ma

Authors
  1. Chengjie Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhengjun Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guangyu Gong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lifen Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sha Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Aimin Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aimin Ma.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ma, C., Chen, Z., Gong, G. et al. Starter culture design to overcome phage infection during yogurt fermentation. Food Sci Biotechnol 24, 521–527 (2015). https://doi.org/10.1007/s10068-015-0068-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10068-015-0068-1

Keywords

Search

Navigation