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Evaluation of autochthonous Lactococcus lactis subsp. lactis strain as a candidate starter culture in white-brined cheese

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Abstract

Lactococcus lactis subsp. lactis NCCB100539 isolated from an artisanal raw ewe’s milk cheese was evaluated as a potential starter culture in white-brined cheese. As a safety criteria, the cytotoxicity of the viable and heat-killed cells and CFE of this strain were determined on Caco-2 cell line by MTT assay. The antibiotic sensitivity of the strain to nine different antibiotics was also investigated. Cheeses produced using this strain were compared with control cheese in terms of physicochemical, microbiological, sensory properties as well as the peptide and volatile profiles during the 90-days of ripening period. Experimental cheeses had more extensive proteolysis as well as higher sensory scores. Incorporated L. lactis also led to an improvement in the microbial cheese quality. Neither living nor the dead cells and CFE of the strain showed cytotoxicity on Caco-2 cells. Therefore, L. lactis NCCB100539 strain could be a good starter candidate for the industrial white-brined cheeses.

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References

  • Axelsson L. Lactic Acid Bacteria: Classification and physiology. Food Science and Technology. 139: 1-66 (2004)

    CAS  Google Scholar 

  • Bhaskaracharya RK, Shah, NP. Texture characteristics and microstructure of skim milk mozzarella cheeses made using exopolysaccharide or non-exopolysaccharide producing starter cultures. Australian Journal of Dairy Technology. 55: 132-138 (2000)

    Google Scholar 

  • Bulajić S, Mijačević Z, Ledina T, Golić B. Safety evaluation of Sjenica Cheese with regard to coagulase-positive staphylococci and antibiotic resistance of lactic acid bacteria and Staphylococci. Acta Veterinaria. 65(4): 518–537 (2015)

    Article  Google Scholar 

  • Cadwallader KR, Singh TK. Flavours and off-flavours in milk and dairy products. Advanced Dairy Chemistry. 14: 631–690 (2009)

    Article  Google Scholar 

  • Carbonell M, Nunez M, Fernández-Garcia E. Evolution of the volatile components of ewe raw milk La Serena cheese during ripening. Correlation with flavour characteristics. EDP Sciences. 82: 683-698 (2002)

    CAS  Google Scholar 

  • Chimchang J, Theparee T, Wongein S, Trivirot T, Tanasupawa S, Taweechotipatr M, Wongsatayanon B. Screening of potential probiotic lactic acid bacteria with anticancer properties. Journal of the Medical Association of Thailand. 8: 70-78 (2016)

    Google Scholar 

  • Clark S, Costello M. Dairy products evaluation competitions. The sensory evaluation of dairy products. 43–71 (2009).

    Book  Google Scholar 

  • Coelho MC, Malcata FX, Silva CCG. Lactic Acid Bacteria in Raw-Milk Cheeses: From Starter Cultures to Probiotic Functions. Foods. 11: 2276. (2022)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Curioni PMG, Bosset JO. Key odorants in various cheese types as determined by gas chromatography-olfactometry. International Dairy Journal. 12: 959-984 (2002)

    Article  CAS  Google Scholar 

  • Delahunty CM, Drake M. Sensory Character of Cheese and its Evaluation. Cheese: Chemistry, Physics and Microbiology. 1: 455-487 (2004)

    Google Scholar 

  • Dolci P, Ferrocino I, Giordano M, Pramotton R, Vernetti-Prot L, Zenato S, Barmaz A. Impact of Lactococcus lactis as starter culture on microbiota and metabolome profile of an Italian raw milk cheese. International Dairy Journal. 110: 104804 (2020)

    Article  CAS  Google Scholar 

  • Dowdell P, Chankhamhaengdecha S, Panbangred W, Janvilisri T, Arroonual, A. Probiotic Activity of Enterococcus faecium and Lactococcus lactis Isolated from Thai Fermented Sausages and Their Protective Effect Against Clostridium difficile. Probiotics and Antimicrobial Proteins. 12: 641–648 (2020)

    Article  CAS  PubMed  Google Scholar 

  • Fernandez E, Alegría A, Delgado S, Martín MC, Mayo, B. Comparative phenotypic and molecular genetic profiling of wild Lactococcus lactis subsp. lactis strains of the L. lactis subsp. lactis and L. lactis subsp. cremoris genotypes, isolated from starter-free cheeses made of raw milk. Applied and Environmental Microbiology. 77: 5324-5335 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fox PF, Guinee TP, Cogan TM, McSweeney PLH. Fundamentals of Cheese Science. ISBN 978-1-4899-7681-9 (2017)

    Book  Google Scholar 

  • Fraqueza MJ. Antibiotic resistance of lactic acid bacteria isolated from dry fermented sausages. International Journal of Food Microbiology. 212: 76-88 (2015)

    Article  CAS  PubMed  Google Scholar 

  • Guinee TP Salting and the role of salt in cheese. International Journal of Dairy Technology. 57(2-3): 99-109 (2004)

    Article  Google Scholar 

  • Harrigan WF, McCance ME. Laboratory methods in food and dairy microbiology. London. ISBN: 0-12-326043-4 (1976)

    Google Scholar 

  • Kimoto-Nira H, Aoki R, Sasaki K, Suzuki C, Mizumachi K. Oral intake of heat-killed cells of Lactococcus lactis strain H61 promotes skin health in women. Journal of Nutritional Science. 6: 1-18 (2012)

    Google Scholar 

  • Kuchroo CN, Fox PF. Fractionation of the water-soluble nitrogen from cheddar cheese- Chemical methods. Milchwissenschaft-Milk Science International, 37(11): 651-653 (1982)

    CAS  Google Scholar 

  • Law BA. Proteolysis in relation to normal and accelerated cheese ripening. Cheese; chemistry, physics and microbiology. Elsevier Applied Science. 365–392 (1987)

  • Le Bars D, Yvon M. Formation of diacetyl and acetoin by Lactococcus lactis via aspartate catabolism. Journal of Applied Microbiology. 104: 171–177 (2008).

    PubMed  Google Scholar 

  • Lozo J, Topisirovic L, Kojic M. Natural bacterial isolates as an inexhaustible source of new bacteriocins. Applied Microbiology and Biotechnology. 105(2): 477-492 (2021)

    Article  CAS  PubMed  Google Scholar 

  • Malesevic M, Stanisavljevic N, Miljkovic M, Jovcic B, Filipic B, Studholme DJ, Kojic M. The large plasmidome of Lactococcus lactis subsp. lactis bv. diacetylactis S50 confers its biotechnological properties. International Journal of Food Microbiology. 16: 337:108935 (2021)

    Article  CAS  PubMed  Google Scholar 

  • McSweeney P. Biochemistry of cheese ripening. International Journal of Dairy Technology. 57 (2-3): 147-155 (2004)

    Article  Google Scholar 

  • McSweeney PLH, Sousa MJ. Biochemical pathways for the production of flavour compounds in cheeses during ripening: A review. EDP Sciences. 80: 293–324 (2000)

    CAS  Google Scholar 

  • Messaoudi S, Madi A, Prévost H, Feuilloley M, Manai M, Dousset X, Connil N. In vitro evaluation of the probiotic potential of Lactobacillus salivarius SMXD51. Anaerobe. 18(6): 584–589 (2012)

    Article  CAS  PubMed  Google Scholar 

  • Mokoena MP. Lactic Acid Bacteria and Their Bacteriocins: Classification, Biosynthesis and Applications against Uropathogens: A Mini-Review. Molecules. 22: 1255 (2017)

    Article  PubMed  PubMed Central  Google Scholar 

  • National Committee for Clinical Laboratory Standards (NCCLS). Performance standards for antimicrobial susceptibility testing; Twenty second informational supplement. M100-S22, 32,3 (2012)

  • Ozturkoglu-Budak S, Figge MJ, Houbraken ., de Vries RP. The diversity and evolution of microbiota in traditional Turkish divle cave cheese during ripening. International Dairy Journal. 58: 50-53 (2016a)

    Article  CAS  Google Scholar 

  • Ozturkoglu-Budak S, Gursoy A, Aykas DP, Kocak C, Donmez S, de Vries RP, Bron PA. Volatile compound profiling of Turkish Divle Cave cheese during production and ripening. Journal of Dairy Science. 99(7): 5120-5131 (2016b)

    Article  CAS  PubMed  Google Scholar 

  • Ozturkoglu-Budak S, Wiebenga A, Bron P, Vries R. Protease and lipase activities of fungal and bacterial strains derived from an artisanal raw ewe's milk cheese. International Journal of Food Microbiology. 237: 17–27 (2016c)

    Article  CAS  PubMed  Google Scholar 

  • Pytka M, Kordowska-Wiater M, Wajs J, Glibowski P, Sajnaga E. Usefulness of Potentially Probiotic L. lactis Isolates from Polish Fermented Cow Milk for the Production of Cottage Cheese. Applied Sciences. 12(23): 12088 (2022)

    Article  CAS  Google Scholar 

  • Qian MC, Burbank HM. Hard Italian cheeses: Parmigiano- Reggiano and Grana Padano in Improving the Flavour of Cheese. Cambridge: Woodhead, p 421–443 (2007)

    Google Scholar 

  • Ramírez-Nunez J, Romero-Medrano R, Nevarez-Moorillon GV, Gutierrez-Mendez N. Effect of pH and salt gradient on the autolysis of Lactococcus lactis strains. Brazilian Journal of Microbiology. 42: 1495-1499 (2011)

    Article  PubMed  PubMed Central  Google Scholar 

  • Reyes-Díaz R, González-Córdova AF, Estrada-Montoya MC, Méndez-Romero JI, Mazorra-Manzano M., Soto-Valdez H, Vallejo-Cordoba B. Volatile and sensory evaluation of Mexican Fresco cheese as affected by specific wild Lactococcus lactis strains. Journal of Dairy Science. 103, 242–253 (2020)

    Article  PubMed  Google Scholar 

  • Smit G, Smit BA, Engels WJM. Flavour formation by lactic acid bacteria and biochemical flavour profiling of cheese products. FEMS Microbiology Reviews. 29: 591-610 (2005)

    Article  CAS  PubMed  Google Scholar 

  • Soares Pinto M, Fernández de Carvalho A, Dos Santos Pires A, de Paula J, Sobral D, Resplande Magalhães F. Survival of Listeria innocua in Minas traditional Serro cheese during ripening. Food Control. 20(12): 1167-1170 (2009)

    Article  Google Scholar 

  • Thokchom S, Joshi SR. Antibiotic resistance and probiotic properties of dominant lactic microflora from Tungrymbai, an ethnic fermented soybean food of India. Journal of Microbiology. 50: 535–539 (2012)

    Article  CAS  PubMed  Google Scholar 

  • Topisirovic L, Kojic M, Fira D, Golic N, Strahinic I, Lozo J. Potential of lactic acid bacteria isolated from specific natural niches in food production and preservation. International Journal of Microbiology. 112(3): 230-5 (2006)

    Article  CAS  Google Scholar 

  • Wilkins TD, Holdeman LV, Abramson IJ, Moore WEC. (Standardized single-disc method for antibiotic susceptibility testing of anaerobic bacteria. Antimicrobial Agents Chemotheraphy. 1: 451-459 (1972)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to the Dairy Plant of Ankara University, Ankara, Turkey, for facilitating and providing equipment for this work. The authors state that they did not receive any funding for this work.

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Correspondence to Sebnem Ozturkoglu-Budak.

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Altin, C., Kabwanga, T.I., Kiran, F. et al. Evaluation of autochthonous Lactococcus lactis subsp. lactis strain as a candidate starter culture in white-brined cheese. Food Sci Biotechnol 33, 115–127 (2024). https://doi.org/10.1007/s10068-023-01332-y

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