Bryndza cheese of Slovak origin as potential resources of probiotic bacteria
DOI:
https://doi.org/10.5219/1413Keywords:
bryndza, Gram-positive bacteria, Gram-negative bacteria, lactic acid bacteria, probiotic effect, mass spectrometryAbstract
Bryndza cheese includes several predominant lactic acid bacteria. The aim of our study was the antagonistic effect of lactic acid bacteria supernatant isolated from ewes´ cheese bryndza against ten Gram-positive and Gram-negative bacteria. Isolated strains of bacteria were obtained from bryndza which were produced in five different regions of Slovakia. Isolated strains of lactic acid bacteria were identified with mass spectrometry MALDI-TOF MS Biotyper. A total of one hundred and thirty lactic bacteria include Enterococcus faecalis, Enterococcus faecium, Enterococcus hirae, Lactobacillus brevis, Lactobacillus harbinensis, Lactobacillus johnsonii, Lactobacillus plantarum, Lactobacillus paracasei ssp. paracasei, Lactobacillus paraplantarum, Lactobacillus suebicus, Lactococcus lactis ssp. lactis, Lactococcus lactis, and Pediococcus acidilactici were tested in this study against Gram-negative bacteria: Escherichia coli CCM 3988, Klebsiella pneumoniae CCM 2318, Salmonella enterica subsp. enterica CCM 3807, Shigella sonnei CCM 1373, Yersinia enterocolitica CCM 5671 and Gram-positive bacteria: Bacillus thuringiensis CCM 19, Enterococcus faecalis CCM 4224, Listeria monocytogenes CCM 4699, Staphylococcus aureus subsp. aureus CCM 2461, Streptococcus pneumonia CCM 4501 with agar diffusion method. Lactic acid bacteria showed activity 92% against Yersinia enterocolitica, 91% against Klebsiella pneumoniae, 88% against Escherichia coli, 84% against Listeria monocytogenes. The most effective bacteria against Gram-positive and Gram-negative bacteria tested was Lactobacillus paracasei ssp. paracasei.
Downloads
Metrics
References
Andrade, C. C. P., Mandelli, F., Echeverrygaray, S., Delamare, A. P. 2008. Microbial dynamics during cheese production and ripening: Physicochemical and biological Factors. Food Global Science Books, vol. 2, no. 2, p. 91-101.
Arqués, J. L., Rodríguez, E., Langa, S., Landete, J. M., Medina, M. 2015. Antimicrobial activity of lactic acid bacteria in dairy products and gut: Effect on pathogens. BioMed Research International, p. 1-9. https://doi.org/10.1155/2015/584183 DOI: https://doi.org/10.1155/2015/584183
Belicová, A., Mikulášová, M., Dušinský, R. 2013. Probiotic potential and safety properties of Lactobacillus plantarum from Slovak bryndza cheese. BioMed Research International, p. 1-8. https://doi.org/10.1155/2013/760298 DOI: https://doi.org/10.1155/2013/760298
Belicová, A., Mikulášova, M., Krajčovič, J., Dušinský, R. 2011. Antibacterial activity and enterocin genes in enterococci isolated from Bryndza cheese. Journal of Food and Nutrition Research, vol. 50, p. 21-32.
Berta, G., Chebeňová, V., Brežná, B., Pangallo, D., Valík, Ľ., Kuchta, T. 2009. Identification of lactic acid bacteria in Slovakian bryndza cheese. Journal of Food and Nutrition Research, vol. 48, no. 2, p. 65-71.
Brashears, M. M., Reilly, S. S., Gilliland, S. E. 1998. Antagonistic action of cells of Lactobacillus lactis toward Escherichia coli O157:H7 on refrigerated raw chicken meat. Journal of Food Protection, vol. 61, no. 2, p. 166-170. https://doi.org/10.4315/0362-028x-61.2.166 DOI: https://doi.org/10.4315/0362-028X-61.2.166
Buyong, N., Kok, J., Luchansky, J. B. 1998. Use of a genetically enhanced, pediocin-producing starter culture, Lactococcus lactis subsp. Lactis MM217, to control Listeria monocytogenes in Cheddar cheese. Applied and Environmental Microbiology, vol. 64, no. 12, p. 4842-4845. https://doi.org/10.1128/aem.64.12.4842-4845.1998 DOI: https://doi.org/10.1128/AEM.64.12.4842-4845.1998
Commission Regulation (EC) No. 676/2008 of 16 July 2008 registering certain names in the Register of protected designations of origin and protected geographical indications (Ail de la Drôme (PGI), Všestarská cibule (PDO), Slovenská bryndza (PGI), Ajo Morado de Las Pedroñeras (PGI), Gamoneu or Gamonedo (PDO), Alheira de Vinhais (PGI), Presunto de Vinhais or Presunto Bísaro de Vinhais (PGI)). Official Journal of the European Union, L 189/19.
Dicks, L. M. T., Botes, M. 2010. Probiotic lactic acid bacteria in the gastro-intestinal tract: health benefits, safety and mode of action. Beneficial Microbes, vol. 1, no. 1, p. 11-29. https://doi.org/10.3920/bm2009.0012 DOI: https://doi.org/10.3920/BM2009.0012
Diepers, A. C., Krömker, V., Zinke, C., Wente, N., Pan, L., Paulsen, K., Paduch, J. H. 2016. In vitro ability of lactic acid bacteria to inhibit mastitis-causing pathogens. Sustainable Chemistry and Pharmacy, vol. 5, p. 84-92. https://doi.org/10.1016/j.scp.2016.06.002 DOI: https://doi.org/10.1016/j.scp.2016.06.002
Dodd, M. C. 2012. Potential impacts of disinfection processes on elimination and deactivation of antibiotic resistance genes during water and wastewater treatment. Journal of Environmental Monitoring, vol. 14, no. 7, p. 1754-1771. https://doi.org/10.1039/c2em00006g DOI: https://doi.org/10.1039/c2em00006g
Du, J. C., Xu, M., Li, B. L., Ding, X. Y., Huo, G. C. 2016. Preliminary screening of lactic acid bacteria against Escherichia coli and the research of probiotic potential for the screening bacteria. Science and Technology of Food Industry, vol. 37, no. 13, p. 152-156.
Ennahar, S., Assobhei, O., Hasselmann, C. 1998. Inhibition of Listeria monocytogenes in a smear-surface soft cheese by Lactobacillus plantarum WHE 92, a pediocin AcH producer. Journal of Food Protection, vol. 61, no. 2, p. 186-191. https://doi.org/10.4315/0362-028x-61.2.186 DOI: https://doi.org/10.4315/0362-028X-61.2.186
Ennahar, S., Deschamps, N. 2000. Anti-Listeria effect of enterocin A, produced by cheese-isolated Enterococcus faecium EFM01, relative to other bacteriocins from lactic acid bacteria. Journal of Applied Microbiology, vol. 88, no. 3, p. 449-457. https://doi.org/10.1046/j.1365-2672.2000.00985.x DOI: https://doi.org/10.1046/j.1365-2672.2000.00985.x
Fooladi, A. A. I., Forooshai, M. C., Saffarian, P., Mehrab, R. 2014. Antimicrobial effects of four lactobacilli strains isolated from yoghurt against Escherichia coli O157:H7. Journal of Food Safety, vol. 34, no. 2, p. 150-160. https://doi.org/10.1111/jfs.12108 DOI: https://doi.org/10.1111/jfs.12108
Jamuna, M., Jeevaratnam, K. 2004. Isolation and partial characterization of bacteriocins from Pediococcus species. Applied Microbiology and Biotechnology, vol. 65, no. 4, p. 433-439. https://doi.org/10.1007/s00253-004-1576-8 DOI: https://doi.org/10.1007/s00253-004-1576-8
Kačániová, M., Kunová, S., Štefániková, J., Felšöciová, S., Godočíková, L., Horská, E., Nagyová, Ľ., Haščík, P., Terentjeva, M. 2019. Microbiota of the traditional Slovak sheep cheese “Bryndza”. Journal of Microbiology, Biotechnology and Food Sciences, vol. 9, p. 482-486. https://doi.org/10.15414/jmbfs.2019.9.special.482-486 DOI: https://doi.org/10.15414/jmbfs.2019.9.special.482-486
Kačániová, M., Nagyová, Ľ., Štefániková, J., Felsöciová, S., Godočíková, L., Haščík, P., Horská, E., Kunová, S. 2020. The characteristic of sheep cheese “Bryndza” from different regions of Slovakia based on microbiological quality. Potravinarstvo Slovak Journal of Food Sciences, vol. 14, p. 69-75. https://doi.org/10.5219/1239 DOI: https://doi.org/10.5219/1239
Kao, C. T., Frazier, W. C. 1966. Effect of lactic acid bacteria on growth of Staphylococcus aureus. Applied Microbiology, vol. 14, no. 2, p. 251-255. https://doi.org/10.1128/aem.14.2.251-255.1966 DOI: https://doi.org/10.1128/am.14.2.251-255.1966
Keersmaecker, S. C. J. D., Verhoeven, T. L. A., Desair, J., Marchal, K., Vanderleyden, J., Nagy, I. 2006. Strong antimicrobial activity of Lactobacillus rhamnosus GG against Salmonella Typhimurium is due to accumulation of lactic acid. FEMS Microbiology Letters, vol. 259, no. 1, p. 89-96. https://doi.org/10.1111/j.1574-6968.2006.00250.x DOI: https://doi.org/10.1111/j.1574-6968.2006.00250.x
Maragkoudakis, P. A., Mountzouris, K. C., Psyrras, D., Cremonese, S., Fischer, J., Cantor, M. D., Tsakalidou, E. 2009. Functional properties of novel protective lactic acid bacteria and application in raw chicken meat against Listeria monocytogenes and Salmonella enteritidis. International Journal of Food Microbiology, vol. 130, no. 3, p. 219-226. https://doi.org/10.1016/j.ijfoodmicro.2009.01.027 DOI: https://doi.org/10.1016/j.ijfoodmicro.2009.01.027
Messens, W., De Vuyst, L. 2002. Inhibitory substances produced by lactobacilli isolated from sourdoughs – a review. International Journal of Food Microbiology, vol. 72, no. 1-2, p. 31-43. https://doi.org/10.1016/s0168-1605(01)00611-0 DOI: https://doi.org/10.1016/S0168-1605(01)00611-0
Mojgani, N., Amimia, C. 2007. Kinetics of growth and bacteriocin production in L. casei RN 78 isolated from dairy sample in IR Iran. International Journal of Dairy Science, vol. 2, no. 1, p. 1-12. https://doi.org/10.3923/ijds.2007.1.12 DOI: https://doi.org/10.3923/ijds.2007.1.12
Plaza-Diaz, J., Ruiz-Ojeda, F. J., Gil-Campos, M., Gil, A. 2019. Mechanisms of action of probiotics. Advances in Nutrition, vol. 10 (suppl_1): S49–S66. https://doi.org/10.1093/advances/nmy063 DOI: https://doi.org/10.1093/advances/nmy063
Ponce, A. G., Moreira, M. R., Del Valle, C. E., Roura, S. I. 2008. Preliminary characterization of bacteriocin-like substances from lactic acid bacteria isolated from organic leafy vegetables. LWT - Food Science and Technology, vol. 41, no. 3, p. 432-444. https://doi.org/10.1016/j.lwt.2007.03.021 DOI: https://doi.org/10.1016/j.lwt.2007.03.021
Reviriego, C., Fernández, A., Horn, N., Rodrı́guez, E., Marı́n, M. L., Fernández, L., Rodrı́guez, J. M. 2005. Production of pediocin PA-1, and coproduction of nisin a and pediocin PA-1, by wild Lactococcus lactis strains of dairy origin. International Dairy Journal, vol. 15, no. 1, p. 45-49. https://doi.org/10.1016/j.idairyj.2004.05.003 DOI: https://doi.org/10.1016/j.idairyj.2004.05.003
Reviriego, C., Fernández, L., Rodríguez, J. M., 2007. A food-grade system for production of pediocin PA-1 in nisin-producing and non-nisin-producing Lactococcus lactis strains: application to inhibit Listeria growth in a cheese model system. Journal of Food Protection, vol. 70, no. 11, p. 2512-2517. https://doi.org/10.4315/0362-028X-70.11.2512 DOI: https://doi.org/10.4315/0362-028X-70.11.2512
Rodríguez, E., Calzada, J., Arqués, J. L., Rodríguez, J. M., Nuñez, M., Medina, M. 2005. Antimicrobial activity of pediocin-producing Lactococcus lactis on Listeria monocytogenes, Staphylococcus aureus and Escherichia coli O157:H7 in cheese. International Dairy Journal, vol. 15, no. 1, p. 51-57. https://doi.org/10.1016/j.idairyj.2004.05.004 DOI: https://doi.org/10.1016/j.idairyj.2004.05.004
Sádecká, J., Čaplová, Z., Tomáška, M., Šoltys, K., Kopuncová, M., Budiš, J., Drončovský, M., Kolek, E., Koreňová, J., Kuchta, T. 2019. Microorganisms and volatile aroma-active compounds in bryndza cheese produced and marketed in Slovakia. Journal of Food and Nutrition Research, vol. 58, no. 4, p. 382-392.
Šaková, N., Sádecká, J., Lejková, J., Puškárová, A., Koreňová, J., Kolek, E., Valík, Ľ., Kuchta, T., Pangallo, D. 2015. Characterization of May bryndza cheese from various regions in Slovakia based on microbiological, molecular and principal volatile odorants examination. Journal of food and nutrition research, vol. 54, no. 3, p. 239-251.
Sharma, C., Singh, B. P., Thakur, N., Gulati, S., Gupta, S., Mishra, S. K., Panwar, H. 2017. Antibacterial effects of Lactobacillus isolates of curd and human milk origin against food-borne and human pathogens. 3 Biotech, vol. 7, no. 31, p. 1-9. https://doi.org/10.1007/s13205-016-0591-7 DOI: https://doi.org/10.1007/s13205-016-0591-7
Soerjadi, A. S., Stehman, S. M., Snoeyenbos, G. H., Weinack, O. M., Smyser, C. F. 1981. The influence of lactobacilli on the competitive exclusion of paratyphoid salmonellae in chickens. Avian Diseases, vol. 25, no. 4, p. 1027-1033. https://doi.org/10.2307/1590078 DOI: https://doi.org/10.2307/1590078
Šušković, J., Kos, B., Beganović, J., Pavunc, A. L., Habjanič, K., Matošić, S. 2010. Antimicrobial activity – the most important property of probiotic and starter lactic acid bacteria. Food Technology and Biotechnology, vol. 48, no. 3, p. 296-307.
Tharrington, G., Sorrells, K. M. 1992. Inhibition of Listeria monocytogenes by milk culture filtrates from Lactobacillus delbrueckii subsp. lactis. Journal of Food Protection, vol. 55, no. 7, p. 542-544. https://doi.org/10.4315/0362-028x-55.7.542 DOI: https://doi.org/10.4315/0362-028X-55.7.542
Tilocca, B., Costanzo, N., Morittu, V. M., Spina, A. A., Soggiu, A., Britti, D., Roncada, P., Piras, C. 2020. Milk microbiota: Characterization methods and role in cheese production. Journal of Proteomics, vol. 210, 103534. https://doi.org/10.1016/j.jprot.2019.103534 DOI: https://doi.org/10.1016/j.jprot.2019.103534
Toth, D., Brindza, J., Panghyova, E., Silhar, S. 2016. Traditional Slovak products as functional foods in Kristbergsson, K., Ötles, S. Functional Properties of Traditional Foods. Springer, p. 75-86. ISBN 978-1-4899-7662-8. DOI: https://doi.org/10.1007/978-1-4899-7662-8_5
Yang, Y., Latorre, J. D., Khatri, B., Kwon, Y. M., Kong, B. W., Teague, K. D., Graham, L. E., Wolfenden, A. D., Mahaffey, B. D., Baxter, M., Hernandez-Velasco, X., Merino-Guzman, R., Hargis, B. M., Tellez, G. 2017. Characterization and evaluation of lactic acid bacteria candidates for intestinal epithelial permeability and Salmonella Typhimurium colonization in neonatal turkey poults. Poultry Science, vol. 97, no. 2, p. 515-521. https://doi.org/10.3382/ps/pex311 DOI: https://doi.org/10.3382/ps/pex311
Yu, Y., Zhang, Y., Liu, R., Zeng, D., Huang, W., Jiang, H. 2006. Studies on the antagonistic property of Lactobacillus. Southwest China Journal of Agricultural Sciences, vol. 19, no. 2, p. 294-296.
Zhang, H., Qian, G. Q., Bin, L. I. 2016. Study of Lactobacillus strains with antagonistic activity against Salmonella. Food Research and Development, vol. 37, no. 16, p. 171-174.
Zhang, P. H., Gu, G. Z., Zhang, J. J., Chen, J. C. 2011. Inhibition of Listeria monocytogenes growth by using combined bacteriocinproducing strains in raw beef. Science and Technology of Food Industry, vol. 32, no. 6, p. 118-120.
Zhong, L., Zhang, X., Covasa, M. 2014. Emerging roles of lactic acid bacteria in protection against colorectal cancer. World Journal of Gastroenterology, vol. 20, no. 24, p. 7878-7886. https://doi.org/10.3748/wjg.v20.i24.7878 DOI: https://doi.org/10.3748/wjg.v20.i24.7878
Zhu, C. S., Gao, Y. R., Xu, G. D. 2014. Screening of lactic acid bacteria for production of anti-Listeria bacteriocin. Modern Food Science and Technology, vol. 30, no. 5, p. 86-91.
Published
How to Cite
Issue
Section
License
This license permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited, and is not altered, transformed, or built upon in any way.
