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Identification of Lactobacillus plantarum TW29-1 isolated from Iranian fermented cereal-dairy product (Yellow Zabol Kashk): probiotic characteristics, antimicrobial activity and safety evaluation

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Abstract

In this study, the probiotic characteristics of Lactobacillus plantarum isolated from an Iranian traditional fermented product, Yellow Zabol Kashk (YZK), were evaluated. The isolated strain was identified as Lactobacillus plantarum TW29-1 by 16S rRNA gene sequencing. L. plantarum TW29-1 had a remarkable tolerance to acidic pHs, bile salts, and simulated gastrointestinal juices. The strain also showed a 51.44% cell surface hydrophobicity, 40.49% auto-aggregation, and 28.63% co-aggregation. L. plantarum TW29-1 was found to have 12.5% adhesion, and it was also able to compete (50.19%) and inhibit (48.87%) Salmonella typhimurium adherence to Caco-2 cells. The growth of pathogenic bacteria (i.e., Pseudomonas aeruginosa, Listeria innocua, Staphylococcus aureus, Escherichia coli, and S. typhimurium) was strongly inhibited by the isolate and S. aureus was the sensitive strain. L. plantarum TW29-1 did not induce DNase or haemolytic activity, confirming its safety aspects. Based on the results, L. plantarum TW29-1 could be introduced as a novel probiotic strain with therapeutic and preservation properties for food and health-promoting purposes.

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References

  1. S. Rezac, C.R. Kok, M. Heermann, R. Hutkins, Fermented foods as a dietary source of live organisms. Front. Microbiol. 9, 1785 (2018)

    Article  PubMed  PubMed Central  Google Scholar 

  2. A. Peters, P. Krumbholz, E. Jäger, A. Heintz-Buschart, M.V. Çakir, S. Rothemund, A. Gaudl, U. Ceglarek, T. Schöneberg, C. Stäubert, Metabolites of lactic acid bacteria present in fermented foods are highly potent agonists of human hydroxycarboxylic acid receptor 3. PLoS Genet. 15(3), e1008145 (2019)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. S.E. Gilliland, Health and nutritional benefits from lactic acid bacteria. FEMS Microbiol. Rev. 7(1–2), 175–188 (1990)

    Article  CAS  PubMed  Google Scholar 

  4. A. Vasiee, F. Falah, B. Alizadeh Behbahani, F. Tabatabaee-Yazdi, Probiotic characterization of Pediococcus strains isolated from Iranian cereal-dairy fermented product: interaction with pathogenic bacteria and the enteric cell line Caco-2. J. Biosci. Bioeng. 130(5), 471–479 (2020)

    Article  CAS  PubMed  Google Scholar 

  5. F. Falah, A. Vasiee, B. Alizadeh Behbahani, F.T. Yazdi, S. Moradi, S.A. Mortazavi, S. Roshanak, Evaluation of adherence and anti-infective properties of probiotic Lactobacillus fermentum strain 4–17 against Escherichia coli causing urinary tract infection in humans. Microb. Pathog. 131, 246–253 (2019)

    Article  CAS  PubMed  Google Scholar 

  6. Y.F. Tabatabaei, A. Vasiee, B.B. Alizadeh, S. Mortazavi, Diversity of lactic acid bacteria isolated from yellow zabol kashk using 16S rRNA gene sequence analysis. Iran. J. Food Sci. Technol. 59(13), 25–36 (2017)

    Google Scholar 

  7. A. Guidone, T. Zotta, R.P. Ross, C. Stanton, M.C. Rea, E. Parente, A. Ricciardi, Functional properties of Lactobacillus plantarum strains: a multivariate screening study. LWT-Food Sci. Technol. 56(1), 69–76 (2014)

    Article  CAS  Google Scholar 

  8. S.S. Behera, R.C. Ray, N. Zdolec, Lactobacillus plantarum with functional properties: an approach to increase safety and shelf-life of fermented foods. BioMed. Res. Int. 2018, 9361614 (2018)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. E.P.O.B. Hazards, A. Ricci, A. Allende, D. Bolton, M. Chemaly, R. Davies, P.S.F. Escámez, Update of the list of QPS-recommended biological agents intentionally added to food or feed as notified to EFSA 5: suitability of taxonomic units notified to EFSA until September 2016. EFSA J. 15(3), e04663 (2017)

    Google Scholar 

  10. F.F. Jia, L.J. Zhang, X.H. Pang, X.X. Gu, A. Abdelazez, Y. Liang, S.R. Son, X.C. Meng, Complete genome sequence of bacteriocin-producing Lactobacillus plantarum KLDS1.0391, a probiotic strain with gastrointestinal tract resistance and adhesion to the intestinal epithelial cells. Genomics 109(5–6), 432–437 (2017)

    Article  CAS  PubMed  Google Scholar 

  11. M. Hojjati, B. Alizadeh Behabahani, F. Falah, Aggregation, adherence, anti-adhesion and antagonistic activity properties relating to surface charge of probiotic Lactobacillus brevis gp104 against Staphylococcus aureus. Microb. Pathog. 147, 104420 (2020)

    Article  CAS  PubMed  Google Scholar 

  12. A.M.O. Leite, M.A.L. Miguel, R.S. Peixoto, P. Ruas-Madiedo, V.M.F. Paschoalin, B. Mayo, S. Delgado, Probiotic potential of selected lactic acid bacteria strains isolated from Brazilian kefir grains. J. Dairy Sci. 98(6), 3622–3632 (2015)

    Article  CAS  PubMed  Google Scholar 

  13. M.E. Fadda, V. Mosa, M. Deplano, M.B. Pisano, S. Cosentino, In vitro screening of Kluyveromyces strains isolated from Fiore Sardo cheese for potential use as probiotics. LWT 75, 100–106 (2017)

    Article  CAS  Google Scholar 

  14. E. Kiray, E. Kariptas, S.Y. Azarkan, Evaluation of vaginal lactobacilli with potential probiotic properties and biotherapeutic effects isolated from healthy Turkish women. PSM Microbiol. 4(3), 56–70 (2019)

    Google Scholar 

  15. R. Georgieva, L. Yocheva, L. Tserovska, G. Zhelezova, N. Stefanova, A. Atanasova et al., Antimicrobial activity and antibiotic susceptibility of Lactobacillus and Bifidobacterium spp. intended for use as starter and probiotic cultures. Biotechnol. Biotech. Eq. 29(1), 84–91 (2015)

    Article  CAS  Google Scholar 

  16. S. Momenzadeh, H. Jooyandeh, B. Alizadeh Behbahani, H. Barzegar, Evaluation of probiotic and antibacterial properties of Lactobacillus fermentum SL163–4. Iran. J. Food Sci. Technol. Res. 17(2), 233–242 (2021)

    Google Scholar 

  17. J.S. Zhou, C.J. Pillidge, P.K. Gopal, H.S. Gill, Antibiotic susceptibility profiles of new probiotic Lactobacillus and Bifidobacterium strains. Int. J. Food Microbiol. 98(2), 211–217 (2005)

    Article  CAS  PubMed  Google Scholar 

  18. H. Gupta, R.K. Malik, Incidence of virulence in bacteriocin-producing enterococcal isolates. Le Lait. 87(6), 587–601 (2007)

    Article  CAS  Google Scholar 

  19. S. Pieniz, R. Andreazza, T. Anghinoni, F. Camargo, A. Brandelli, Probiotic potential, antimicrobial and antioxidant activities of Enterococcus durans strain LAB18s. Food Control 37, 251–256 (2014)

    Article  CAS  Google Scholar 

  20. P.D. Cotter, C. Hill, Surviving the acid test: responses of Gram-positive bacteria to low pH. Microbiol. Mol. Boil. Rev. 67(3), 429–453 (2003)

    Article  CAS  Google Scholar 

  21. A.R. Madureira, C.I. Pereira, K. Truszkowska, A.M. Gomes, M.E. Pintado, F.X. Malcata, Survival of probiotic bacteria in a whey cheese vector submitted to environmental conditions prevailing in the gastrointestinal tract. Int. Dairy J. 15(6–9), 921–927 (2005)

    Article  CAS  Google Scholar 

  22. M. Nooshkam, A. Babazadeh, H. Jooyandeh, Lactulose: properties, techno-functional food applications, and food grade delivery system. Trends Food Sci. Technol. 80, 23–34 (2018)

    Article  CAS  Google Scholar 

  23. J. Šušković, B. Kos, S. Matošić, V. Besendorfer, The effect of bile salts on survival and morphology of a potential probiotic strain Lactobacillus acidophilus M92. World. J. Microbiol. Biotechnol. 16(7), 673–678 (2000)

    Article  Google Scholar 

  24. A. Bezkorovainy, Probiotics: determinants of survival and growth in the gut. Am. J. Clin. Nutr. 73(3), 399s–405s (2001)

    Article  CAS  PubMed  Google Scholar 

  25. H. Zhu, C.A. Hart, D. Sales, N.B. Roberts, Bacterial killing in gastric juice–effect of pH and pepsin on Escherichia coli and Helicobacter pylori. J. Med. Microbiol. 55(9), 1265–1270 (2006)

    Article  CAS  PubMed  Google Scholar 

  26. B. Alizadeh Behbahani, M. Noshad, F. Falah, Inhibition of Escherichia coli adhesion to human intestinal Caco-2 cells by probiotic candidate Lactobacillus plantarum strain L15. Microb. Pathog. 136, 103677 (2019)

    Article  CAS  PubMed  Google Scholar 

  27. H. Gandomi, A. Farhangfar, A. Akhondzadeh Basti, A. Misaghi, N. Noori, Auto and co-aggregation, hydrophobicity and adhesion properties of Lactobacillus plantarum strains isolated from Siahmazgi traditional cheese. Food Health 2(1), 1–5 (2019)

    Google Scholar 

  28. S.H. Son, H.L. Jeon, S.J. Yang, N.K. Lee, H.D. Paik, In vitro characterization of Lactobacillus brevis KU15006, an isolate from kimchi, reveals anti-adhesion activity against foodborne pathogens and antidiabetic properties. Microb. Pathog. 112, 135–141 (2017)

    Article  CAS  PubMed  Google Scholar 

  29. K.M.G.M.M. Kariyawasam, S.J. Yang, N.K. Lee, H.D. Paik, Probiotic properties of Lactobacillus brevis KU200019 and synergistic activity with Fructooligosaccharides in antagonistic activity against foodborne pathogens. Food Sci. Anim. Resour. 40(2), 297–310 (2020)

    Article  PubMed  PubMed Central  Google Scholar 

  30. T. Janković, J. Frece, M. Abram, I. Gobin, Aggregation ability of potential probiotic Lactobacillus plantarum strains. Int. J. Sanit. Eng. Res 6(1), 19–24 (2012)

    Google Scholar 

  31. D.N. Furtado, S.D. Todorov, M. Landgraf, M.T. Destro, B.D.G.M. Franco, Bacteriocinogenic Lactococcus lactis subsp: lactis DF04Mi isolated from goat milk: evaluation of the probiotic potential. Braz. J. Microbiol. 45(3), 1047–1054 (2014)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. R.K. Duary, Y.S. Rajput, V.K. Batish, S. Grover, Assessing the adhesion of putative indigenous probiotic lactobacilli to human colonic epithelial cells. Indian J. Med. Res. 134(6), 664–671 (2011)

    CAS  PubMed  PubMed Central  Google Scholar 

  33. E.M. Tuomola, S.J. Salminen, Adhesion of some probiotic and dairy Lactobacillus strains to Caco-2 cell cultures. Int. J. Food Microbiol. 41(1), 45–51 (1998)

    Article  CAS  PubMed  Google Scholar 

  34. M.A. Bianchi, D. Del Rio, N. Pellegrini, G. Sansebastiano, E. Neviani, F. Brighenti, A fluorescence-based method for the detection of adhesive properties of lactic acid bacteria to Caco-2 cells. Lett. Appl. Microbiol. 39(3), 301–305 (2004)

    Article  CAS  PubMed  Google Scholar 

  35. A. Nowak, I. Motyl, In vitro anti-adherence effect of probiotic Lactobacillus strains on human enteropathogens. Biotechnol. Food Sci. 81, 103–112 (2017)

    Google Scholar 

  36. A.S. Dhanani, S.B. Gaudana, T. Bagchi, The ability of Lactobacillus adhesin EF-Tu to interfere with pathogen adhesion. Eur. Food Res. Technol. 232(5), 777–785 (2011)

    Article  CAS  Google Scholar 

  37. A.C. Ouwehand, S. Salminen, In vitro adhesion assays for probiotics and their in vivo relevance: a review. Microb. Ecol. Health Dis. 15(3), 175–184 (2003)

    Google Scholar 

  38. Y.K. Lee, C.Y. Lim, W.L. Teng, A.C. Ouwehand, E.M. Tuomola, S. Salminen, Quantitative approach in the study of adhesion of lactic acid bacteria to intestinal cells and their competition with enterobacteria. Appl. Environ. Microb. 66(9), 3692–3697 (2000)

    Article  CAS  Google Scholar 

  39. M.L. Chikindas, R. Weeks, D. Drider, V.A. Chistyakov, L.M. Dicks, Functions and emerging applications of bacteriocins. Curr. Opin. Biotechnol. 49, 23–28 (2018)

    Article  CAS  PubMed  Google Scholar 

  40. C. Altieri, A. Bevilacqua, D. Cardillo, M. Sinigaglia, Effectiveness of fatty acids and their monoglycerides against Gram-negative pathogens. Int. J. Food Sci. Technol. 44(2), 359–366 (2009)

    Article  CAS  Google Scholar 

  41. L. Makras, L. De Vuyst, The in vitro inhibition of Gram-negative pathogenic bacteria by bifidobacteria is caused by the production of organic acids. Int. Dairy J. 16(9), 1049–1057 (2006)

    Article  CAS  Google Scholar 

  42. E.H. Ryu, H.C. Chang, In vitro study of potentially probiotic lactic acid bacteria strains isolated from kimchi. Ann. Microbiol. 63(4), 1387–1395 (2013)

    Article  CAS  Google Scholar 

  43. C.C. Tsai, H.Y. Hsih, H.H. Chiu, Y.Y. Lai, J.H. Liu, B. Yu, H.Y. Tsen, Antagonistic activity against Salmonella infection in vitro and in vivo for two Lactobacillus strains from swine and poultry. Int. J. Food Microbiol. 102(2), 185–194 (2005)

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors would like to express their sincere gratitude to the Vice-chancellor for Research and Technology of Agricultural Sciences and Natural Resources University of Khuzestan for supporting this study.

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Correspondence to Behrooz Alizadeh Behbahani.

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Saboktakin-Rizi, M., Alizadeh Behbahani, B., Hojjati, M. et al. Identification of Lactobacillus plantarum TW29-1 isolated from Iranian fermented cereal-dairy product (Yellow Zabol Kashk): probiotic characteristics, antimicrobial activity and safety evaluation. Food Measure 15, 2615–2624 (2021). https://doi.org/10.1007/s11694-021-00846-5

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