Some lactobacillus, leuconostoc and acetobacter strains in traditional turkish yoghurt, cheese, kefir samples as a probiotic candidate

Year 2023, , 326 - 334, 29.06.2023

Nazan Tokatlı Demirok , Mehmet Alpaslan , Seydi Yıkmış

https://doi.org/10.31015/jaefs.2023.2.10

Abstract

Lactic acid bacteria which are important for production of fermented milk products contain may strains called Lactobacillus, Streptococcus, Lactococcus and Leuconostoccus. As a result, lactic acid bacteria are called ‘milk-souring (fermenting)’ organisms. In addition to the fermentation abilities of Lactobacillus spp., it is important for aroma, texture and acid formation and comprises the most important group of lactic acid bacteria. Their critical importance comes from their metabolic capacity and probiotic features. In this research, yogurt, cheese and kefir samples were collected from cities in Turkey and used to isolate. Isolates were identified phenotypically and genotypically characterized. The probiotic features antibacterial activity against Staphylococcus aureus ATCC6538, Listeria monocytogenes DSM12464, Escherichia coli ATCC 25922, Enterococcus faecalis ATCC51299, and Salmonella Enteritidis ATCC 130762; bile and acid salt tolerance, susceptibility to chloramphenicol, erythromycin, penicillin G, gentamicin, vancomycin, streptomycin, kanamycin, and tetracycline of isolates were determined. Isolates, were identified as Lactobacillus paracasei subspecies (subsp.) paracasei, Lactobacillus delbrueckii subsp. bulgaricus, Acetobacter ghanensis, Acetobacter fabarum, Acetobacter subsp., Leuconostoc pseudomesenteroides, and Leuconostoc mesenteroides subsp. mesenteroides. Some isolates were tolerant of acid and bile salt, some strains were resistant to antibiotics, and some could inhibit pathogens. In this study, isolates were determined to have probiotic features. As a result of the study, it was determined that some isolates showed probiotic properties and had strong antibacterial activity. Isolates can be use as natural alternative in infections.

Keywords

lactobacillus, leuconostoc, ecetobacter, probiotic properties

Project Number

NKUBAP.23.GA.16.082

References

• Abosereh, N. A., El Ghani, S. A., Gomaa, R. S., & Fouad, M. T. (2016). Molecular Identification of Potential Probiotic Lactic Acid Bacteria Strains Isolated from Egyptian Traditional Fermented Dairy Products. Biotechnology, 15(1/2), 35. https://doi.org/10.3923/biotech.2016.35.43
• Akpinar, A., & Yerlikaya, O. (2021). Some potential beneficial properties of Lacticaseibacillus paracasei subsp. paracasei and Leuconostoc mesenteroides strains originating from raw milk and kefir grains. Journal of Food Processing and Preservation, 45(12), e15986. https://doi.org/10.1111/jfpp.15986
• Aldrete-Tapia, A., Escobar-Ramírez, M. C., Tamplin, M. L., & Hernández-Iturriaga, M. (2014). High-throughput sequencing of microbial communities in Poro cheese, an artisanal Mexican cheese. Food microbiology, 44, 136-141. https://doi.org/10.1016/j.fm.2014.05.022
• Allameh, S. K., Daud, H., Yusoff, F. M., Saad, C. R., & Ideris, A. (2012). Isolation, identification and characterization of Leuconostoc mesenteroides as a new probiotic from intestine of snakehead fish (Channa striatus). Afr J Biotechnol 11:3810–3816. https://doi.org/10.5897/AJB11.1871
• Arici, M., Bilgin, B., Sagdic, O., & Ozdemir, C. (2004). Some characteristics of Lactobacillus isolates from infant faeces. Food Microbiology, 21(1), 19-24. https://doi.org/10.1016/S0740-0020(03)00044-3
• Aswathy, R. G., Ismail, B., John, R. P., & Nampoothiri, K. M. (2008). Evaluation of the probiotic characteristics of newly isolated lactic acid bacteria. Appl Biochem Biotech 151:244–255. https://doi.org/10.1007/s12010-008-8183-6
• Beasley, S. S., & Saris, P. E. J. (2004). Nisin-producing Lactococcus lactis strains from human milk. Appl. Environ. Microbiol., 70: 5051- 5053. https://doi.org/10.1128/AEM.70.8.5051-5053.2004
• Buttriss, J. (1997). Nutritional properties of fermented milk products. International Journal of Dairy Technology, 50(1), 21-27. https://doi.org/10.1111/j.1471-0307.1997.tb01731.x
• Chang, J. H., Shim, Y. Y., Cha, S. K., & Chee, K. M. (2010). Probiotic characteristics of lactic acid bacteria isolated from kimchi. J. Appl. Microbiol., 109: 220–230. https://doi.org/10.1111/j.1365-2672.2009.04648.x
• Charteris, W. P., Kelly, P. M., Morelli, L., & Collins, J. K. (1998). Development and application of an in vitro methodology to determine the transit tolerance of potentially probiotic Lactobacillus and Bifidobacterium species in the upper human gastrointestinal tract. Journal of applied microbiology, 84(5), 759-768. https://doi.org/10.1046/j.1365-2672.1998.00407.x
• Coeuret, V., Dubernet, S., Bernardeau, M., Gueguen, M., & Vernoux, J. P. (2003). Isolation, characterisation and identification of lactobacilli focusing mainly on cheeses and other dairy products. Le Lait, 83(4), 269-306. https://doi.org/10.1051/lait:2003019
• Demirok, N. T., Durak, M. Z., & Arıcı, M. (2021). Probiotic Lactobacilli İn Faeces Of Breastfed Babies. Food Science And Technology. https://doi.org/10.1590/fst.24821
• De Paula, A. T., Jeronymo-Ceneviva, A. B., Silva, L. F., Todorov, S. D., Franco, B. D. G. M., & Penna, A. L. B. (2015). Leuconostoc mesenteroides SJRP55: a potential probiotic strain isolated from Brazilian water buffalo mozzarella cheese. Annals of Microbiology, 65(2), 899-910. https://doi.org/10.1007/s13213-014-0933-9
• Erginkaya, Z., Turhan, E. U., & Tatlı, D. (2018). Determination of antibiotic resistance of lactic acid bacteria isolated from traditional Turkish fermented dairy products. Iranian journal of veterinary research, 19(1), 53. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5960774/pdf/ijvr-19-053.pdf
• Garofalo, C., Osimani, A., Milanović, V., Aquilanti, L., De Filippis, F., Stellato, G., ... & Clementi, F. (2015). Bacteria and yeast microbiota in milk kefir grains from different Italian regions. Food microbiology, 49, 123-133. https://doi.org/10.1016/j.fm.2015.01.017
• Gopal, P. K., Prasad, J., Smart, J., & Gill, H. S. (2001). In-vitro adherence properties of Lactobacillus rhamnosus DR20 and Bifidobacterium lactis DR10 strains and their antagonistic activity against an enterotoxigenic Escherichia coli. International Journal of Food Microbiology, 67, 207–216. https://doi.org/10.1016/S0168-1605(01)00440-8
• Haghshenas, B., Nami, Y., Abdullah, N., Radiah, D., Rosli, R., & Khosroushahi, A. Y. (2015). Anticancer impacts of potentially probiotic acetic acid bacteria isolated from traditional dairy microbiota. LWT-food Science and Technology, 60(2), 690-697. https://doi.org/10.1016/j.lwt.2014.09.058
• Irigoyen, A., Ortigosa, M., Juansaras, I., Oneca, M., & Torre, P. (2007). Influence of an adjunct culture of Lactobacillus on the free amino acids and volatile compounds in a Roncal-type ewe’s-milk cheese. Food chemistry, 100(1), 71-80. https://doi.org/10.1016/j.foodchem.2005.09.011
• Katla, A. K., Kruse, H., Johnsen, G., & Herikstad, H. (2001). Antimicrobial susceptibility of starter culture bacteria used in Norwegian dairy products. International journal of food microbiology, 67(1), 147-152. https://doi.org/10.1016/S0168-1605(00)00522-5
• Kolacek, S., Hojsak, I., Canani, R. B., Guarino, A., Indrio, F., Pot, B., ... & Weizman, Z. (2017). Commercial probiotic products: a call for improved quality control. A position paper by the ESPGHAN Working Group for Probiotics and Prebiotics. Journal of pediatric gastroenterology and nutrition, 65(1), 117-124. https://doi.org/ 10.1097/MPG.0000000000001603
• Kotsou, M. G., Mitsou, E. K., Oikonomou, I. G., & Kyriacou, A. A. (2008). In vitro assessment of probiotic properties of Lactobacillus strains from infant gut microflora. Food Biotechnology, 22(1), 1-17. https://doi.org/10.1080/08905430701707844
• Manolopoulou, E., Sarantinopoulos, P., Zoidou, E., Aktypis, A., Moschopoulou, E., Kandarakis, I. G., & Anifantakis, E. M. (2003). Evolution of microbial populations during traditional Feta cheese manufacture and ripening. International Journal of Food Microbiology, 82(2), 153-161. https://doi.org/10.1016/S0168-1605(02)00258-1
• Maragkoudakis, P. A., Zoumpopoulou, G., Miaris, C., Kalantzopoulos, G., Pot, B., & Tsakalidou, E. (2006). Probiotic potential of Lactobacillus strains isolated from dairy products. Int. Dairy J, 16: 189-199. https://doi.org/10.1016/j.idairyj.2005.02.009
• Minelli, E. B., Benini, A., Marzotto, M., Sbarbati, A., Ruzzenente, O., Ferrario, R., & Dellaglio, F. (2004). Assessment of novel probiotic Lactobacillus casei strains for the production of functional dairy foods. International Dairy Journal, 14(8), 723-736. https://doi.org/10.1016/j.idairyj.2004.01.007
• Nakamura, S., Kuda, T., An, C., Kanno, T., Takahashi, H., & Kimura, B. (2012). Inhibitory effects of Leuconostoc mesenteroides 1RM3 isolated from Narezushi, a fermented fish with rice, on Listeria monocytogenes infection to Caco-2 cells and A/J mice. Anaerobe, 18(1), 19– 24. https://doi.org/10.1016/j.anaerobe.2011.11.006
• Ouwehand, A. C., Kirjavainen, P. V., Shortt, C., & Salminen, S. (1999). Probiotics: Mechanisms and established effects. International Dairy Journal, 9, 43–52. https://doi.org/10.1016/S0958-6946(99)00043-6
• Patra, A., Sil, J., & Das, B. K. (2011). Isolation and characterization of dominant lactic acid bacteria from Dahi at Medinipur and evaluation of their antibacterial activity. Internet Journal of Food Safety, 13:157-163.
• PereaVelez, M., Hermans, K., Verhoeven, T. L., Lebeer, S. E., Vanderleyden, J., De Keersmaecker S. C. (2007). Identification and characterization of starter lactic acid bacteria and probiotics from Columbian dairy products. J. Appl. Microbiol. , 103, 666–674. https://doi.org/10.1111/j.1365-2672.2007.03294.x
• Pérez, P. F., Minnaard, Y., Disalvo, E. A., & De Antoni, G. L. (1998). Surface properties of bifidobacterial strains of human origin. Applied and Environmental Microbiology, 64(1), 21-26. https://doi.org/ 10.1128/aem.64.1.21-26.1998
• Pisano, M. B., Fadda, M. E., Viale, S., Deplano, M., Mereu, F., Blažić, M., & Cosentino, S. (2022). Inhibitory effect of Lactiplantibacillus plantarum and Lactococcus lactis autochtonous strains against Listeria monocytogenes in a laboratory cheese model. Foods, 11(5), 715. https://doi.org/10.3390/foods11050715
• Prasad, J., Gill, H., Smart, J., & Gopal, P. K. (1998). Selection and characterisation of Lactobacillus and Bifidobacterium strains for use as probiotics. International Dairy Journal, 8(12), 993-1002. https://doi.org/10.1016/S0958-6946(99)00024-2
• Raghavendra, P., & Halami, P. M. (2009). Screening, selection and characterization of phytic acid degrading lactic acid bacteria from chicken intestine. Int J Food Microbiol 133:129–134. https://doi.org/10.1016/j.ijfoodmicro.2009.05.006
• Rani, P.S., & Agrawal, R. (2008). Effect on cellular membrane fatty acids in the stressed cells of Leuconostoc mesenteroides: A native probiotic lactic acid bacteria. Food Biotechnol. 22, 47–63. https://doi.org/10.1080/08905430701863977
• Ryu, E. H., & Chang, H. C. (2013). In vitro study of potentially probiotic lactic acid bacteria strains isolated from kimchi. Ann. Microbiol., 63, 1387–1395. https://link.springer.com/article/10.1007/s13213-013-0599-8
• Sadrani, H., Dave, J., & Manuel Vyas, BR. (2014). Screening of Potential Probiotic Lactobacillus Strains Isolated From Fermented Foods, Fruits and of Human Origin. Asian Journal of Pharmaceutical and Clinical Research, 7 (2),216-225. https://citeseerx.ist.psu.edu/document?repid=rep1&type=pdf&doi=e9e14575ef3a79a8e357923982b5e9c0051c460d
• Salminen, S., von Wright, A., Morelli, L., Marteau, P., Brassart, D., de Vos, W.M., Fonden, R., Saxelin, M., Collins, K., Mogensen, G., Birkeland, S.-E., Mattila-Sandholm, T., (1998). Demonstration of safety of probiotics—a review. Int. J. Food Microbiol. 44, 93–106. https://doi.org/10.1016/S0168-1605(98)00128-7
• Sarikkha, P., Nitisoravut, R., Poljungreed, I., & Boonyarattanakalin, S. (2015). Identification of bacteria and yeast communities in a Thai sugary kefir by Polymerase Chain Reaction-Denaturing Gradient Gel Electrophoresis (PCR-DGGE) analyses. The Journal of Industrial Technology, 11(2), 25-39. http://j.cit.kmutnb.ac.th/wp-content/uploads/2015/10/581102-3-1-023-58-p25-39.pdf
• Schillinger, U., Guigas, C., & Holzapfel, W. H. (2005). In vitro adherence and other properties of lactobacilli used in probiotic yoghurt-like products. International Dairy Journal, 15(12), 1289-1297. https://doi.org/10.1016/j.idairyj.2004.12.008
• Simova, E., Beshkova, D., Angelov, A., Hristozova, T., Frengova, G., & Spasov, Z. (2002). Lactic acid bacteria and yeasts in kefir grains and kefir made from them. Journal of Industrial Microbiology and Biotechnology, 28(1), 1-6. https://doi.org/ 10.1038/sj/jim/7000186
• Seo, B.J., Rather, I. A., Kumar, V. J., Choi, U. H., Moon, M. R., Lim, J. H., & Park, Y. H. (2012). Evaluation of Leuconostoc mesenteroides YML003 as a probiotic against low-pathogenic avian influenza (H9N2) virus in chickens. J. Appl. Microbiol. 113, 163–171. https://doi.org/10.1111/j.1365-2672.2012.05326.x
• Tambekar, D. H., & Bhutada, S. A. (2010). Acid and bile tolerance, antibacterial activity, antibiotic resistance and bacteriocins activity of probiotic Lactobacillus species, Recent Research in Science and Technology, 2: 94-98.
• Todorov, S. D., Leblanc, J. G., & Franco, B. D. (2012). Evaluation of the probiotic potential and effect of encapsulation on survival for Lactobacillus plantarum ST16Pa isolated from papaya. World J Microbiol Biotechnol 28:973–984. https://doi.org/
• Temmerman, R., Pot, B., Huys, G., & Swings, J. (2003). Identification and antibiotic susceptibility of bacterial isolates from probiotic products. International Journal of Food Microbiology, 81(1), 1-10.. https://doi.org/ 10.1007/s11274-011-0895-z
• Tynkkynen, S., Singh, K.V., & Varmanen, P., (1998). Vancomycin resistance factor of Lactobacillus rhamnosus GG in relation to enterococcal vancomycin resistance Ž. Õan genes. Int. J. Food Microbiol. 41, 195–204. https://doi.org/10.1016/S0168-1605(98)00051-8
• Vieco-Saiz, N., Belguesmia, Y., Raspoet, R., Auclair, E., Gancel, F., Kempf, I., & Drider, D. (2019). Benefits and inputs from lactic acid bacteria and their bacteriocins as alternatives to antibiotic growth promoters during food-animal production. Frontiers in microbiology, 10, 57. https://doi.org/10.3389/fmicb.2019.00057
• Waldherr, F. W., Doll, V. M., Meißner, D., & Vogel, R. F. (2010). Identification and characterization of a glucan-producing enzyme from Lactobacillus hilgardii TMW 1.828 involved in granule formation of water kefir. Food Microbiology, 27(5), 672-678. https://doi.org/10.1016/j.fm.2010.03.013
• Xue, J., Yang, Y., Wang, Z., Guo, Y., & Shao, Y. (2018). Bacterial Diversity in Chinese Rushan Cheese From Different Geographical Origins. Frontiers in microbiology, 9, 1920. https://doi.org/10.3389/fmicb.2018.01920
• Zamfir, M., Vancanneyt, M., Makras, L., Vaningelgem, F., Lefebvre, K., Pot, B., ... & De Vuyst, L. (2006). Biodiversity of lactic acid bacteria in Romanian dairy products. Systematic and applied microbiology, 29(6), 487-495. https://doi.org/10.1016/j.syapm.2005.10.002