TURŞU KÖKENLİ LAKTİK ASİT BAKTERİLERİNİN STARTER KÜLTÜR ÖZELLİKLERİ VE ANTİFUNGAL AKTİVİTELERİNİN İNCELENMESİ

Öz

Dünyada yaygın olarak tüketilen fermente gıdalar insan sağlığı için büyük öneme sahiptir. Fermente ürünlerin raf ömürlerinin uzatılması ve insan sağlığına olumlu etkilerinin artırılması için standart üretimlere ihtiyaç duyulmaktadır. Bu sebeple, fermente ürünlerin üretiminde kullanılabilecek starter kültürlere duyulan ihtiyaç giderek artmaktadır. Bu çalışmada, 5 laktik asit bakterisinin (Lactobacillus brevis, Lactobacillus plantarum, Lactobacillus paracasei, Pediococcus parvulus ve Leuconostoc holzapfel) 9 maya izolatı üzerinde antifungal aktivitesi, antibiyotik dirençleri, farklı sıcaklık, pH ve tuz konsantrasyonlarında gelişim, arginin hidrolizi etme ve glukozdan gaz oluşturma yetenekleri incelenmiştir. Laktik asit bakterilerinin Hanseniaspora opuntiae, Kazachstania exigua ve Pichia fermentans hariç tüm mayalar üzerinde antifungal etkiye sahip olduğu, 10 ve 25 oC’de, 3.9 ve 5 pH'da ve %4 tuz konsatrasyonunda gelişim gösterdikleri tespit edilmiştir. Bunun yanında, izolatların tamamı vankomisine direnç göstermiştir. Çalışma sonuçları değerlendirildiğinde L. brevis, L. plantarum, L. paracasei suşlarının standart turşu üretimi ve antifungal etki açısından starter kültür olarak kullanılabileceği görülmektedir.

Anahtar Kelimeler

• Laktik asit bakterisi
• antifungal aktivite
• starter kültür
• turşu

INVESTIGATION OF STARTER CULTURE PROPERTIES AND ANTIFUNGAL ACTIVITIES OF PICKLE-DERIVED LACTIC ACID BACTERIA

Öz

Fermented foods, which are widely consumed around the world, are of great importance for human health. Standard production should be carried out in order to extend the shelf life of fermented products and increase their positive effects on human health. Therefore, there is a need for starter cultures that can be used in the production of fermented products. In this study, antifungal activity on 9 yeast isolates, antibiotic resistance, growth at different temperatures, pH and salt concentrations, arginine hydrolysis and gas production from glucose of 5 lactic acid bacteria (Lactobacillus brevis, Lactobacillus plantarum, Lactobacillus paracasei, Pediococcus parvulus, Leuconostoc holzapfel) were investigated. The lactic acid bacteria have antifungal effects on all yeasts except Hanseniaspora opuntiae, Kazachstania exigua and Pichia fermentans, and they grow at 10 and 25 oC, 3.9 and 5 pH and 4% salt concentration. In addition, all of the isolates showed resistance to vancomycin. The results indicated that L. brevis, L. plantarum, L. paracasei strains can be used as starter cultures in term of standart pickle production and antifungal effect.

Anahtar Kelimeler

• Lactic acid bacteria
• antifungal activity
• starter culture
• pickles

Kaynakça

1. Abouloifaa, H., Gaamouchea, S., Roknia, Y., Hasnaouia, I., Bellaouchia, R., Ghabboura, N., Karbouneb, S., Brascac, M., D'Hallewind, G., Ben Salahe, R., Saalaouia, E., Asehraoua, A. (2021). Antifungal activity of probiotic Lactobacillus strains isolated from natural fermented green olives and their application as food bio-preservative. Biol Control, 152, 104450.
2. Akdeniz Oktay, B., Özbaş, Z.Y. (2020). The effects of fermented foods on human health. GIDA, 45(6): 1215-1226.
3. Aktan, N., Yücel, U., Kalkan, H. (2003). Pickle technology. Ege University Vocational School Publications, İzmir-Turkey.
4. Balouiri, M., Sadiki, M., iIbnsouda, S.K. (2016). Methods for in vitro evaluating antimicrobial activity: A review. Journal of Pharmaceutical Analysis, 6(2): 71-79.
5. Barbosa, M.S., Todorov, S.D., Ivanova, I.V., Belguesmia, Y., Choiset, Y., Rabesona, H., Chobert, J.M., Haertlé, T., Franco, B.D.G.M. (2016). Characterization of a two-peptide plantaricin produced by Lactobacillus plantarum MBSa4 isolated from Brazilian salami. Food Control, 60: 103-112. https://doi.org/https://doi.org/10.1016/j.foodcont.2015.07.029
6. Basdogan, M.G. (2020). Determination of probiotic potential of lactic acid bacteria isolated from pickles produced traditionally. Master's thesis, Ege University Graduate School of Natural and Applied Sciences, İzmir, Turkey, 98 p.
7. Bayrak, N. (2019). Investigation of some probiotic properties of lactic acid bacteria obtained from pickle. Master's thesis, Atatürk University Graduate School of Natural and Applied Sciences Department of Food Engineering, Erzurum, Turkey, 73 p.
8. Bulgasem, Y.B. Mohd, N.L., Zaiton, H., Wan Mohtar, W.Y., Sumaya, G.F. (2016). Antifungal activity of lactic acid bacteria strains ısolated from natural honey against pathogenic candida species. Mycobiology, 44(4): 302-309.

9. Cetin, B. (2011). Production of probiotic mixed pickles (tursu) and microbiological properties. African Journal of Biotechnology, 10(66): 14926-14931.
10. Chang, H.C. (2018). Healthy and safe Korean traditional fermented foods: kimchi and chongkukjang. Journal of Ethnic Foods, 5(3): 161-166.
11. Chen, Y., Ying, T.J. (2017). Isolation and ıdentification of lactic acid bacteria from xiaoshan pickle radish, a traditional fermented vegetable. Food Sci Technol Res, 23(1): 129-136.
12. Crowley, S., Mahony, J., Sinderen, D. (2013). Current perspectives on antifungal lactic acid bacteria as natural bio-preservatives. Trends in Food Science & Technology, 33(2): 93-109.
13. Dallal, M.M.S., Zamaniahari, S., Davoodabadi, A., Hosseini, M., Rajabi, Z. (2017). Identification and characterization of probiotic lactic acid bacteria isolated from traditional persian pickled vegetables. GMS Hygiene and Infection Control, 12, Article Number: Doc15, DOI: 10.3205/dgkh000300.
14. Demirgul, F., Sagdıc, O. (2018). The effect of fermented milk products on human health. European Journal of Science and Technology, 13: 45-53.
15. Diker, A., Akar, E., Akgun, R., Tarhan, Ö. (2021). Investigation of Some Quality Parameters in Cucumber Pickles Prepared by Different Types of Vinegars. Journal of Food and Feed Scence – Technology, 26: 30-39.
16. Drosinos, E.H., Paramithiotis, S., Kolovos, G., Tsikouras, I., Metaxopoulos, I. (2007). Phenotypic and technological diversity of lactic acid bacteria and staphylococci isolated from traditionally fermented sausages in Southern Greeece. Food Microbiol, 24: 260-270.
17. Dundar, R. (2017). Isolation and identification of lactic acid bacteria from traditionally produced home-type pickle. Master's thesis, Atatürk University Graduate School of Natural and Applied Sciences Department of Food Engineering, Erzurum, Turkey, 65 p.
18. Elmaci, S.B., Tokatli, M., Dursun, D., Ozcelik, F., Sanlibaba, P. (2015). Phenotypic and genotypic identification of lactic acid bacteria isolated from traditional pickles of the Cubuk region in Turkey. Folia Microbiol, 60(3): 241-251.
19. Erdem Buyukkiraz, M., Avcı, E., Kahraman, N., Kesmen, Z. (2020). Identification of spoilage yeasts isolated from some foods. Çukurova J. Agric. Food Sci., 35(1): 15-28.
20. EUCAST (European committee on antimicrobial susceptibility testing), 2021. Disk diffusion method for antimicrobial susceptibility testing, Version 9.0.
21. Evren, M., Apan, M., Tutkun, E., Evren, S. (2011). Lactic acid bacteria found in traditional fermented foods. Elektronik Mikrobiyoloji Dergisi, 9(1): 11-17.
22. Gezginc, Y., Inanc, O. (2021). Chemical, microbiological and sensory properties of acur (cucumis melo var. flexuosus) pickles produced using salt and vinegar at different concentrations. International Journal of Innovative Approaches in Agricultural Research, 5(3): 290-302.
23. Guo, H., Pan, L., Li, L., Lu, J., Kwok, L., Menghe, B., Zhang, H., Zhang, W. (2017). Characterization of antibiotic resistance genes from lactobacillus isolated from traditional dairy products. J Food Sci, 82(3): 724-730.
24. Gutiérrez-Cortés, C., Suarez, H., Buitrago, G., Nero, L.A., Todorov, S.D. (2018). Characterization of bacteriocins produced by strains of Pediococcus pentosaceus isolated from Minas cheese. Ann Microbiol, 68(6): 383-398.
25. Hammes, W.P., Vogel, R.F. (1995). The genus Lactobacillus. Wood, B.J.B., Holzapfel, W.H. ed. Glasgow, Scotland: Academic & Professional, pp 19–54.
26. Hébert, E.M., Raya, R.R., Tailliez, P., de Giori, G.S. (2000). Characterization of natural isolates of Lactobacillus strains to be used as starter cultures in dairy fermenation. Int J Food Microbiol, 59: 19-27.
27. Hernández, A., Pérez-Nevado, F., Ruiz-Moyano, S., Serradilla, M.J., Villalobos, M.C., Martín, A., Córdoba, M.G. (2018). Spoilage yeasts: What are the sources of contamination of foods and beverages? International Journal of Food Microbiology, 286: 98-110.
28. Hittinger, C.T., Steele, J.L., Ryder, D.S. (2018). Diverse yeasts for diverse fermented beverages and foods. Curr Opin Biotechnol, 49: 199-206.
29. Islam, M.S., Choi, H. (2009). Antidiabetic effect of korean traditional Baechu (Chinese cabbage) kimchi in a type 2 diabetes model of rats. J Med Food, 12: 292–297.
30. Karasu, N., Şimşek, Ö., Çon, AH. (2010). Technological and probiotic characteristics of Lactobacillus plantarum strains isolated from traditionally produced fermented vegetables. Ann Microbiol, 60: 227–234.
31. Kask, S., Adamberk, K., Orłowski, A., Vogensen, F.K., Møller, P.L., Ardo, Y., Paalme, T. (2003). Physiological properties of Lactobacillus paracasei, L. danicus and L. curvatus strains isolated from Estonian semi-hard cheese. Food Research International 36: 1037-1046.
32. Kaur, M., Singh, H., Jangra, M., Kaur, L., Jaswal, P., Dureja, C., Pinnaka, A.K. (2017). Lactic acid bacteria isolated from yak milk show probiotic potential. Appl Microbiol Biotechnol, 101(20): 7635-7652.
33. Khodaei, M., Soltani Nezhad, S. (2018). Isolation and molecular identification of bacteriocin producing enterococci with broad antibacterial activity from traditional dairy products in Kerman province of Iran. Korean Journal for Food Science of Animal Resources, 38(1): 172-179.
34. Kim, B., Park, K.Y., Kim, H.Y., Ahn, S.C., Cho, E.J. (2011). Antiaging effects and mechanisms of kimchi during fermentation under stress-induced premature senescence cellular system. Food Science and Biotechnology, 20: 643–649.
35. Kim, E.K., An, S.Y., Lee, M.S., Kim, T.H., Lee, H.K., Hwang, W.S., Lee, K.W. (2011). Fermented kimchi reduces body weight and improves metabolic parameters in overweight and obese patients. Nutr Res, 31: 436–443.
36. Kostinek, M., Specht, I., Edward, V.A., Pinto, C., Egounlety, M., Sossa, C., Mbugua, S., Dortu, C., Thonart, P., Taljaard, L., Mengu, M., Franz, C.M.A.P., Holzapfel, W.H. (2007). Characterisation and biochemical properties of predominant lactic acid bacteria from fermenting cassava for selection as starter cultures. Int J Food Microbiol, 114: 342-351.
37. Lee, H.A., Kim, H., Lee, K.W., Park, K.Y. (2016). Dietary nanosized Lactobacillus plantarum enhances the anticancer effect of kimchi on azoxymethane and dextran sulfate sodium-induced colon cancer in C57BL/6J mice. J Environ Pathol Toxicol Oncol, 35(2): 147–159.
38. Lee, M.E., Jang, J.Y., Lee, J.H., Park, H.W., Choi, H.J., Kim, T.W. (2015). Starter cultures for kimchi fermentation. J Microbiol Biotechnol, 25(5): 559-568.
39. Lee, Y.M., Kwan, M.J., Kim, J.K., Suh, H.S., Choi, J.S., Song, Y.O. (2004). Isolation and identification of active principle in Chinese cabbage kimchi responsible for antioxidant effect. Korean Journal of Food Science and Technology, 36: 129–133.
40. Liasi, S.A., Azmi, T.I., Hassan, M.D., Shuhaimi, M., Rosfarizan, M., Ariff, A.B. (2009). Antimicrobial activity and antibiotic sensitivity of three isolates of lactic acid bacteria from fermented fish product, Budu. Malaysian Journal of Microbiology, 5(1): 33-37.
41. Magaldi, S., Mata-Essayag, S., de Caprilesa, C.H., Perez, C., Colella, M.T., Olaizola, C., Ontiveros, Y. (2004). Well diffusion for antifungal susceptibility testing. Int J Infect Dis, 8(1): 39-45.
42. Meral, H., Korukluoglu, M. (2014). Antibiotic resistance mechanisms of lactic acid bacteria. Journal of Agricultural Faculty of Uludag University, 28(2): 71-82.
43. Misihairabgwi, J., Cheikhyoussef, A. (2017). Traditional fermented foods and beverages of Namibia. Journal of Ethnic Foods, 4(3): 145-153.
44. Nagpal, R., Wang, S., Ahmadi, S., Hayes, J., Gagliano, J., Subashchandrabose, S., Kitzman, D.W., Becton, T., Read, R., Yadav, H. (2018). Human-origin probiotic cocktail increases short-chain fatty acid production via modulation of mice and human gut microbiome. Scientific reports, 8(1): 12649.
45. Özogul, F., Özogul, Y. (2007). The ability of biogenic amines and ammonia production by single bacterial cultures. Eur Food Res Technol, 225(3-4): 385-394.
46. Papamanoli, E., Tzanetakis, N., Litopoulou-Tzanetaki, E., Kotzekidou, P. (2003). Characterization of lactic acid bacteria isolated from a Greek dry-fermented sausage in respect of their technological and probiotic properties. Meet Science, 65: 859-867.
47. Randazzo, C.L., Restuccia, C., Romano, A.D., Caggia, C. (2004). Lactobacillus casei, dominant species in naturally fermented Sicilian green olives. Int J Food Microbiol, 90: 9-14.
48. Ribes, S., Fuentes, A., Talens, P., Barat, J.M. (2018). Prevention of fungal spoilage in food products using natural compounds: A review. Crit Rev Food Sci Nutr, 58(12): 2002-2016.
49. Saez, G.D., Flomenbaum, L., Zarate, G. (2018). Lactic acid bacteria from Argentinean fermented foods: isolation and characterization for their potential use as starters for fermentation of vegetables. Food Technol Biotechnol, 56(3): 398-410.
50. Sanchez, I., Palop, L., Ballesteros, C. (2000). Biochemical characterization of lactic acid bacteria isolated fromspontaneous fermentation of ‘Almagro’ eggplants. Int J Food Microbiol, 59: 9–17.
51. Şimşek, Ö., Çon, A.H., Tulumoğlu, Ş. (2006). Isolating lactic starter cultures with antimicrobial activity for sourdough processes. Food Control, 17: 263- 270.
52. Tang, Y.Y., Zhou, X.R., Huang, S.L., Li, Y.Z., Long, M., Zhao, X., Du, M.Y. (2019). Microbial community analysis of different qualities of pickled radishes by Illumina MiSeq sequencing. Journal of Food Safety, 39(2): 1-8.
53. Terzic-Vidojevic, A., Tolinacki, M., Nikolic, M., Lozo, J., Begovic, J., Gurban oglu Gulahmadov, S., Kuliev, A.A., Dalgalarrondo, M., Chobert, J.M., Haertlé, T., Topisirovic, L. (2009). Phenotypic and genotypic characterization of lactic acid bacteria isolated from Azerbaijani traditional dairy products. Afr J Biotechnol, 8: 2576-2588.
54. Tokatli, M. (2013). Identification of lactic acid bacteria isolated from pickles in Ankara Çubuk region, determination of their technological and functional properties and their potential for using as a starter culture. Ph. D. Thesis, Ankara University Graduate School of Natural and Applied Sciences Department of Food Engineering, Ankara, Turkey, 183 p.
55. Valgas, C., de Souza, S.M., Smânia, E.F.A., Smânia Jr, A. (2007). Screening methods to determine antibacterial activity of natural products. Braz J Microbiol, 38: 369-380.
56. Wu, C.J., Lin, X.P., Tong, L., Dai, C.W., Lv, H., Zhou, X.H., Zhang, J. (2021). In vitro evaluation of lactic acid bacteria with probiotic activity isolated from local pickled leaf mustard from Wuwei in Anhui as substitutes for chemical synthetic additives. Open Chemistry, 19(1): 755-771.
57. Xia, Y., Liu, X., Wang, G., Zhang, H., Xiong, Z., Sun, Y., Ai, L. (2017). Characterization and selection of Lactobacillus brevis starter for nitrite degradation of Chinese pickle. Food Control, 78: 126-131.
58. Yildiz, H. (2011). Isolation-identification of lactic acid bacteria and yeasts from pickle and olive and determination of some properties of isolates. Ph.D. Thesis, Atatürk University Graduate School of Natural and Applied Sciences Department of Food Engineering, Erzurum, Turkey, 134 p.
59. Yildiz, S. (2019). Investigation of starter culture and exopolysaccharide production characteristics of yoghurt derived lactic acid bacteria. Master's thesis, Atatürk University Graduate School of Naturel and Applied Sciences Department and Food Engineering, Erzurum, Turkey, 70 p.
60. Zeng, Y., Li, Y., Wu, Q.P., Zhang, J.M., Xie, X.Q., Ding, Y., Cai, S.Z., Ye, Q.H., Chen, M.T., Xue, L., Wu, S., Zeng, H.Y., Yang, X.J., Wang, J. (2020). Evaluation of the antibacterial activity and probiotic potential of lactobacillus plantarum isolated from chinese homemade pickles. Canadian Journal of Infectious Diseases & Medical Microbiology, Article ID 8818989, https://doi.org/10.1155/2020/8818989.