The antifungal effect of di-acetyl produced by the isolated lactobacilli from traditional dairy products

Document Type : Research Paper

Authors

1 Department of Microbiology, Faculty of Sciences, Neyshabur Branch, Islamic Azad University, Neyshabur, Iran

2 Department of Microbiology, Faculty of Sciences, Kerman Branch, Islamic Azad University, Kerman, Iran

3 Department of Animal Science, Kashmar Branch, Islamic Azad University, Kashmar, Iran

Abstract

Filamentous fungi or molds are the major group of spoilage microorganisms responsible for significant economic losses and serious health risks in the food chain. This study was conducted to evaluate the antifungal effect of di-acetyl produced by Lactobacillus species isolated from traditional fermented product against Penicillium sp. Thirty-three samples of traditional yoghurt, dough, and kefir were cultured, then the isolates were identified by molecular methods (specific PCR and 16S rRNA sequence analysis) and biochemical test. The effects of different media were analyzed in biomass and di-acetyl production. Antifungal activity of di-acetyl was assessed against Penicillium sp. Out of 16 isolates from kefir, yoghurt, and dough, 10 lactic acid bacteria (LAB) isolates were identified as L. casei by biochemical test and molecular methods. MR-VP medium has exhibited the best effect on biomass and di-acetyl production by isolates. GC analysis showed that yoghurt- LABs producing of high di-acetyl have a considerable inhibitory effect on Penicillium sp. The antifungal properties of di-acetyl generated by novel L. casei isolates seem to present a promising advantage, indicating the potential of di-acetyl as a bio-preservative in the food and dairy industries. It may recommended to apply the di-acetyl in fermented product-surface papers to prevent mildew cause by Penicillium sp.

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Main Subjects


Awuchi, C. G., Ondari, E. N., Nwozo, S., Odongo, G. A., Eseoghene, I. J., Winomuhwezi, H., Ogbonna, C. U., Upadhyay, A. K., Adeleye, A. O., & Okpala, C. O. R. (2022). Mycotoxins’ toxicological mechanisms involving humans, livestock and their associated health concerns: A review. Toxins, 14(3), 167. https://doi.org/10.3390/toxins14030167
Brul, S., & Coote, P. (1999). Preservative agents in foods: Mode of action and microbial resistance mechanisms. International Journal of Food Microbiology, 50(1-2), 1-17. https://doi.org/10.1016/S0168-1605(99)00072-0
Calvo, H., Mendiara, I., Pilar Gracia, A., Venturini, M. E. (2020). Antifungal activity of the volatile organic compounds produced by Bacillus velezensis strains against postharvest fungal pathogens. Postharvest Biology and Technology, 166, 111208. https://doi.org/10.1016/j.postharvbio.2020.111208
Chen, H., Yan, X., Du, G., Guo, Q., Shi, Y., Chang, J., & Yue, T. (2021). Recent developments in antifungal lactic acid bacteria: Application, screening methods, separation, purification of antifungal compounds and antifungal mechanisms. Critical Reviews in Food Science and Nutrition, 63(15), 2544–2558. https://doi.org/10.1080/10408398.2021.1977610
Clinical and Laboratory Standards Institute. (2012). Performance standards for antimicrobial susceptibility testing (CLSI M100-S22). https://clsi.org/blog/2012/01/13/clsi-publishes-2012-antimicrobial-susceptibility-testing-standards/
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. https://doi.org/10.1016/j.tifs.2013.07.004
Dali, D. K. D., Deschamps, A. M., & Richard-Forget, F. (2010). Lactic acid bacteria—potential for control of mould growth and mycotoxins: A review. Food Control, 21(4), 370–380. https://doi.org/10.1016/j.foodcont.2009.07.011
Danova, S., Petrov, K., Pavlov, P., & Petrova, P. (2005). Isolation and characterization of Lactobacillus strains involved in koumiss fermentation. International Journal of Dairy Technology, 58(2), 100–105. https://doi.org/10.1111/j.1471-0307.2005.00194.x
Delavenne, E., Ismail, R., Pawtowski, A., Mounier, J., Barbier, G., & Le Blay, G. (2012). Assessment of lactobacilli strains as yogurt bioprotective cultures. Food Control, 30(1), 206–213. https://doi.org/10.1016/j.foodcont.2012.06.043
Erfani, A., Shakeri, G., Moghimani, M., & Afshari, A. (2024). Specific species of probiotic bacteria as bio-preservative cultures for control of fungal contamination and spoilage in dairy products. International Dairy Journal, 151, 105863. https://doi.org/10.1016/j.idairyj.2023.105863
Gerez, C. L., Torres, M. J., Font de Valdez, G., & Rollan, G. (2013). Control of spoilage fungi by lactic acid bacteria. Biological Control, 64, 231–237. https://doi.org/10.1016/j.biocontrol.2012.11.008
Godana, E. A., Yang, Q., Zhang, X., Zhao, L., Wang, K., Dhanasekaran, S., & Zhang, H. (2023). Biotechnological and biocontrol approaches for mitigating postharvest diseases caused by fungal pathogens and their mycotoxins in fruits: A review. Journal of Agricultural and Food Chemistry, 71(46), 17584–17596. https://doi.org/10.1021/acs.jafc.3c06448
Gouy, M., Guindon, S., & Gascuel, O. (2010). A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution, 27(2), 221–224. https://doi.org/10.1093/molbev/msp259
Hossain, T. J. (2024). Methods for screening and evaluation of antimicrobial activity: A review of protocols, advantages, and limitations. European Journal of Microbiology and Immunology, 14(2), 97–115. https://doi.org/10.1556/1886.2024.00035
Jay, J. M. (1982). Antimicrobial properties of diacetyl. Applied and Environmental Microbiology, 44(3), 525–532. https://doi.org/10.1128/aem.44.3.525-532.1982
Jyoti, B. D., Suresh, A. K., & Venkatesh, K. V. (2003). Diacetyl production and growth of Lactobacillus rhamnosus on multiple substrates. World Journal of Microbiology & Biotechnology, 19(5), 509–514. https://doi.org/10.1023/A:1025170630905
Kavková, M., Cihlář, J., Dráb, V., & Bár, L. (2021). Differentiation of Penicillium roqueforti from closely related species contaminating cheeses and dairy environment. Fermentation, 7(4), 222. https://doi.org/10.3390/fermentation7040222
Li, Y., Zhao, X., Yao, M., Jia, P., Feng, P., Jin, M., Wang, X., Wang, Y., Zhang, W., Chen, J., & Wen, J. (2023). Mechanism of microbial production of acetoin and 2,3-butanediol optical isomers and substrate specificity of butanediol dehydrogenase. Microbial Cell Factories, 22(1), 165. https://doi.org/10.1186/s12934-023-02163-6
Ling, L., Pang, M., Luo, H., Cheng, W., Jiang, K., & Wang, Y. (2023). Antifungal activity of diacetyl, a volatile organic compound, on Trichoderma lixii F2 isolated from postharvest Lanzhou lily bulbs. Food Bioscience, 51, 102365. https://doi.org/10.1016/j.fbio.2023.102365
Lipińska, L., Klewicki, R., Sójka, M., Bonikowski, R., Żyżelewicz, D., Kołodziejczyk, K., & Klewicka, E. (2018). Antifungal activity of Lactobacillus pentosus ŁOCK 0979 in the presence of polyols and galactosyl-polyols. Probiotics and Antimicrobial Proteins, 10(1), 186–200. https://doi.org/10.1007/s12602-017-9344-0
Marcelli, V., Osimanin, A., & Aquilanti, L. (2024). Research progress in the use of lactic acid bacteria as natural biopreservatives against Pseudomonas spp. in meat and meat products: A review. Food Research International, 196, 115129. https://doi.org/10.1016/j.foodres.2024.115129
Morelli, L., Calleagri, M. L., Vogensen, F. K., & Von Wright, A. (2011). Lactic acid bacteria: Microbiological and functional aspects. In S. Salminen, A. von Wright, & A. Ouwehand (Eds.), Lactic acid bacteria: Microbiological and functional aspects (4th ed., pp. 18-33). CRC Press. https://doi.org/10.1201/9780429057465
Nielsen, J., & Villadsen, J. (1994). Bioreaction engineering principles. Plenum Press.
Oliveira, P. M., Zannini, E., & Arendt, E. K. (2014). Cereal fungal infection, mycotoxins, and lactic acid bacteria mediated bioprotection: From crop farming to cereal products. Journal of Food Microbiology, 37, 78–95. https://doi.org/10.1016/j.fm.2013.06.003
Pawlowska, A. M., Zannini, E., Coffey, A., & Arendt, E. K. (2012). Green preservatives: Combating fungi in the food and feed industry by applying antifungal lactic acid bacteria. In S. Taylor (Ed.), Advances in food and nutrition research (Vol. 66, pp. 217-238). Academic Press. https://doi.org/10.1016/b978-0-12-394597-6.00005-7
Quere, F., Deschamps, A., & Urdaci, M. C. (1997). DNA probe and PCR-specific reaction for Lactobacillus plantarum. Journal of Applied Microbiology, 82(6), 783–790. https://doi.org/10.1046/j.1365-2672.1997.00157.x
Raman, J., Kim, J.-S., Choi, K. R., Eun, H., Yang, D., Ko, Y.-J., & Kim, S.-J. (2022). Application of lactic acid bacteria (LAB) in sustainable agriculture: Advantages and limitations. International Journal of Molecular Sciences, 23(14), 7784. https://doi.org/10.3390/ijms23147784
Russo, P., Arena, M. P., Fiocco, D., Capozzi, V., Drider, D., & Spano, G. (2016). Lactobacillus plantarum with broad antifungal activity: A promising approach to increase safety and shelf-life of cereal-based products. International Journal of Food Microbiology, 247, 48–54. https://doi.org/10.1016/j.ijfoodmicro.2016.04.027
Salas, M. L., Thierry, A., Lemaître, M., Garric, G., Harel-Oger, M., Chatel, M., Lê, S., Mounier, J., Valence, F., & Coton, E. (2018). Antifungal activity of lactic acid bacteria combinations in dairy mimicking models and their potential as bioprotective cultures in pilot scale applications. Frontiers in Microbiology, 9, 1787. https://doi.org/10.3389/fmicb.2018.01787
Santra, H. K., Dutta, R., & Banerjee, D. (2024). Antifungal activity of bio-active cell-free culture extracts and volatile organic compounds (VOCs) synthesised by endophytic fungal isolates of Garden Nasturtium. Scientific Reports, 14(1), 11228. https://doi.org/10.1038/s41598-024-60948-0
Shi, C., & Maktabdar, M. (2022). Lactic acid bacteria as biopreservation against spoilage molds in dairy products - A review. Frontiers in Microbiology, 12, 819684. https://doi.org/10.3389/fmicb.2021.819684
Szczerbiec, D., Piechocka, J., Głowacki, R., & Torzewska, A. (2022). Organic acids secreted by Lactobacillus spp. isolated from urine and their antimicrobial activity against uropathogenic Proteus mirabilis. Molecules, 27(17), 5557. https://doi.org/10.3390/molecules27175557
Temitope, F. P., & Oluchi, U. E. (2015). Studies on the antifungal activity of Lactobacillus plantarum and Lactobacillus fermentum on spoilage fungi of tomato fruit. Journal of Microbiology Research, 5(3), 95–100. https://doi.org/10.5923/j.microbiology.20150503.03
Tropcheva, R., Nikolova, D., Evstatieva, Y., & Danova, S. (2014). Antifungal activity and identification of lactobacilli, isolated from traditional dairy product “katak”. Anaerobe, 28, 78–84. https://doi.org/10.1016/j.anaerobe.2014.05.010
Tuma, S., Vogensen, F. K., Plockova, M., & Chumchalova, J. (2007). Isolation of antifungally active lactobacilli from Edam cheese. Acta Alimentaria, 36(4), 405–414. https://doi.org/10.1556/aalim.2007.0015
Wang, J., Chen, X., Liu, W., Yang, M., & Zhang, H. (2008). Identification of Lactobacillus from koumiss by conventional and molecular methods. European Food Research and Technology, 227(5), 1555–1561. https://doi.org/10.1007/s00217-008-0880-4
Zhao, S., Hao, X., Yang, F., Wang, Y., Fan, X., & Wang, Y. (2022). Antifungal activity of Lactobacillus plantarum ZZUA493 and its application to extend the shelf life of Chinese steamed buns. Foods, 11(2), 195. https://doi.org/10.3390/foods11020195
Zhao, X., Tang, F., Cai, W., Peng, B., Zhang, P., & Shan, C. (2023). Effect of fermentation by lactic acid bacteria on the phenolic composition, antioxidant activity, and flavor substances of jujube–wolfberry composite juice. Food and Chemical Toxicology, 184, 114884. https://doi.org/10.1016/j.lwt.2023.114884