Leuconostoc mesenteroides M13: optimization of bioprocesses and antioxidant property for food industry application
DOI:
https://doi.org/10.5327/fst.00423Palavras-chave:
Probiotics, Bioprocess, Antioxidant, Shelf-lifeResumo
Several reactive oxygen species are related to physiological functions but also play roles in the development of certain human diseases. Reactive oxygen species are counterbalanced by a physiological defense network such as antioxidants. Probiotic strains have been used as natural antioxidants, but its viable scalability is a challenger. The objective of this work was to optimize the bioprocesses of Leuconostoc mesenteroides M13 and evaluate its antioxidant activity and its shelf-life. The optimized production of M13 biomass was 2,542% greater than non-optimized processes, resulting in a yield of 2.67 × 1010 CFU mL-1 under conditions comprising 13.67 g L-1 of yeast extract and .73 g L-1 of magnesium sulfate. The aggregated spherical structure observed in scanning electron microscopy may have a certain protective effect. The viability of the lyophilized strain storage at 4°C was maintained for a period of up to 8 months. Antioxidant activity assays revealed efficacies for intact and lysed cells as 81 and 65%, respectively. The survival rate of the M13 strain in the presence of hydrogen peroxide was observed at 86% (1.0 mM for 8 h). M13 demonstrated a cost-effective strategy for probiotic application in the food industry as an antioxidant supplement.
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Ali, S. M., Salem, F. E., Aboulwafa, M. M., & Shawky, R. M. (2022). Hypolipidemic activity of lactic acid bacteria: Adjunct therapy for potential probiotics. Plos One, 17(6), Article e0269953. https://doi.org/10.1371/journal.pone.0269953
Baranyi, J., Pin, C., & Ross, T. (1999). Validating and comparing predictive models. International Journal of Food Microbiology, 48(3), 159–166. https://doi.org/10.1016/S0168-1605(99)00035-5
Bolla, P. A., Serradell, M. A., Urraza, P. J., & De Antoni, G. L. (2011). Effect of freeze-drying on viability and in vitro probiotic properties of a mixture of lactic acid bacteria and yeasts isolated from kefir. Journal of Dairy Research, 78(1), 15–22. https://doi.org/10.1017/S0022029910000610
Buchmeier, N., Bossie, S., Chen, C. Y., Fang, F. C., Guiney, D. G., & Libby, S. J. (1997). SlyA, a transcriptional regulator of Salmonella typhimurium, is required for resistance to oxidative stress and is expressed in the intracellular environment of macrophages. Infection and Immunity, 65(9), 3725–3730. https://doi.org/10.1128/iai.65.9.3725-3730.1997
Burton, G. J., & Jauniaux, E. (2011). Oxidative stress. Best Practice & Research Clinical Obstetrics & Gynaecology, 25(3), 287–299. https://doi.org/10.1016/j.bpobgyn.2010.10.016
Capanoglu, E., Nemli, E., & Tomas-Barberan, F. (2022). Novel approaches in the valorization of agricultural wastes and their applications. Journal of Agricultural and Food Chemistry, 70(23), 6787–6804. https://doi.org/10.1021/acs.jafc.1c07104
Carvalho, F., Prazeres, A. R., & Rivas, J. (2013). Cheese whey wastewater: characterization and treatment. Science of the Total Environment, 445–446, 385–396. https://doi.org/10.1016/J.SCITOTENV.2012.12.038
Colares, H. C., Guimarães, G. M., Couto, C. A. P., Gil, P. O., Santos, S. L. E. N., Silva, T. N. L., Carvalho, I. L. Q., Fonseca, F. G., Gagnon, M., Roy, D., Magalhães, J. T., Gonçalves, D. B., & Granjeiro, P. A. (2021). Optimization of bioprocess of Schleiferilactobacillus harbinensis Ca12 and its viability in frozen Brazilian berries (Açai, Euterpe oleracea Mart.). Brazilian Journal of Microbiology, 52, 2271–2285. https://doi.org/10.1007/s42770-021-00559-3
Colares, H. C., Tarabal, V. S., Silva, C. I., Meira, H. G. R., Toledo, M. M. L. M., Guimarães, P. P. G., Parreira, A. G., Silva, J. A., Gonçalves, D. B., Magalhães, J. T., & Granjeiro, P. A. (2024). Optimization of bioprocesses of Lactiplantibacillus plantarum UFSJP2 with antioxidant activity and its viability in graviola (Annona muricata) sorbet. Food Science and Technology, 44, Article e00373. https://doi.org/10.5327/fst.00373
Endres, L., Begley, U., Clark, R., Gu, C., Dziergowska, A., Małkiewicz, A., Melendez, J. A., Dedon, P. C., & Begley, T. J. (2015). Alkbh8 regulates selenocysteine-protein expression to protect against reactive oxygen species damage. Plos One, 10(7), Arcticle e0131335. https://doi.org/10.1371/journal.pone.0131335
Feng, T., & Wang, J. (2020). Oxidative stress tolerance and antioxidant capacity of lactic acid bacteria as probiotic: a systematic review. Gut Microbes, 12(1), Article e1801944. https://doi.org/10.1080/19490976.2020.1801944
Ficoseco, C. A., Mansilla, F. I., Maldonado, N. C., Miranda, H., Nader-Macias, M. E. F., & Vignolo, G. M. (2018). Safety and growth optimization of lactic acid bacteria isolated from feedlot cattle for probiotic formula design. Frontiers in Microbiology, 9, Article 2220. https://doi.org/10.3389/fmicb.2018.02220
Guimarães, G. M., Soares, L. A., Silva, T. N. L., Carvalho, I. L. Q., Valadares, H. M. S., Sodré, G. A., Gonçalves, D. B., Neumann, E., Fonseca, F. G., Vinderola, G., Granjeiro, P. A., & Magalhães, J. T. (2020). Cocoa pulp as alternative food matrix for probiotic delivery. Recent Patents on Food, Nutrition & Agriculture, 11(1), 82–90. https://doi.org/10.2174/2212798410666190408151826
Halliwell, B. (2024). Understanding mechanisms of antioxidant action in health and disease. Nature Reviews Molecular Cell Biology, 25, 13–33. https://doi.org/10.1038/s41580-023-00645-4
Hayek, S. A., Gyawali, R., Aljaloud, S. O., Krastanov, A., & Ibrahim, S. A. (2019). Cultivation media for lactic acid bacteria used in dairy products. Journal of Dairy Research, 86(4), 490–502. https://doi.org/10.1017/S002202991900075X
Hayek, S. A., & Ibrahim, S. A. (2013). Current limitations and challenges with lactic acid bacteria: a review. Food and Nutrition Sciences, 4(11A), 73–87. https://doi.org/10.4236/FNS.2013.411A010
Hill, C., Guarner, F., Reid, G., Gibson, G. R., Merenstein, D. J., Pot, B., Morelli, L., Canani, R. B., Flint, H. J., Salminen, S., Calder, P. C., & Sanders, M. E. (2014). The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nature Reviews. Gastroenterology & Hepatology, 11(8), 506–514. https://doi.org/10.1038/NRGASTRO.2014.66
Hiremath, S., & Viswanathan, P. (2022). Oxalobacter formigenes: A new hope as a live biotherapeutic agent in the management of calcium oxalate renal stones. Anaerobe, 75, 102572. https://doi.org/10.1016/j.anaerobe.2022.102572
Hoffmann, A., Kleniewska, P., & Pawliczak, R. (2021). Antioxidative activity of probiotics. Archives of Medical Science, 17(3), 792–804. https://doi.org/10.5114/aoms.2019.89894
Houldsworth, A. (2023). Role of oxidative stress in neurodegenerative disorders: a review of reactive oxygen species and prevention by antioxidants. Brain Communications, 6(1). https://doi.org/10.1093/braincomms/fcad356
Iosca, G., Turetta, M., Vero, L., Bang-Berthelsen, C. H., Gullo, M., & Pulvirenti, A. (2023). Valorization of wheat bread waste and cheese whey through cultivation of lactic acid bacteria for bio-preservation of bakery products. LWT, 176, 114524. https://doi.org/10.1016/j.lwt.2023.114524
Jeong, S.-G., Choi, I. S., Kim, H. M., Chang, J. Y., & Park, H. W. (2022). Supercooling Pretreatment Improves the Shelf-Life of Freeze-Dried Leuconostoc mesenteroides WiKim32. Journal of Microbiology and Biotechnology, 32(12), 1599–1604. https://doi.org/10.4014/jmb.2209.09022
Kim, H., Eom, H.-J., Lee, J., Han, J., & Han, N. S. (2004). Statistical optimization of medium composition for growth of Leuconostoc citreum. Biotechnology and Bioprocess Engineering, 9(4), 278–284. https://doi.org/10.1007/BF02942344
Kim, M., Nam, D.-G., Kim, S.-B., Im, P., Choe, J.-S., & Choi, A.-J. (2018). Enhancement of viability, acid, and bile tolerance and accelerated stability in lyophilized Weissella cibaria JW15 with protective agents. Food Science & Nutrition, 6(7), 1904–1913. https://doi.org/10.1002/fsn3.762
Kim, S., Lee, J. Y., Jeong, Y., & Kang, C.-H. (2022). Antioxidant Activity and Probiotic Properties of Lactic Acid Bacteria. Fermentation, 8(1), 29. https://doi.org/10.3390/fermentation8010029
Kumar, S., Bansal, K., & Sethi, S. K. (2022). Comparative genomics analysis of genus Leuconostoc resolves its taxonomy and elucidates its biotechnological importance. Food Microbiology, 106, 104039. https://doi.org/10.1016/j.fm.2022.104039
Lang, Y., Gao, N., Zang, Z., Meng, X., Lin, Y., Yang, S., Yang, Y., Jin, Z., & Li, B. (2024). Classification and antioxidant assays of polyphenols: a review. Journal of Future Foods, 4(3), 193–204. https://doi.org/10.1016/j.jfutfo.2023.07.002
Lee, J., Hwang, K., Chung, M., Cho, D., & Park, C. (2005). Resistance of Lactobacillus casei KCTC 3260 to reactive oxygen species (ROS): role for a metal ion chelating effect. Journal of Food Science, 70(8), m388–m391. https://doi.org/10.1111/j.1365-2621.2005.tb11524.x
Li, S., Zhao, Y., Zhang, L., Zhang, X., Huang, L., Li, D., Niu, C., Yang, Z., & Wang, Q. (2012). Antioxidant activity of Lactobacillus plantarum strains isolated from traditional Chinese fermented foods. Food Chemistry, 135(3), 1914–1919. https://doi.org/10.1016/j.foodchem.2012.06.048
Lü, J.-M., Lin, P. H., Yao, Q., & Chen, C. (2010). Chemical and molecular mechanisms of antioxidants: experimental approaches and model systems. Journal of Cellular and Molecular Medicine, 14(4), 840–860. https://doi.org/10.1111/j.1582-4934.2009.00897.x
Makowski, K., Matusiak, K., Borowski, S., Bielnicki, J., Tarazewicz, A., Maroszyńska, M., Leszczewicz, M., Powałowski, S., & Gutarowska, B. (2017). Optimization of a culture medium using the taguchi approach for the production of microorganisms active in odorous compound removal. Applied Sciences, 7(8), 756. https://doi.org/10.3390/app7080756
Mateen, S., Moin, S., Khan, A. Q., Zafar, A., & Fatima, N. (2016). Increased Reactive Oxygen Species Formation and Oxidative Stress in Rheumatoid Arthritis. Plos One, 11(4), Article e0152925. https://doi.org/10.1371/journal.pone.0152925
Mathur, H., Beresford, T. P., & Cotter, P. D. (2020). Health benefits of lactic acid bacteria (LAB) fermentates. Nutrients, 12(6), 1679. https://doi.org/10.3390/nu12061679
McLaughlin, H. P., Motherway, M. O., Lakshminarayanan, B., Stanton, C., Ross, R. P., Brulc, J., Menon, R., O’Toole, P. W., & van Sinderen, D. (2015). Carbohydrate catabolic diversity of bifidobacteria and lactobacilli of human origin. International Journal of Food Microbiology, 203, 109–121. https://doi.org/10.1016/j.ijfoodmicro.2015.03.008
Mohammadian, K., Fakhar, F., Keramat, S., & Stanek, A. (2024). The role of antioxidants in the treatment of metabolic dysfunction-associated fatty liver disease: a systematic review. Antioxidants, 13(7), 797. https://doi.org/10.3390/antiox13070797
Mohsin, M., Abbas, R. Z., Yin, G., Sindhu, Z.-U.-D., Abbas, A., Huang, Z., Aleem, M. T., Saeed, Z., Afzal, M. Z., Ejaz, A., & Shoaib, M. (2021). Probiotics as therapeutic, antioxidant and immunomodulatory agents against poultry coccidiosis. World’s Poultry Science Journal, 77(2), 331–345. https://doi.org/10.1080/00439339.2021.1883412
Muchtaridi, M., Amirah, S. R., Harmonis, J. A., & Ikram, E. H. K. (2022). Role of nuclear factor erythroid 2 (Nrf2) in the recovery of long COVID-19 using natural antioxidants: a systematic review. Antioxidants, 11(8), 1551. https://doi.org/10.3390/antiox11081551
Muchtaridi, M., Az-Zahra, F., Wongso, H., Setyawati, L. U., Novitasari, D., & Ikram, E. H. K. (2024). Molecular mechanism of natural food antioxidants to regulate ROS in treating cancer: a review. Antioxidants, 13(2), 207. https://doi.org/10.3390/antiox13020207
Muscolo, A., Mariateresa, O., Giulio, T., & Mariateresa, R. (2024). Oxidative stress: the role of antioxidant phytochemicals in the prevention and treatment of diseases. International Journal of Molecular Sciences, 25(6), 3264. https://doi.org/10.3390/ijms25063264
Nascimento, S. S. C., Passos, T. S., & Júnior, F. C. S. (2024). Probiotics in plant-based food matrices: a review of their health benefits. PharmaNutrition, 28, 100390. https://doi.org/10.1016/j.phanu.2024.100390
Panesar, P. S., Kennedy, J. F., Gandhi, D. N., & Bunko, K. (2007). Bioutilisation of whey for lactic acid production. Food Chemistry, 105(1), 1–14. https://doi.org/10.1016/j.foodchem.2007.03.035
Paula, A. T., Jeronymo-Ceneviva, A. B., Todorov, S. D., & Penna, A. L. B. (2015). The Two Faces of Leuconostoc mesenteroides in Food Systems. Food Reviews International, 31(2), 147–171. https://doi.org/10.1080/87559129.2014.981825
Ragaza, J. A., Hossain, Md. S., Meiler, K. A., Velasquez, S. F., & Kumar, V. (2020). A review on Spirulina: alternative media for cultivation and nutritive value as an aquafeed. Reviews in Aquaculture, 12(4), 2371–2395. https://doi.org/10.1111/raq.12439
Sharifi, S., Rezazad-Bari, M., Alizadeh, M., Almasi, H., & Amiri, S. (2021). Use of whey protein isolate and gum Arabic for the co-encapsulation of probiotic Lactobacillus plantarum and phytosterols by complex coacervation: Enhanced viability of probiotic in Iranian white cheese. Food Hydrocolloids, 113, 106496. https://doi.org/10.1016/j.foodhyd.2020.106496
Sies, H., Belousov, V. V., Chandel, N. S., Davies, M. J., Jones, D. P., Mann, G. E., Murphy, M. P., Yamamoto, M., & Winterbourn, C. (2022). Defining roles of specific reactive oxygen species (ROS) in cell biology and physiology. Nature Reviews Molecular Cell Biology, 23(7), 499–515. https://doi.org/10.1038/s41580-022-00456-z
Spyropoulos, B. G., Misiakos, E. P., Fotiadis, C., & Stoidis, C. N. (2011). Antioxidant Properties of Probiotics and Their Protective Effects in the Pathogenesis of Radiation-Induced Enteritis and Colitis. Digestive Diseases and Sciences, 56(2), 285–294. https://doi.org/10.1007/s10620-010-1307-1
Suez, J., Zmora, N., Segal, E., & Elinav, E. (2019). The pros, cons, and many unknowns of probiotics. Nature Medicine, 25(5), 716–729. https://doi.org/10.1038/s41591-019-0439-x
Sun, W., Nguyen, Q. D., Sipiczki, G., Ziane, S. R., Hristovski, K., Friedrich, L., Visy, A., Hitka, G., Gere, A., & Bujna, E. (2023). Microencapsulation of Lactobacillus plantarum 299v Strain with Whey Proteins by Lyophilization and Its Application in Production of Probiotic Apple Juices. Applied Sciences, 13(1), 318. https://doi.org/10.3390/app13010318
Tang, Z., Wang, P., Dong, C., Zhang, J., Wang, X., & Pei, H. (2022). Oxidative Stress Signaling Mediated Pathogenesis of Diabetic Cardiomyopathy. Oxidative Medicine and Cellular Longevity, 2022, 1–8. https://doi.org/10.1155/2022/5913374
Vougiouklaki, D., Tsironi, T., Tsantes, A. G., Tsakali, E., Van Impe, J. F. M., & Houhoula, D. (2023). Probiotic Properties and Antioxidant Activity In Vitro of Lactic Acid Bacteria. Microorganisms, 11(5), 1264. https://doi.org/10.3390/microorganisms11051264
Wang, A., & Zhong, Q. (2024). Drying of probiotics to enhance the viability during preparation, storage, food application, and digestion: A review. Comprehensive Reviews in Food Science and Food Safety, 23(1), Article e13287. https://doi.org/10.1111/1541-4337.13287
Wieërs, G., Belkhir, L., Enaud, R., Leclercq, S., Foy, J.-M. P., Dequenne, I., Timary, P., & Cani, P. D. (2020). How probiotics affect the microbiota. Frontiers in Cellular and Infection Microbiology, 9, Article 454. https://doi.org/10.3389/FCIMB.2019.00454
Yeboah, P. J., Ibrahim, S. A., & Krastonov, A. (2023). A review of fermentation and the nutritional requirements for effective growth media for lactic acid bacteria. Food Science and Applied Biotechnology, 6(2), 215. https://doi.org/10.30721/fsab2023.v6.i2.269