Enhancement of Antioxidant Activity and Bioactive Compounds in Soy Whey Fermented with Lactiplantibacillus plantarum and Weissella confusa

Document Type : Research Article-en

Authors

• Shadi Atashgahi
• Ali Moayedi
• Alireza Sadeghi Mahoonak
• Hoda Shahiri Tabarestani
• Alireza Sadeghi

Department of Food Science and Technology, Faculty of Food Science, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran

https://doi.org/10.22067/ifstrj.2024.87477.1325

Abstract

Soy whey (SW) is a byproduct from tofu and soy protein isolate (SPI) production that contains various nutrients such as protein, amino acids, minerals, carbohydrates, isoflavones. In this study, SW was fermented with lactic acid bacteria (LAB) with the aim to enhance total phenolic contents (TPC), Gamma amino butyric acid (GABA) and antioxidant activity. Eight different LAB strains were selected and the activity and cell counts of the most potent strains were investigated during fermentation. The results showed that all the isolates were able to grow in SW and the increase in incubation time led to significantly (p<0.05) decrease the pH of all samples from 5.75 to 4.5. Among eight LAB isolates, Lactiplantibacillus plantarum MCM4 and Weissella confusa MDM8 showed higher activity in terms of acid production, increase in TPC content and proteolytic activity. The sample fermented by L. plantarum MCM4 had the highest content of free amino acids (1.73 mg/ml) and the unfermented sample with 0.9 mg/ml had the lowest content. GABA concentration varied from 6.15 mg/mL (unfermented) to 24.175 mg/100 mL (SW fermented with L. plantarum MCM4). In this research, it was found that fermentation increased the antioxidant capacity of SW in such a way that the highest amount was observed in sample fermented with Lactiplantibacillus plantarum MCM4. A positive correlation (R²= +0.72) was found between viable cell counts and proteolysis. It can be concluded that, fermentation with L. plantarum MCM4 and W. confusa MDM8 can be applied as an approach to valorize SW.

Keywords

• Biorefinery
• Fermentation
• Gamma aminobutyric acid
• Lactic acid bacteria

Main Subjects

• Food Biotechnology

©2024 The author(s). This is an open access article distributed under Creative Commons Attribution 4.0 International License (CC BY 4.0).

References

1. Aoki, H., Uda, I., Tagami, K., Furuya, Y., Endo, Y., & Fujimoto, K. (2003). The production of a new Tempeh-like fermented soybean containing a high level of & gamma;-aminobutyric acid by anaerobic incubation with Rhizopus. Bioscience, Biotechnology, and Biochemistry, 67(5), 1018-1023. https://doi.org/10.1271/bbb.67.1018
2. Baumann, U., & Bisping, B. (1995). Proteolysis during tempe fermentation. Food Microbiology, 12, 39-47. https://doi.org/10.1016/S0740-0020(95)80077-8
3. Bekiroglu, H., Karimidastjerd, A., Ozmen, D., Toker, O.S., Inan, M., Sagdic, O., & Dertli, E. (2023). Improvement of some techno-functional properties of aquafaba by pre-fermentation with Lactobacillus plantarum Food Bioscience, 54, 102807. https://doi.org/10.1016/j.fbio.2023.102807
4. Belén, F., Benedetti, S., Sánchez, J., Hernández, E., Auleda, J.M., Prudêncio, E.S., & Raventós, M. (2013). Behavior of functional compounds during freeze concentration of tofu whey. Journal of Food Engineering, 116(3), 681-688. https://doi.org/10.1016/j.jfoodeng.2013.01.019
5. Candow, D.G., Burke, N.C., Smith-Palmer, T., & Burke, D.G. (2006). Effect of whey and soy protein supplementation combined with resistance training in young adults. International Journal of Sport Nutrition and Exercise Metabolism, 16(3), 233-244. https://doi.org/10.1123/ijsnem.16.3.233
6. Chandrasekara, A., & Shahidi, F. (2012). Bioaccessibility and antioxidant potential of millet grain phenolics as affected by simulated in vitro digestion and microbial fermentation. Journal of Functional Foods, 4(1), 226-237. https://doi.org/10.1016/j.jff.2011.11.001
7. Chua, J.-Y., & Liu, S.-Q. (2019). Soy whey: More than just wastewater from tofu and soy protein isolate industry. Trends in Food Science & Technology, 91, 24-32. https://doi.org/10.1016/j.tifs.2019.06.016
8. Chua, J.-Y., Lu, Y., & Liu, S.-Q. (2017). Biotransformation of soy whey into soy alcoholic beverage by four commercial strains of Saccharomyces cerevisiae. International Journal of Food Microbiology, 262, 14-22. https://org/10.1016/j.ijfoodmicro.2017.09.007
9. Chua, J.-Y., Lu, Y., & Liu, S.-Q. (2018). Evaluation of five commercial non-Saccharomyces yeasts in fermentation of soy (tofu) whey into an alcoholic beverage. Food Microbiology, 76, 533-542. https://doi.org/11016/j.fm.2018.07.016
10. Chung, I.-M., Seo, S.-H., Ahn, J.-K., & Kim, S.-H. (2011). Effect of processing, fermentation, and aging treatment to content and profile of phenolic compounds in soybean seed, soy curd and soy paste. Food Chemistry, 127(3), 960-96 . https://doi.org/10.1016/j.foodchem.2011.01.065
11. Church, F.C., Swaisgood, H.E., Porter, D.H., & Catignani, G.L. (1983). Spectrophotometric assay using o-phthaldialdehyde for determination of proteolysis in milk and isolated milk proteins1. Journal of Dairy Science, 66(6), 1219-1227. https://doi.org/10.3168/jds.S0022-0302(83)81926-2
12. Fei, Y., Liu, L., Liu, D., Chen, L., Tan, B., Fu, L., & Li, L. (2017). Investigation on the safety of Lactobacillus amylolyticus L6 and its fermentation properties of tofu whey. LWT, 84, 314-322. https://doi.org/10.1016/j.lwt.2017.05.072
13. Fernandez-Orozco, R., Frias, J., Muñoz, R., Zielinski, H., Piskula, M.K., Kozlowska, H., & Vidal-Valverde, C. (2007). Fermentation as a bio-process to obtain functional soybean flours. Journal of Agricultural and Food Chemistry, 55(22), 8972-8979. https://doi.org/10.1021/jf071823b
14. Gan, R.Y., Shah, N.P., Wang, M.F., Lui, W.Y., & Corke, H. (2017). Lactobacillus plantarum WCFS1 fermentation differentially affects antioxidant capacity and polyphenol content in mung bean (Vigna radiata) and soya bean (Glycine max) milks. Journal of Food processing and Preservation, 41(1), e12944. https://doi.org/10.1111/jfpp.12944
15. Gül, H., Özçelik, S., Sağdıç, O., & Certel, M. (2005). Sourdough bread production with Lactobacilli and cerevisiae isolated from sourdoughs. Process Biochemistry, 40(2), 691-697. https://doi.org/10.1016/j.procbio.2004.01.044
16. Han, M., Liao, W.-y., Wu, S.-m., Gong, X., & Bai, C. (2020). Use of Streptococcus thermophilus for the in situ production of γ-aminobutyric acid-enriched fermented milk. Journal of Dairy Science, 103(1), 98-105. https://doi.org/10.3168/jds.2019-16856
17. Hur, S.J., Lee, S.Y., Kim, Y.-C., Choi, I., & Kim, G.-B. (2014). Effect of fermentation on the antioxidant activity in plant-based foods. Food Chemistry, 160, 346-356. https://doi.org/10.1016/j.foodchem.2014.03.112
18. Karimian, E., Moayedi, A., Khomeiri, M., Aalami, M., & Mahoonak, A.S. (2020). Application of high-GABA producing Lactobacillus plantarum isolated from traditional cabbage pickle in the production of functional fermented whey-based formulate. Journal of Food Measurement and Characterization, 14, 3408-3416. https://doi.org/10.1007/s11694-020-00587-x
19. Khanlari, Z., Moayedi, A., Ebrahimi, P., Khomeiri, M., & Sadeghi, A. (2021). Enhancement of γ-aminobutyric acid (GABA) content in fermented milk by using Enterococcus faecium and Weissella confusa isolated from sourdough. Journal of Food Processing and Preservation, 45(10), e15869. https://doi.org/10.1111/jfpp15869
20. König, H., Unden, G., & Fröhlich, J. (2009). Lactic acid bacteria: biology of microorganisms on grapes, in must and in wine: Springer-Verlag Berlin Heidelberg.
21. Kumar, V., Sharma, N., Umesh, M., Selvaraj, M., Al-Shehri, B.M., Chakraborty, P., & Maitra, S.S. (2022). Emerging challenges for the agro-industrial food waste utilization: A review on food waste biorefinery. Bioresource Technology, 362, 127790. https://doi.org/10.1016/j.biortech.2022.127790
22. Lee, I.H., Hung, Y.-H., & Chou, C.-C. (2008). Solid-state fermentation with fungi to enhance the antioxidative activity, total phenolic and anthocyanin contents of black bean. International Journal of Food Microbiology, 121(2), 150-156. https://doi.org/10.1016/j.ijfoodmicro.2007.09.008
23. Li, S., Jin, Z., Hu, D., Yang, W., Yan, Y., Nie, X., Chen, X. (2020). Effect of solid-state fermentation with Lactobacillus casei on the nutritional value, isoflavones, phenolic acids and antioxidant activity of whole soybean flour. LWT, 125, 109264. https://doi.org/10.1016/j.lwt.2020.109264
24. Li, W., & Wang, T. (2021). Effect of solid-state fermentation with Bacillus subtilis lwo on the proteolysis and the antioxidative properties of chickpeas. International Journal of Food Microbiology, 338, 108988. https://doi.org/10.1016/j.ijfoodmicro.2020.108988
25. Lim, Y.H., Foo, H.L., Loh, T.C., Mohamad, R., & Abdullah, N. (2019). Comparative studies of versatile extracellular proteolytic activities of lactic acid bacteria and their potential for extracellular amino acid productions as feed supplements. Journal of Animal Science and Biotechnology, 10(1), 15. https://doi.org/10.1186/s40104-019-0323-z
26. Liu, X., Qian, M., Shen, Y., Qin, X., Huang, H., Yang, H., Bai, W. (2021). An high-throughput sequencing approach to the preliminary analysis of bacterial communities associated with changes in amino acid nitrogen, organic acid and reducing sugar contents during soy sauce fermentation. Food Chemistry, 349, 129131. https://doi.org/10.1016/j.foodchem.2021.129131
27. Meshginfar, N., Sadeghi Mahoonak, A., Hosseinian, F., Ghorbani, M., & Tsopmo, A. (2018). Production of antioxidant peptide fractions from a by-product of tomato processing: mass spectrometry identification of peptides and stability to gastrointestinal digestion. Journal of Food Science and Technology, 55(9), 3498-3507. https://doi.org/10.1007/s13197-018-3274-z
28. Moayedi, A., Mahmoudi, M., Khomeiri, M., & Loghman, S. (2019). Isolation, molecular identification and safety assessment of proteolytic lactic acid bacteria obtained from different raw milks. Journal of Food Science and Technology (Iran), 16(89), 59-69.
29. Moayedi, A., Zareie, Z., Yaghoubi, F., & Khomeiri, M. (2022). Optimization of gamma aminobutyric acid production from various protein hydrolysates by Lactiplantibacillus plantarum Applied Food Biotechnology, 9(4), 287-296. https://doi.org/10.22037/afb.v9i4.38553
30. Monajjemi, M., Aminin, A., Ilkhani, A., & Mollaamin, F. (2012). Nano study of antioxidant activities of fermented soy whey prepared with lactic acid bacteria and kefir. African Journal of Microbiology Research, 6(2), 426-430. https://doi.org/10.5897/AJMR11.1249
31. Moslemi, M., Moayedi, A., Khomeiri, M., & Maghsoudlou, Y. (2023). Development of a whey-based beverage with enhanced levels of conjugated linoleic acid (CLA) as facilitated by endogenous walnut lipase. Food Chemistry: X, 17, 100547. https://doi.org/10.1016/j.fochx.2022.100547
32. Pannerchelvan, S., Muhamad, F. N., Wasoh, H., Mohamed, M.S., Wong, F.W.F., Mohamad, R., & Halim, M. (2023). Improvement of ɣ-aminobutyric acid production and cell viability of Lactiplantibacillus plantarum B7 via whole-cell immobilisation in repeated batch fermentation system. Probiotics and Antimicrobial Proteins. https://doi.org/10.1007/s12602-023-10200-4
33. Pannerchelvan, S., Rios-Solis, L., Faizal Wong, F.W., Zaidan, U.H., Wasoh, H., Mohamed, M.S., & Halim, M. (2023). Strategies for improvement of gamma-aminobutyric acid (GABA) biosynthesis via lactic acid bacteria (LAB) fermentation. Food & Function, 14(9), 3929-3948. https://doi.org/10.1039/D2FO03936B
34. Sanjukta, S., Rai, A.K., Muhammed, A., Jeyaram, K., & Talukdar, N.C. (2015). Enhancement of antioxidant properties of two soybean varieties of Sikkim Himalayan region by proteolytic Bacillus subtilis Journal of Functional Foods, 14, 650-6658. https://doi.org/10.1016/j.jff.2015.02.033
35. Sharma, R., Garg, P., Kumar, P., Bhatia, S.K., & Kulshrestha, S. (2020). Microbial fermentation and its role in quality improvement of fermented foods. Fermentation, 6(4). https://doi.org/10.3390/fermentation6040106
36. Tu, C., Tang, S., Azi, F., Hu, W., & Dong, M. (2019). Use of kombucha consortium to transform soy whey into a novel functional beverage. Journal of Functional Foods, 52, 81-89. https://doi.org/10.1016/j.jff.2018.10.024
37. Undhad Trupti, J., Das, S., Solanki, D., Kinariwala, D., & Hati, S. (2021). Bioactivities and ACE-inhibitory peptides releasing potential of lactic acid bacteria in fermented soy milk. Food Production, Processing and Nutrition, 3, 1-14. https://doi.org/10.1186/s43014-021-00056-y
38. Wang, Q., & Ying, T. (2007). Research progress on waste water utilization in soybean processing. Food Science, 28(9), 594-599.
39. Xiao, Y., Wang, L., Rui, X., Li, W., Chen, X., Jiang, M., & Dong, M. (2015). Enhancement of the antioxidant capacity of soy whey by fermentation with Lactobacillus plantarum B1–6. Journal of Functional Foods, 12, 33-44. https://doi.org/10.1016/j.jff.2014.10.033
40. Xu, Y., Ye, Q., Zhang, H., Yu, Y., Li, X., Zhang, Z., & Zhang, L. (2019). Naturally fermented acid slurry of soy whey: high-throughput sequencing-based characterization of microbial flora and mechanism of tofu coagulation. Frontiers in Microbiology, 10, 1088.
41. Yang, X., Ke, C., & Li, L. (2021). Physicochemical, rheological and digestive characteristics of soy protein isolate gel induced by lactic acid bacteria. Journal of Food Engineering, 292, 110243. https://doi.org/10.1016/j.jfoodeng.2020.110243
42. Yıldırım, I., Uğur, Y., & Kutlu, T. (2017). Investigation of antioxidant activity and phytochemical compositions of Celtis tournefortii. Free Radicals and Antioxidants, 7(2), 160-165.
43. Zhang, S., Shi, Y., Zhang, S., Shang, W., Gao, X., & Wang, H. (2014). Whole soybean as probiotic lactic acid bacteria carrier food in solid-state fermentation. Food Control, 41, 1-6. https://doi.org/10.1016/foodcont.2013.12.026