Development of Fermentation-induced Soymilk Gel: Effects of Different Lactic Acid Bacteria on the Physicochemical Characteristics

مجله پژوهشهای علوم و صنایع غذایی ایران

Article 4, Volume 20, Issue 6 - Serial Number 90, January and February 2025, Pages 155-169   

Document Type: Research Article-en

DOI: 10.22067/ifstrj.2024.89764.1366

Authors

Fatemeh Rahmani; Ali Moayedi^* ; Marteza Khomeiri; Mahboobeh Kashiri

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

Abstract

Nowadays, plant-based dairy alternatives have gained considerable attention. However, the textural and sensorial characteristics of plant-based products limit their acceptance. The exploitation of lactic acid bacteria has been proposed as a promising approach to developing plant-based dairy analogs. In this study, the performance of three proteolytic lactic acid bacteria in the induction of soymilk gelation was compared and their effects on the physicochemical properties of resulting gels were investigated. Lactiplantibacillus plantarum MCM4, Streptococcus thermophilus, and Weissella confusa MDM8) were inoculated to the soy milk matrix, and incubated at 37 °C until reaching pH 4.7. To understand the effects of acidifying and proteolytic activity of starter culture, syneresis, cell counts, free amino acid content (O-phthalaldehyde method), evaluation of proteolysis using sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) and textural parameters of soymilk gels during fermentation were investigated. There was a significant difference among the strains in terms of viable cell counts and proteolytic activity during fermentation (p < 0.05). The amount of syneresis was also different among the resulted gels as it was in the range from 61% (sample fermented with S. thermophilus) to 69.5% (fermented with L. plantarum MCM4). The main soy proteins were degraded to different extents as a function of fermentation time. Texture analysis showed that fermentation of soymilk with W. confusa MDM8 resulted in soy gel with higher firmness and consistency, while the sample fermented with L. plantarum MCM4 had higher adhesiveness and viscosity index. Overall, it can be concluded that L. plantarum MCM4, W. confusa MDM8, and S. thermophilus can be introduced as starter cultures for the production of novel soymilk gels with reasonable properties.

Keywords

Dairy alternatives; Lactic acid bacteria; Plant-based Proteins; Sustainable food production

References

1. Aguirre, L., Hebert, E.M., Garro, M.S., & de Giori, G.S. (2014). Proteolytic activity of Lactobacillus strains on soybean proteins. LWT-Food Science and Technology, 59(2), 780-785. https://doi.org/10.1016/j.lwt.2014.06.061
2. Atashgahi, S., Moayedi, A., Sadeghi Mahoonak, A., Shahiri Tabarestani, H., & Sadeghi, A. (2024). Enhancement of antioxidant activity and bioactive compounds in soy whey fermented with Lactiplantibacillus plantarum and Weissella confusa. Iranian Food Science and Technology Research Journal, 20(3), 65-79. https://doi.org/10.22067/ifstrj.2024.87477.1325
3. Beal, C., Skokanova, J., Latrille, E., Martin, N., & Corrieu, G. (1999). Combined effects of culture conditions and storage time on acidification and viscosity of stirred yogurt. Journal of Dairy Science, 82(4), 673-681. https://doi.org/10.3168/jds.S0022-0302(99)75283-5
4. Böni, L., Rühs, P.A., Windhab, E.J., Fischer, P., & Kuster, S. (2016). Gelation of soy milk with hagfish exudate creates a flocculated and fibrous emulsion-and particle gel. PLoS One, 11(1), e0147022. https://doi.org/10.1371/journal.pone.0147022
5. Cavallieri, A.L.F., & Da Cunha, R.L. (2008). The effects of acidification rate, pH and ageing time on the acidic cold set gelation of whey proteins. Food Hydrocolloids, 22(3), 439-448.
6. Ciron, C., Gee, V., Kelly, A., & Auty, M. (2010). Comparison of the effects of high-pressure microfluidization and conventional homogenization of milk on particle size, water retention and texture of non-fat and low-fat yoghurts. International Dairy Journal, 20(5), 314-320. https://doi.org/10.1016/j.idairyj.2009.11.018
7. De Vuyst, L., & Degeest, B. (1999). Heteropolysaccharides from lactic acid bacteria. FEMS Microbiology Reviews, 23(2), 153-177. https://doi.org/10.1111/j.1574-6976.1999.tb00395.x
8. Folkenberg, D.M., Dejmek, P., Skriver, A., Guldager, H.S., & Ipsen, R. (2006). Sensory and rheological screening of exopolysaccharide producing strains of bacterial yoghurt cultures. International Dairy Journal, 16(2), 111-118. https://doi.org/10.1016/j.idairyj.2004.10.013
9. Gänzle, M.G. (2015). Lactic metabolism revisited: metabolism of lactic acid bacteria in food fermentations and food spoilage. Current Opinion in Food Science, 2, 106-117. https://doi.org/10.1016/j.cofs.2015.03.001
10. Gänzle, M.G., Loponen, J., & Gobbetti, M. (2008). Proteolysis in sourdough fermentations: mechanisms and potential for improved bread quality. Trends in Food Science & Technology, 19(10), 513-521. https://doi.org/10.1016/j.tifs.2008.04.002
11. García-Cano, I., Rocha-Mendoza, D., Ortega-Anaya, J., Wang, K., Kosmerl, E., & Jiménez-Flores, R. (2019). Lactic acid bacteria isolated from dairy products as potential producers of lipolytic, proteolytic and antibacterial proteins. Applied Microbiology and Biotechnology, 103, 5243-5257. https://doi.org/10.1007/s00253-019-09844-6
12. Genet, B.M., Xiao, H., Christensen, L.F., Laforce, I.N., Mohammadifar, M.A., Bang-Berthelsen, C.H., & Hansen, E.B. (2023). Selection of proteolytic LAB starter cultures for acidification of soy based dairy alternatives. LWT, 184, 115082.
13. Holzhauser, T., Wackermann, O., Ballmer-Weber, B.K., Bindslev-Jensen, C., Scibilia, J., Perono-Garoffo, L., Utsumi, S., Poulsen, L.K., & Vieths, S. (2009). Soybean (Glycine max) allergy in Europe: Gly m 5 (β-conglycinin) and Gly m 6 (glycinin) are potential diagnostic markers for severe allergic reactions to soy. Journal of Allergy and Clinical Immunology, 123(2), 452-458. e454. https://doi.org/10.1016/j.jaci.2008.09.034
14. Joshi, R., Sharma, V., & Kuila, A. (2018). Fermentation technology: current status and future prospects. Principles and Applications of Fermentation Technology, 1-13. https://doi.org/10.1002/9781119460381
15. Kamarinou, C.S., Papadopoulou, O.S., Doulgeraki, A.I., Tassou, C.C., Galanis, A., Chorianopoulos, N.G., & Argyri, A.A. (2022). Mapping the key technological and functional characteristics of indigenous lactic acid bacteria isolated from Greek traditional dairy products. Microorganisms, 10(2), 246. https://doi.org/10.3390/microorganisms10020246
16. 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
17. 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/jfpp.15869
18. Klost, M., Brzeski, C., & Drusch, S. (2020). Effect of protein aggregation on rheological properties of pea protein gels. Food Hydrocolloids, 108, 106036. https://doi.org/10.1016/j.foodhyd.2020.106036
19. Kong, X., Xiao, Z., Du, M., Wang, K., Yu, W., Chen, Y., Liu, Z., Cheng, Y., & Gan, J. (2022). Physicochemical, textural, and sensorial properties of soy yogurt as affected by addition of low acyl gellan gum. Gels, 8(7), 453.
20. Korcz, E., & Varga, L. (2021). Exopolysaccharides from lactic acid bacteria: Techno-functional application in the food industry. Trends in Food Science & Technology, 110, 375-384. https://doi.org/10.1016/j.tifs.2021.02.014
21. Kuipers, B.J., van Koningsveld, G.A., Alting, A.C., Driehuis, F., Gruppen, H., & Voragen, A.G. (2005). Enzymatic hydrolysis as a means of expanding the cold gelation conditions of soy proteins. Journal of Agricultural and Food Chemistry, 53(4), 1031-1038. https://doi.org/10.1021/jf048622h
22. Leksono, B.Y., Cahyanto, M.N., Rahayu, E.S., Yanti, R., & Utami, T. (2022). Enhancement of antioxidant activities in black soy milk through isoflavone aglycone production during indigenous lactic acid bacteria fermentation. Fermentation, 8(7), 326.
23. Li, Q., Xia, Y., Zhou, L., & Xie, J. (2013). Evaluation of the rheological, textural, microstructural and sensory properties of soy cheese spreads. Food and Bioproducts Processing, 91(4), 429-439. https://doi.org/10.1016/j.fbp.2013.03.001
24. Liu, L., Huang, Y., Zhang, X., Zeng, J., Zou, J., Zhang, L., & Gong, P. (2023). Texture analysis and physicochemical characteristics of fermented soymilk gel by different lactic acid bacteria. Food Hydrocolloids, 136, 108252. https://doi.org/10.1016/j.foodhyd.2022.108252
25. Lorusso, A., Coda, R., Montemurro, M., & Rizzello, C.G. (2018). Use of selected lactic acid bacteria and quinoa flour for manufacturing novel yogurt-like beverages. Foods, 7(4), 51. https://doi.org/10.3390/foods7040051
26. Masiá, C., Jensen, P.E., Petersen, I.L., & Buldo, P. (2022). Design of a functional pea protein matrix for fermented plant-based cheese. Foods, 11(2), 178. https://doi.org/10.3390/foods11020178
27. McCarthy, K., Parker, M., Ameerally, A., Drake, S., & Drake, M. (2017). Drivers of choice for fluid milk versus plant-based alternatives: What are consumer perceptions of fluid milk? Journal of Dairy Science, 100(8), 6125-6138.
28. Meinlschmidt, P., Ueberham, E., Lehmann, J., Schweiggert-Weisz, U., & Eisner, P. (2016). Immunoreactivity, sensory and physicochemical properties of fermented soy protein isolate. Food Chemistry, 205, 229-238.
29. Mende, S., Peter, M., Bartels, K., Dong, T., Rohm, H., & Jaros, D. (2013). Concentration dependent effects of dextran on the physical properties of acid milk gels. Carbohydrate Polymers, 98(2), 1389-1396. https://doi.org/10.1016/j.carbpol.2013.07.072
30. Mishra, S., & Mishra, H.N. (2018). Comparative study of the synbiotic effect of inulin and fructooligosaccharide with probiotics with regard to the various properties of fermented soy milk. Food Science and Technology International, 24(7), 564-575. https://doi.org/10.1177/1082013218776529
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. Nasaruddin, F., Chin, N., & Yusof, Y. (2012). Effect of processing on instrumental textural properties of traditional dodol using back extrusion. International Journal of Food Properties, 15(3), 495-506. https://doi.org/10.1080/10942912.2010.491932
33. Ningtyas, D.W., Tam, B., Bhandari, B., & Prakash, S. (2021). Effect of different types and concentrations of fat on the physico-chemical properties of soy protein isolate gel. Food Hydrocolloids, 111, 106226. https://doi.org/10.1016/j.foodhyd.2020.106226
34. Purohit, D., Hassan, A., Bhatia, E., Zhang, X., & Dwivedi, C. (2009). Rheological, sensorial, and chemopreventive properties of milk fermented with exopolysaccharide-producing lactic cultures. Journal of Dairy Science, 92(3), 847-856. https://doi.org/10.3168/jds.2008-1256
35. Rahmani, F., Gandomi, H., Noori, N., Faraki, A., & Farzaneh, M. (2021). Microbial, physiochemical and functional properties of probiotic yogurt containing Lactobacillus acidophilus and Bifidobacterium bifidum enriched by green tea aqueous extract. Food Science & Nutrition, 9(10), 5536-5545. https://doi.org/10.1002/fsn3.2512
36. Rastogi, Y.R., Thakur, R., Thakur, P., Mittal, A., Chakrabarti, S., Siwal, S.S., Thakur, V.K., Saini, R.V., & Saini, A.K. (2022). Food fermentation–significance to public health and sustainability challenges of modern diet and food systems. International Journal of Food Microbiology, 371, 109666.
37. Rojas-Nery, E., Garcia-Martinez, I., & Totosaus, A. (2015). Effect of emulsified soy oil with different carrageenans in rennet-coagulated milk gels. International Food Research Journal, 22(2), 606.
38. Saraniya, A., & Jeevaratnam, K. (2015). In vitro probiotic evaluation of phytase producing Lactobacillus species isolated from Uttapam batter and their application in soy milk fermentation. Journal of Food Science and Technology, 52, 5631-5640.
39. Shahbandari, J., Golkar, A., Taghavi, S.M., & Amiri, A. (2016). Effect of storage period on physicochemical, textural, microbial and sensory characteristics of stirred soy yogurt. International Journal of Farming and Allied Sciences, 5(6), 476-484.
40. Shakerian, M., Razavi, S.H., Ziai, S.A., Khodaiyan, F., Yarmand, M.S., & Moayedi, A. (2015). Proteolytic and ACE-inhibitory activities of probiotic yogurt containing non-viable bacteria as affected by different levels of fat, inulin and starter culture. Journal of Food Science and Technology, 52, 2428-2433. https://doi.org/10.1007/s13197-013-1202-9
41. Shams-Abadi, S.T., & Razavi, S.M.A. (2021). Cress seed gum improves rheological, textural and physicochemical properties of native wheat starch-sucrose mixture. International Journal of Biological Macromolecules, 181, 945-955. https://doi.org/10.1016/j.ijbiomac.2021.04.093
42. Shewry, P.R., Napier, J.A., & Tatham, A.S. (1995). Seed storage proteins: structures and biosynthesis. The Plant Cell, 7(7), 945. https://doi.org/10.1105/tpc.7.7.945
43. Shirotani, N., Hougaard, A.B., Lametsch, R., Petersen, M.A., Rattray, F.P., & Ipsen, R. (2021). Proteolytic activity of selected commercial Lactobacillus helveticus strains on soy protein isolates. Food Chemistry, 340, 128152. https://doi.org/10.1016/j.foodchem.2020.128152
44. Somjid, P., Panpipat, W., Cheong, L.-Z., & Chaijan, M. (2022). Comparative effect of cricket protein powder and soy protein isolate on gel properties of Indian mackerel surimi. Foods, 11(21), 3445. https://doi.org/10.3390/foods11213445
45. Taheri, S., Khomeiri, M., Aalami, M., & Moayedi, A. (2019). Non-fermented synbiotic drink based on lactic cheese whey which incorporates Lactobacillus rhamnosus GG and Lactobacillus paracasei. International Journal of Food Studies, 8(2). https://doi.org/10.7455/ijfs/8.2.2019.a9
46. Tang, J., Luan, F., & Chen, X. (2006). Binding analysis of glycyrrhetinic acid to human serum albumin: fluorescence spectroscopy, FTIR, and molecular modeling. Bioorganic & Medicinal Chemistry, 14(9), 3210-3217. https://doi.org/10.1016/j.bmc.2005.12.034
47. Tavano, O.L. (2013). Protein hydrolysis using proteases: An important tool for food biotechnology. Journal of Molecular Catalysis B: Enzymatic, 90, 1-11. https://doi.org/10.1016/j.molcatb.2013.01.011
48. Wang, R., & Guo, S. (2016). Effects of endogenous small molecular compounds on the rheological properties, texture and microstructure of soymilk coagulum: Removal of phytate using ultrafiltration. Food Chemistry, 211, 521-529. https://doi.org/10.1016/j.foodchem.2016.05.086
49. Wang, T., Chen, X., Wang, N., Wu, N., Jiang, L., Wu, F., Yu, D., Cheng, J., & Wang, L. (2022). Effect of electrochemical treatment on the formation and characteristics of induced soybean milk gel. Journal of Food Engineering, 323, 111007. https://doi.org/10.1016/j.jfoodeng.2022.111007
50. Wang, Y.-C., Yu, R.-C., Yang, H.-Y., & Chou, C.-C. (2003). Sugar and acid contents in soymilk fermented with lactic acid bacteria alone or simultaneously with bifidobacteria. Food Microbiology, 20(3), 333-338. https://doi.org/10.1016/S0740-0020(02)00125-9
51. Worsztynowicz, P., Schmidt, A.O., Białas, W., & Grajek, W. (2019). Identification and partial characterization of proteolytic activity of Enterococcus faecalis relevant to their application in dairy industry. Acta Biochimica Polonica, 66(1), 61-69. https://doi.org/10.18388/abp.2018_2714
52. Xing, G., Giosafatto, C.V.L., Rui, X., Dong, M., & Mariniello, L. (2019). Microbial transglutaminase-mediated polymerization in the presence of lactic acid bacteria affects antigenicity of soy protein component present in bio-tofu. Journal of Functional Foods, 53, 292-298. https://doi.org/10.1016/j.jff.2018.12.035
53. Yang, H., Qu, Y., Li, J., Liu, X., Wu, R., & Wu, J. (2020). Improvement of the protein quality and degradation of allergens in soybean meal by combination fermentation and enzymatic hydrolysis. LWT, 128, 109442. https://doi.org/10.1016/j.lwt.2020.109442
54. Yang, X., Su, Y., & Li, L. (2020). Study of soybean gel induced by Lactobacillus plantarum: Protein structure and intermolecular interaction. LWT, 119, 108794. https://doi.org/10.1016/j.lwt.2019.108794
55. Zannini, E., Jeske, S., Lynch, K.M., & Arendt, E.K. (2018). Development of novel quinoa-based yoghurt fermented with dextran producer Weissella cibaria MG1. International Journal of Food Microbiology, 268, 19-26. https://doi.org/10.1016/j.ijfoodmicro.2018.01.001