Proteolytic Activity of Indigenous Lactic Acid Bacteria and Angiotensin-I-Converting Enzyme (ACE) Inhibitory Activity in Fermented Soy Milk
DOI:
https://doi.org/10.3923/pjn.2020.295.302Keywords:
ACE inhibitory activity, fermented soy milk, indigenous lactic acid bacteria, peptides, proteolytic activityAbstract
Background and Objective: Lactic acid bacteria with its proteolytic system hydrolyzes proteins to produce angiotensin-I-converting enzyme inhibitor during fermentation. A total of 108 indigenous lactic acid bacteria isolated from fermented food were screened based on proteolytic activity for the potential formation of angiotensin-I-converting enzyme inhibitory activity in fermented soy milk. Materials and Methods: Indigenous lactic acid bacteria (from tempe, kefir and breast milk) were screened based on proteolytic activity. Semi-qualitative screening of proteolytic activity of lactic acid bacteria was performed on skim milk agar. Thirty lactic acid bacteria isolates were further selected based on the formation of peptides in 11% reconstituted skim milk. A total of 10 lactic acid bacteria isolates with high proteolytic activity were selected as starter cultures for soy milk fermentation at 37°C until pH 4.6 was reached. Evaluation of fermented soy milk was performed by enumeration of lactic acid bacteria population, analyses of titratable acidity, soluble protein content, peptide content and determination of angiotensin-I-converting enzyme inhibitory activity. Results: Of 108 lactic acid bacteria isolates, 13.8% isolates had strong proteolytic activity and 15 isolates (13.8%) had moderate proteolytic activity based on clear zones formed surround the colony on skim milk agar after 48 h of incubation. The amount of peptide produced by isolates with strong and moderate proteolytic activity and the ability to reduce pH of soy milk varied among isolates. The pH value of 4.6 of fermented soy milk was reached after 24-48 h of incubation. Of 10 selected isolates, Lactobacillus plantarum 1W22408 and Lactobacillus fermentum R6 produced the highest angiotensin-I-converting enzyme inhibitory activity in fermented soy milk. Conclusion: Proteolytic activity and acidification ability of the lactic acid bacteria varied between isolates. Lactic acid bacteria isolates of Lactobacillus plantarum 1W22408 and Lactobacillus fermentum R6 were potential to be used as a starter culture to produce fermented soymilk which has angiotensin-I-converting enzyme inhibitory activity.
References
Castro, R.J.S.d. and H.H. Sato, 2015. Biologically active peptides: Processes for their generation, purification and identification and applications as natural additives in the food and pharmaceutical industries. Food Res. Int., 74: 185-198.
Sanjukta, S. and A.K. Rai, 2016. Production of bioactive peptides during soybean fermentation and their potential health benefits. Trends Food Sci. Technol., 50: 1-10.
Zeng, Y., N. Wang and W. Qian, 2013. Production of angiotensin i converting enzyme inhibitory peptides from peanut meal fermented with lactic acid bacteria and facilitated with protease. Adv. J. Food Sci. Technol., 9: 1198-1203.
Lin, Y.S., Y.L. Lu, G.J. Wang, H.J. Liang and W.C. Hou, 2014. Vasorelaxing and antihypertensive activities of synthesized peptides derived from computer-aided simulation of pepsin hydrolysis of yam dioscorin. Bot. Stud., Vol. 55, No. 49.
Wang, J., C. Li, J. Xue, J. Yang, Q. Zhang, H. Zhang, Y. Chen, 2015. Fermentation characteristics and angiotensin I-converting enzyme–inhibitory activity of Lactobacillus helveticus isolate H9 in cow milk, soy milk, and mare milk. J. Dairy Sci., 98: 3655-3664.
Georgalakia, M., G. Zoumpopouloua, E. Mavrogonatoub, G.V. Driesschec, V. Alexandrakia et al., 2017. Evaluation of the antihypertensive angiotensin-converting enzyme inhibitory (ACE-I) activity and other probiotic properties of lactic acid bacteria isolated from traditional Greek dairy products. Int. Dairy J., 75: 10-21.
Li, C., L.Y. Kwok, Z. Mi, J. Bala and J. Xue et al., 2017. Characterization of the angiotensin-converting enzyme inhibitory activity of fermented milks produced with Lactobacillus casei. J. Dairy Sci., 100: 9495-9507.
Daliri, E.B.M., B.H. Lee, M.H. Park, J.H. Kim and D.H. Oh, 2018. Novel angiotensin I-converting enzyme inhibitory peptides from soybean protein isolates fermented by Pediococcus pentosaceus SDL1409. LWT, 93: 88-93.
Chen, Y., C. Li, J. Xue, L.y. Kwok, J. Yang, H. Zhang and B. Menghe, 2015. Characterization of angiotensin-converting enzyme inhibitory activity of fermented milk produced by Lactobacillus helveticus. J. Dairy Sci., 98: 5113-5124.
Singh, B.P., S. Vij and S. Hati, 2014. Functional significance of bioactive peptides derived from soybean. Peptides, 54: 171-179.
Mun, E.G., H.S. Sohn, M.S. Kim and Y.S. Cha, 2017. Antihypertensive effect of ganjang (traditional korean soy sauce) on sprague-dawley rats. Nutr. Res. Pract., 11: 388-395.
Hermanto, S., F. Hatiningsih and D.K. Putera, 2018. Antihypertensive bioactive peptides from hydrolysates of soy milk yoghurt (soygurt). J. Phys. Conf. Ser., Vol. 1095.
El-Ghaish, S., M. Dalgalarrondo, Y. Choiset, M. Sitohy, I. Ivanova, T. Haertle and J.M. Chobert, 2010. Screening of strains of Lactococci isolated from Egyptian dairy products for their proteolytic activity. Food Chem., 120: 758-764.
Donkor, O.N., A. Henriksson, T.K. Singh, T. Vasiljevic and N.P. Shah, 2007. ACE-inhibitory activity of probiotic yoghurt. Int. Dairy J., 17: 1321-1331.
Church, F.C., H.E. Swaisgood, D.H. Porter and G.L. Catignani, 1983. Spectrophotometric assay using o-phthaldialdehyde for determination of proteolysis in milk and isolated milk proteins. J. Dairy Sci., 66: 1219-1227.
Bradford, M.M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72: 248-254.
Cushman, D.W. and H.S. Cheung, 1971. Spectrophotometric assay and properties of the angiotensin-converting enzyme of rabbit lung. Biochem. Pharmacol., 20: 1637-1648.
Fuglsang, A., F.P. Rattray, D. Nilsson and N.C.B. Nyborg, 2003. Lactic acid bacteria: Inhibition of angiotensin converting enzyme in vitro and in vivo. Antonie van Leeuwenhoek, 83: 27-34.
Phyu, H.E., Z.K. OO and K.N. Aye, 2015. Screening on proteolytic activity of lactic acid bacteria from various yogurts and fermented milk. Int. J. Adv. Sci. Eng. Technol., 5: 34-37.
Tulini, F.L., N. Hymery, T. Haertlé, G.L. Blay and E.C.P.D. Martinis, 2016. Screening for antimicrobial and proteolytic activities of lactic acid bacteria isolated from cow, buffalo and goat milk and cheeses marketed in the southeast region of Brazil. J. Dairy Res., 83: 115-124.
Gonzalez-Gonzalez, C., T. Gibson and P. Jauregi, 2013. Novel probiotic-fermented milk with angiotensin I-converting enzyme inhibitory peptides produced by Bifidobacterium bifidum MF 20/5. Int. J. Food Microbiol., 167: 131-137.
Mugula, J.K., T. Sørhaug and L. Stepaniak, 2003. Proteolytic activities in togwa, a Tanzanian fermented food. Int. J. Food Microbiol., 84: 1-12.
Hati, S., N. Patel and S. Mandal, 2018. Comparative growth behaviour and biofunctionality of lactic acid bacteria during fermentation of soy milk and bovine milk. Probiotics Antimicrob. Proteins, 10: 277-283.
Quirós, A., B. Hernandez-Ledesma, M. Ramos, L. Amigo and I. Recio, 2005. Angiotensin-converting enzyme inhibitory activity of peptides derived from caprine kefir. J. Dairy Sci., 88: 3480-3487.
Hebert, E.M., G.S.D. Giori and R.R. Raya, 2001. Isolation and characterization of a slowly milk-coagulating variant of Lactobacillus helveticus deficient in purine biosynthesis. Applied Environ. Microbiol., 67: 1846-1850.
Yamamoto, N., A. Akino and T. Takano, 1993. Purification and specificity of a cell-wall-associated proteinase from Lactobacillus helveticus CP790. J. Biochem., 114: 740-745.
Hafeez, Z., C. Cakir-Kiefer, E. Roux, C. Perrin, L. Miclo and A. Dary-Mourot, 2014. Strategies of producing bioactive peptides from milk proteins to functionalize fermented milk products. Food Res. Int., 63: 71-80.
Savijoki, K., H. Ingmer and P. Varmanen, 2006. Proteolytic systems of lactic acid bacteria. Appl. Microbiol. Biotechnol., 71: 394-406.
Gilbert, C., B. Blanc, J. Frot-Coutaz, R. Portalier and D. Atlan, 1997. Comparison of cell surface proteinase activities within the Lactobacillus genus. J. Dairy Res., 64: 561-571.
Leclerc, P.L., S.F. Gauthier, H. Bachelard, M. Santure and D. Roy, 2002. Antihypertensive activity of casein-enriched milk fermented by Lactobacillus helveticus. Int. Dairy J., 12: 995-1004.
Pan, D. and Y. Guo, 2010. Optimization of sour milk fermentation for the production of ACE-inhibitory peptides and purification of a novel peptide from whey protein hydrolysate. Int. Dairy J., 20: 472-479.
Nielsen, M.S., T. Martinussen, B. Flambard, K.I. Sørensen and J. Otte, 2009. Peptide profiles and angiotensin-I-converting enzyme inhibitory activity of fermented milk products: Effect of bacterial strain, fermentation pH, and storage time. Int. Dairy J., 19: 155-165.
Youssef, C.B., G. Goma and A. Olmos-Dichara, 2005. Kinetic modelling of Lactobacillus casei ssp. rhamnosus growth and lactic acid production in batch cultures under various medium conditions. Biotechnol. Lett., 27: 1785-1789.
Gibbs, B.F., A. Zougman, R. Masse and C. Mulligan, 2004. Production and characterization of bioactive peptides from soy hydrolysate and soy-fermented food. Food Res. Int., 37: 123-131.
Singh, B.P. and S. Vij, 2017. Growth and bioactive peptides production potential of Lactobacillus plantarum strain C2 in soy milk: A LC-MS/MS based revelation for peptides biofunctionality. LWT, 86: 293-301.
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