Antioxidant Activity of Skimmed Cow and Soy Milks Fermented by Lactic Isolates of Kefir Granules
Applied Food Biotechnology,
Vol. 10 No. 3 (2023),
17 Ordibehesht 2023
,
Page 177-190
https://doi.org/10.22037/afb.v10i3.41673
Abstract
Background and Objective: The proteolytic system of lactic acid bacteria hydrolyzes milk protein into several peptides, including those with antioxidative activities. The aim of this study was to assess antioxidant activities in cow and soy milks fermented by Lacticaseibacillus rhamnosus BD2, Lentilactobacillus kefiri YK4 and Lentilactobacillus kefiri JK17 previously isolated from kefir granules and their correlations with the peptide contents.
Material and Methods: Reconstitutes of skimmed cow and soy milks were fermented by the highlighted isolates at 37 ℃ for 0, 24, 48 and 72 h. Fermented products were analyzed for the isolates, pH, total titratable acidity, antioxidant activity (% radical 2,2-diphenyl-1-picrylhydrazil inhibition and antioxidant capacity expressed in µg AAE.ml-1 whey) and total peptides. Fermented skimmed cow and soy milks with the highest antioxidant activity were then partially fractionated using molecular filters of 10 and 3 kDa. Fractions with the highest activity were analyzed further for peptide identification. Statistical analysis was carried out using one-way analysis of variance and Duncan multiple range tests (p≤0.05) using SPSS software v.16.0.
Results and Conclusion: All isolates were able to grow in reconstituted skimmed cow and soy milks, while total count of reached to 9 log CFU.ml-1 with significant (p≤0.05) increases in titratable acidity and total peptides and decreased pH. Growth of the three isolates was mildly slower in soy milk than in skimmed cow milk. The maximum antioxidant activities were seen after 72-h fermentation of cow and soy milks. No differences were observed in antioxidant activity of cow milk fermented by the three isolates; however, Lacticaseibacillus rhamnosus BD2 produced the highest antioxidant activity in soy milk. In general, increases in antioxidant activities correlated with increases in the peptide contents. Fraction of less than 3 kDa of the two milks fermented by Lacticaseibacillus rhamnosus BD2 showed the highest antioxidant activity. Analyses of peptides present in these fractions using high resolution LC-MS/MS and in silico identification of peptides with antioxidant activity have been reported in this study. The present study suggests that the three isolates can be used as starter cultures in fermenting cow and soy milks to increase their antioxidant activities. Peptides with molecular weight of less than 3 kDa play key roles in antioxidant activity.
Conflict of interest: The authors declare no conflict of interest.
- ▪ Fermented milk ▪ Lacticaseibacillus rhamnosus ▪ Lentilactobacilluskefiri ▪ Peptides ▪Starter culture
How to Cite
References
Phaniendra A, Babu Jestady D, Periyasamy L. Free radicals: properties, sources, targets and their implication in various diseases. Ind J Clin Biochem. 2015; 30 (1):11-26.
https://doi.org/10.1007/s12291-014-0446-0
Li Y, Liu T, He G. Antioxidant activity of peptides from fermented milk with mix culture of lactic acid bacteria and yeast. Adv J Food SciTechnol. 2015; 7 (6): 422-427.
http://doi.org/10.19026/ajfst.7.1335
Fadlillah HN, Nuraida L, Sitanggang AB, Palupi NS. Produ-ction of antioxidants through lactic acid fermentation: Current developments and outlook. Fascicle VI Food Technol. 2021; 45(2):203-228.
https://doi.org/10.35219/foodtechnology.2021.2.13
Yilmaz-Ersan L, Ozcan T, Akpinar-Bayizit A, Sahin S. Compa-rison of antioxidant capacity of cow and ewe milk kefirs. J Dairy Sci. 2018; 101: 3788-3798.
https://doi.org/10.3168/jds.2017-13871
Shi X, Chen H, Li Y, Huang J, He Y. Effects of kefir grains on fermentation and bioactivity of goat milk. Acta Univ Cibinien-sis Ser E Food Technol. 2018; 22 (1):43-50.
https://doi.org/10.2478/aucft-2018-0005
Mahdi C, Untari H, Padaga MC. Identification and characteri-zation of bioactive peptides of fermented goat milk as a sources of antioxidant as a therapeutic natural product. IOP Conf Mat Sci Eng. 2018; 299 (1):1-6.
https://doi.org/10.1088/1757-899X/299/1/012014
Soleymanzadeh N, Mirdamadi S, Kianirad M. Antioxidant activity of camel and bovine milk fermented by lactic acid bacteria isolated from traditional fermented camel milk (Chal). Dairy Sci Technol. 2016; 96 (4):443-457.
https://doi.org/10.1007/s13594-016-0278-1
Marazza A, Nazareno A, Savoy G, Giori D, Garro MS. Enhancement of the antioxidant capacity of soymilk by fermentation with Lactobacillus rhamnosus. J Funct Foods. 2012; 4:594-601.
https://doi.org/10.1016/j.jff.2012.03.005
Yamamoto N, Shoji M, Hoshigami H, Watanabe K, Watanabe K, Takatsuzu T, Yasuda S, Igoshi K, Kinoshita H. Antioxidant capacity of soymilk yogurt and exopolysaccharides produced by lactic acid bacteria. Biosc Microbiota Food Health. 2019; 38(3): 97-104.
https://doi.org/10.12938/bmfh.18-017
Kleekayai T, Harnedy PA, O’Keeffe MB, Poyarkov AA, CunhaNeves A, Suntornsuk W, FitzGerald RJ. Extraction of antioxidant and ACE inhibitory peptides from thai traditional fermented shrimp pastes. Food Chem. 2015; 176 (6): 441-447.
https://doi.org/10.1016/j.foodchem.2014.12.026
Najafian L, Salam A. Fractionation and identification of novel antioxidant peptides from fermented fish (pekasam). J Food Meas Charact. 2018; 12 (3): 2174-2183.
https://doi.org/10.1007/s11694-018-9833-1
Ryu E, Yang J, Lee M, Kim SH, Seo H, Jung J. Antioxidant effects of kimchi supplemented with black raspberry during fermentation protect against liver cirrhosis-induced oxidative stress in rats. Nutr Res Pract. 2019; 13 (2):87-94.
https://doi.org/10.4162/nrp.2019.13.2.87
Athaillah ZA, Muzdalifah D, Lestari A, Fitria A, Udin LZ, Artanti N, Lioe HN. Phenolic compound profile and functionality of aqueous overripe tempe extracts. Curr Res Nutr Food Sci. 2019; 7 (2):382-392.
https://dx.doi.org/10.12944/CRNFSJ.7.2.08
Raveschot C, Cudennec B, Coutte F, Flahaut C, Fremont M, Drider D, Dhulster P. Production of bioactive peptides by Lactobacillus Species: From gene to application. Front Microbiol. 2018; 9: 2354.
https://doi.org/10.3389/fmicb.2018.02354
Phelan M, Aherne A, Fitzgerald RJ, Brien NMO. Casein-derived bioactive peptides: Biological effects, industrial uses, safety aspects and regulatory status. Int Dairy J. 2009; 19 (11): 643-654.
https://doi.org/10.1016/j.idairyj.2009.06.001
Sanjukta S, Rai AK. Production of bioactive peptides during soybean fermentation and their potential health benefits. Trends Food Sci Technol. 2016; 50:1-10.
https://doi.org/10.1016/j.tifs.2016.01.010
Yousefi L, Habibi Najafi MB, Edalatian Dovom MR. Production of bioactive peptides in milk using two native strains of Levilactobacillus brevis. Appl Food Biotechnol. 2023; 10 (2): 103-111
https://doi.org/10.22037/afb.v10i2.40640
Abubakr MAS, Hassan Z, Imdakim MMA. Antioxidant activity of lactic acid bacteria (LAB) fermented skim milk as determined by 1,1-diphenyl-2- picrylhydrazyl (DPPH) and ferrous chelating activity (FCA). Afr J Microbiol Res. 2012; 6 (34): 6358-6364.
https://doi.org/10.5897/AJMR12.702
Taha S, El M, Cristian A, Mahmoud DG. Antioxidant and antibacterial activities of bioactive peptides in buffalo yoghurt fermented with different starter cultures. Food Sci Biotechnol. 2017; 26 (5): 1325-1332.
https://doi.org/10.1007/s10068-017-0160-9
Balakrishnan G, Agrawal R. Antioxidant activity and fatty acid profile of fermented milk prepared by Pediococcus pento-saceus. J Food Sci Technol. 2014; 51 (12):4138-4142.
https://doi.org/10.1007/s13197-012-0891-9
Moslehishad M, Reza M, Salami M, Mirdamadi S. The comparative assessment of ACE - inhibitory and antioxidant activities of peptide fractions obtained from fermented camel and bovine milk by Lactobacillus rhamnosus PTCC 1637. Int Dairy J. 2013; 29 (2): 82-87.
https://doi.org/10.1016/j.idairyj.2012.10.015
Uugantsetseg E, Batjargal B. Antioxidant activity of probiotic lactic acid bacteria isolated from Mongolian airag. Mong J Chem. 2014; 15 (41): 73-78.
https://doi.org/10.5564/mjc.v15i0.327
Yusuf D, Nuraida L, Dewanti-hariyadi R, Hunaefi D. In vitro antioxidant and α -glucosidase inhibitory activities of Lactoba-cillus spp. isolated from Indonesian kefir grains. Appl Food Biotechnol. 2021; 8 (1): 39-46.
https://doi.org/10.22037/afb.v8i1.30367
Yusuf D, Nuraida L, Dewanti-hariyadi R, Hunaefi D. Lactic acid bacteria and yeasts from Indonesian kefir grains and their growth interaction. Asian J Microbiol Biotech Env Sc. 2020; 22(1):44-49.
Rubak YT, Nuraida L, Iswantini D, Prangdimurti E. Angiotensin-I-converting enzyme inhibitory peptides in milk fermented by indigenous lactic acid bacteria. Vet World. 2020; 13 (2): 345-353.
https://doi.org/10.14202/vetworld.2020.345-353
FDA. 2011. Bacteriological analytical method-bacteriological analytical manual chapter 3 aerobic plate count.
AOAC. Official methods of analysis association of official analytical chemistry. AOAC Int. Washington D.C. 2006.
Kim DO, Lee KW, Lee HJ, Lee CYo. Vitamin C equivalent antioxidant capacity (VCEAC) of phenolic phytochemicals. J Agric Food Chem. 2002; 50: 3713-3717.
https://doi.org/10.1021/jf020071c
Lowry H, Rosebrough NJ, A. Lewis Farr RJR. Protein measurement with the folin phenol reagent. J Biol Chem. 1951; 193 (1): 265-275.
https://doi.org/10.1016/S0021-9258(19)52451-6
Minkiewicz P, Iwaniak A, Darewicz M. BIOPEP-UWM database of bioactive peptides: Current opportunities. Int J Mol Sci. 2019; 20(23) : 5978.
https://doi.org/10.3390/ijms20235978
Muncan J, Tei K, Tsenkova R. Real-Time Monitoring of Yogurt Fermentation Process by Aquaphotomics Near-Infrared Spectroscopy. Sensors. 2021; 21: 177.
https://doi.org/10.3390/s21010177
Marya DT, Nurliyani, Widodo, Sunarti. Characterization and antioxidant activity of fermented milk produced with a starter combination. Pakistan J Nutr. 2017; 6 (16): 451-456.
https://doi.org/10.3923/pjn.2017.451.456
Li Changkun, Kwok L, Mi Z, Bala J, Xue J, Yang J, Ma Y. Characterization of the angiotensin-converting enzyme inhibitory activity of fermented milks produced with Lactoba-cillus casei. J Dairy Sci. 2017; 100:1-13.
https://doi.org/10.3168/jds.2017-12970
Yusmarini Y, Indriati R, Utami T, Marsono Y. Aktivitas proteolitik bakteri asam laktat dalam fermentasi susu kedelai (proteolytic activities of lactic acid bacteria in fermentation of soymilk). J Teknol dan Ind Pangan. 2010; 21 (2): 129-134.
Hajirostamloo B, Mahastie P. Comparison of soymilk and cow milk nutritional parameter. Res J Biol Sci. 2008; 3 (11): 1324-1326.
https://doi.org/?doi=rjbsci.2008.1324.1326
Gamba RR, Yamammoto S, Abdel-Hamid M, Sasaki T, Michihata T, Koyanagi T, Enomoto T. Chemical, microbi-ological and functional characterization of kefir produced from cow’s milk and soy milk. Int J Microbiol. 2020; 2020:1-11.
https://doi.org/10.1155/2020/7019286
Singh BP, Vij S. Growth and bioactive peptides production potential of Lactobacillus plantarum strain C2 in soy milk: A LC-MS / MS based revelation for peptides biofunctionality. LWT Food Sci Technol. 2017; 86: 293-301.
https://doi.org/10.1016/j.lwt.2017.08.013
Karadag A, Ozcelik B, Saner S. Review of methods to determine antioxidant capacities. Food Anal Methods. 2009; 2 (1): 41-60.
https://doi.org/10.1007/s12161-008-9067-7
Yang X, Zhou J, Fan L, Qin Z. Antioxidant properties of a vegetable-fruit beverage fermented with two Lactobacillus plantarum strains. Food Sci Biotechnol. 2018; 6: 1-8.
https://doi.org/10.1007/s10068-018-0411-4
Farvin KHS, Baron CP, Skall N, Otte J, Jacobsen C. Antioxidant activity of yoghurt peptides: Part 2- characterisation of peptide fractions. Food Chem. 2010; 123 (4): 1090-1097.
https://doi.org/10.1016/j.foodchem.2010.05.029
Ramesh V, Kumar R, Singh RRB, Kaushik JK, Man B. Comparative evaluation of selected strains of Lactobacilli for the development of antioxidant activity in milk. Dairy Sci Technol. 2012; 92(2): 179-188.
https://doi.org/10.1007/s13594-011-0048-z
Hafees Z, Cakir-Kiefer C, Roux E, Perrin C, Miclo L, Dary-Mourot A. Strategies of producing bioactive peptides from milk proteins to functionalize fermented milk products. Food Res Int. 2014; 6: 1-46.
https://doi.org/10.1016/j.foodres.2014.06.002
Vasconcellos FCS, Woiciechowski AL, Soccol VT, Mantovani D, Soccol CR. Antimicrobial and antioxidant properties of β-conglycinin and glycinin from soy protein isolate. Int J Curr Micorbio App Sci. 2014; 3(8): 144-157.
Tonolo F, Moretto L, Grinzato A, Fiorese F, Folda A, Scalcon V, Ferro S, Arrigoni G, Bellamio M, Feller E. Fermented soy-derived bioactive peptides selected by a molecular docking antioxidants fermented soy-derived bioactive peptides selected by a molecular docking approach show antioxidant properties involving the Keap1/Nrf2 pathway. Antioxidants. 2020; 9 (117): 1-22.
https://doi.org/10.3390/antiox9121306
El-fattah AA, Azzam M, Elkashef H, Elhadydy A. Antioxidant properties of milk: effect of milk species, milk fractions and heat treatments. Int J Dairy Sci. 2020; 15 (1): 1-9.
https://doi.org/10.3923/ijds.2020.1.9
Ramos LR, Santos JS, Daguer H, Valese AC, Cruz AG, Granato D. Analytical optimization of a phenolic-rich herbal extract and supplementation in fermented milk containing sweet potato pulp. Food Chem. 2016; 11:1-37.
https://doi.org/10.1016/j.foodchem.2016.11.069
Park H, Lee M, Kim K, Park E, Paik H. Antioxidant and antigenotoxic effect of dairy products supplemented with red ginseng extract. J Dairy Sci. 2018; 101: 1-9.
https://doi.org/10.3168/jds.2018-14690
Kieliszek M, Pobiega K, Piwowarek K, Kot AM. Characteristics of the proteolytic enzymes produced by lactic acid bacteria. Molecules. 2021; 26(7):1858.
https://doi.org/10.3390/molecules26071858
Solieri L, Rutella GS, Tagliazucchi D. Impact of non-starter Lactobacilli on release of peptides with angiotensin-converting enzyme inhibitory and antioxidant activities during bovine milk fermentation. Food Microbiol. 2015; 51: 108-116.
https://doi.org/10.1016/j.fm.2015.05.012
- Abstract Viewed: 239 times
- pdf Downloaded: 345 times