Bioconversion of isoflavones glycoside to aglycone during edamame (Glycine max) soygurt production using Streptococcus thermophillus FNCC40, Lactobacillus delbrueckii FNCC41, and L. plantarum FNCC26
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Abstract. Lovabyta NS, Jayus J, Nugraha AS. 2020. Bioconversion of isoflavones glycoside to aglycone during edamame (Glycine max) soygurt production using Streptococcus thermophillus FNCC40, Lactobacillus delbrueckii FNCC41, and L. plantarum FNCC26. Biodiversitas 21: 1358-1364. Due to its strong radical-scavenging and antioxidative activity, isoflavones in soybeans have received great attention for the development of functional foods. This study focused on bioconversion of isoflavones glycoside into its aglycone form of edamame green soymilk fermented with three lactic acid bacteria (LAB), i.e., S. thermophilus FNCC40, L. bulgaricus FNCC41, and L. plantarum FNCC26 to produce soygurt. Green soymilk was fermented with 6% (v/v) of LABs as a starter culture for 24 hours at 37ºC. Its antioxidative activity were measured using DPPH free radical scavenging activity method. Daidzein and genistein released during fermentation were fractionated using HPLC and detected further by LCMS to confirm the presence of these two substances. The results showed that the population density of starter culture in green soymilk reached 109 CFU/mL, and the pH decrease from 6.8 to 3.5. All LABs cultures used in the fermentation process were able to produce free aglycone, releasing more daidzein and genistein. Increasing daidzein and genistein content in soygurt results in increasing antioxidative activity. The highest antioxidative activity (IC50 = 41.01 mg/mL) was found in the soygurt fermented with S. thermophilus FNCC40. This finding indicates that S. thermophilus FNCC40, L. bulgaricus FNCC41, and L. plantarum FNCC26 are potential as an effective starter culture to produce a soygurt with good antioxidant activity.
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References
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Campos MDGR, Matos MP. 2010. Bioactivity of Isoflavones: Assessment through a Theoretical Model as a Way to Obtain a ‘Theoretical Efficacy Related to Estradiol (TERE). International Journal of Molecular Sciences 11 (2): 480–91. https://doi.org/10.3390/ijms11020480.
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Choi EJ, Kim GH. 2014. The Antioxidant Activity of Daidzein Metabolites, O-Desmethylangolensin and Equol, in HepG2 Cells. Molecular Medicine Reports 9 (1): 328–32. https://doi.org/10.3892/mmr.2013.1752.
Chun J, Kim GM, Lee KW, Choi ID, Kwon GH, Park JY, Jeong SJ, Kim SJ, Kim JH. 2007. Conversion of Isoflavone Glucosides to Aglycones in Soymilk by Fermentation with Lactic Acid Bacteria. 2007. Journal of Food Science 72 (2): 39–44. https://doi.org/10.1111/j.1750-3841.2007.00276.x.
Dhayakaran RPA, Neethirajan S, Xue J, Shi J. 2015. Characterization of Antimicrobial Efficacy of Soy Isoflavones against Pathogenic Biofilms. LWT - Food Science and Technology 63 (2): 859–65. https://doi.org/10.1016/j.lwt.2015.04.053.
Donkor ON, Henriksson A, Vasiljevic T, Shah NP. 2007. Original Article Proteolytic Activity of Dairy Lactic Acid Bacteria and Probiotics as Determinant of Growth and in Vitro Angiotensin-Converting Enzyme Inhibitory Activity in Fermented Milk. Lait 86 (2007) 21–38. https://doi.org/10.1051/lait.
Foong YJ, Lee ST, Ramli N, Tan YN, Ayob MK. 2013. Incorporation of Potential Probiotic Lactobacillus plantarum Isolated from Fermented Cocoa Beans into Dark Chocolate: Bacterial Viability and Physicochemical Properties Analysis. Journal of Food Quality 36 (3): 164–71. https://doi.org/10.1111/jfq.12028.
Fu YH, Zhang FC. 2013. Changes in Isoflavone Glucoside and Aglycone Contents of Chickpea Yoghurt during Fermentation by Lactobacillus bulgaricus and Streptococcus thermophilus. Journal of Food Processing and Preservation 37 (5): 744–50. https://doi.org/10.1111/j.1745-4549.2012.00713.x.
Hammond BG, Jez JM. 2011. Impact of Food Processing on the Safety Assessment for Proteins Introduced into Biotechnology-Derived Soybean and Corn Crops. Food and Chemical Toxicology 49 (4): 711–21. https://doi.org/10.1016/j.fct.2010.12.009.
Hasim, Astuti P, Falah S, Faridah DN. 2015. Bacillus subtilis Natto Fermentation to Improve Aglycone Isoflavones Content of Black Soybean Varieties Detam 2. International Food Research Journal 22 (6): 2558–64.
Iovine B, Iannella ML, Gasparri F, Monfrecola G, Bevilacqua MA. 2011. Synergic Effect of Genistein and Daidzein on UVB-Induced DNA Damage: An Effective Photoprotective Combination. Journal of Biomedicine and Biotechnology 2011. https://doi.org/10.1155/2011/692846.
Isa JK, Razavi SH. 2017. Characterization of Lactobacillus plantarum as a Potential Probiotic In Vitro and Use of a Dairy Product (Yogurt) as Food Carrier. Applied Food Biotechnology 4 (1): 11–18. https://doi.org/10.22037/afb.v4i1.13738.
Islam MA, Punt A, Spenkelink B, Murk AJ, van Leeuwen FXR, Rietjens IMCM. 2014. Conversion of Major Soy Isoflavone Glucosides and Aglycones in in Vitro Intestinal Models. Molecular Nutrition and Food Research 58 (3): 503–15. https://doi.org/10.1002/mnfr.201300390.
James A. 2007. Edamame Soybean Development in Australia. Rural Industries Research and Development Corporation, Australian Government.
Jooyandeh H. 2011. Soy Products as Healthy and Functional Foods. Middle-East Journal of Sciintific Research 7 (1): 71–80.
Ko KP. 2014. Isoflavones: Chemistry, Analysis, Functions and Effects on Health and Cancer. Asian Pac J Cancer Prev 15 (17): 7001-7010. https://doi.org/10.7314/APJCP.2014.15.17.7001.
Kobayashi M, Egusa S, Fukuda M. 2014. Isoflavone and Protein Constituents of Lactic Acid-Fermented Soy Milk Combine to Prevent Dyslipidemia in Rats Fed a High Cholesterol Diet. Nutrients 6 (12): 5704–23. https://doi.org/10.3390/nu6125704.
Kok FS, Muhamad II, Lee CT, Razali F, Pa'e N, Shaharuddin S. 2012. Effects of PH and Temperature on the Growth and ?-Glucosidase Activity of Lactobacillus rhamnosus NRRL 442 in Anaerobic Fermentation. International Review of Chemical Engineering (I.RE.CH.E.), Vol. 4, N. 3 May 2012.
Lee CH, Yang L, Xu JZ, Yeung SYV, Huang Y, Chen ZY. 2005. Relative Antioxidant Activity of Soybean Isoflavones and Their Glycosides. Food Chemistry 90 (4): 735–41. https://doi.org/10.1016/j.foodchem.2004.04.034.
Lee M, Hong GE, Zhang H, Yang CY, Han KH. 2015. Production of the Isoflavone Aglycone and Antioxidant Activities in Black Soymilk Using Fermentation with Streptococcus thermophilus S10. Food Sci. Biotechnol. 24(2): 537-544 (2015). https://doi.org/10.1007/s10068-015-0070-7.
Li C, Chen Y, Kwok LY, Chen X, Yu H, Yang H, Yang J, Xue J, Sun T, Zhang H. 2015. Identification of Potential Probiotic Lactobacillus plantarum Isolates with Broad-Spectrum Antibacterial Activity. Dairy Science and Technology 95 (3): 381–92. https://doi.org/10.1007/s13594-014-0206-1.
Li C, Song J, Kwok LY, Wang J, Dong Y, Yu H, Hou Q, Zhang H, Chen Y. 2017. Influence of Lactobacillus plantarum on Yogurt Fermentation Properties and Subsequent Changes during Postfermentation Storage. Journal of Dairy Science 100 (4): 2512–25. https://doi.org/10.3168/jds.2016-11864.
Mebrahtu T, Mohamed A, Wang CY, Andebrhan T. 2004. Analysis of Isoflavone Contents in Vegetable Soybeans. Plant Foods for Human Nutrition 59: 55–61, 2004.
Medjakovic S, Mueller M, Jungbauer A. 2010. Potential Health-Modulating Effects of Isoflavones and Metabolites via Activation of PPAR and AhR. Nutrients 2 (3): 241–79. https://doi.org/10.3390/nu2030241.
Molina V, Médici M, de Valdez GF, Taranto MP. 2012. Soybean-Based Functional Food with Vitamin B 12-Producing Lactic Acid Bacteria. Journal of Functional Foods 4 (4): 831–36. https://doi.org/10.1016/j.jff.2012.05.011.
Montero G, Günther G, Valdés K, Arriagada F, Morales J. 2018. An HPLC Method for the Determination of Isoflavones and the Evaluation of Their Antioxidant Capacity in Both Homogeneous and Microheterogeneous Systems. Journal of AOAC International 101 (1): 235–41. https://doi.org/10.5740/jaoacint.17-0104.
Peng X, Guo S. 2015. Texture Characteristics of Soymilk Gels Formed by Lactic Fermentation: A Comparison of Soymilk Prepared by Blanching Soybeans under Different Temperatures. Food Hydrocolloids 43: 58–65. https://doi.org/10.1016/j.foodhyd.2014.04.034.
Prasad LN, Shah NP. 2012. Conversion of Isoflavone Glycoside to Aglycones in Soy Protein Isolate (SPI) Using Crude Enzyme Extracted from Bifidobacterium animalis Bb12 and Lactobacillus delbrueckii ssp. bulgaricus ATCC 11842. International Food Research Journal 19 (2): 433–39.
Rafii F. 2015. The Role of Colonic Bacteria in the Metabolism of the Natural Isoflavone Daidzin to Equol. Metabolites 5 (1): 56–73. https://doi.org/10.3390/metabo5010056.
Rekha CR, Vijayalakshmi G. 2010. Bioconversion of Isoflavone Glycosides to Aglycones, Mineral Bioavailability and Vitamin B Complex in Fermented Soymilk by Probiotic Bacteria and Yeast. Journal of Applied Microbiology. https://doi.org/10.1111/j.1365-2672.2010.04745.x.
Rigo AA, Dahmer AM, Steffens C, Steffens J, Carrão-Panizzi. 2015. Characterization of Soybean Cultivars Genetically Improved for Human Consumption. International Journal of Food Engineering 1 (1): 1–7. https://doi.org/10.18178/ijfe.1.1.1-7.
Sirilun S, Chaiyasut C, Kesika P, Peerajan S, Sivamaruthi BS. 2017a. Screening of Lactic Acid Bacteria with Immune Modulating Property, and the Production of Lactic Acid Bacteria Mediated Fermented Soymilk. National Journal of Physiology, Pharmacy and Pharmacology 7 (12): 1397–1405. https://doi.org/10.5455/njppp.2017.7.0933926092017.
Sirilun S, Sivamaruthi BS, Kesika P, Peerajan S, Chaiyasut C. 2017b. Lactic Acid Bacteria Mediated Fermented Soybean as a Potent Nutraceutical Candidate. Asian Pacific Journal of Tropical Biomedicine 7 (10): 930–36. https://doi.org/10.1016/j.apjtb.2017.09.007.
Tsuda H, Shibata E. 2017. Bioconversion of Daidzin to Daidzein by Lactic Acid Bacteria in Fermented Soymilk. Food Science and Technology Research 23 (1): 157–62. https://doi.org/10.3136/fstr.23.157.
U.S. Department of Agriculture. 2008. USDA Database for the Isoflavone Content of Selected Foods. In Release 2.0. U.S. Department of Agriculture Agricultural Research Service Beltsville Human Nutrition Research Center, U.S. Department of Agriculture. http://www.ars.usda.gov/nutrientdata.
Baglio E. 2014. Chemistry and Technology of Yoghurt Fermentation. Springer, Catania–Italy. https://doi.org/10.1007/978-3-319-07377-4.
Campos MDGR, Matos MP. 2010. Bioactivity of Isoflavones: Assessment through a Theoretical Model as a Way to Obtain a ‘Theoretical Efficacy Related to Estradiol (TERE). International Journal of Molecular Sciences 11 (2): 480–91. https://doi.org/10.3390/ijms11020480.
Chang TS. 2014. Isolation, Bioactivity, and Production of Ortho-Hydroxydaidzein and Ortho-Hydroxygenistein. International Journal of Molecular Sciences 15 (4): 5699–5716. https://doi.org/10.3390/ijms15045699.
Choi EJ, Kim GH. 2014. The Antioxidant Activity of Daidzein Metabolites, O-Desmethylangolensin and Equol, in HepG2 Cells. Molecular Medicine Reports 9 (1): 328–32. https://doi.org/10.3892/mmr.2013.1752.
Chun J, Kim GM, Lee KW, Choi ID, Kwon GH, Park JY, Jeong SJ, Kim SJ, Kim JH. 2007. Conversion of Isoflavone Glucosides to Aglycones in Soymilk by Fermentation with Lactic Acid Bacteria. 2007. Journal of Food Science 72 (2): 39–44. https://doi.org/10.1111/j.1750-3841.2007.00276.x.
Dhayakaran RPA, Neethirajan S, Xue J, Shi J. 2015. Characterization of Antimicrobial Efficacy of Soy Isoflavones against Pathogenic Biofilms. LWT - Food Science and Technology 63 (2): 859–65. https://doi.org/10.1016/j.lwt.2015.04.053.
Donkor ON, Henriksson A, Vasiljevic T, Shah NP. 2007. Original Article Proteolytic Activity of Dairy Lactic Acid Bacteria and Probiotics as Determinant of Growth and in Vitro Angiotensin-Converting Enzyme Inhibitory Activity in Fermented Milk. Lait 86 (2007) 21–38. https://doi.org/10.1051/lait.
Foong YJ, Lee ST, Ramli N, Tan YN, Ayob MK. 2013. Incorporation of Potential Probiotic Lactobacillus plantarum Isolated from Fermented Cocoa Beans into Dark Chocolate: Bacterial Viability and Physicochemical Properties Analysis. Journal of Food Quality 36 (3): 164–71. https://doi.org/10.1111/jfq.12028.
Fu YH, Zhang FC. 2013. Changes in Isoflavone Glucoside and Aglycone Contents of Chickpea Yoghurt during Fermentation by Lactobacillus bulgaricus and Streptococcus thermophilus. Journal of Food Processing and Preservation 37 (5): 744–50. https://doi.org/10.1111/j.1745-4549.2012.00713.x.
Hammond BG, Jez JM. 2011. Impact of Food Processing on the Safety Assessment for Proteins Introduced into Biotechnology-Derived Soybean and Corn Crops. Food and Chemical Toxicology 49 (4): 711–21. https://doi.org/10.1016/j.fct.2010.12.009.
Hasim, Astuti P, Falah S, Faridah DN. 2015. Bacillus subtilis Natto Fermentation to Improve Aglycone Isoflavones Content of Black Soybean Varieties Detam 2. International Food Research Journal 22 (6): 2558–64.
Iovine B, Iannella ML, Gasparri F, Monfrecola G, Bevilacqua MA. 2011. Synergic Effect of Genistein and Daidzein on UVB-Induced DNA Damage: An Effective Photoprotective Combination. Journal of Biomedicine and Biotechnology 2011. https://doi.org/10.1155/2011/692846.
Isa JK, Razavi SH. 2017. Characterization of Lactobacillus plantarum as a Potential Probiotic In Vitro and Use of a Dairy Product (Yogurt) as Food Carrier. Applied Food Biotechnology 4 (1): 11–18. https://doi.org/10.22037/afb.v4i1.13738.
Islam MA, Punt A, Spenkelink B, Murk AJ, van Leeuwen FXR, Rietjens IMCM. 2014. Conversion of Major Soy Isoflavone Glucosides and Aglycones in in Vitro Intestinal Models. Molecular Nutrition and Food Research 58 (3): 503–15. https://doi.org/10.1002/mnfr.201300390.
James A. 2007. Edamame Soybean Development in Australia. Rural Industries Research and Development Corporation, Australian Government.
Jooyandeh H. 2011. Soy Products as Healthy and Functional Foods. Middle-East Journal of Sciintific Research 7 (1): 71–80.
Ko KP. 2014. Isoflavones: Chemistry, Analysis, Functions and Effects on Health and Cancer. Asian Pac J Cancer Prev 15 (17): 7001-7010. https://doi.org/10.7314/APJCP.2014.15.17.7001.
Kobayashi M, Egusa S, Fukuda M. 2014. Isoflavone and Protein Constituents of Lactic Acid-Fermented Soy Milk Combine to Prevent Dyslipidemia in Rats Fed a High Cholesterol Diet. Nutrients 6 (12): 5704–23. https://doi.org/10.3390/nu6125704.
Kok FS, Muhamad II, Lee CT, Razali F, Pa'e N, Shaharuddin S. 2012. Effects of PH and Temperature on the Growth and ?-Glucosidase Activity of Lactobacillus rhamnosus NRRL 442 in Anaerobic Fermentation. International Review of Chemical Engineering (I.RE.CH.E.), Vol. 4, N. 3 May 2012.
Lee CH, Yang L, Xu JZ, Yeung SYV, Huang Y, Chen ZY. 2005. Relative Antioxidant Activity of Soybean Isoflavones and Their Glycosides. Food Chemistry 90 (4): 735–41. https://doi.org/10.1016/j.foodchem.2004.04.034.
Lee M, Hong GE, Zhang H, Yang CY, Han KH. 2015. Production of the Isoflavone Aglycone and Antioxidant Activities in Black Soymilk Using Fermentation with Streptococcus thermophilus S10. Food Sci. Biotechnol. 24(2): 537-544 (2015). https://doi.org/10.1007/s10068-015-0070-7.
Li C, Chen Y, Kwok LY, Chen X, Yu H, Yang H, Yang J, Xue J, Sun T, Zhang H. 2015. Identification of Potential Probiotic Lactobacillus plantarum Isolates with Broad-Spectrum Antibacterial Activity. Dairy Science and Technology 95 (3): 381–92. https://doi.org/10.1007/s13594-014-0206-1.
Li C, Song J, Kwok LY, Wang J, Dong Y, Yu H, Hou Q, Zhang H, Chen Y. 2017. Influence of Lactobacillus plantarum on Yogurt Fermentation Properties and Subsequent Changes during Postfermentation Storage. Journal of Dairy Science 100 (4): 2512–25. https://doi.org/10.3168/jds.2016-11864.
Mebrahtu T, Mohamed A, Wang CY, Andebrhan T. 2004. Analysis of Isoflavone Contents in Vegetable Soybeans. Plant Foods for Human Nutrition 59: 55–61, 2004.
Medjakovic S, Mueller M, Jungbauer A. 2010. Potential Health-Modulating Effects of Isoflavones and Metabolites via Activation of PPAR and AhR. Nutrients 2 (3): 241–79. https://doi.org/10.3390/nu2030241.
Molina V, Médici M, de Valdez GF, Taranto MP. 2012. Soybean-Based Functional Food with Vitamin B 12-Producing Lactic Acid Bacteria. Journal of Functional Foods 4 (4): 831–36. https://doi.org/10.1016/j.jff.2012.05.011.
Montero G, Günther G, Valdés K, Arriagada F, Morales J. 2018. An HPLC Method for the Determination of Isoflavones and the Evaluation of Their Antioxidant Capacity in Both Homogeneous and Microheterogeneous Systems. Journal of AOAC International 101 (1): 235–41. https://doi.org/10.5740/jaoacint.17-0104.
Peng X, Guo S. 2015. Texture Characteristics of Soymilk Gels Formed by Lactic Fermentation: A Comparison of Soymilk Prepared by Blanching Soybeans under Different Temperatures. Food Hydrocolloids 43: 58–65. https://doi.org/10.1016/j.foodhyd.2014.04.034.
Prasad LN, Shah NP. 2012. Conversion of Isoflavone Glycoside to Aglycones in Soy Protein Isolate (SPI) Using Crude Enzyme Extracted from Bifidobacterium animalis Bb12 and Lactobacillus delbrueckii ssp. bulgaricus ATCC 11842. International Food Research Journal 19 (2): 433–39.
Rafii F. 2015. The Role of Colonic Bacteria in the Metabolism of the Natural Isoflavone Daidzin to Equol. Metabolites 5 (1): 56–73. https://doi.org/10.3390/metabo5010056.
Rekha CR, Vijayalakshmi G. 2010. Bioconversion of Isoflavone Glycosides to Aglycones, Mineral Bioavailability and Vitamin B Complex in Fermented Soymilk by Probiotic Bacteria and Yeast. Journal of Applied Microbiology. https://doi.org/10.1111/j.1365-2672.2010.04745.x.
Rigo AA, Dahmer AM, Steffens C, Steffens J, Carrão-Panizzi. 2015. Characterization of Soybean Cultivars Genetically Improved for Human Consumption. International Journal of Food Engineering 1 (1): 1–7. https://doi.org/10.18178/ijfe.1.1.1-7.
Sirilun S, Chaiyasut C, Kesika P, Peerajan S, Sivamaruthi BS. 2017a. Screening of Lactic Acid Bacteria with Immune Modulating Property, and the Production of Lactic Acid Bacteria Mediated Fermented Soymilk. National Journal of Physiology, Pharmacy and Pharmacology 7 (12): 1397–1405. https://doi.org/10.5455/njppp.2017.7.0933926092017.
Sirilun S, Sivamaruthi BS, Kesika P, Peerajan S, Chaiyasut C. 2017b. Lactic Acid Bacteria Mediated Fermented Soybean as a Potent Nutraceutical Candidate. Asian Pacific Journal of Tropical Biomedicine 7 (10): 930–36. https://doi.org/10.1016/j.apjtb.2017.09.007.
Tsuda H, Shibata E. 2017. Bioconversion of Daidzin to Daidzein by Lactic Acid Bacteria in Fermented Soymilk. Food Science and Technology Research 23 (1): 157–62. https://doi.org/10.3136/fstr.23.157.
U.S. Department of Agriculture. 2008. USDA Database for the Isoflavone Content of Selected Foods. In Release 2.0. U.S. Department of Agriculture Agricultural Research Service Beltsville Human Nutrition Research Center, U.S. Department of Agriculture. http://www.ars.usda.gov/nutrientdata.
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