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References

  1. Cho KM, Hong SY, Math RK, Lee JH, Kambiranda DM, Kim JM, et al. 2009. Biotransformation of phenolics (isoflavones, flavanols and phenolic acids) during the fermentation of cheonggukjang by Bacillus pumilus HY1. Food Chem. 114: 413419.
    CrossRef
  2. Cho KM, Lee JH, Yun HD, Ahn BY, Kim H, Seo WT. 2011. Changes of phytochemical constituents (isoflavones, flavanols, and phenolic acids) during cheonggukjang soybeans fermentation using potential probiotics Bacillus subtilis CS90. J. Food Comp. Anal. 24: 402-410.
    CrossRef
  3. Choi JS, Kim HY, Seo WT, Lee JH, Cho KM. 2012. Roasting enhances antioxidant effect of bitter melon (Momordica charantia L.) increasing in flavan-3-ol and phenolic acid contents. Food Sci. Biotechnol. 21: 19-26.
    CrossRef
  4. Coward L, Smith M, Kirk M, Barnes S. 1998. Chemical modification of isoflavones in soyfoods during cooking and processing. Am. J. Clin. Nutr. 68: 1486-1491.
  5. Hu Y, Ge C, Yuan W, Zhu R, Zhang W, Du L, Xue J. 2010. Characterization of fermented black soybean natto inoculated with Bacillus natto during fermentation. J. Sci. Food Agric. 90:1194-1202.
    CrossRef
  6. Hwang CE, Seo WT, Cho KM. 2013. Enhanced antioxidant effect of black soybean by cheonggukjang with potential probiotic Bacillus subtilis CSY191. Korean J. Microbiol. 49: 391397.
    CrossRef
  7. Jang CH, Lim JK, Kim JH, Park CS, Kwon DY, Kim YS, et al. 2006. Change of isoflavone content during manufacturing of cheonggukjang, a traditional Korean fermented soyfood. Food Sci. Biotechnol. 15: 643-646.
  8. Juan MY, Chou CC. 2010. Enhancement of antioxidant activity, total phenolic and flavonoid content of black soybeans by solid state fermentation with Bacillus subtilis BCRC 14715. Food Microbiol. 27: 586-591.
    CrossRef
  9. Kao TH, Chen BH. 2006. Functional components in soybean cake and their effects on antioxidant activity. J. Agric. Food Chem. 54: 7544-7555.
    CrossRef
  10. Kim HG, Kim GW, Oh H, Yoo SY, Kim YO, Oh MS. 2011. Influence of roasting on the antioxidant activity of small black soybean (Glycine max L. Merrill). LWT Food Sci. Technol. 44: 992-998.
    CrossRef
  11. Kim HY, Sin SM, Lee SH, Cho KM, Cho EJ. 2013. The butanol fraction of bitter melon (Momordica charantia) scavenges free radicals and attenuates oxidative stress. Prev. Nutr. Food Sci. 18: 18-22.
    CrossRef
  12. Kim JS, Kang OJ, Gweon OC. 2013. Comparison of phenolic acids and flavonoids in black garlic at different thermal processing steps. J. Funct. Foods 5: 80-86.
    CrossRef
  13. Kim MH, Kim SY, Ko JM, Jeong DY, Kim YS. 2012. Biological activities of cheonggukjang prepared with several soybean cultivars. Food Sci. Biotechnol. 21: 475-483.
    CrossRef
  14. Kim NY, Song EJ, Kwon DY, Kim HP, Heo MY. 2008. Antioxidant and antigenotoxic activities of Korean fermented soybean. Food Chem. Toxicol. 46: 1184-1189.
    CrossRef
  15. Kwak CS, Lee MS, Park SC. 2007. Higher antioxidant of chungkookjang, a fermented soybean paste, may be due to increased aglycone and malonylglycoside isoflavone during fermentation. Nutr. Res. 27: 719-727.
    CrossRef
  16. Lee CH, Yang L, Xu JZ, Yeung SYV, Huang Y, Chen Z-Y. 2005. Relative antioxidant activity of soybean isoflavones and their glycosides. Food Chem. 90: 735-741.
    CrossRef
  17. Lee HA, Kim JH. 2012. Isolation of Bacillus amyloliquefaciens strains with antifungal activities from meju. Prev. Nutr. Food Sci. 17: 64-70.
    CrossRef
  18. Lee JH, Cho KM. 2012. Changes occurring in compositional components of black soybeans maintained at room temperature for different storage periods. Food Chem. 131: 161-169.
    CrossRef
  19. Lee JH, Choung MG. 2011. Determination of optimal acid hydrolysis time of soybean isoflavones using drying oven and microwave assisted methods. Food Chem. 129: 577-582.
    CrossRef
  20. Lee SW, Lee JH. 2009. Effects of oven-drying, roasting, and explosive puffing process on isoflavone distributions in soybeans. Food Chem. 112: 316-320.
    CrossRef
  21. Nam YD, Yi SH, Lim SI. 2012. Bacterial diversity of cheonggukjang, a traditional Korean fermented food, analyzed by barcoded pyrosequencing. Food Control 28: 135-142.
    CrossRef
  22. Otieno DO, Ashton JF, Shah N. 2005. Stability of β-glucosidase activity produced by Bifidobacterium and Lactobacillus spp. in fermented soymilk during processing and storage. J. Food Sci. 70: M236-M241.
    CrossRef
  23. Prabhakaran MP, Perera CO, Valiyaveettil S. 2006. Effect of different coagulants on the isoflavones levels and physical properties of prepared firm tofu. Food Chem. 99: 492-499.
    CrossRef
  24. Pratt DE, Birac PM, Porter WL, Giffee JW. 1981. Phenolic antioxidants of soy protein hydrolyzates. J. Food Sci. 47: 2425.
  25. Robbins RJ. 2003. Phenolic acids in foods: an overview of analytical methodology. J. Agric. Food Chem. 51: 2866-2887.
    CrossRef
  26. Seo A, Morr CV. 1984. Improved high-performance liquid chromatographic analysis of phenolic acids. J. Agric. Food Chem. 32: 530-533.
    CrossRef
  27. Seo WT, Nam SH, Lee CK, Cho KM. 2011. Identification of potential Bacillus subtilis probiotics from Korean soybean paste and their antimicrobial and immune activities. J. Food Sci. Nutr. 16: 37-44.
    CrossRef
  28. Shon MY, Lee J, Choi SY, Nam SH, Seo KI, Lee SW, et al. 2007. Antioxidant and free radical scavenging activity of methanol extract of chungkukjang. J. Food Comp. Anal. 20:113-118.
    CrossRef
  29. Shon MY, Seo KI, Lee SW, Choi SH, Sung NJ. 2000. Biological activities of cheonggukjang prepared with black bean and changes in phytoestrogen content during fermentation. Korean J. Food Sci. Technol. 32: 936-941.
  30. Slavin M, Cheng Z, Luther M, Kenworthy W, Yu L. 2009. Antioxidant properties and phenolic, isoflavone, tocopherol and carotenoid composition of Maryland-grown soybean lines with altered fatty acid profiles. Food Chem. 114: 20-27.
    CrossRef
  31. Wang L, Yin L, Li D, Zou L, Saito M, Tatsumi E, Li L. 2007. Influences of processing and NaCl supplementation on isoflavone contents and composition during douchi manufacturing. Food Chem. 101: 1247-1253.
    CrossRef
  32. Yang SO, Chang PS, Lee JH. 2006. Isoflavone distribution and β-glucosidase activity in cheonggukjang, a traditional Korean whole soybean-fermented food. Food Sci. Biotechnol. 15: 96-101.

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Article

Research article

J. Microbiol. Biotechnol. 2014; 24(7): 959-968

Published online July 28, 2014 https://doi.org/10.4014/jmb.1310.10065

Copyright © The Korean Society for Microbiology and Biotechnology.

Characteristics and Antioxidant Effect of Garlic in the Fermentation of Cheonggukjang by Bacillus amyloliquefaciens MJ1-4

Jeong Hwan Kim 1, 2, Chung Eun Hwang 3, Chang Kwon Lee 4, Jin Hwan Lee 5, Gyoung Min Kim 6, Seong Hoon Jeong 6, Jeong Hee Shin 6, Jong Sang Kim 7 and Kye Man Cho 3, 8*

1Division of Applied Life Science BK21, Graduate School, Gyeongsang National University, Jinju 660-701, Republic of Korea, 2Institute of Agriculture and Life Science, Gyeongsang National University, Jinju 660-701, Republic of Korea, 3Department of Food Science, Gyeongnam National University of Science and Technology, Jinju 660-758, Republic of Korea, 4Mong-Go Foods Co., Ltd., Changwon 641-465, Republic of Korea, 5National Institute of Chemical Safety, Ministry of Environment, Daejeon 305-343, Republic of Korea, 6Namhae Garlic Research Institute, Namhae 668-812, Republic of Korea, 7School of Applied Biosciences and Food Science and Biotechnology, Kyungpook National University, Daegu 702-701, Republic of Korea, 8College of Pharmacy, Sunchon National University, Suncheon 540-950, Republic of Korea

Received: October 18, 2013; Accepted: March 28, 2014

Abstract

The changes in the β-glucosidase activity, total phenolic contents, isoflavone contents, and
antioxidant activities during the fermentation of cheonggukjang by Bacillus amyloliquefaciens
MJ1-4 with and without garlic were investigated. The levels of total phenolic and isoflavonemalonylglycoside,
-acetylglycoside, and -aglycone contents increased, whereas the 2,2-diphenyl-
1-picrylhydrazyl (DPPH) and 2,2’-azino-bis (3-ethylbenzthiazoline-6-sulfonic acid) (ABTS)
radical scavenging activities and ferric reducing/antioxidant power (FRAP) assay results
increased, but isoflavone-glycoside levels decreased during cheonggukjang fermentation. The
levels of total phenolic and total isoflavone contents and the antioxidant activities were higher
in cheonggukjang fermented without garlic (CFWOG) than in cheonggukjang fermented with
garlic (CFWG) after 24 h of fermentation, but they were lower in CFWOG than in CFWG after
72h of fermentation. In particular, the highest levels of total phenolic, daidzein, glycitein, and
genistein were present at concentrations of 15.18 mg/g, 264.4 μg/g, 16.4 μg/g, and 31.1 μg/g
after 72h of fermentation in CFWG, showing 82.89% in DPPH radical scavenging activity,
106.32% in ABTS radical scavenging activity, and 1.47 (OD593 nm) in FRAP assay, respectively.
From these results, we suggest that the high antioxidant activity of CFWG might be related to
the markedly higher levels of total phenolic contents, isoflavone-malonylglycosides, -
acetylglycosides, and -aglycones achieved during fermentation.

Keywords: cheonggukjang, Bacillus amyloqufiecens MJ1-4, garlic, total phenolic contents, isoflavones, antioxidant activity

References

  1. Cho KM, Hong SY, Math RK, Lee JH, Kambiranda DM, Kim JM, et al. 2009. Biotransformation of phenolics (isoflavones, flavanols and phenolic acids) during the fermentation of cheonggukjang by Bacillus pumilus HY1. Food Chem. 114: 413419.
    CrossRef
  2. Cho KM, Lee JH, Yun HD, Ahn BY, Kim H, Seo WT. 2011. Changes of phytochemical constituents (isoflavones, flavanols, and phenolic acids) during cheonggukjang soybeans fermentation using potential probiotics Bacillus subtilis CS90. J. Food Comp. Anal. 24: 402-410.
    CrossRef
  3. Choi JS, Kim HY, Seo WT, Lee JH, Cho KM. 2012. Roasting enhances antioxidant effect of bitter melon (Momordica charantia L.) increasing in flavan-3-ol and phenolic acid contents. Food Sci. Biotechnol. 21: 19-26.
    CrossRef
  4. Coward L, Smith M, Kirk M, Barnes S. 1998. Chemical modification of isoflavones in soyfoods during cooking and processing. Am. J. Clin. Nutr. 68: 1486-1491.
  5. Hu Y, Ge C, Yuan W, Zhu R, Zhang W, Du L, Xue J. 2010. Characterization of fermented black soybean natto inoculated with Bacillus natto during fermentation. J. Sci. Food Agric. 90:1194-1202.
    CrossRef
  6. Hwang CE, Seo WT, Cho KM. 2013. Enhanced antioxidant effect of black soybean by cheonggukjang with potential probiotic Bacillus subtilis CSY191. Korean J. Microbiol. 49: 391397.
    CrossRef
  7. Jang CH, Lim JK, Kim JH, Park CS, Kwon DY, Kim YS, et al. 2006. Change of isoflavone content during manufacturing of cheonggukjang, a traditional Korean fermented soyfood. Food Sci. Biotechnol. 15: 643-646.
  8. Juan MY, Chou CC. 2010. Enhancement of antioxidant activity, total phenolic and flavonoid content of black soybeans by solid state fermentation with Bacillus subtilis BCRC 14715. Food Microbiol. 27: 586-591.
    CrossRef
  9. Kao TH, Chen BH. 2006. Functional components in soybean cake and their effects on antioxidant activity. J. Agric. Food Chem. 54: 7544-7555.
    CrossRef
  10. Kim HG, Kim GW, Oh H, Yoo SY, Kim YO, Oh MS. 2011. Influence of roasting on the antioxidant activity of small black soybean (Glycine max L. Merrill). LWT Food Sci. Technol. 44: 992-998.
    CrossRef
  11. Kim HY, Sin SM, Lee SH, Cho KM, Cho EJ. 2013. The butanol fraction of bitter melon (Momordica charantia) scavenges free radicals and attenuates oxidative stress. Prev. Nutr. Food Sci. 18: 18-22.
    CrossRef
  12. Kim JS, Kang OJ, Gweon OC. 2013. Comparison of phenolic acids and flavonoids in black garlic at different thermal processing steps. J. Funct. Foods 5: 80-86.
    CrossRef
  13. Kim MH, Kim SY, Ko JM, Jeong DY, Kim YS. 2012. Biological activities of cheonggukjang prepared with several soybean cultivars. Food Sci. Biotechnol. 21: 475-483.
    CrossRef
  14. Kim NY, Song EJ, Kwon DY, Kim HP, Heo MY. 2008. Antioxidant and antigenotoxic activities of Korean fermented soybean. Food Chem. Toxicol. 46: 1184-1189.
    CrossRef
  15. Kwak CS, Lee MS, Park SC. 2007. Higher antioxidant of chungkookjang, a fermented soybean paste, may be due to increased aglycone and malonylglycoside isoflavone during fermentation. Nutr. Res. 27: 719-727.
    CrossRef
  16. Lee CH, Yang L, Xu JZ, Yeung SYV, Huang Y, Chen Z-Y. 2005. Relative antioxidant activity of soybean isoflavones and their glycosides. Food Chem. 90: 735-741.
    CrossRef
  17. Lee HA, Kim JH. 2012. Isolation of Bacillus amyloliquefaciens strains with antifungal activities from meju. Prev. Nutr. Food Sci. 17: 64-70.
    CrossRef
  18. Lee JH, Cho KM. 2012. Changes occurring in compositional components of black soybeans maintained at room temperature for different storage periods. Food Chem. 131: 161-169.
    CrossRef
  19. Lee JH, Choung MG. 2011. Determination of optimal acid hydrolysis time of soybean isoflavones using drying oven and microwave assisted methods. Food Chem. 129: 577-582.
    CrossRef
  20. Lee SW, Lee JH. 2009. Effects of oven-drying, roasting, and explosive puffing process on isoflavone distributions in soybeans. Food Chem. 112: 316-320.
    CrossRef
  21. Nam YD, Yi SH, Lim SI. 2012. Bacterial diversity of cheonggukjang, a traditional Korean fermented food, analyzed by barcoded pyrosequencing. Food Control 28: 135-142.
    CrossRef
  22. Otieno DO, Ashton JF, Shah N. 2005. Stability of β-glucosidase activity produced by Bifidobacterium and Lactobacillus spp. in fermented soymilk during processing and storage. J. Food Sci. 70: M236-M241.
    CrossRef
  23. Prabhakaran MP, Perera CO, Valiyaveettil S. 2006. Effect of different coagulants on the isoflavones levels and physical properties of prepared firm tofu. Food Chem. 99: 492-499.
    CrossRef
  24. Pratt DE, Birac PM, Porter WL, Giffee JW. 1981. Phenolic antioxidants of soy protein hydrolyzates. J. Food Sci. 47: 2425.
  25. Robbins RJ. 2003. Phenolic acids in foods: an overview of analytical methodology. J. Agric. Food Chem. 51: 2866-2887.
    CrossRef
  26. Seo A, Morr CV. 1984. Improved high-performance liquid chromatographic analysis of phenolic acids. J. Agric. Food Chem. 32: 530-533.
    CrossRef
  27. Seo WT, Nam SH, Lee CK, Cho KM. 2011. Identification of potential Bacillus subtilis probiotics from Korean soybean paste and their antimicrobial and immune activities. J. Food Sci. Nutr. 16: 37-44.
    CrossRef
  28. Shon MY, Lee J, Choi SY, Nam SH, Seo KI, Lee SW, et al. 2007. Antioxidant and free radical scavenging activity of methanol extract of chungkukjang. J. Food Comp. Anal. 20:113-118.
    CrossRef
  29. Shon MY, Seo KI, Lee SW, Choi SH, Sung NJ. 2000. Biological activities of cheonggukjang prepared with black bean and changes in phytoestrogen content during fermentation. Korean J. Food Sci. Technol. 32: 936-941.
  30. Slavin M, Cheng Z, Luther M, Kenworthy W, Yu L. 2009. Antioxidant properties and phenolic, isoflavone, tocopherol and carotenoid composition of Maryland-grown soybean lines with altered fatty acid profiles. Food Chem. 114: 20-27.
    CrossRef
  31. Wang L, Yin L, Li D, Zou L, Saito M, Tatsumi E, Li L. 2007. Influences of processing and NaCl supplementation on isoflavone contents and composition during douchi manufacturing. Food Chem. 101: 1247-1253.
    CrossRef
  32. Yang SO, Chang PS, Lee JH. 2006. Isoflavone distribution and β-glucosidase activity in cheonggukjang, a traditional Korean whole soybean-fermented food. Food Sci. Biotechnol. 15: 96-101.