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References

  1. Ariffin H, Abdullah N, Kalsom MSU, Shirai Y, Hassan MA. 2006. Production and characterization of cellulase by Bacillus pumilus EB3. Int. J. Eng. Technol. 3: 47-53.
  2. Astrup T, Müllertz S. 1952. The fibrin plate method for estimating fibrinolytic activity. Arch. Biochem. Biophys. 40:346-351.
    CrossRef
  3. Carruthers FL, Conner AJ, Mashanty HK. 1994. Identification of a genetic locus in Pseudomonas aureofaciens involved in fungal inhibition. Appl. Environ. Microbiol. 60: 71-77.
    Pubmed PMC
  4. Chang M, Chang HC. 2012. Development of a screening method for biogenic amine producing Bacillus spp. Int. J. Food Microbiol. 153: 269-274.
    Pubmed CrossRef
  5. Cho TY, Han GH, Bahn KN, Son YW, Jang MR, Lee CH, et al. 2006. Evaluation of biogenic amines in Korean commercial fermented foods. Kor. J. Food Sci. Technol. 38: 730-737.
  6. Cho MJ, Lee JY, Kim JH. 2014. Microbial and physiochemical properties of Cheonggukjang fermented using Bacillus strains with antibacterial or antifungal activities. Food Sci. Biotechnol. 23: 1525-1532.
    CrossRef
  7. Choi N S, C hung DM, H an Y J, K im SH, S ong JJ. 2009. Purification and characterization of a subtilisin D5, a fibrinolytic enzyme of Bacillus amyloliquefaciens DJ-5 isolated from doenjang. Food Sci. Biotechnol. 18: 500-505.
  8. Dabbagh F, Negahdaripour M, Berenjian A, Behfar A, Mohammadi F, Zamani M, et al. 2014. Nattokinase: production and application. Appl. Microbiol. Biotechnol. 98: 9199-9206.
    Pubmed CrossRef
  9. Felsenstein J. 2002. PHYLIP (phylogeny inference package), version 3.6a. Department of Genetics, University of Washington, Seattle, WA, USA.
  10. Gálvez A, López RL, Abriouel H, Valdivia E, Omar NB. 2008. Application of bacteriocins in the control of foodborne pathogenic and spoilage bacteria. Crit. Rev. Biotechnol. 28:125-152.
    Pubmed CrossRef
  11. Guan L, C ho K H, L ee JH. 2 011. A nalysis of the c ultivable bacterial community in jeotgal, a Korean salted and fermented seafood, and identification of its dominant bacteria. Food Microbiol. 28: 101-113.
    Pubmed CrossRef
  12. Guinebretière MH, Broussolle V, Nguyen-The C. 2002. Enterotoxigenic profiles of food-poisoning and food-borne Bacillus cereus strains. J. Clin. Microbiol. 40: 3053-3056.
    Pubmed PMC CrossRef
  13. Ham SS, Choi KK, Cui CB, Lee BG, Joo DS, Lee DS. 2004. Quality characteristics of soy sauce fermented by Bacillus licheniformis NH20 isolated from traditional meju and Aspergillus oryzae. Food Sci. Biotechnol. 13: 537-543.
  14. He FJ, MacGregor GA. 2002. Effect of modest salt reduction on blood pressure: a meta-analysis of randomized trials. implications for public health. J. Hum. Hypertens. 16: 761-770.
    Pubmed CrossRef
  15. Jeong DW, Kim HR, Jung G, Han S, Kim CT, Lee JH. 2014. Bacterial community migration in the ripening of doenjang, a traditional Korean fermented soybean food. J. Microbiol. Biotechnol. 24: 648-660.
    Pubmed CrossRef
  16. Jeong JK, Chang HK, Park KY. 2014. Doenjang prepared with mixed starter cultures attenuates azoxymethane and dextran sulfate sodium-induced colitis-associated colon carcinogenesis in mice. J. Carcinog. 13: 9.
    Pubmed PMC CrossRef
  17. Jung HK, Jeong YS, Youn KS, Kim DI, Hong JH. 2009. Quality characteristics of soybean paste (doenjang) prepared with Bacillus subtilis DH3 expressing high protease levels, and deep-sea water. Kor. J. Food Preserv. 16: 348-354.
  18. Jung JH, Lee MY, Chang HC. 2012. Evaluation of the probiotic potential of Bacillus polyfermenticus CJ6 isolated from meju, a Korean soybean fermentation starter. J. Microbiol. Biotechnol. 22: 1510-1517.
    Pubmed CrossRef
  19. Jung JY, Lee SH, Jeon CO. 2014. Microbial community dynamics during fermentation of doenjang-meju, traditional Korean fermented soybean. Int. J. Food Microbiol. 185: 112-120.
    Pubmed CrossRef
  20. Jung K O, P ark SY, Park K Y. 2 006. L onger a ging t ime increases the anticancer and antimetastatic properties of doenjang. Nutrition 22: 539-545.
    Pubmed CrossRef
  21. Kim JY, Gum SN, Paik JK, Lim HH, Kim KC, Ogasawara K, et al. 2008. Effects of nattokinase on blood pressure: a randomized, controlled trial. Hypertens. Res. 31: 1583-1588.
    Pubmed CrossRef
  22. K im J B, K im JM, Cho SH, O h HS, Choi NJ, Oh DH. 2 011. Toxin genes profiles and toxin production ability of Bacillus cereus isolated from clinical and food samples. J. Food Sci. 76: T25-T29.
    Pubmed CrossRef
  23. Kim M, Kim YS. 2012. Detection of foodborne pathogens and analysis of aflatoxin levels in home-made doenjang samples. Prev. Nutr. Food Sci. 17: 172-176.
    Pubmed PMC CrossRef
  24. Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, et al. 2012. Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int. J. Syst. Evol. Microbiol. 62: 716-721.
    Pubmed CrossRef
  25. Kim TW, Kim YH, Jung HJ, Park CS, Kim HY. 2012. Screening of strains with fibrinolytic activity and angiotensinconverting enzyme inhibitory activity from doenjang. Food Sci. Biotechnol. 21: 581-585.
    CrossRef
  26. Kim TW, Lee JH, Kim SE, Park MH, Chang HC, Kim HY. 2009. Analysis of microbial communities in doenjang, a Korean fermented soybean paste, using nested PCR-denaturing gradient gel electrophoresis. Int. J. Food Microbiol. 131: 265271.
    Pubmed CrossRef
  27. Lo N, Lee SH, Jin HM, Jung JY, Schumann P, Jeon CO. 2015. Garicola koreensis gen. nov., sp. nov., isolated from saeu-jeot, traditional Korean fermented shrimp. Int. J. Syst. Evol. Microbiol. 65: 1015-1021.
    Pubmed CrossRef
  28. Mah JH, Ahn JB, Park JH, Sung HC, Hwang HJ. 2003. Characterization of biogenic amine-producing microorganisms isolated from myeolchi-jeot, Korean salted and fermented anchovy. J. Microbiol. Biotechnol. 13: 692-699.
  29. Mo AY, Kwon B, Kamala-Kannan S, Lee KJ, Oh BT, Kim DH, et al. 2010. Isolation and characterization of Bacillus polyfermenticus isolated from Meju, Korean soybean fermentation starter. World J. Microbiol. Biotechnol. 26: 1099-1105.
    CrossRef
  30. Moon JS, Cho S K , Choi HY, K im JE, K im SY, Cho K J, Han NS. 2010. Isolation and characterization of biogenic amineproducing bacteria in fermented soybean pastes. J. Microbiol. 48: 257-261.
    Pubmed CrossRef
  31. Nam YD, Lee SY, Lim SI. 2012. Microbial community analysis of Korean soybean pastes by next-generation sequencing. Int. J. Food Microbiol. 155: 36-42.
    Pubmed CrossRef
  32. Namgung HJ, Park HJ, Cho IH, Choi HK, Kwon DY, Shim SM, Kim YS. 2010. Metabolite profiling of doenjang, fermented soybean paste, during fermentation. J. Sci. Food Agric. 90: 1926-1935.
    CrossRef
  33. Ogunleye A, Bhat A, Irorere VU, Hill D, Williams C. Radecka I. 2015. Poly-γ-glutamic acid: production, properties and applications. Microbiology 161: 1-17.
    Pubmed CrossRef
  34. Park JS, Park HY, Kim DH, Kim DH, Kim HK. 2008. Orthodihydroxyisoflavone derivatives from aged doenjang (Korean fermented soypaste) and its radical scavenging activity. Bioorg. Med. Chem. Lett. 18: 5006-5009.
    Pubmed CrossRef
  35. Park KY, Jung KO, Rhee SH, Choi YH. 2003. Antimutagenic effects of doenjang (Korean fermented soypaste) and its active compounds. Mutat. Res. 523-524: 43-53.
    CrossRef
  36. Park HK, Shukla S, Lee JS, Kim JK, Kim M. 2014. Reduction of foodborne pathogens and aflatoxins in doenjang samples using defined meju. J. Food Saf. 34: 161-167.
    CrossRef
  37. Park JW, K im E K , Shon DH, K im Y B. 2 002. N atural c ooccurrence of aflatoxin B1, fumonisin B1 and ochratoxin A in barley and corn foods from Korea. Food Addit. Contam. 19:1073-1080.
    Pubmed CrossRef
  38. Piskula MK, Yamakoshi J, Iwai Y. 1999. Daidzein and genistein but not their glucosides are absorbed from the rat stomach. FEBS Lett. 447: 287-291.
    CrossRef
  39. Pruesse E, Quast C, Knittel K, Fuchs B, Ludwig W, Peplies J, Glöckner FO. 2007. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 35: 7188-7196.
    Pubmed PMC CrossRef
  40. Silla Santos MH. 1996. Biogenic amines: their importance in foods. Int. J. Food Microbiol. 29: 213-231.
    CrossRef
  41. Shukla S, Park HK, Kim JK, Kim M. 2010. Determination of biogenic amines in Korean traditional fermented soybean paste (doenjang). Food Chem. Toxicol. 48: 1191-1195.
    Pubmed CrossRef
  42. Urushibata Y, Tokuyama S, Tahara Y. 2002. Characterization of the Bacillus subtilis ywsC gene, involved in γ-polyglutamic acid production. J. Bacteriol. 184: 337-343.
    Pubmed PMC CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2016; 26(4): 666-674

Published online April 28, 2016 https://doi.org/10.4014/jmb.1512.12014

Copyright © The Korean Society for Microbiology and Biotechnology.

Screening and Characterization of Potential Bacillus Starter Cultures for Fermenting Low-Salt Soybean Paste (Doenjang)

Hye Hee Jeon 1, Ji Young Jung 1, Byung-Hee Chun 1, Myoung-Dong Kim 2, Seong Yeol Baek 3, Ji Young Moon 3, Soo-Hwan Yeo 3 and Che Ok Jeon 1*

1Department of Life Science, Chung-Ang University, Seoul 06974, Republic of Korea, 2Department of Food Science and Biotechnology, Kangwon National University, Chuncheon 24341, Republic of Korea, 3Department of Agrofood Resources, National Institute of Agricultural Sciences, RDA, Wanju-gun 55365, Republic of Korea

Received: December 7, 2015; Accepted: December 30, 2015

Abstract

The bacterial strains were screened as potential starters for fermenting low-salt doenjang (a
Korean traditional fermented soybean paste) using Korean doenjang based on proteolytic and
antipathogenic activities under 6.5–7.5% NaCl conditions. Phylogenetic analysis based on 16S
rRNA gene sequences showed that they all belonged to the genus Bacillus. Proteolytic and
antipathogenic activities against Escherichia coli, Bacillus cereus, Staphylococcus aureus, Listeria
monocytogenes, and Aspergillus flavus, as well as fibrinolytic, amylase, and cellulase activities of
the 10 strains were quantitatively evaluated. Of these, strains D2-2, JJ-D34, and D12-5 were
selected, based on their activities. The functional, phenotypic, and safety-related characteristics
of these three strains were additionally investigated and strains D2-2 and D12-5, which lacked
antibiotic resistance, were finally selected. Strains D2-2 and D12-5 produced poly-γ-glutamic
acid and showed various enzyme activities, including α-glucosidase and β-glucosidase.
Growth properties of strains D2-2 and D12-5 included wide temperature and pH ranges,
growth in up to 16% NaCl, and weak anaerobic growth, suggesting that they facilitate low-salt
doenjang fermentation. Strains D2-2 and D12-5 were not hemolytic, carried no toxin genes,
and did not produce biogenic amines. These results suggest that strains D2-2 and D12-5 can
serve as appropriate starter cultures for fermenting low-salt doenjang with high quality and
safety.

Keywords: Doenjang, Bacillus, fermented soybean paste, starter culture, protease, antipathogenic activity

References

  1. Ariffin H, Abdullah N, Kalsom MSU, Shirai Y, Hassan MA. 2006. Production and characterization of cellulase by Bacillus pumilus EB3. Int. J. Eng. Technol. 3: 47-53.
  2. Astrup T, Müllertz S. 1952. The fibrin plate method for estimating fibrinolytic activity. Arch. Biochem. Biophys. 40:346-351.
    CrossRef
  3. Carruthers FL, Conner AJ, Mashanty HK. 1994. Identification of a genetic locus in Pseudomonas aureofaciens involved in fungal inhibition. Appl. Environ. Microbiol. 60: 71-77.
    Pubmed KoreaMed
  4. Chang M, Chang HC. 2012. Development of a screening method for biogenic amine producing Bacillus spp. Int. J. Food Microbiol. 153: 269-274.
    Pubmed CrossRef
  5. Cho TY, Han GH, Bahn KN, Son YW, Jang MR, Lee CH, et al. 2006. Evaluation of biogenic amines in Korean commercial fermented foods. Kor. J. Food Sci. Technol. 38: 730-737.
  6. Cho MJ, Lee JY, Kim JH. 2014. Microbial and physiochemical properties of Cheonggukjang fermented using Bacillus strains with antibacterial or antifungal activities. Food Sci. Biotechnol. 23: 1525-1532.
    CrossRef
  7. Choi N S, C hung DM, H an Y J, K im SH, S ong JJ. 2009. Purification and characterization of a subtilisin D5, a fibrinolytic enzyme of Bacillus amyloliquefaciens DJ-5 isolated from doenjang. Food Sci. Biotechnol. 18: 500-505.
  8. Dabbagh F, Negahdaripour M, Berenjian A, Behfar A, Mohammadi F, Zamani M, et al. 2014. Nattokinase: production and application. Appl. Microbiol. Biotechnol. 98: 9199-9206.
    Pubmed CrossRef
  9. Felsenstein J. 2002. PHYLIP (phylogeny inference package), version 3.6a. Department of Genetics, University of Washington, Seattle, WA, USA.
  10. Gálvez A, López RL, Abriouel H, Valdivia E, Omar NB. 2008. Application of bacteriocins in the control of foodborne pathogenic and spoilage bacteria. Crit. Rev. Biotechnol. 28:125-152.
    Pubmed CrossRef
  11. Guan L, C ho K H, L ee JH. 2 011. A nalysis of the c ultivable bacterial community in jeotgal, a Korean salted and fermented seafood, and identification of its dominant bacteria. Food Microbiol. 28: 101-113.
    Pubmed CrossRef
  12. Guinebretière MH, Broussolle V, Nguyen-The C. 2002. Enterotoxigenic profiles of food-poisoning and food-borne Bacillus cereus strains. J. Clin. Microbiol. 40: 3053-3056.
    Pubmed KoreaMed CrossRef
  13. Ham SS, Choi KK, Cui CB, Lee BG, Joo DS, Lee DS. 2004. Quality characteristics of soy sauce fermented by Bacillus licheniformis NH20 isolated from traditional meju and Aspergillus oryzae. Food Sci. Biotechnol. 13: 537-543.
  14. He FJ, MacGregor GA. 2002. Effect of modest salt reduction on blood pressure: a meta-analysis of randomized trials. implications for public health. J. Hum. Hypertens. 16: 761-770.
    Pubmed CrossRef
  15. Jeong DW, Kim HR, Jung G, Han S, Kim CT, Lee JH. 2014. Bacterial community migration in the ripening of doenjang, a traditional Korean fermented soybean food. J. Microbiol. Biotechnol. 24: 648-660.
    Pubmed CrossRef
  16. Jeong JK, Chang HK, Park KY. 2014. Doenjang prepared with mixed starter cultures attenuates azoxymethane and dextran sulfate sodium-induced colitis-associated colon carcinogenesis in mice. J. Carcinog. 13: 9.
    Pubmed KoreaMed CrossRef
  17. Jung HK, Jeong YS, Youn KS, Kim DI, Hong JH. 2009. Quality characteristics of soybean paste (doenjang) prepared with Bacillus subtilis DH3 expressing high protease levels, and deep-sea water. Kor. J. Food Preserv. 16: 348-354.
  18. Jung JH, Lee MY, Chang HC. 2012. Evaluation of the probiotic potential of Bacillus polyfermenticus CJ6 isolated from meju, a Korean soybean fermentation starter. J. Microbiol. Biotechnol. 22: 1510-1517.
    Pubmed CrossRef
  19. Jung JY, Lee SH, Jeon CO. 2014. Microbial community dynamics during fermentation of doenjang-meju, traditional Korean fermented soybean. Int. J. Food Microbiol. 185: 112-120.
    Pubmed CrossRef
  20. Jung K O, P ark SY, Park K Y. 2 006. L onger a ging t ime increases the anticancer and antimetastatic properties of doenjang. Nutrition 22: 539-545.
    Pubmed CrossRef
  21. Kim JY, Gum SN, Paik JK, Lim HH, Kim KC, Ogasawara K, et al. 2008. Effects of nattokinase on blood pressure: a randomized, controlled trial. Hypertens. Res. 31: 1583-1588.
    Pubmed CrossRef
  22. K im J B, K im JM, Cho SH, O h HS, Choi NJ, Oh DH. 2 011. Toxin genes profiles and toxin production ability of Bacillus cereus isolated from clinical and food samples. J. Food Sci. 76: T25-T29.
    Pubmed CrossRef
  23. Kim M, Kim YS. 2012. Detection of foodborne pathogens and analysis of aflatoxin levels in home-made doenjang samples. Prev. Nutr. Food Sci. 17: 172-176.
    Pubmed KoreaMed CrossRef
  24. Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, et al. 2012. Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int. J. Syst. Evol. Microbiol. 62: 716-721.
    Pubmed CrossRef
  25. Kim TW, Kim YH, Jung HJ, Park CS, Kim HY. 2012. Screening of strains with fibrinolytic activity and angiotensinconverting enzyme inhibitory activity from doenjang. Food Sci. Biotechnol. 21: 581-585.
    CrossRef
  26. Kim TW, Lee JH, Kim SE, Park MH, Chang HC, Kim HY. 2009. Analysis of microbial communities in doenjang, a Korean fermented soybean paste, using nested PCR-denaturing gradient gel electrophoresis. Int. J. Food Microbiol. 131: 265271.
    Pubmed CrossRef
  27. Lo N, Lee SH, Jin HM, Jung JY, Schumann P, Jeon CO. 2015. Garicola koreensis gen. nov., sp. nov., isolated from saeu-jeot, traditional Korean fermented shrimp. Int. J. Syst. Evol. Microbiol. 65: 1015-1021.
    Pubmed CrossRef
  28. Mah JH, Ahn JB, Park JH, Sung HC, Hwang HJ. 2003. Characterization of biogenic amine-producing microorganisms isolated from myeolchi-jeot, Korean salted and fermented anchovy. J. Microbiol. Biotechnol. 13: 692-699.
  29. Mo AY, Kwon B, Kamala-Kannan S, Lee KJ, Oh BT, Kim DH, et al. 2010. Isolation and characterization of Bacillus polyfermenticus isolated from Meju, Korean soybean fermentation starter. World J. Microbiol. Biotechnol. 26: 1099-1105.
    CrossRef
  30. Moon JS, Cho S K , Choi HY, K im JE, K im SY, Cho K J, Han NS. 2010. Isolation and characterization of biogenic amineproducing bacteria in fermented soybean pastes. J. Microbiol. 48: 257-261.
    Pubmed CrossRef
  31. Nam YD, Lee SY, Lim SI. 2012. Microbial community analysis of Korean soybean pastes by next-generation sequencing. Int. J. Food Microbiol. 155: 36-42.
    Pubmed CrossRef
  32. Namgung HJ, Park HJ, Cho IH, Choi HK, Kwon DY, Shim SM, Kim YS. 2010. Metabolite profiling of doenjang, fermented soybean paste, during fermentation. J. Sci. Food Agric. 90: 1926-1935.
    CrossRef
  33. Ogunleye A, Bhat A, Irorere VU, Hill D, Williams C. Radecka I. 2015. Poly-γ-glutamic acid: production, properties and applications. Microbiology 161: 1-17.
    Pubmed CrossRef
  34. Park JS, Park HY, Kim DH, Kim DH, Kim HK. 2008. Orthodihydroxyisoflavone derivatives from aged doenjang (Korean fermented soypaste) and its radical scavenging activity. Bioorg. Med. Chem. Lett. 18: 5006-5009.
    Pubmed CrossRef
  35. Park KY, Jung KO, Rhee SH, Choi YH. 2003. Antimutagenic effects of doenjang (Korean fermented soypaste) and its active compounds. Mutat. Res. 523-524: 43-53.
    CrossRef
  36. Park HK, Shukla S, Lee JS, Kim JK, Kim M. 2014. Reduction of foodborne pathogens and aflatoxins in doenjang samples using defined meju. J. Food Saf. 34: 161-167.
    CrossRef
  37. Park JW, K im E K , Shon DH, K im Y B. 2 002. N atural c ooccurrence of aflatoxin B1, fumonisin B1 and ochratoxin A in barley and corn foods from Korea. Food Addit. Contam. 19:1073-1080.
    Pubmed CrossRef
  38. Piskula MK, Yamakoshi J, Iwai Y. 1999. Daidzein and genistein but not their glucosides are absorbed from the rat stomach. FEBS Lett. 447: 287-291.
    CrossRef
  39. Pruesse E, Quast C, Knittel K, Fuchs B, Ludwig W, Peplies J, Glöckner FO. 2007. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 35: 7188-7196.
    Pubmed KoreaMed CrossRef
  40. Silla Santos MH. 1996. Biogenic amines: their importance in foods. Int. J. Food Microbiol. 29: 213-231.
    CrossRef
  41. Shukla S, Park HK, Kim JK, Kim M. 2010. Determination of biogenic amines in Korean traditional fermented soybean paste (doenjang). Food Chem. Toxicol. 48: 1191-1195.
    Pubmed CrossRef
  42. Urushibata Y, Tokuyama S, Tahara Y. 2002. Characterization of the Bacillus subtilis ywsC gene, involved in γ-polyglutamic acid production. J. Bacteriol. 184: 337-343.
    Pubmed KoreaMed CrossRef