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References

  1. Sato A, Oshima K, Noguchi H, Ogawa M, Takahashi T, Oguma T, et al. 2011. Draft genome sequencing and comparative analysis of Aspergillus sojae NBRC4239. DNA Res. 18: 165-176.
    Pubmed PMC CrossRef
  2. Kitamoto K. 2002. Molecular biology of the koji molds. Adv. Appl. Microbiol. 51: 129-154.
    CrossRef
  3. Nampoothiri KM, Nagy V, Kovacs K, Szakacs G, Pandey A. 2005. L-Leucine aminopeptidase production by filamentous Aspergillus fungi. Lett. Appl. Microbiol. 41: 498-504.
    Pubmed CrossRef
  4. Toldrá F, Aristoy M-C, Flores M. 2000. Contribution of muscle aminopeptidases to flavor development in dry-cured ham. Food Res. Int. 33: 181-185.
    CrossRef
  5. Kim D-H, Kim S-H, Kwon S-W, Lee J-K, Hong S-B. 2013. Mycoflora of soybeans used for meju fermentation. Mycobiology 41: 100-107.
    Pubmed PMC CrossRef
  6. Buyukkileci AO, Tari C, Fernandez-Lahore M. 2011. Enhanced production of exo-polygalacturonase from agrobased products by Aspergillus sojae. Bioresources 6: 3452-3468.
  7. Chang P-K. 2004. Lack of interaction between AFLR and AFLJ contributes to nonaflatoxigenicity of Aspergillus sojae. J. Biotechnol. 107: 245-253.
    Pubmed CrossRef
  8. Gurkok S, Cekmecelioglu D, Ogel ZB. 2011. Optimization of culture conditions for Aspergillus sojae expressing an Aspergillus fumigatus α-galactosidase. Bioresour. Technol. 102: 4925-4929.
    Pubmed CrossRef
  9. Heerd D, Yegin S, Tari C, Fernandez-Lahore M. 2012. Pectinase enzyme-complex production by Aspergillus spp. in solid-state fermentation: a comparative study. Food Bioprod. Process. 90: 102-110.
    CrossRef
  10. Lin C-H, Wei Y-T, Chou C-C. 2006. Enhanced antioxidative activity of soybean koji prepared with various filamentous fungi. Food Microbiol. 23: 628-633.
    Pubmed CrossRef
  11. Oncu S, Tari C, Unluturk S. 2007. Effect of various process parameters on morphology, rheology, and polygalacturonase production by Aspergillus sojae in a batch bioreactor. Biotechnol. Prog. 23: 836-845.
    Pubmed CrossRef
  12. Chang P-K, Matsushima K, Takahashi T, Yu J, Abe K, Bhatnagar D, et al. 2007. Understanding nonaflatoxigenicity of Aspergillus sojae: a windfall of aflatoxin biosynthesis research. Appl. Microbiol. Biotechnol. 76: 977-984.
    Pubmed CrossRef
  13. Wicklow DT. 1984. Conidium germination rate in wild and domesticated yellow-green aspergilli. Appl. Environ. Microbiol. 47: 299-300.
    Pubmed PMC
  14. Chang H-Y, Lee Y-B, Bae H-A, Huh J-Y, Nam S-H, Sohn HS, et al. 2011. Purification and characterisation of Aspergillus sojae naringinase: the production of prunin exhibiting markedly enhanced solubility with in vitro inhibition of HMG-CoA reductase. Food Chem. 124: 234-241.
    CrossRef
  15. Murakami H, Hayashi K, Ushijima S. 1982. Useful key characters separating three Aspergillus taxa: A. sojae, A. parasiticus, and A. toxicarius. J. Gen. Appl. Microbiol. 28: 55-60.
    CrossRef
  16. Klich M, Mullaney E. 1989. Use of a bleomycin-containing medium to distinguish Aspergillus parasiticus from A. sojae. Mycologia 81: 159-160.
    CrossRef
  17. Glass NL, Donaldson GC. 1995. Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl. Environ. Microbiol. 61:1323-1330.
    Pubmed PMC
  18. Hubka V, Kolarik M. 2012. β-Tubulin paralogue tubC is frequently misidentified as the benA gene in Aspergillus section Nigri taxonomy: primer specificity testing and taxonomic consequences. Persoonia 29: 1.
    Pubmed PMC CrossRef
  19. Peterson SW. 2008. Phylogenetic analysis of Aspergillus species using DNA sequences from four loci. Mycologia 100:205-226.
    Pubmed CrossRef
  20. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406-425.
    Pubmed
  21. Godet M, Munaut F. 2010. Molecular strategy for identification in Aspergillus section Flavi. FEMS Microbiol. Lett. 304: 157-168.
    Pubmed CrossRef
  22. Yuan GF, Liu CS, Chen CC. 1995. Differentiation of Aspergillus parasiticus from Aspergillus sojae by random amplification of polymorphic DNA. Appl. Environ. Microbiol. 61: 2384-2387.
    Pubmed PMC
  23. Miller GL. 1959. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal. Chem. 31: 426-428.
    CrossRef
  24. Sahnoun M, Kriaa M, Elgharbi F, Ayadi D-Z, Bejar S, Kammoun R. 2015. Aspergillus oryzae S2 alpha-amylase production under solid state fermentation: optimization of culture conditions. Int. J. Biol. Macromol. 75: 73-80.
    Pubmed CrossRef
  25. Kum S-J, Yang S-O, Lee SM, Chang P-S, Choi YH, Lee JJ, et al. 2015. Effects of Aspergillus species inoculation and their enzymatic activities on the formation of volatile components in fermented soybean paste (doenjang). J. Agric. Food Chem. 63: 1401-1418.
    Pubmed CrossRef
  26. Cupp-Enyard C. 2008. Sigma’s non-specific protease activity assay - casein as a substrate. J. Vis. Exp. 19: e899.
    CrossRef
  27. Tan PST, Konings WN. 1990. Purification and characterization of an aminopeptidase from Lactococcus lactis subsp. cremoris Wg2. Appl. Environ. Microbiol. 56: 526-532.
    Pubmed PMC
  28. Lee JH, Jo EH, Hong EJ, Kim KM, Lee I. 2014. Safety evaluation of filamentous fungi isolated from industrial doenjang koji. J. Microbiol. Biotechnol. 24: 1397-1404.
    Pubmed CrossRef
  29. Jørgensen TR. 2007. Identification and toxigenic potential of the industrially important fungi, Aspergillus oryzae and Aspergillus sojae. J. Food Prot. 70: 2916-2934.
    Pubmed CrossRef
  30. Murakami H. 1971. Classification of the koji mold. J. Gen. Appl. Microbiol. 17: 281-309.
    CrossRef
  31. Laforgue R, Guérin L, Pernelle JJ, Monnet C, Dupont J, Bouix M. 2009. Evaluation of PCR-DGGE methodology to monitor fungal communities on grapes. J. Appl. Microbiol. 107: 1208-1218.
    Pubmed CrossRef
  32. Lee C-Z, Liou G-Y, Yuan G-F. 2006. Comparison of the aflR gene sequences of strains in Aspergillus section Flavi. Microbiology 152: 161-170.
    Pubmed CrossRef
  33. Watson AJ, Fuller LJ, Jeenes DJ, Archer DB. 1999. Homologs of aflatoxin biosynthesis genes and sequence of aflR in Aspergillus oryzae and Aspergillus sojae. Appl. Environ. Microbiol. 65: 307-310.
    Pubmed PMC
  34. Chang P-K, Horn BW, Dorner JW. 2009. Clustered genes involved in cyclopiazonic acid production are next to the aflatoxin biosynthesis gene cluster in Aspergillus flavus. Fungal Genet. Biol. 46: 176-182.
    Pubmed CrossRef
  35. Sardjono, Zhu Y, Knol W. 1998. Comparison of fermentation profiles between lupine and soybean by Aspergillus oryzae and Aspergillus sojae in solid-state culture systems. J. Agric. Food Chem. 46: 3376-3380.
    CrossRef
  36. Felsenstein J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783-791.
    CrossRef
  37. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30: 2725-2729.
    Pubmed PMC CrossRef
  38. Tominaga M, Lee Y-H, Hayashi R, Suzuki Y, Yamada O, Sakamoto K, et al. 2006. Molecular analysis of an inactive aflatoxin biosynthesis gene cluster in Aspergillus oryzae RIB strains. Appl. Environ. Microbiol. 72: 484-490.
    Pubmed PMC CrossRef
  39. Chang P-K, Bhatnagar D, Cleveland TE, Bennett JW. 1995. Sequence variability in homologs of the aflatoxin pathway gene aflR distinguishes species in Aspergillus section Flavi. Appl. Environ. Microbiol. 61: 40-43.
    Pubmed PMC

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Article

Research article

J. Microbiol. Biotechnol. 2017; 27(2): 251-261

Published online February 28, 2017 https://doi.org/10.4014/jmb.1610.10013

Copyright © The Korean Society for Microbiology and Biotechnology.

Characterization of Aspergillus sojae Isolated from Meju, Korean Traditional Fermented Soybean Brick

Kyung Min Kim 1, Jaeho Lim 1, Jae Jung Lee 2, Byung-Serk Hurh 2 and Inhyung Lee 1*

1Department of Bio and Fermentation Convergence Technology, BK21 PLUS Project, Kookmin University, Seoul 02707, Republic of Korea, 2Sempio Fermentation Research Center, Sempio Foods Company, Chungcheongbukdo 28156, Republic of Korea

Received: October 7, 2016; Accepted: November 21, 2016

Abstract

Initially, we screened 18 Aspergillus sojae-like strains from Aspergillus spp. isolated from meju
(Korean traditional fermented soybean brick) according to their morphological characteristics.
Because members of Aspergillus section Flavi are often incorrectly identified because of their
phylogenetic similarity, we re-identified these strains at the morphological and molecular
genetic levels. Fourteen strains were finally identified as A. sojae. The isolates produced
protease and α-amylase with ranges of 2.66-10.64 and 21.53-106.73 unit/g-initial dry
substrate (U/g-IDS), respectively, which were equivalent to those of the koji (starter mold)
strains employed to produce Japanese soy sauce. Among the isolates and Japanese koji strains,
strains SMF 127 and SMF 131 had the highest leucine aminopeptidase (LAP) activities at 6.00
and 6.06 U/g-IDS, respectively. LAP plays an important role in flavor development because of
the production of low-molecular-weight peptides that affect the taste and decrease bitterness.
SMF 127 and SMF 131 appeared to be non-aflatoxigenic because of a termination point
mutation in aflR and the lack of the polyketide synthase gene found in other A. sojae strains. In
addition, SMF 127 and SMF 131 were not cyclopiazonic acid (CPA) producers because of the
deletion of maoA, dmaT, and pks/nrps, which are involved in CPA biosynthesis. Therefore,
A. sojae strains such as SMF 127 and SMF 131, which have high protease and LAP activities
and are free of safety issues, can be considered good starters for soybean fermentations, such
as in the production of the Korean fermented soybean products meju, doenjang, and ganjang.

Keywords: Aspergillus sojae, starter mold, soybean fermentation, protease, leucine aminopeptidase

References

  1. Sato A, Oshima K, Noguchi H, Ogawa M, Takahashi T, Oguma T, et al. 2011. Draft genome sequencing and comparative analysis of Aspergillus sojae NBRC4239. DNA Res. 18: 165-176.
    Pubmed KoreaMed CrossRef
  2. Kitamoto K. 2002. Molecular biology of the koji molds. Adv. Appl. Microbiol. 51: 129-154.
    CrossRef
  3. Nampoothiri KM, Nagy V, Kovacs K, Szakacs G, Pandey A. 2005. L-Leucine aminopeptidase production by filamentous Aspergillus fungi. Lett. Appl. Microbiol. 41: 498-504.
    Pubmed CrossRef
  4. Toldrá F, Aristoy M-C, Flores M. 2000. Contribution of muscle aminopeptidases to flavor development in dry-cured ham. Food Res. Int. 33: 181-185.
    CrossRef
  5. Kim D-H, Kim S-H, Kwon S-W, Lee J-K, Hong S-B. 2013. Mycoflora of soybeans used for meju fermentation. Mycobiology 41: 100-107.
    Pubmed KoreaMed CrossRef
  6. Buyukkileci AO, Tari C, Fernandez-Lahore M. 2011. Enhanced production of exo-polygalacturonase from agrobased products by Aspergillus sojae. Bioresources 6: 3452-3468.
  7. Chang P-K. 2004. Lack of interaction between AFLR and AFLJ contributes to nonaflatoxigenicity of Aspergillus sojae. J. Biotechnol. 107: 245-253.
    Pubmed CrossRef
  8. Gurkok S, Cekmecelioglu D, Ogel ZB. 2011. Optimization of culture conditions for Aspergillus sojae expressing an Aspergillus fumigatus α-galactosidase. Bioresour. Technol. 102: 4925-4929.
    Pubmed CrossRef
  9. Heerd D, Yegin S, Tari C, Fernandez-Lahore M. 2012. Pectinase enzyme-complex production by Aspergillus spp. in solid-state fermentation: a comparative study. Food Bioprod. Process. 90: 102-110.
    CrossRef
  10. Lin C-H, Wei Y-T, Chou C-C. 2006. Enhanced antioxidative activity of soybean koji prepared with various filamentous fungi. Food Microbiol. 23: 628-633.
    Pubmed CrossRef
  11. Oncu S, Tari C, Unluturk S. 2007. Effect of various process parameters on morphology, rheology, and polygalacturonase production by Aspergillus sojae in a batch bioreactor. Biotechnol. Prog. 23: 836-845.
    Pubmed CrossRef
  12. Chang P-K, Matsushima K, Takahashi T, Yu J, Abe K, Bhatnagar D, et al. 2007. Understanding nonaflatoxigenicity of Aspergillus sojae: a windfall of aflatoxin biosynthesis research. Appl. Microbiol. Biotechnol. 76: 977-984.
    Pubmed CrossRef
  13. Wicklow DT. 1984. Conidium germination rate in wild and domesticated yellow-green aspergilli. Appl. Environ. Microbiol. 47: 299-300.
    Pubmed KoreaMed
  14. Chang H-Y, Lee Y-B, Bae H-A, Huh J-Y, Nam S-H, Sohn HS, et al. 2011. Purification and characterisation of Aspergillus sojae naringinase: the production of prunin exhibiting markedly enhanced solubility with in vitro inhibition of HMG-CoA reductase. Food Chem. 124: 234-241.
    CrossRef
  15. Murakami H, Hayashi K, Ushijima S. 1982. Useful key characters separating three Aspergillus taxa: A. sojae, A. parasiticus, and A. toxicarius. J. Gen. Appl. Microbiol. 28: 55-60.
    CrossRef
  16. Klich M, Mullaney E. 1989. Use of a bleomycin-containing medium to distinguish Aspergillus parasiticus from A. sojae. Mycologia 81: 159-160.
    CrossRef
  17. Glass NL, Donaldson GC. 1995. Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl. Environ. Microbiol. 61:1323-1330.
    Pubmed KoreaMed
  18. Hubka V, Kolarik M. 2012. β-Tubulin paralogue tubC is frequently misidentified as the benA gene in Aspergillus section Nigri taxonomy: primer specificity testing and taxonomic consequences. Persoonia 29: 1.
    Pubmed KoreaMed CrossRef
  19. Peterson SW. 2008. Phylogenetic analysis of Aspergillus species using DNA sequences from four loci. Mycologia 100:205-226.
    Pubmed CrossRef
  20. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406-425.
    Pubmed
  21. Godet M, Munaut F. 2010. Molecular strategy for identification in Aspergillus section Flavi. FEMS Microbiol. Lett. 304: 157-168.
    Pubmed CrossRef
  22. Yuan GF, Liu CS, Chen CC. 1995. Differentiation of Aspergillus parasiticus from Aspergillus sojae by random amplification of polymorphic DNA. Appl. Environ. Microbiol. 61: 2384-2387.
    Pubmed KoreaMed
  23. Miller GL. 1959. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal. Chem. 31: 426-428.
    CrossRef
  24. Sahnoun M, Kriaa M, Elgharbi F, Ayadi D-Z, Bejar S, Kammoun R. 2015. Aspergillus oryzae S2 alpha-amylase production under solid state fermentation: optimization of culture conditions. Int. J. Biol. Macromol. 75: 73-80.
    Pubmed CrossRef
  25. Kum S-J, Yang S-O, Lee SM, Chang P-S, Choi YH, Lee JJ, et al. 2015. Effects of Aspergillus species inoculation and their enzymatic activities on the formation of volatile components in fermented soybean paste (doenjang). J. Agric. Food Chem. 63: 1401-1418.
    Pubmed CrossRef
  26. Cupp-Enyard C. 2008. Sigma’s non-specific protease activity assay - casein as a substrate. J. Vis. Exp. 19: e899.
    CrossRef
  27. Tan PST, Konings WN. 1990. Purification and characterization of an aminopeptidase from Lactococcus lactis subsp. cremoris Wg2. Appl. Environ. Microbiol. 56: 526-532.
    Pubmed KoreaMed
  28. Lee JH, Jo EH, Hong EJ, Kim KM, Lee I. 2014. Safety evaluation of filamentous fungi isolated from industrial doenjang koji. J. Microbiol. Biotechnol. 24: 1397-1404.
    Pubmed CrossRef
  29. Jørgensen TR. 2007. Identification and toxigenic potential of the industrially important fungi, Aspergillus oryzae and Aspergillus sojae. J. Food Prot. 70: 2916-2934.
    Pubmed CrossRef
  30. Murakami H. 1971. Classification of the koji mold. J. Gen. Appl. Microbiol. 17: 281-309.
    CrossRef
  31. Laforgue R, Guérin L, Pernelle JJ, Monnet C, Dupont J, Bouix M. 2009. Evaluation of PCR-DGGE methodology to monitor fungal communities on grapes. J. Appl. Microbiol. 107: 1208-1218.
    Pubmed CrossRef
  32. Lee C-Z, Liou G-Y, Yuan G-F. 2006. Comparison of the aflR gene sequences of strains in Aspergillus section Flavi. Microbiology 152: 161-170.
    Pubmed CrossRef
  33. Watson AJ, Fuller LJ, Jeenes DJ, Archer DB. 1999. Homologs of aflatoxin biosynthesis genes and sequence of aflR in Aspergillus oryzae and Aspergillus sojae. Appl. Environ. Microbiol. 65: 307-310.
    Pubmed KoreaMed
  34. Chang P-K, Horn BW, Dorner JW. 2009. Clustered genes involved in cyclopiazonic acid production are next to the aflatoxin biosynthesis gene cluster in Aspergillus flavus. Fungal Genet. Biol. 46: 176-182.
    Pubmed CrossRef
  35. Sardjono, Zhu Y, Knol W. 1998. Comparison of fermentation profiles between lupine and soybean by Aspergillus oryzae and Aspergillus sojae in solid-state culture systems. J. Agric. Food Chem. 46: 3376-3380.
    CrossRef
  36. Felsenstein J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783-791.
    CrossRef
  37. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30: 2725-2729.
    Pubmed KoreaMed CrossRef
  38. Tominaga M, Lee Y-H, Hayashi R, Suzuki Y, Yamada O, Sakamoto K, et al. 2006. Molecular analysis of an inactive aflatoxin biosynthesis gene cluster in Aspergillus oryzae RIB strains. Appl. Environ. Microbiol. 72: 484-490.
    Pubmed KoreaMed CrossRef
  39. Chang P-K, Bhatnagar D, Cleveland TE, Bennett JW. 1995. Sequence variability in homologs of the aflatoxin pathway gene aflR distinguishes species in Aspergillus section Flavi. Appl. Environ. Microbiol. 61: 40-43.
    Pubmed KoreaMed