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Molecular and Morphological Identification of Fungal Species Isolated from Bealmijang Meju

  • Kim, Ji-Yeun (Department of Agro-food Resources, National Academy of Agricultural Science, RDA) ;
  • Yeo, Soo-Hwan (Department of Agro-food Resources, National Academy of Agricultural Science, RDA) ;
  • Baek, Sung-Yeol (Department of Agro-food Resources, National Academy of Agricultural Science, RDA) ;
  • Choi, Hye-Sun (Department of Agro-food Resources, National Academy of Agricultural Science, RDA)
  • Received : 2011.05.12
  • Accepted : 2011.08.05
  • Published : 2011.12.28

Abstract

Bealmijang is a short-term aged paste made from meju, which is a brick of fermented soybeans and other ingredients. Different types of bealmijang are available depending on the geographic region or ingredients used. However, no study has clarified the microbial diversity of these types. We identified 17 and 14 fungal species from black soybean meju (BSM) and buckwheat meju (BWM), respectively, on the basis of morphology, culture characteristics, and internal transcribed spacer and ${\beta}$-tubulin gene sequencing. In both meju, Aspergillus oryzae, Rhizopus oryzae, Penicillium polonicum, P. steckii, Cladosporium tenuissimum, C. cladosporioides, C. uredinicola, and yeast species Pichia burtonii were commonly found. Moreover, A. flavus, A. niger, P. crustosum, P. citrinum, Eurotium niveoglaucum, Absidia corymbifera, Setomelanomma holmii, Cladosporium spp. and unclassified species were identified from BSM. A. clavatus, Mucor circinelloides, M. racemosus, P. brevicompactum, Davidiella tassiana, and Cladosporium spp. were isolated from BWM. Fast growing Zygomycetous fungi is considered important for the early stage of meju fermentation, and A. oryae and A. niger might play a pivotal role in meju fermentation owing to their excellent enzyme productive activities. It is supposed that Penicillium sp. and Pichia burtonii could contribute to the flavor of the final food products. Identification of this fungal diversity will be useful for understanding the microbiota that participate in meju fermentation, and these fungal isolates can be utilized in the fermented foods and biotechnology industries.

Keywords

References

  1. An, B. J., G. M. Son, and C. Choi. 1986. Changes in protein and amino acid composition of native meju during fermentation. J. Korean Soc. Food Nutr. 15: 152-157.
  2. Bae, S. I., B. Y. Kwak, Y. K. Park, Y. H. Kim, and D. H. Shon. 2003. Survey of aflatoxin B1 in domestic doenjang and kochujang determined by enzyme-linked immunosorbent assay. J. Food Hyg. Safety 18: 89-100.
  3. Bensch, K., J. Z. Groenevald, J. Dijksterhuis, M. Starink- Willemse, B. Andersen, B. B. Summerell, et al. 2010. Species and ecological diversity within the Cladosporium cladosporioides complex (Davidiellaceae, Capnodiales). Stud. Mycol. 67: 1-94. https://doi.org/10.3114/sim.2010.67.01
  4. Chang, P. K. and K. C. Ehrlich. 2010. What does genetic diversity of Aspergillus flavus tell us about Aspergillus oryzae? Int. J. Food Microbiol. 138: 189-199. https://doi.org/10.1016/j.ijfoodmicro.2010.01.033
  5. Cho, D. H. and W. J. Lee. 1970. Microbiological studies of Korean native soy-sauce fermentation: A study on the microflora of fermented Korean maeju loaves. J. Korean Agric. Chem. Soc. 13: 35-42.
  6. Choi, H. S. 2009. Improvement of byelmijang products. Global Food Culture 4: 40-47.
  7. Flannigan, B. and A. R. Pearce. 1994. Aspergillus spoilage: spoilage of cereals and cereal products by the hazardous species Aspergillus clavatus, pp. 55-62. In K. A. Powell, A. Renwick, J. F. Peberdy (eds.). The Genus Aspergillus. From Taxonomy and Genetics to Industrial Application. Plenum Press, New York.
  8. Glass, N. L. and G. C. Donaldson. 1995. Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl. Environ. Microbiol. 61: 1323-1330.
  9. Hahn, Y. S. and K. J. Kim. 1962. Studies on manufacturing of soy sauce, 5. On genus Mucor in Korean bean meju. Report Natl. Ind. Res. Inst. 11: 140.
  10. Hahn, Y. S., B. D. Park, and K. S. Chun. 1962. Studies on manufacturing of soy sauce, 4. On genus Rhizopus and Mucor in Korean wine kokja. Report Natl. Ind. Res. Inst. 11: 52.
  11. Hwang, J. 1997. Angiotension I converting enzyme inhibitory effect of doenjang fermented by B. subtilis isolated from meju, Korean traditional food. J. Korean Soc. Food Sci. Nutr. 26: 775-783.
  12. Jung, Y., W. Choi, N. Oh, and Minsu Han. 1996. Distribution and physiological characteristics of yeasts in traditional and commercial kochujang. Korean J. Food Sci. Technol. 28: 253- 259.
  13. Kang, M. J., S. H. Kim, H. K. Joo, G. S. Lee, and M. H. Yim. 2000. Isolation and identification of microorganisms producing the soy protein-hydrolyzing enzyme from traditional mejus. J. Korean Soc. Agric. Chem. Biotechnol. 43: 86-94.
  14. Kantak, J., A. V. Bagade, S. A. Mahajan, S. P. Pawar, Y. S. Shouche, and A. A. Prabhune. 2011. Isolation, identification and optimization of a new extracellular lipase producing strain of Rhizopus sp. Appl. Biochem. Biotechnol. 164: 969-978. https://doi.org/10.1007/s12010-011-9188-0
  15. Kim, D. H. and S. H. Kim. 1999. Biochemical characteristics of whole soybean cereals fermented with Mucor and Rhizopus strains. Korean J. Food Sci. Technol. 31: 176-182.
  16. Kim, E. K., D. H. Shon, J. Y. Yoo, D. Ryu, C. Lee, and Y. B. Kim. 2001. Natural occurrence of aflatoxins in Korean meju. Food Addit. Contam. 18: 151-156. https://doi.org/10.1080/02652030010006104
  17. Kim, J. K. and C. S. Kim. 1980. The taste components of ordinary Korean soy sauce. J. Korean Agric. Chem. Soc. 23: 89-105.
  18. Kim, K., M. Nam, B. R. Nam, H. J. Ryu, J. E. Song, W. B. Shin, et al. 2010. Determination of total aflatoxins in foods by parallelism of ELISA and LC/MS/MS. J. Environ. Health Sci. 36: 52-60.
  19. Kim, S. H. 1998. New trends of studying on potential activities of doenjang, Fibrinolytic activity. Korea Soybean Digest 15: 8-15.
  20. Kimura, M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16: 111-120. https://doi.org/10.1007/BF01731581
  21. Korea Food Research Institute. 2004. A study on the physiological function of Korean traditional fermented food. Rural Development Administration.
  22. Lee, J. H., M. H. Kim, and S. S. Lim. 1991. Antioxidative materials in domestic meju and doenjang-1. Lipid oxidation and browning during fermentation of meju and doenjang. J. Korean Soc. Food Sci. Nutr. 20: 148-155.
  23. Lee, J. H., T. W. Kim, H. Lee, H. C. Chang, and H. Y. Kim. 2010. Determination of microbial diversity in meju, fermented cooked soya beans, using nested PCR-denaturing gradient gel electrophoresis. Lett. Appl. Microbiol. 51: 388-394. https://doi.org/10.1111/j.1472-765X.2010.02906.x
  24. Lee, J. S., S. H. Yi, S. J. Kwon, C. Ahn, and J. Y. Yoo. 1997. Enzyme activities and physiological functionality of yeasts from traditional meju. Kor. J. Appl. Microbiol. Biotechnol. 25: 448-453.
  25. Lee, S. S., C. Sung, J. C. Bae, and J. Y. Yu. 1997. Kanjang and meju made with a single inoculums of the microorganism isolated from the Korean traditional meju. J. Korean Soc. Food Sci. Nutr. 26: 751-758.
  26. Lee, S. S., K. H. Park, K. J. Choi, and S. A. Won. 1993. A study on hyphomycetous fungi found on maejus, a raw material of Korean traditional soysources. Korean J. Mycol. 21: 247- 272.
  27. Lee, S. S., K. H. Park, K. J. Choi, and S. A. Won. 1993. Identification and isolation of Zygomycetous fungi found on maeju, a raw material of Korean traditional soysources. Korean J. Mycol. 21: 172-187.
  28. Lim, S. Y., K. Y. Park, and S. H. Rhee. 1999. Anticancer effect of doenjang in vitro sulforhodamine B (SRB) assay. J. Korean Soc. Food Sci. Nutr. 28: 240-245
  29. Lim, S. I. and J. Y. Yoo. 1999. Characteristics of fungal protease produced by Mucor racemousus f. racemosus from Korean traditional meju. Kor. J. Appl. Microbiol. Biotechnol. 27: 466-470.
  30. Lim, S. I., E. J. Kwak, S. Y. Choi, and J. Y. Yoo. 2002. Characteristics of protease produced by Rhizopus stolonifer, Rhizopus oryzae and Absidia corymbifera from Korean traditional meju. J. Korean Soc. Food Sci. Nutr. 31: 211-215. https://doi.org/10.3746/jkfn.2002.31.2.211
  31. Magnuson, J. K. and L. L. Lasure. 2004. Organic acid production by filamentous fungi. In J. Lange and L. Lange (eds.). Advances in Fungal Biotechnology for Industry, Agriculture, and Medicine. Kluwer Academic/Plenum Publishers.
  32. Oh, H. J. and C. S. Kim. 2007. Antioxidant and nitrite scavaging ability of fermented soybean foods (chungkukjang, doenjang). J. Korean Soc. Food Sci. Nutr. 36: 1503-1510. https://doi.org/10.3746/jkfn.2007.36.12.1503
  33. Olempska-Beer, Z. S., R. I. Merker, M. D. Ditto, and M. J. DiNovi. 2006. Food-processing enzymes from recombinant microorganisms - a review. Regul. Toxicol. Pharmacol. 45: 144-158. https://doi.org/10.1016/j.yrtph.2006.05.001
  34. Park, M. J., M. H. Yoon, H. G. Hong, T. S. Joe, I. S. Lee, J. H. Park, and H. U. Ko. 2008. A survey of the presence of aflatoxins in food. J. Food Hyg. Safety 23: 108-112.
  35. Petruccioli, M. and F. Federici. 1988. Extracellular enzyme production in species of the genus Penicillium. Mycologia 80: 726-728. https://doi.org/10.2307/3807725
  36. Pitt, J. I. 1979. The Genus Pencillium and Its Teleomorphic States Eupenicillum and Talaromyces. Academic Press, London.
  37. Punt, P. and C. den Hondel. 1992. Analysis of transcription control sequences in filamentous fungi. In U. Stahl and P. Tudzynscki (eds.). Proceedings of EMBO Workshop on Molecular Biology of Filamentous Fungi. VCH, Weinheim.
  38. Regueira, T. B., K. R. Kildegaard, B. G. Hansen, U. H. Mortensen, C. Hertweck, and J. Nielsen. 2011. Molecular basis for mycophenolic acid biosynthesis in Penicillium brevicompactum. Appl. Environ. Microbiol. 77: 3035-3043. https://doi.org/10.1128/AEM.03015-10
  39. Rossman, A. Y., D. F. Farr, L. A. Castlebury, R. Soemaker, and A. Mengistu. 2002. Setomelanomma holmii (Pleosporales, Phaeosphaeriaceae) on living spruce twigs in Europe and North America. Can. J. Bot. 80: 1209-1215. https://doi.org/10.1139/b02-111
  40. Rundberget, T., I. Skaar, and A. Flaoyen. 2004. The presence of Penicillium and Penicillium mycotoxins in food wastes. Int. J. Food Microbiol. 90: 181-188. https://doi.org/10.1016/S0168-1605(03)00291-5
  41. Schubert, K., J. Z. Groenewald, U. Braun, J. Dijksterhuis, M. Starink, C. F. Hill, P. Zalar, G. S. de Hong, and P. W. Crous. 2007. Biodiversity in the Cladosporium herbarum complex (Davidiellaceae, Capnodiales), with standardization of methods for Cladosporium taxonomy and diagnostics. Stud. Mycol. 58: 105-156. https://doi.org/10.3114/sim.2007.58.05
  42. Schuster, E., N. Dunn-Coleman, J. C. Frisvad, and P. W. M. van Dijck. 2002. On the saferty of Aspergillus niger - a review. Appl. Microbiol. Biotechnol. 59: 426-435. https://doi.org/10.1007/s00253-002-1032-6
  43. Shimizu, K. and N. P. Keller. 2001. Genetic involvement of a cAMP-dependent protein kinase in a G protein signaling pathway regulating morphological and chemical transitions in Aspergillus nidulans. Genetics 157: 591-600.
  44. Shin, Z. I., C. W. Ahn, H. S. Nam, H. J. Lee, and T. H. Moon. 1995. Fractionation of angiotensin converting enzyme (ACE) inhibitory peptides from soybean paste. Korean J. Food Sci. Technol. 27: 230-234.
  45. Sonjak, S., M. Licen, J. C. Frisvad, and N. Gunde-Cimerman. 2011. The mycobiota of three dry-cured meat products from Slovenia. Food Microbiol. 28: 373-376. https://doi.org/10.1016/j.fm.2010.09.007
  46. Takeuchi, A., A. Shimizu-Ibuka, Y. nishiyama, K. Mura, S. Okada, C. Tokue, and S. Arai. 2006. Purification and characterization of an $\alpha$-amylase of Pichia burtonii isolated from the traditional starter "Murcha" in Nepal. Biosci. Biotechnol. Biochem. 70: 3019-3024. https://doi.org/10.1271/bbb.60430
  47. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596-1599. https://doi.org/10.1093/molbev/msm092
  48. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The Clustal-X Windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25: 4876-4882. https://doi.org/10.1093/nar/25.24.4876
  49. Vega, F. E., S. W. Peterson, and T. J. Gianfagna. 2006. Penicillium species endophytic in coffee plants and ochratoxin A production. Mycologia 98: 31-42. https://doi.org/10.3852/mycologia.98.1.31
  50. Woo, K. S., S. M. Yoo, S. K. Im, and H. K. Chun. 2004. Changes in aroma compounds of several byelijang during aging. J. Korean Soc. Food Sci. Nutr. 33: 1689-1697. https://doi.org/10.3746/jkfn.2004.33.10.1689
  51. Yoo, J. Y., H. G. Kim, and D. J. Kwon. 1998. Improved process for preparation of traditional kanjang (Korean-style soy sauce). J. Korean Soc. Food Sci. Nutr. 27: 268-274.
  52. Yoon, S. S. 1984. Korean Food History and Cooking, Suhaksa, pp. 54-59. Suhaksa.
  53. Yun, Y. H., M. W. Hyun, D. Y. Suh, Y. M. Kim, and S. H. Kim. 2009. Identification and characterization of Eurotium rubrum isolated from meju in Korea. Mycobiology 37: 251-257. https://doi.org/10.4489/MYCO.2009.37.4.251

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