Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Varying Inocula Permutations (Aspergillus oryzae and Bacillus amyloliquefaciens) affect Enzyme Activities and Metabolite Levels in Koji

  • Gil, Hye Jeong (Department of Bioscience and Biotechnology, Konkuk University) ;
  • Lee, Sunmin (Department of Bioscience and Biotechnology, Konkuk University) ;
  • Singh, Digar (Department of Bioscience and Biotechnology, Konkuk University) ;
  • Lee, Choong Hwan (Department of Bioscience and Biotechnology, Konkuk University)
  • Received : 2018.09.28
  • Accepted : 2018.10.11
  • Published : 2018.12.28
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Abstract

In this study, we investigated the altered enzymatic activities and metabolite profiles of koji fermented using varying permutations of Aspergillus oryzae and/or Bacillus amyloliquefaciens. Notably, the protease and ${\beta}$-glucosidase activities were manifold increased in co-inoculated (CO) koji samples (co-inoculation of A. oryzae and B. amyloliquefaciens). Furthermore, gas chromatography-mass spectrometry (GC-MS)-based metabolite profiling indicates that levels of amino acids, organic acids, sugars, sugar alcohols, fatty acids, nucleosides, and vitamins were distinctly higher in CO, SA (sequential inoculation of A. oryzae, followed by B. amyloliquefaciens), and SB (sequential inoculation of B. amyloliquefaciens, followed by A. oryzae). The multivariate principal component analysis (PCA) plot based on GC-MS datasets indicated a clustered pattern for MA and MB (koji samples inoculated either with A. oryzae or B. amyloliquefaciens) across PC2 (20.0%). In contrast, the CO, SA, and SB metabolite profiles displayed segregated patterns across PLS1 (22.2%) and PLS2 (21.1%) in the partial least-square discriminant analysis (PLS-DA) model. Intriguingly, the observed disparity in the levels of primary metabolites was engendered largely by higher relative levels of sugars and sugar alcohols in MA, SA, and CO koji samples, which was commensurate with the relative amylase activities in respective samples. Collectively, the present study emphasizes the utility of integrated biochemical and metabolomic approaches for achieving the optimal permutation of fermentative inocula for industrial koji preparation.

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References

  1. Feron G, Bonnarme P, Durand A. 1996. Prospects for the microbial production of food flavours. Trends Food Sci. Technol. 7: 285-293. https://doi.org/10.1016/0924-2244(96)10032-7
  2. Blandino A, Al-Aseeri ME, Pandiella SS, Cantero D, Webb C. 2003. Cereal-based fermented foods and beverages. Food Res. Int. 36: 527-543. https://doi.org/10.1016/S0963-9969(03)00009-7
  3. 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. https://doi.org/10.1016/j.ijfoodmicro.2014.06.003
  4. Kim DH, Kim SH, Kwon SW, Lee JK, Hong SB. 2013. Fungal diversity of rice straw for meju fermentation. J. Microbiol. Biotechnol. 23: 1654-1663. https://doi.org/10.4014/jmb.1307.07071
  5. Lee S, Lee S, Singh D, Oh JY, Jeon EJ, Ryu HS, et al 2017. Comparative evaluation of microbial diversity and metabolite profiles in doenjang, a fermented soybean paste, during the two different industrial manufacturing processes. Food Chem. 221: 1578-1586. https://doi.org/10.1016/j.foodchem.2016.10.135
  6. Lee S, Lee DE, Singh D, Lee CH. 2018. Metabolomics reveal optimal grain preprocessing (milling) toward rice Koji fermentation. J. Agric. Food Chem. 66: 2694-2703. https://doi.org/10.1021/acs.jafc.7b05131
  7. Lee DE, Lee S, Jang ES, Shin HW, Moon BS, Lee CH. 2016. Metabolomic profiles of Aspergillus oryzae and Bacillus amyloliquefaciens during rice koji fermentation. Molecules 21: 773. https://doi.org/10.3390/molecules21060773
  8. Seo HS, Lee S, S ingh D , Shin HW, Cho SA, L ee CH. 2 018. Untargeted metabolite profiling for koji-fermentative bioprocess unravels the effects of varying substrate types and microbial inocula. Food Chem. 266: 161-169 https://doi.org/10.1016/j.foodchem.2018.05.048
  9. Bechman A, Phillips RD, Chen J. 2012. Changes in selected physical property and enzyme activity of rice and barley koji during fermentation and storage. J. Food Sci. 77: 318-322. https://doi.org/10.1111/j.1750-3841.2012.02691.x
  10. Lin CH, Wei YT, Chou CC. 2006. Enhanced antioxidative activity of soybean koji prepared with various filamentous fungi. Food Microbiol. 23: 628-633. https://doi.org/10.1016/j.fm.2005.12.004
  11. Zhu Y, Tramper J. 2013. Koji-where East meets West in fermentation. Biotechnol. Adv. 31: 1448-1457. https://doi.org/10.1016/j.biotechadv.2013.07.001
  12. Leroy F, De Vuyst L. 2004. Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci. Technol. 15: 67-78. https://doi.org/10.1016/j.tifs.2003.09.004
  13. Kim AJ, Choi JN, Kim J, Park SB, Yeo SH, Choi JH, et al 2010. GC-MS based metabolite profiling of rice koji fermentation by various fungi. Biosci. Biotechnol. Biochem. 74: 2267-2272. https://doi.org/10.1271/bbb.100488
  14. Yen GC, Chang YC, Su SW. 2003. Antioxidant activity and active compounds of rice koji fermented with Aspergillus candidus. Food Chem. 83: 49-54. https://doi.org/10.1016/S0308-8146(03)00035-9
  15. Benoit-Gelber I, Gruntjes T, Vinck A, van Veluw JG, Wosten HA, Boeren S, et al 2017. Mixed colonies of Aspergillus niger and Aspergillus oryzae cooperatively degrading wheat bran. Fungal Genet. Biol. 102: 31-37. https://doi.org/10.1016/j.fgb.2017.02.006
  16. Peng Y, Huang Q, Zhang RH, Zhang YZ. 2003. Purification and characterization of a fibrinolytic enzyme produced by Bacillus amyloliquefaciens DC-4 screened from douchi, a traditional Chinese soybean food. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 134: 45-52. https://doi.org/10.1016/S1096-4959(02)00183-5
  17. Kim YS, Oh BH, Shin DH. 2008. Quality characteristics of Kochujang prepared with different meju fermented with Aspergillus sp. and Bacillus subtilis. Food Sci. Biotechnol. 17: 527-533.
  18. Singracha P, Niamsiri N, Visessanguan W, Lertsiri S, Assavanig A. 2017. Application of lactic acid bacteria and yeasts as starter cultures for reduced-salt soy sauce (moromi) fermentation. LWT-Food Sci. Technol. 78: 181-188. https://doi.org/10.1016/j.lwt.2016.12.019
  19. Benoit I, van den Esker MH, Patyshakuliyeva A, Mattern DJ, Blei F, Zhou M, et al. 2015. Bacillus subtilis attachment to Aspergillus niger hyphae results in mutually altered metabolism. Environ. Microbiol. 17: 2099-2113. https://doi.org/10.1111/1462-2920.12564
  20. Singh D, Lee S, Lee CH. 2017. Metabolomics for empirical delineation of the traditional Korean fermented foods and beverages. Trends Food Sci. Technol. 61: 103-115. https://doi.org/10.1016/j.tifs.2017.01.001
  21. Lee DE, Lee S, Singh D, Jang ES, Shin HW, Moon BS, et al 2017. Time-resolved comparative metabolomes for Koji fermentation with brown-, white-, and giant embryo-rice. Food Chem. 231: 258-266. https://doi.org/10.1016/j.foodchem.2017.03.119
  22. Teng D, Gao M, Yang Y, Liu B, Tian Z, Wang J. 2012, Biomodification of soybean meal with Bacillus subtilis or Aspergillus oryzae. Biocatal. Agric. Biotechnol. 1: 32-38. https://doi.org/10.1016/j.bcab.2011.08.005
  23. Hong K J, Lee CH, Kim SW. 2004. Aspergillus oryzae GB-107 fermentation improves nutritional quality of food soybeans and feed soybean meals. J. Med. Food. 7: 430-436. https://doi.org/10.1089/jmf.2004.7.430
  24. Perez J, Munoz-Dorado J, de la Rubia T, Martinez J. 2002. Biodegradation and biological treatments of cellulose, hemicellulose and lignin: an overview. Int. Microbiol. 5: 53-63. https://doi.org/10.1007/s10123-002-0062-3
  25. Ahamed A, Vermette P. 2008. Enhanced enzyme production from mixed cultures of Trichoderma reesei RUT-C30 and Aspergillus niger LMA grown as fed batch in a stirred tank bioreactor. Biochem. Eng. J. 42: 41-46. https://doi.org/10.1016/j.bej.2008.05.007
  26. Sivaramakrishnan S, Gangadharan D, Nampoothiri KM, Soccol CR, Pandey A. 2006. ${\alpha}$-Amylase from microbial sources - an overview on recent developments. Food Technol. Biotechnol. 44: 173-184.
  27. Tanyildizi MS, Ozer D, Elibol M. 2005. Optimization of ${\alpha}$-amylase production by Bacillus sp. using response surface methodology. Process Biochem. 40: 2291-2296. https://doi.org/10.1016/j.procbio.2004.06.018
  28. Lee GM, Suh DH, Jung ES, Lee CH. 2016. Metabolomics provides quality characterization of commercial gochujang (fermented pepper paste). Molecules 21: E921. https://doi.org/10.3390/molecules21070921
  29. Deng Y, Lu S. 2017. Biosynthesis and regulation of phenylpropanoids in plants. CRC Crit. Rev. Plant Sci. 36: 257-290. https://doi.org/10.1080/07352689.2017.1402852
  30. Herrmann KM. 1995. The shikimate pathway as an entry to aromatic secondary metabolism. Plant Physiol. 107: 7-12. https://doi.org/10.1104/pp.107.1.7
  31. Naumgung HJ, Park HJ, Cho IH, Choi HK, Kwon DY, Shim SM, et al.010. Metabolite profiling of doenjang, fermented soybean paste, during fermentation. J. Sci. Food Agric. 90: 1926-1935.
  32. Karthikeyan A, Sivakumar N. 2010. Citric acid production by Koji fermentation using banana peel as a novel substrate. Bioresour. Technol. 101: 5552-5556. https://doi.org/10.1016/j.biortech.2010.02.063
  33. Yin X, Li J, Shin HD, Du G, Liu L, Chen J. 2015. Metabolic engineering in the biotechnological production of organic acids in the tricarboxylic acid cycle of microorganisms: advances and prospects. Biotechnol. Adv. 33: 830-841. https://doi.org/10.1016/j.biotechadv.2015.04.006
  34. Tran HTM, Cheirsilp B, Hodgson B, Umsakul K. 2010. Potential use of Bacillus subtilis in a co-culture with Clostridum butylicum for acetone-butanol-ethanol production from cassava starch. Biochem. Eng. J. 48: 260-267. https://doi.org/10.1016/j.bej.2009.11.001