Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Taxonomic Variations of Bacterial and Fungal Communities depending on Fermentation Temperature in Traditional Korean Fermented Soybean Food, Doenjang

  • Eunhye Jo (Department of Integrated Biological Science, Pusan National University) ;
  • Hyeyoung Lee (Food Science & Technology Major, Division of Applied Bioengineering, Dong-eui University) ;
  • Younshil Song (JINA F&C Company) ;
  • Jaeho Cha (Department of Integrated Biological Science, Pusan National University)
  • Received : 2023.12.14
  • Accepted : 2024.01.08
  • Published : 2024.04.28
Download PDF
⟨ Previous Next ⟩

Abstract

Meju, a fermented soybean brick, is a key component in soybean foods like doenjang and ganjang, harboring a variety of microorganisms, including bacteria and fungi. These microorganisms significantly contribute to the nutritional and sensory characteristics of doenjang and ganjang. Amplicon-based next-generation sequencing was applied to investigate how the microbial communities of meju fermented at low and high temperatures differ and how this variation affects the microbial communities of doenjang, a subsequently fermented soybean food. Our metagenomic data showed distinct patterns depending on the fermentation temperature. The microbial abundance in the bacterial community was increased under both temperatures during the fermentation of meju and doenjang. Weissella was the most abundant genus before the fermentation of meju, however, it was replaced by Bacillus at high temperature-fermented meju and lactic acid bacteria such as Weissella and Latilactobacillus at low temperature-fermented meju. Leuconostoc, Logiolactobacillus, and Tetragenococcus gradually took over the dominant role during the fermentation process of doenjang, replacing the previous dominant microorganisms. Mucor was dominant in the fungal community before and after meju fermentation, whereas Debaryomyces was dominant under both temperatures during doenjang fermentation. The dominant fungal genus of doenjang was not affected regardless of the fermentation temperature of meju. Strong correlations were shown for specific bacteria and fungi linked to specific fermentation temperatures. This study helps our understanding of meju fermentation process at different fermentation temperatures and highlights different bacteria and fungi associated with specific fermentation periods which may influence the nutritional and organoleptic properties of the final fermented soybean foods doenjang.

Keywords

Acknowledgement

This research was supported by the National Research Foundation of Korea (NRF) grant funded by the Korean government (MSIT) (RS-2023-00247945).

References

  1. Ann YG. 2016. A study on making meju (molded soybean) for traditional jang. J Korean Soc. Food Sci. Nutr. 29: 670-676.  https://doi.org/10.9799/ksfan.2016.29.5.670
  2. Shin D, Jeong D. 2015. Korean traditional fermented soybean products: jang. J. Ethn. Foods. 2: 2-7.  https://doi.org/10.1016/j.jef.2015.02.002
  3. Shin D, Kwon D, Nam Y, Jeong D. 2022. Overview of Korean Jang (Fermented Soybean Products) Manufacturing, pp. 205-208. 1 Ed. Ministry of Agriculture Food and Rural Affairs. 
  4. Park DH. 2014. Effect of incubation temperature on variations in bacterial communities grown in fermenting meju and the nutritional quality of soy sauce. Food Sci. Biotechnol. 23: 1921-1928.  https://doi.org/10.1007/s10068-014-0262-6
  5. Lee SY, Eom JS, Choi HS. 2014. Quality characteristics of fermented soybean products by Bacillus sp. isolated from traditional soybean paste. J. Korean Soc. Food Sci. Nutr. 43: 756-762.  https://doi.org/10.3746/jkfn.2014.43.5.756
  6. Baek JH, So KK, Ko YH, Kim JM, Kim DH. 2014. Mycoflora and enzymatic characterization of fungal isolates in commercial Meju, starter for a Korean traditional fermented soybean product. Mycobiology 42: 291-295.  https://doi.org/10.5941/MYCO.2014.42.3.291
  7. Eom JS, Choi HS. 2016. Inhibition of Bacillus cereus growth and toxin production by Bacillus amyloliquefaciens RD7-7 in fermented soybean products. J. Microbiol. Biotechnol. 26: 44-55.  https://doi.org/10.4014/jmb.1509.09090
  8. Shukla S, Bahuguna A, Park HK, Kim JK, Kim M. 2020. Effect of Rhizopus nigricans (Rhizopus stolonifera)-based novel starter culture on quality and safety attributes of doenjang, a traditional Korean soybean fermented food product. Sci. Rep. 10: 1081-1100.  https://doi.org/10.1038/s41598-019-57382-y
  9. Lee JG, Kwon KI, Choung MG, Kwon OJ, Choi JY, Im MH. 2009. Quality analysis on the size and the preparation method of Meju for the preparation of Korean traditional soy sauce (Kanjang). J. Appl. Biol. Chem. 52: 205-211.  https://doi.org/10.3839/jabc.2009.035
  10. Shin DS, Park HY, Park JY, Sim EY, Kim HS, Choi HS. 2020. Change of quality characteristics of Meju during fermentation with multiple starters. Korean J. Food Nutr. 33: 524-531. 
  11. Kim DH, Kim HS, 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
  12. Kim DH, Kim SH, Kwon SW, Lee JK, Hong SB. 2015. The mycobiota of air inside and outside the Meju fermentation room and the origin of Meju fungi. Mycobiology 43: 258-265.  https://doi.org/10.5941/MYCO.2015.43.3.258
  13. Jeong DW, Heo S, Lee B, Lee H, Jeong K, Her JY, et al. 2017. Effects of the predominant bacteria from meju and doenjang on the production of volatile compounds during soybean fermentation. Int. J. Food Microbiol. 262: 8-13.  https://doi.org/10.1016/j.ijfoodmicro.2017.09.011
  14. Kim DH, Kim SA, Jo YM, Seo H, Kim GY, Cheon SW, et al. 2022. Probiotic potential of Tetragenococcus halophilus EFEL7002 isolated from Korean soy Meju. BMC Microbiol. 22: 149-166.  https://doi.org/10.1186/s12866-022-02561-7
  15. Song NE, Lee DB, Lee SH, Baik SH. 2021. Preparation of high GABA-enriched yeast extract by non-Saccharomyces yeasts isolated from Korean traditional fermented soybean product. Microbiol. Biotechnol. Lett. 49: 320-328.  https://doi.org/10.48022/mbl.2105.05003
  16. Lee JE, Yun JH, Lee E, Hong SP. 2022. Untargeted metabolomics reveals Doenjang metabolites affected by manufacturing process and microorganisms. Food Res. Int. 157: 111422-111434.  https://doi.org/10.1016/j.foodres.2022.111422
  17. Kim HM, Han DM, Baek JH, Chun BH, Jeon CO. 2022. Dynamics and correlation of microbial communities and metabolic compounds in doenjang-meju, a Korean traditional soybean brick. Food Res. Int. 155: 111085. 
  18. Song DH, Chun BH, Lee S, Son SY, Reddy CK, Mun HI, et al. 2021. Comprehensive metabolite profiling and microbial communities of Doenjang (fermented soy paste) and Ganjang (fermented soy sauce): a comparative study. Foods 10: 641-655.  https://doi.org/10.3390/foods10030641
  19. Ryu JA, Kim E, Yang SM, Lee S, Yoon SR, Jang KS, et al. 2021. High-throughput sequencing of the microbial community associated with the physicochemical properties of meju (dried fermented soybean) and doenjang (traditional Korean fermented soybean paste). LWT-Food Sci. Technol. 146: 111473-111481.  https://doi.org/10.1016/j.lwt.2021.111473
  20. Han DM, Chun BH, Feng T, Kim HM, Jeon CO. 2020. Dynamics of microbial communities and metabolites in ganjang, a traditional Korean fermented soy sauce, during fermentation. Food Microbiol. 92: 103591-103600.  https://doi.org/10.1016/j.fm.2020.103591
  21. Cho SH, Park HS, Jo SW, Yim EJ, Yang HY, Ha GS, et al. 2017. Comparison of microbial community profiling on traditional fermented soybean products (Deonjang, Gochujang) produced in Jeonbuk, Jeonnam, and Jeju province area. Korean J. Microbiol. 53: 39-48.  https://doi.org/10.7845/kjm.2017.6074
  22. Herlemann DPR, Labrenz M, Jurgens K, Bertilsson S, Waniek JJ, Andersson AF. 2011. Transitions in bacterial communities along the 2000km salinity gradient of the Baltic sea. ISME J. 5: 1571-1579.  https://doi.org/10.1038/ismej.2011.41
  23. Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, et al. 2013. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 41: e1. 
  24. Turenne CY, Sanche SE, Hoban DJ, Karlowsky JA, Kabani AM. 1999. Rapid identification of fungi by using the ITS2 genetic region and an automated fluorescent capillary electrophoresis system. J. Clin. Microbiol. 37: 1846-1851.  https://doi.org/10.1128/JCM.37.6.1846-1851.1999
  25. Beeck ODM, Lievens B, Busschaert P, Declerck S, Vangronsveld J, Colpaert JV. 2014. Comparison and validation of some ITS primer pairs useful for fungal metabarcoding studies. PLoS One 9: e97629-e97629.  https://doi.org/10.1371/journal.pone.0097629
  26. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP. 2016. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13: 581-583.  https://doi.org/10.1038/nmeth.3869
  27. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. 2012. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41: D590-D596.  https://doi.org/10.1093/nar/gks1219
  28. McMurdie PJ, Holmes S. 2013. Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8: e61217-61228.  https://doi.org/10.1371/journal.pone.0061217
  29. Harrell Jr FE, Dupont C. 2019. Package 'hmisc'. Available from https://CRAN.R-project.org/package=Hmisc. 
  30. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. 2003. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13: 2498-2504.  https://doi.org/10.1101/gr.1239303
  31. Collins MD, Williams AM, Wallbanks S. 1990. The phylogeny of Aerococcus and Pediococcus as determined by 16S rRNA sequence analysis: description of Tetragenococcus gen. nov. FEMS Microbiol. Lett. 70: 255-262.  https://doi.org/10.1111/j.1574-6968.1990.tb14006.x
  32. Jeong DM, Yoo SJ, Jeon MS, Chun BH, Han DM, Jeon CO, et al. 2022. Genomic features, aroma profiles, and probiotic potential of the Debaryomyces hansenii species complex strains isolated from Korean soybean fermented food. Food Microbiol. 105: 104011-104023.  https://doi.org/10.1016/j.fm.2022.104011
  33. Choi JH, Kim GW, Lee HY, Park CS, Shim JY. 2019. Brewing characteristics of Wickerhamomyces anomalus SC-1 isolated from Korean traditional uruk. Food Eng. Progress 23: 223-228.  https://doi.org/10.13050/foodengprog.2019.23.3.223
  34. Cardona C, Weisenhorn P, Henry C, Gilbert JA. 2016. Network-based metabolic analysis and microbial community modeling. Curr. Opin. Microbiol. 31: 124-131.  https://doi.org/10.1016/j.mib.2016.03.008
  35. Dai Y, Xu Z, Wang Z, Li X, Dong J, Xia X. 2023. Effects of fermentation temperature on bacterial community, physicochemical properties and volatile flavor in fermented soy whey and its coagulated tofu. LWT 173: 114355-114363.  https://doi.org/10.1016/j.lwt.2022.114355
  36. Jung WY, Jung JY, Lee HJ, Jeon CO. 2016. Functional characterization of bacterial communities responsible for fermentation of Doenjang: a traditional Korean fermented soybean paste. Front. Microbiol. 7: 827. 
  37. Han DM, Chun BH, Kim HM, Jeon CO. 2021. Characterization and correlation of microbial communities and metabolite and volatile compounds in doenjang fermentation. Food Res. Int. 148: 110645. 
  38. Jeong JK, Zheng Y, Choi HS, Han GJ, Park KY. 2010. Catabolic ezyme ativities and pysiological fnctionalities of lactic acid bacteria isolated from Korean traditional Meju. J. Korean Soc. Food Sci. Nutr. 39: 1854-1859.  https://doi.org/10.3746/jkfn.2010.39.12.1854
  39. Luo YY, Guo Y, Hu XY, Liu WH, Liu BQ, Yang J, et al. 2023. Flavor improvement of fermented soybean foods by co-fermentation with Bacillus velezensis and Lactiplantibacillus plantarum. LWT 186: 115257. 
  40. Na HE, Heo S, Kim YS, Kim T, Lee G, Lee JH, et al. 2022. The safety and technological properties of Bacillus velezensis DMB06 used as a starter candidate were evaluated by genome analysis. LWT 161: 113398. 
  41. Jo HD, Lee HA, Jeong SJ, Kim JH. 2011. Purification and characterization of a major fibrinolytic enzyme from Bacillus amyloliquefaciens MJ5-41 isolated from Meju. J. Microbiol. Biotechnol. 21: 1166-1173.  https://doi.org/10.4014/jmb.1106.06008
  42. Cho SJ, Oh SH, Pridmore RD, Juillerat MA, Lee CH. 2003. Purification and characterization of proteases from Bacillus amyloliquefaciens isolated from traditional soybean fermentation starter. J. Agric. Food Chem. 51: 7664-7670.  https://doi.org/10.1021/jf0259314
  43. Frohlich-Wyder MT, Arias-Roth E, Jakob E. 2019. Cheese yeasts. Yeast 36: 129-141.  https://doi.org/10.1002/yea.3368
  44. Ramos-Moreno L, Ruiz-Perez F, Rodriguez-Castro E, Ramos J. 2021. Debaryomyces hansenii is a real tool to improve a diversity of characteristics in sausages and dry-meat products. Microorganisms. 9: 1512. 
  45. Kharnaior P, Tamang JP. 2022. Metagenomic-metabolomic mining of Kinema, a naturally fermented soybean food of the eastern Himalayas. Front. Microbiol. 13: 868383. 
  46. Song Z, Hu Y, Chen X, Li G, Zhong Q, He X, et al. 2021. Correlation between bacterial community succession and propionic acid during gray sufu fermentation. Food Chem. 353: 129447. 
  47. Yang B, Liu Y, Sang Y, Sun J. 2023. Bacterial diversity and physicochemical properties of low-salt shrimp paste fermented at different temperatures. LWT 187: 115277.