Journal of Microbiology and Biotechnology

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

DOI QR Code

Effect of Enterotoxigenic Escherichia coli on Microbial Communities during Kimchi Fermentation

  • Lee, Woojung (Division of Food Microbiology, National Institute of Food and Drug Safety Evaluation, Ministry of Food and Drug Safety) ;
  • Choi, Hyo Ju (Division of Food Microbiology, National Institute of Food and Drug Safety Evaluation, Ministry of Food and Drug Safety) ;
  • Zin, Hyunwoo (Division of Food Microbiology, National Institute of Food and Drug Safety Evaluation, Ministry of Food and Drug Safety) ;
  • Kim, Eiseul (Institute of Life Sciences and Resources and Department of Food Science and Biotechnology, Kyung Hee University) ;
  • Yang, Seung-Min (Institute of Life Sciences and Resources and Department of Food Science and Biotechnology, Kyung Hee University) ;
  • Hwang, Jinhee (Division of Food Microbiology, National Institute of Food and Drug Safety Evaluation, Ministry of Food and Drug Safety) ;
  • Kwak, Hyo-Sun (Division of Food Microbiology, National Institute of Food and Drug Safety Evaluation, Ministry of Food and Drug Safety) ;
  • Kim, Soon Han (Division of Food Microbiology, National Institute of Food and Drug Safety Evaluation, Ministry of Food and Drug Safety) ;
  • Kim, Hae-Yeong (Institute of Life Sciences and Resources and Department of Food Science and Biotechnology, Kyung Hee University)
  • Received : 2021.08.30
  • Accepted : 2021.09.06
  • Published : 2021.11.28
Download PDF
⟨ Previous Next ⟩

Abstract

The diverse microbial communities in kimchi are dependent on fermentation period and temperature. Here, we investigated the effect of enterotoxigenic Escherichia coli (ETEC) during the fermentation of kimchi at two temperatures using high-throughput sequencing. There were no differences in pH between the control group, samples not inoculated with ETEC, and the ETEC group, samples inoculated with ETEC MFDS 1009477. The pH of the two groups, which were fermented at 10 and 25℃, decreased rapidly at the beginning of fermentation and then reached pH 3.96 and pH 3.62. In both groups, the genera Lactobacillus, Leuconostoc, and Weissella were predominant. Our result suggests that microbial communities during kimchi fermentation may be affected by the fermentation parameters, such as temperature and period, and not enterotoxigenic E. coli (ETEC).

Keywords

Acknowledgement

This research was supported by grants (nos. 17161MFDS033 and 20161MFDS030) from the Ministry of Food and Drug Safety. The findings and conclusions of this article are ours and do not necessarily represent the views of the Ministry of Food and Drug Safety.

References

  1. Hong Y, Yang HS, Chang HC, Kim HY. 2013. Comparison of bacterial community changes in fermenting Kimchi at two different temperatures using a denaturing gradient gel electrophoresis analysis. J. Microbiol. Biotechnol. 23: 76-84. https://doi.org/10.4014/jmb.1210.10002
  2. Lee M, Song JH, Jung MY, Lee SH, Chang JY. 2017. Large-scale targeted metagenomics analysis of bacterial ecological changes in 88 kimchi samples during fermentation. Food Microbiol. 66: 173-183. https://doi.org/10.1016/j.fm.2017.05.002
  3. Noh BS, Seo HY, Park WS, Oh S. 2016. Safety of Kimchi. In Regulating Safety of Traditional and Ethnic Foods, pp. 369-380.
  4. Jang JY, Lee ME, Lee HW, Lee JH, Park HW, Choi HJ, et al. 2015. Extending the shelf life of kimchi with Lactococcus lactis strain as a starter culture. Food Sci. Biotechnol. 24: 1049-1053. https://doi.org/10.1007/s10068-015-0134-8
  5. Jung JY, Lee SH, Jeon CO. 2014. Kimchi microflora: history, current status, and perspectives for industrial kimchi production. Appl. Microbiol. Biotechnol. 98: 2385-2393. https://doi.org/10.1007/s00253-014-5513-1
  6. Yun JW, Kang SC, Song SK. 1996. Mannitol accumulation during fermentation of Kimchi. J. Ferment. Bioeng. 81: 279-280. https://doi.org/10.1016/0922-338X(96)82224-0
  7. Sartz L, De Jong B, Hjertqvist M, Plym-Forshell L, Alsterlund R, Lofdahl S, et al. 2008. An outbreak of Escherichia coli O157:H7 infection in southern Sweden associated with consumption of fermented sausage; aspects of sausage production that increase the risk of contamination. Epidemiol. Infect. 136: 370-380. https://doi.org/10.1017/S0950268807008473
  8. Inatsu Y, Bari ML, Kawasaki S, Isshiki K. 2004. Survival of Escherichia coli O157:H7, Salmonella enteritidis, Staphylococcus aureus, and Listeria monocytogenes in kimchi. J. Food Prot. 67: 1497-1500. https://doi.org/10.4315/0362-028X-67.7.1497
  9. Mitsuda T, Muto T, Yamada M, Kobayashi N, Toba M, Aihara Y, et al. 1998. Epidemiological study of a food-borne outbreak of enterotoxigenic Escherichia coli O25:NM by pulsed-field gel electrophoresis and randomly amplified polymorphic DNA analysis. J. Clin. Microbiol. 36: 652-656. https://doi.org/10.1128/JCM.36.3.652-656.1998
  10. Qadri F, Svennerholm AM, Faruque AS, Sack RB. 2005 Enterotoxigenic Escherichia coli in developing countries: epidemiology, microbiology, clinical features, treatment, and prevention. Clin. Microbiol. Rev. 18: 465-483. https://doi.org/10.1128/CMR.18.3.465-483.2005
  11. Galdos-Balzategui A, Carmona-de la Torre J, Sanchez-Perez HJ, Morales-Lopez JJ, Torres-Dosal A, Gomez-Urbina S. 2017 Evaluacion cuantitativa del riesgo microbiologico por consumo de agua en San Cristobal de Las Casas, Chiapas, Mexico. Tecnol. Ciencias del Agua. 8: 133-153. https://doi.org/10.24850/j-tyca-2017-01-10
  12. Barragan, JM, Cuesta LD, Susa MR. 2021. Quantitative microbial risk assessment to estimate the public health risk from exposure to enterotoxigenic E. coli in drinking water in the rural area of Villapinzon, Colombia. Microb. Risk Anal. 9: P100173.
  13. Cho SH, Kim J, Oh KH, Hu JK, Seo J, Oh SS, et al. 2014. Outbreak of enterotoxigenic Escherichia coli O169 enteritis in schoolchildren associated with consumption of kimchi, Republic of Korea, 2012. Epidemiol. Infect. 142: 616-623. https://doi.org/10.1017/S0950268813001477
  14. Cho GY, Lee MH, Choi C. 2011. Survival of Escherichia coli O157:H7 and Listeria monocytogenes during kimchi fermentation supplemented with raw pork meat. Food Control 22: 1253-1260. https://doi.org/10.1016/j.foodcont.2011.01.026
  15. Hugenholtz P, Tyson GW. 2008. Microbiology: Metagenomics. Nature 455: 481-483. https://doi.org/10.1038/455481a
  16. Jung JY, Lee SH, Kim JM, Park MS, Bae JW, Hahn Y, et al. 2011. Metagenomic analysis of kimchi, a Traditional Korean fermented food. Appl. Environ. Microbiol. 77: 2264-2274. https://doi.org/10.1128/AEM.02157-10
  17. Kim E, Cho EJ, Yang SM, Kim MJ, Kim HY. 2021. Novel approaches for the identification of microbial communities in kimchi: MALDI-TOF MS analysis and high-throughput sequencing. Food Microbiol. 94: 103641. https://doi.org/10.1016/j.fm.2020.103641
  18. Park EJ, Chun J, Cha CJ, Park WS, Jeon CO, Bae JW. 2012. Bacterial community analysis during fermentation of ten representative kinds of kimchi with barcoded pyrosequencing. Food Microbiol. 30: 197-204. https://doi.org/10.1016/j.fm.2011.10.011
  19. Roh SW, Kim KH, Nam YD, Chang HW, Park EJ, Bae JW. 2010. Investigation of archaeal and bacterial diversity in fermented seafood using barcoded pyrosequencing. ISME J. 4: 1-16. https://doi.org/10.1038/ismej.2009.83
  20. 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. https://doi.org/10.1016/j.ijfoodmicro.2012.01.013
  21. Ryu JA, Kim E, Kim MJ, Lee S, Yoon SR, Ryu JG, et al. 2021. Physicochemical characteristics and microbial communities in Gochujang, a Traditional Korean fermented hot pepper paste. Front. Microbiol. 11: 620478. https://doi.org/10.3389/fmicb.2020.620478
  22. Lee HW, Yoon SR, Kim SJ, Lee HM, Lee JY, Lee JH, et al. 2017. Identification of microbial communities, with a focus on foodborne pathogens, during kimchi manufacturing process using culture-independent and -dependent analyses. Lwt 81: 153-159. https://doi.org/10.1016/j.lwt.2017.04.001
  23. Nam YD, Chang HW, Kim KH, Roh SW, Bae JW. 2009. Metatranscriptome analysis of lactic acid bacteria during kimchi fermentation with genome-probing microarrays. Int. J. Food Microbiol. 130: 140-146. https://doi.org/10.1016/j.ijfoodmicro.2009.01.007
  24. National Institute of Food and Drug Safety Evaluation (Fed. Regist. 11-1471057-000036-17). Available online: https://www.nifds.go.kr/brd/m_18/view.do?seq=12536.
  25. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, et al. 2012. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 6: 610-618. https://doi.org/10.1038/ismej.2011.139
  26. Hong SP, Lee EJ, Kim YH, Ahn DU. 2016. Effect of fermentation temperature on the volatile composition of Kimchi. J. Food Sci. 81: C2623-C2629. https://doi.org/10.1111/1750-3841.13517
  27. Lee JJ, Choi YJ, Lee MJ, Park SJ, Oh SJ, Yun YR, et al. 2020. Effects of combining two lactic acid bacteria as a starter culture on model kimchi fermentation. Food Res. Int. 136: 109591. https://doi.org/10.1016/j.foodres.2020.109591
  28. Conner DE, Kotrola JS. 1995. Growth and survival of Escherichia coli O157:H7 under acidic conditions. Appl. Environ. Microbiol. 61: 382-385. https://doi.org/10.1128/aem.61.1.382-385.1995
  29. Sainz T, Wacher C, Espinoza J, Centurion D, Navarro A, Molina J, et al. 2001. Survival and characterization of Escherichia coli strains in a typical Mexican acid fermented food. Int. J. Food Microbiol. 71: 169-176. https://doi.org/10.1016/S0168-1605(01)00617-1
  30. Simango C. 1995. Effective acidification of traditional fermented foods. J. Trop. Med. Hyg. 98: 465-468.
  31. Choi Y, Lee S, Kim HJ, Lee H, Kim S, Lee J, et al. 2018. Pathogenic Escherichia coli and Salmonella can survive in Kimchi during fermentation. J. Food Prot. 81: 942-946. https://doi.org/10.4315/0362-028X.JFP-17-459
  32. Philip P, Kern D, Goldmanns J, Seiler F, Schulte A, Habicher T, et al. 2018. Parallel substrate supply and pH stabilization for optimal screening of E. coli with the membrane-based fed-batch shake flask. Microb. Cell Fact. 17: 69. https://doi.org/10.1186/s12934-018-0917-8
  33. Jeong SE, Chun BH, Kim KH, Park D, Roh SW, Lee SH, et al. 2018. Genomic and metatranscriptomic analyses of Weissella koreensis reveal its metabolic and fermentative features during kimchi fermentation. Food Microbiol. 76: 1-10. https://doi.org/10.1016/j.fm.2018.04.003
  34. Kim E, Yang SM, Kim HY. 2021. Analysis of cultivable microbial community during Kimchi fermentation using MALDI-TOF MS. Foods 10: 1068. https://doi.org/10.3390/foods10051068