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Effect of biogenic amine forming and degrading bacteria on quality characteristics of Kimchi

바이오제닉 아민 생성균과 분해균이 김치의 품질 특성에 미치는 영향

  • Lim, Eun-Seo (Department of Food Science & Nutrition, Tongmyong University)
  • Received : 2020.09.23
  • Accepted : 2020.10.29
  • Published : 2020.12.31

Abstract

The purpose of this study was to investigate the quality characteristics of kimchi prepared with a single starter culture of biogenic amines (BA)-forming lactic acid bacteria (LAB) or a combined starter cultures composed of BA-forming and BA-degrading LAB. As the fermentation proceeded, the lactic acid bacterial count, titratable acidity, and BA content in kimchi prepared with myeolchi-aekjeot were slightly higher than those of kimchi prepared with saeu-jeot. The amount and type of BA produced by LAB were mostly strain dependent rather than species specific. Among all of the isolated LAB strains, the highest levels of cadaverine, histamine, putrescine and tyramine were produced by Leuconostoc mesenteroides MBK32, Lactobacillus brevis MBK34, Lactobacillus curvatus MBK31 and Enterococcus faecalis SBK31, respectively. BA-forming and BA-degrading starter cultures played an important role in the growth rate and organic acid-producing ability of LAB in kimchi. Interestingly, BA contents in kimchi increased by adding single BA-forming LAB starter were effectively lowered by the mixed cultures with BA-degrading LAB.

본 연구의 목적은 발효 기간 동안 멸치 액젓과 새우젓으로 담근 배추 김치로부터 분리 동정된 바이오제닉 아민(biogenic amines, BA) 생성 유산균 단독 스타터 혹은 BA 분해 유산균과의 혼합 스타터로 제조한 김치의 품질 특성을 조사하고자 하였다. 발효가 진행될수록 새우젓 보다 멸치 액젓을 첨가하여 제조한 김치에서 유산균수, 산도 및 BA 함량이 높게 나타났다. 유산균이 생산하는 BA의 종류 및 생성량은 균종 보다는 균주에 의존적이었다. 분리 균주 중에서 가장 많은 양의 카다베린, 히스타민, 푸트레신 및 티라민은 각각 Leuconostoc mesenteroides MBK32, Lactobacillus brevis MBK34, Lactobacillus curvatus MBK31 및 Enterococcus faecalis SBK31로부터 생산되었다. BA 생성능과 분해능이 있는 스타터는 김치 내 유산균의 증식 속도와 산 생성능에 중요한 역할을 하였다. BA 생성균 단독 스타터에 의해 증가된 김치의 BA 함량은 BA 분해균과의 혼합 스타터에 의해 효과적으로 감소되었다.

Keywords

References

  1. Food and Agricultural Organisation (FAO) (1998) Fermented fruits and vegetables: A global perspective. In Mike Battock et al. (eds.), FAO of United Nations, Rome, Italy
  2. Steinkraus KH (2002) Fermentations in World Food Processing. Comp Rev Food Sci Food Safety 1: 23-32 https://doi.org/10.1111/j.1541-4337.2002.tb00004.x
  3. Cooke RD, Twiddy DR, Reilly PJA (1987) Lactic acid fermentation as a low cost means of food preservation in tropical countries. FEMS Microbiol Rev 46: 369-379 https://doi.org/10.1111/j.1574-6968.1987.tb02473.x
  4. Altay F, Karbancyoglu-Gculer F, Daskaya-Dikmen C, Heperkan D (2013) A review on traditional Turkish fermented non-alcoholic beverages: microbiota, fermentation process and quality characteristics. Int J Food Microbiol 167: 44-56 https://doi.org/10.1016/j.ijfoodmicro.2013.06.016
  5. Tamang JP, Kailasapathy K (2010) Fermented foods and beverages of the world, pp. 149-160. CRC press. Taylor & Francis Group. New York, USA
  6. Nout MJR (1994) Fermented foods and food safety. Food Res Int 27: 291-298 https://doi.org/10.1016/0963-9969(94)90097-3
  7. Halasz A, Barath A, Simon-Sarkadi L, Holzapfel W (1994) Biogenic amines and their production by microorganisms in food. Trends Food Sci Technol 5: 42-49 https://doi.org/10.1016/0924-2244(94)90070-1
  8. Stratton JE, Hutkins RW, Taylor SL (1991) Biogenic amines in cheese and other fermented foods: A review. J. Food Prot 54: 460-470 https://doi.org/10.4315/0362-028x-54.6.460
  9. Mah JH, Park YK, Jin YH, Lee JH, Hwang HJ (2019) Bacterial production and control of biogenic amines in Asian fermented soybean foods. Foods 8: 85-99 https://doi.org/10.3390/foods8020085
  10. Spano G, Russo P, Lonvaud-Funel A, Lucas P, Alexandre H, Grandvalet C, Coton E, Coton M, Barnavon L, Bach B, Rattray F, Bunte A, Magni C, Ladero V, Alvarez M, Fernandez M, Lopez P, De Palencia PF, Corbi A, Trip H, Lolkema JS (2010) Biogenic amines in fermented foods. Eur J Clin Anutr 64: S95-S100 https://doi.org/10.1038/ejcn.2010.218
  11. Sanlier N, Gokcen BB, Sezgin AC (2017) Health benefits of fermented foods. Crit Rev Food Sci Nutr 59: 506-527 https://doi.org/10.1080/10408398.2017.1383355
  12. Park YK, Lee JH, Mah JH (2019) Occurrence and reduction of biogenic amines in kimchi and Korean fermented seafood products. Foods 8: 547-561 https://doi.org/10.3390/foods8110547
  13. Kalae P, Spieka J, Koizek M, Steidlova S, Pelikanova T (1999) Concentrations of seven biogenic amines in sauerkraut. Food Chem 67: 275-280 https://doi.org/10.1016/S0308-8146(99)00131-4
  14. Barbieri F, Montanari C, Gardini F, Tabanelli G (2019) Biogenic amine production by lactic acid bacteria: A review. Foods 8: 17-43 https://doi.org/10.3390/foods8010017
  15. Niu T, Li X, Guo Y, Ma Y (2019) Identification of a lactic acid bacteria to degrade biogenic amines in Chinese rice wine and its enzymatic mechanisms. Foods 8: 312-325 https://doi.org/10.3390/foods8080312
  16. Lim ES (2020) Evaluation of microbial contamination levels and biogenic amines content in over-ripened kimchi. Korean Soc Food Pres 27: 635-650 https://doi.org/10.11002/kjfp.2020.27.5.635
  17. Toy N, Ozogul F, Ozogul Y (2015) The influence of the cell free solution of lactic acid bacteria on tyramine production by food borne-pathogens in tyrosine decarboxylase broth. Food Chem 173: 45-53 https://doi.org/10.1016/j.foodchem.2014.10.001
  18. Lim ES (2016) Effect of the mixed culture of heterfermentative lactic acid bacteria and acid-tolerant yeast on the shelf-life of sourdough. Korean J Microbiol 52: 471-481 https://doi.org/10.7845/kjm.2016.6069
  19. Han GH, Cho TY, Yoo MS, Kim CS, Kim JM, Kim HA, Kim MO, Kim SC, Lee SA, Ko YS (2007) Biogenic amines formation and content in fermented soybean paste (Cheonggukjang). Korean J Food Sci Technol 39: 541-545
  20. Lee YK, Lee MY, Kim SD (2004) Effect of monosodium glutamate and temperateure change on the content of free amino acids in kimchi. J Korean Soc Food Sci Nutr 33: 399-404 https://doi.org/10.3746/JKFN.2004.33.2.399
  21. Lee GI, Lee HM, Lee CH (2012) Food safety issues in industrialization of traditional Korean foods. Food Control 24: 1-5 https://doi.org/10.1016/j.foodcont.2011.09.014
  22. Park JM, Shin JH, Lee DW, Song JC, Suh HJ, Chang UJ, Kim JM (2010) Identification of the lactic acid bacteria in kimchi according to initial and over-ripened fermentation using PCR and 16S rRNA gene sequence analysis. Food Sci Biotechnol 19: 541-546 https://doi.org/10.1007/s10068-010-0075-1
  23. Mheen TI, Kwon TW (1984) Effect of temperature and salt concentration on kimchi fermentation. Korean J Food Sci Technol 16: 443-450
  24. Jung JY, Lee SH, Lee HJ, Seo HY, Park WS, Jeon CO (2012) Effects of Leuconostoc mesenteroides starter cultures on microbial communities and metabolites during kimchi fermentation. Int J Food Microbiol 153: 378-387 https://doi.org/10.1016/j.ijfoodmicro.2011.11.030
  25. Hong SW, Choi YJ, Lee HW, Yang JH, Lee MA (2016) Microbial community structure of Korean cabbage kimchi and ingredients with denaturing gradient gel electrophoresis. J Microbiol Biotechnol 26: 1057-1062 https://doi.org/10.4014/jmb.1512.12035
  26. Cheigh HS, Park KY (1994) Biochemical, microbiological, and nutritional aspects of kimchi. Crit Rev Food Sci Nutr 34: 175-203 https://doi.org/10.1080/10408399409527656
  27. Patra JK, Das G, Paramithiotis S, Shin HS (2016) Kimchi and other widely consumed traditional fermented foods of Korea: a review. Front Microbiol 7: 1493-1507
  28. Jung MY, Kim TW, Lee CS, Kim JY, Song HS, Kim YB, Ahn SW, Kim JS, Roh SW, Lee SH (2018) Role of jeotgal, a Korean traditional fermented fish sauce, in microbial dynamics and metabolite profiles during kimchi fermentation. Korean Soc Food Sci Nutr 10: 370
  29. Choi HJ, Lee NK, Paik HD (2015) Health benefits of lactic acid bacteria isolated from kimchi, with respect to immunomodulatory effects. Food Sci Biotechnol 24: 783-789 https://doi.org/10.1007/s10068-015-0102-3
  30. Kwak SH, Cho YM, Noh GM, Om AS (2014) Cancer preventive potential of kimchi lactic acid bacteria (Weissella cibaria, Lactobacillus plantarum). J Cancer Prev 19: 253-258 https://doi.org/10.15430/JCP.2014.19.4.253
  31. Ozogul F, Hamed I (2018) The importance of lactic acid bacteria for the prevention of bacterial growth and their biogenic amines formation: A review. Crit Rev Food Sci Nutr 58: 1660-1670 https://doi.org/10.1080/10408398.2016.1277972
  32. Tsai YH, Kung HF, Lin QL, Hwang JH, Cheng SH, Wei CI, Hwang DF (2005) Occurrence of histamine and histamine-forming bacteria in kimchi products in Taiwan. Food Chem 90: 635-641 https://doi.org/10.1016/j.foodchem.2004.04.024
  33. Kim MJ, Kim KS (2014) Tyramine production among lactic acid bacteria and other species isolated from kimchi. LWT-Food Sci Technol 56: 406-413 https://doi.org/10.1016/j.lwt.2013.11.001
  34. Jeong DW, Lee JH (2015) Antibiotic resistance, hemolysis and biogenic amine production assessments of Leuconostoc and Weissella isolates for kimchi starter development. LWT-Food Sci Technol 64: 1078-1084 https://doi.org/10.1016/j.lwt.2015.07.031
  35. Sgarbi E, Bottari B, Gatti M, Neviani E (2014) Investigation of the ability of dairy nonstarter lactic acid bacteria to grow using cell lysates of other lactic acid bacteria as the exclusive source of nutrients. Int J Dairy Technol 67: 342-347 https://doi.org/10.1111/1471-0307.12132
  36. Connil N, Plissoneau L, Onno B, Pilet MF, Prevost H, Dousset X (2002) Growth of Carnobacterium divergens V41 and production of biogenic amines and divercin V41 in sterile cold-smoked salmon extract at varying temperatures, NaCl levels, and glucose concentrations. J Food Prot 65: 333-338 https://doi.org/10.4315/0362-028X-65.2.333
  37. Lee KW, Shim JM, Yao Z, Kim JA, Kim JH (2018) Properties of kimchi fermented with GABA-producing lactic acid bacteria as a starter. J Microbiol Biotechnol 28: 534-541 https://doi.org/10.4014/jmb.1709.09011
  38. Jung SJ, Kim MJ, Chae SW (2016) Quality and functional characteristics of kimchi made with organically cultivated young Chinese cabbage (olgari-baechu). J Ethn Foods 3: 150-158 https://doi.org/10.1016/j.jef.2016.05.003
  39. You SY, Yang JS, Kim SH, Hwang IM (2017) Changes in the physicochemical quality characteristics of cabbage kimchi with respect to storage conditions. J Food Qual 2017: 1-7
  40. Lee HH, Kim GH (2013) Changes in the levels of γ-aminobutyric acid and free amino acids during kimchi fermentation. Korean J Food Cookery Sci 29: 671-677 https://doi.org/10.9724/kfcs.2013.29.6.671
  41. Oh YE, Kim SD (1997) Changes in enzyme activities of salted Chinese cabbage and kimchi during salting and fermentation. J Korean Soc Food Sci Nutr 26: 404-410
  42. Nam HG, Jang MS, Seo KC, Nam KH, Park HY (2013) Changes in the taste compounds of kimchi with seafood added during its fermentation. J Food Preserv 20: 404-418 https://doi.org/10.11002/kjfp.2013.20.3.404
  43. Joung BC, Min JG (2018) Changes in post-fermentation quality during the distribution process of anchovy (Engraulis japonicus) fish sauce. J Food Prot 81: 969-976 https://doi.org/10.4315/0362-028X.JFP-17-348
  44. Shin SW, Kim YS, Kim YH, Kim HT, Eum KS, Hong SR, Kang HJ, Park KH, Yoon MH (2019) Biogenic-amine contents of Korean commercial salted fishes and cabbage kimchi. Korean J Fish Aquat Sci 52: 13-18 https://doi.org/10.5657/KFAS.2019.0013
  45. Cho TY, Han GH, Bahn KN, Son YW, Jang MR, Lee CH, Kim SH, Kim DB, Kim SB (2006) Evaluation of biogenic amines in Korean commercial fermented foods. Korean J Food Sci Technol 38: 730-737
  46. Mah JH, Kim YJ, No HK, Hwang HJ (2004) Determination of biogenic amines in kimchi, Korean traditional fermented vegetable products. Food Sci Biotechnol 13: 826-829
  47. Kim SH, Kang KH, Lee S, Kim SJ, Kim JG, Chung MJ (2017) Kimchi probiotic bacteria contribute to reduced amounts of N-nitrosodimethylamine in lactic acid bacteria-fortified kimchi. LWT-Food Sci Technol 84: 196-203 https://doi.org/10.1016/j.lwt.2017.05.060
  48. Kalae P, Spieka J, Koizek M, Steidlova S, Pelikanova T (2000) The effects of lactic acid bacteria inoculants on biogenic amines formation in sauerkraut. Food Chem. 70: 355-359 https://doi.org/10.1016/S0308-8146(00)00103-5
  49. Herrero-Fresno A, Martinez N, Sanchez-Llana E, Diaz M (2012) Lactobacillus casei strains isolated from cheese reduce biogenic amine accumulation in an experimental mode. Int J Food Microbiol 157: 297-304 https://doi.org/10.1016/j.ijfoodmicro.2012.06.002
  50. Ladero V, Herrerofresno A, Martinez N, Rio BD, Linares DM, Fernandez M (2014) Genome sequences analysis of the biogenic amine-degrading strain Lactobacillus casei 5b. Genome Announcements 2: e1199-121
  51. Moon GS, Kang CH, Pyun YR, Kim WJ (2004) Isolation, identification, and characterization of a bacteriocin-producing Enterococcus sp. from kimchi and its application to kimchi fermention. J Microbiol Biotechnol 14: 924-931
  52. Kim DS, Cho HW, Kim DH, Oh KH (2013) Functional characterization of Lactobacillus sakei JK-17 isolated from long-term fermented kimchi, Muk Eun Ji. Kor Soc Biotechnol Bioeng 28: 18-23
  53. Casquete R, Benito MJ, Martin A, Ruiz-Moyano S, Hernandez A, Cordoba MG (2011) Effect of autochthonous starter cultures in the production of "salchichon", a traditional Iberian dry-fermented sausage, with different ripening processes. Food Sci Technol 44: 1562-1571
  54. Alvarez MA, Moreno-Arribas MV (2014) The problem of biogenic amines in fermented foods and the use of potential biogenic amine-degrading microorganisms as a solution. Trend Food Sci Technol 39: 146-155 https://doi.org/10.1016/j.tifs.2014.07.007

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