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Formation of Biogenic Amines by Lactobacillus plantarum Isolated from Makgeolli

막걸리에서 분리한 Lactobacillus plantarum의 biogenic amine 생성능

  • Received : 2014.01.09
  • Accepted : 2014.04.16
  • Published : 2014.08.31

Abstract

We examined biogenic amine (BA) production as well as the diversity of bacterial flora in 11 types of commercial makgeolli stored at 4 and $20^{\circ}C$. Moreover, we studied the BA-producing activity of three L. plantarum strains isolated from makgeolli. At $20^{\circ}C$, the BA content was highly increased and the denatured DNA bands were more variable in non-sterilized makgeolli compared to sterilized makgeolli. The major BAs produced in commercial makgeolli were histamine and putrescine. Histamine, tyramine, putrescine, and cadaverine were produced in excess by inoculation of the three L. plantarum isolates to makgeolli stored at $20^{\circ}C$ for 21 days. These results suggest that some L. plantarum strains in makgeolli can produce different types of BAs, depending on the extent of degradation of makgeolli.

Keywords

makgeolli;Lactobacillus plantarum;biogenic amine;storage temperature

References

  1. Chang KJ, Yu TJ. Studies on the components of sokokju, and commercial yakju. Korean J. Food Sci. Technol. 13: 307-313 (1981)
  2. Han EH, Lee TS, Noh BS, Lee DS. Volatile flavor components in mash of takju prepared by using different nuruks. Korean J. Food Sci. Technol. 29: 563-570 (1997)
  3. Jeon BY, Seo HN, Yun A, Lee IH, Park DH. Effect of glasswort (Salicornia herbacea L.) on nuruk-making process and makgeolli quality. Food Sci. Biotechnol. 19: 999-1004 (2010) https://doi.org/10.1007/s10068-010-0140-9
  4. Kim AR, Lee SY, Kim KBWR, Song EJ, Kim JH, Kim MJ, Ji KW, Ahn IS, Ahn DH. Effect of Glycyrrhiza uralensis in shelf-life and quality of takju. Korean J. Food Sci. Technol. 40: 194-200 (2008)
  5. Kim SM, Han AR. Storage properties and biogenic amines production of makgeolli brewed with different proportions of rice and wheat flour. Korean J. Food Sci. Technol. 44: 583-591 (2012) https://doi.org/10.9721/KJFST.2012.44.5.583
  6. Lee SS, Kim KS, Eom AH, Sung CK, Hong IP. Production of Korean traditional rice-wine made from cultures of the single ungal isolates under laboratory conditions. Korean J. Mycol. 30: 61-65 (2002) https://doi.org/10.4489/KJM.2002.30.1.061
  7. Kim JO, Lee BH. Taxonomical studies of yeasts in Korea -On yeasts isolated from takju-. Korean J. Microbiol. 8: 77-84 (1970)
  8. Shin YD, Cho DH. A study on the microflora changes during takju brewing. Korean J. Microbiol. 8: 53-64 (1970)
  9. Yang JY, Lee KH. Shelf-life and microbiological study of sansung takju. Korean J. Food Sci. Technol. 28: 779-785 (1996)
  10. Yu TS, Kim J, Kim HS, Hyun JS, Ha HP, Park MK. Bibliographical study on microorganisms of traditional Korean nuruk (since 1945). J. Korean Soc. Food Sci. Nutr. 27: 789-799 (1998)
  11. Yu TS, Kim HS, Hong J, Ha HP, Kim TY, Yoon IW. Bibliographical study on microorganisms of nuruk (until 1945). J. Korean Soc. Food Sci. Nutr. 25: 170-179 (1996)
  12. Kim TY, Yoon IW. Fermentation characteristics of traditional alcoholic beverages brewed with improved-nuruk. J. East Asian Soc Dietary Life 7: 399-404 (1997)
  13. Kim HS, Hyun JS, Kim J, Ha HP, Yu TS. Characteristics of useful fungi isolated from traditional Korea nuruk. J. Korean Soc. Food Sci. Nutr. 26: 767-774 (1997)
  14. Seo MY, Lee JK, Ahn BH, Cha SK. The changes of microflora during the fermentation of takju and yakju. Korean J. Food Sci. Technol. 37: 61-66 (2005)
  15. Lee TS, Choi JY. Volatile flavor components in mash of takju prepared by using Aspergillus kawachii nuruks. Korean J. Food Sci. Technol. 37: 944-950 (2005)
  16. Jo KY, Ha DM. Isolation and identification of the lactic acid bacteria from nuruk. Agr. Chem. Biotechnol. 38: 95-99 (1995)
  17. Lee JH, Yu TS. Identification and characteristics of lactic acid bacteria isolated from nuruk. Korean J. Biotechnol. Bioeng. 15: 359-365 (2000)
  18. Jin J, Kim SY, Jin Q, Eom HJ, Han NS. Diversity analysis of lactic acid bacteria in takju, Korean Rice Wine. J. Microbiol. Biotechnol. 18: 1678-1682 (2008)
  19. Kim SY, Yoo KS, Kim JE, Kim JS, Jung JY, Jin Q, Eom HJ, Han NS. Diversity analysis of lactic acid bacteria in Korean rice wines by culture-independent method using PCR-denaturing gradient gel electrophoresis. Food Sci. Biotechnol. 19: 749-755 (2010) https://doi.org/10.1007/s10068-010-0105-z
  20. Ancn-Azpilicueta C, Gonzlez-Marco A, Jimnez-Moreno N. Current knowledge about the presence of amines in wine. Crit. Rev. Food Sci. Nutr. 48: 257-275 (2008) https://doi.org/10.1080/10408390701289441
  21. Min JH, Baek SY, Lee JS, Kim HK. Changes of yeasts and bacterial flora during the storage of Korean traditional makgeolli. Korean J. Mycol. 39: 151-153 (2011) https://doi.org/10.4489/KJM.2010.39.2.151
  22. Kim JY, Kim D, Park P, Kang HI, Ryu EK, Kim SM. Effects of storage temperature and time on the biogenic amine content and microflora in Korean turbid rice wine, makgeolli. Food Chem. 128: 87-92 (2011) https://doi.org/10.1016/j.foodchem.2011.02.081
  23. Coton M, Romano A, Spano G, Ziegler K, Vetrana C, Desmarais C, Lonvaud-Funel A, Lucas P, Coton E. Occurrence of biogenic amine-forming lactic acid bacteria in wine and cider. Food Microbiol. 27: 1078-1085 (2010) https://doi.org/10.1016/j.fm.2010.07.012
  24. Jorgensen LV, Huss HH, Dalgaard P. The effect of biogenic amine production by single bacterial cultures and metabiosis on cold-smoked salmon. J. Appl. Microbiol. 89: 920-934 (2000) https://doi.org/10.1046/j.1365-2672.2000.01196.x
  25. Lonvaud-Funel A. Biogenic amines in wines: role of lactic acid bacteria. FEMS Microbiol. Lett. 199: 9-13 (2001) https://doi.org/10.1111/j.1574-6968.2001.tb10643.x
  26. Fernndez M, Ziga M. Amino Acid Catabolic Pathways of Lactic Acid Bacteria. Crit. Rev. Microbiol. 32: 155-183 (2006) https://doi.org/10.1080/10408410600880643
  27. Herbert P, Cabrita MJ, Ratola N, Laureano O, Alves A. Relationship between biogenic amines and free amino acid contents of wines and musts from Alentejo (Portugal). J. Environ. Sci. Health B. 41: 1171-1186 (2006) https://doi.org/10.1080/03601230600856967
  28. Ten Brink B, Damink C, Joosten HM, Huis in't Veld JH. Occurrence and formation of biologically active amines in foods. Int. J. Food Microbiol. 11: 73-84 (1990) https://doi.org/10.1016/0168-1605(90)90040-C
  29. Shalaby AR. Significance of biogenic amines to food safety and human health. Food Res. Int. 29: 675-690 (1996) https://doi.org/10.1016/S0963-9969(96)00066-X
  30. Jung MJ, Nam YD, Roh SW, Bae JW. Unexpected convergence of fungal and bacterial communities during fermentation of traditional Korean alcoholic beverages inoculated with various natural starters. Food Microbiol. 30: 112-123 (2012) https://doi.org/10.1016/j.fm.2011.09.008
  31. Han GH, Cho TY, Yoo MS, Kim CS, Kim JM, Kim HA, Kim MO, Kim SC, Lee SA, Ko YS, Kim SH, Kim DB. Biogenic amines formation and content in fermented soybean paste (cheonggukjang). Korean J. Food Sci. Technol. 39: 541-545 (2007)
  32. Silla Santos MH. Biogenic amines: their importance in foods. Int. J. Food Microbiol. 29: 213-231 (1996) https://doi.org/10.1016/0168-1605(95)00032-1
  33. Smit AY, Du Toit WJ, Du Toit M. Biogenic amines in wine: understanding the headache. S. Afr. J. Enol. Vitic. 29: 109-127 (2008)
  34. Kwon SJ, Ahn TY, Sohn JH. Analysis of microbial diversity in makgeolli fermentation using PCR-DGGE. J. Life Sci. 22: 232-238 (2012) https://doi.org/10.5352/JLS.2012.22.2.232
  35. Min JH, Kim YH, Kim JH, Choi SY, Lee JS, Kim HK. Comparison of microbial diversity of Korean commercial makgeolli showing high ${\beta}$-glucan content and high Antihypertensive activity, respectively. Mycobiol. 40: 138-141 (2012) https://doi.org/10.5941/MYCO.2012.40.2.138
  36. Landete JM, Ferrer S, Polo L, Pardo I. Biogenic amine in wines from three spanish regions. J. Agr. Food Chem. 53: 1119-1124 (2005) https://doi.org/10.1021/jf049340k
  37. Fadda S, Vignolo G, Oliver G. Tyramine degradation and tyramine/histamine production by lactic acid bacteria and Kocuria strains. Biotechnol. Lett. 23: 2015-2019 (2001) https://doi.org/10.1023/A:1013783030276
  38. Tang T, Shi T, Qian K, Li P, Li J, Cao Y. Determination of biogenic amines in beer with pre-column derivatization by high performance liquid chromatography. J. Chromatogr. B 877: 507-512 (2009) https://doi.org/10.1016/j.jchromb.2008.12.064
  39. Kirby KS. A new method for the isolation of deoxyribonucleic acids: evidence on the nature of bonds between deoxyribonucleic acid and protein. Biochem. J. 66: 495-504 (1957)
  40. Marcobal A, Martin-Alvarez PJ, Polo MC, Munoz R, Moreno-Arribas MV. Formation of biogenic amines throughout the industrial manufacture of red wine. J. Food Prot. 69: 397-404 (2006)
  41. Xueliang R, Xiaoyang Z, Warndorff M, Bucheli P, Qingyao S. DNA extraction and fingerprinting of commercial rice cereal products. Food Res. Int. 39: 433-439 (2006) https://doi.org/10.1016/j.foodres.2005.09.006
  42. Ros-Chumillas M, Egea-Cortines M, Lopez-Gomez A, Weiss J. Evaluation of a rapid DNA extraction method to detect yeast cells by PCR in orange juice. Food Control 18: 33-39 (2007) https://doi.org/10.1016/j.foodcont.2005.08.004
  43. Soufleros E, Barrios, ML, Bertrand A. Correlation between the content of biogenic amines and other wine compounds. Am. J. Enol. Vitic. 49: 266-278 (1998)
  44. Forsythe WI, Redmond A. Two controlled trials of tyramine in children with migraine. Dev. Med. Child Neurol. 16: 794-799 (1974)
  45. Straub BW, Kicherer M, Schilcher SM, Hammes WP. The formation of biogenic amines by fermentation organisms. Z. Lebensm. Unters. Forsch. 201: 79-82 (1995) https://doi.org/10.1007/BF01193205
  46. Kek M, KalaP. Biogenic amines in foods and their roles in human nutrition. Czech J. Food Sci. 16: 151-159 (1998)
  47. Maijala R, Eerola S. Contaminant lactic acid bacteria of dry sausages produce histamine and tyramine. Meat Sci. 35: 387-395 (1993) https://doi.org/10.1016/0309-1740(93)90043-H
  48. Halsz A, Barth, Simon-Sarkadi L, Holzapfel W. Biogenic amines and their production by microorganisms in food. Trends Food Sci. Tech. 5: 42-49 (1994) https://doi.org/10.1016/0924-2244(94)90070-1
  49. Ogawa H, Tsuji H, Seto A, Hara S, Totani Y. Synergistic effect of spermine on antioxidation of polyunsaturated oil. J. Japan Oil Chem. Soc. 45: 1327-1332 (1996) https://doi.org/10.5650/jos1996.45.1327
  50. Chang HW, Kim KH, Nam YD, Roh SW, Kim MS, Jeon CO, Oh HM, Bae JW. Analysis of yeast and archaeal population dynamics in kimchi using denaturing gradient gel electrophoresis. Int. J. Food Microbiol. 126: 159-166 (2008) https://doi.org/10.1016/j.ijfoodmicro.2008.05.013
  51. Kim TW, Lee JH, Kim SE, Park MH, Chang HC, Kim HY. Analysis of microbial communities in doenjang, a Korean fermented soybean paste, using nested PCR-denaturing gradient gel electrophoresis. Int. J. Food Microbiol. 131: 265-271 (2009) https://doi.org/10.1016/j.ijfoodmicro.2009.03.001
  52. Martin-Alvarez PJ, Marcobal A, Polo C, Moreno-Arribas MV. Influence of technological practices on biogenic amine contents in red wines. Eur. Food Res. Technol. 222: 420-424 (2006) https://doi.org/10.1007/s00217-005-0142-7
  53. Maijala RL, Eerola SH, Aho MA, Hirn JA. The effect of GDL-induced pH decrease on the formation of biogenic amines in meat. J. Food Protect. 56: 125-129 (1993)
  54. Bardcz S. Polyamines in food and their consequences for food quality and human health. Trends Food Sci. Tech. 6: 341-346 (1995) https://doi.org/10.1016/S0924-2244(00)89169-4
  55. Karovicova J, Kohajdova Z. Biogenic Amines in Food. Chem. Pap. 59: 70-79 (2005)

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Acknowledgement

Grant : 한식 세계화 및 전통식품 산업화 기술 개발

Supported by : 농촌진흥청