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References

  1. Bover-Cid S, Holzapfel WH. 1999. Improved screening procedure for biogenic amine production by lactic acid bacteria. Int. J. Food Microbiol. 53: 33-41.
    CrossRef
  2. Burdychova R, Komprda T. 2007. Biogenic amine-forming microbial communities in cheese. FEMS Microbiol. Lett. 276:149-155.
    Pubmed CrossRef
  3. Calzad a J, d el O lmo A, P icon A , Gaya P , Nunez M. 2 013. Reducing biogenic-amine-producing bacteria, decarboxylase activity, and biogenic amines in raw milk cheese by highpressure treatments. Appl. Environ. Microbiol. 79: 1277-1283.
    Pubmed PMC CrossRef
  4. Choi JY, Hong SW, Chung KS. 2012. Selection of biogenic amine-reducing microorganisms from a traditional Koreanstyle fermented food, cheonggukjang. Korean J. Food Sci. Technol. 44: 196-201.
    CrossRef
  5. Coton E, Coton M. 2005. Multiplex PCR for colony direct detection of gram-positive histamine- and tyramine-producing bacteria. J. Microb. Methods 63: 296-304.
    Pubmed CrossRef
  6. Coton M, Coton E, Lucas P, Lonvaud A. 2004. Identification of the gene encoding a putative tyrosine decarboxylase of Carnobacterium divergens 508. Development of molecular tools for the detection of tyramine-producing bacteria. Food Microbiol. 21: 125-130.
    CrossRef
  7. Garcia-Ruiz A, Gonzalez-Rompinelli EM, Bartolome B, Moreno-Arribas MV. 2011. Potential of wine-associated lactic acid bacteria to degrade biogenic amines. Int. J. Food Microbiol. 148: 115-120.
    Pubmed CrossRef
  8. Gardini F, Zaccarelli A, Belletti N, Faustini F, Cavazza A, Martuscelli M, et al. 2005. Factors influencing biogenic amine production by a strain of Oenococcus oeni in a mod el system. Food Control 16: 609-616.
    CrossRef
  9. Haak-Frendscho M, Darvas Z, Hegyesi H, Karpati S, Hoffman RL, Laszlo V, et al. 2000. Histidine decarboxylase expression in human melanoma. J. Invest. Dermatol. 115: 345352.
  10. Hagel JM, Facchini PJ. 2005. Elevated tyrosine decarboxylase and tyramine hydroxycinnamoyltransferase levels increase wound-induced tyramine-derived hydroxycinnamic acid amide accumulation in transgenic tobacco leaves. Planta 221:904-914.
    Pubmed CrossRef
  11. Hemarajata P, Gao C, Pflughoeft KJ, Thomas CM, Saulnier DM, Spinler JK, Versalovic J. 2013. Lactobacillus reuterispecific immunoregulatory gene rsiR modulates histamine production and immunomodulation by Lactobacillus reuteri. J. Bacteriol. 195: 5567-5576.
    Pubmed PMC CrossRef
  12. Hwang DF, Chang SH, Shiua CY, Chai T. 1997. Highperformance liquid chromatographic determination of biogenic amines in fish implicated in food poisoning. J. Chromatogr. Biomed. 693: 23-29.
    CrossRef
  13. Kim YS, Cho SH, Jeong DY, Uhm TB. 2012. Isolation of biogenic amines-degrading strains of Bacillus subtilis and Bacillus amyloliquefaciens from traditionally fermented soybean products. Korean J. Microbiol. 48: 220-224.
    CrossRef
  14. Largeron M, Neudorffer A, Fleury MB. 2003. Oxidation of unactivated primary aliphatic amines catalyzed by an electrogenerated 3,4-azaquinone species: a small-molecule mimic of amine oxidases. Angew. Chem. 42: 1026-1029.
    Pubmed CrossRef
  15. Latorre-Moratalla ML, Bover-Cid S, Aymerich T, Marcos B, Vidal-Carou MC, Garriga M. 2007. Aminogenesis control in fermented sausages manufactured with pressurized meat batter and starter culture. Meat Sci. 75: 460-469.
    Pubmed CrossRef
  16. Lee JI, Kim YW. 2013. Characterization of amine oxidases from Arthrobacter aurescens and application for determination of biogenic amines. World J. Microbiol. Biotechnol. 29: 673-682.
    Pubmed CrossRef
  17. Maintz L, Novak N. 2007. Histamine and histamine intolerance. Am. J. Clin. Nutr. 85: 1185-1196.
    Pubmed
  18. Masini E, Fabbroni V, Giannini L, Vannacci A, Messerini L, Perna F, et al. 2005. Histamine and histidine decarboxylase up-regulation in colorectal cancer: correlation with tumor stage. Inflamm. Res. 54(Suppl 1): S80-S81.
    Pubmed CrossRef
  19. Mbarki R, Sadok S, Barkallah I. 2008. Influence of gamma irradiation on microbiological, biochemical, and textural properties of bonito (sarda sarda) during chilled storage. Food Sci. Technol. Int. 14: 367-373.
    CrossRef
  20. Naila A, Flint S, Fletcher G, Bremer P, and Meerdink G. 2010. Control of biogenic amines in food - existing and emerging approaches. J. Food Sci. 75: R139-R150.
    Pubmed PMC CrossRef
  21. Nieto-Arribas P, Poveda JM, Sesena S, Palop L, Cabezas L. 2009. Technological characterization of Lactobacillus isolates from traditional Manchego cheese for potential use as adjunct starter cultures. Food Control 20: 1092-1098.
    CrossRef
  22. Ozd estan O, U ren A. 2 009. A m ethod for benzoyl c hloride derivatization of biogenic amines for high performance liquid chromatography. Talanta 78: 1321-1326.
    Pubmed CrossRef
  23. Rodriguez-Jerez JJ, Mora-Ventura MT, Lopez-Sabater EI, Hernandez-Herrero M. 1994. Histidine, lysine and ornithine decarboxylase bacteria in Spanish salted semipreserved anchovies. J. Food Protect. 57: 784-787.
  24. Saaid M, Saad B, Hashim NH, Ali ASM, and Saleh MI. 2009. Determination of biogenic amines in selected Malaysian food. Food Chem. 113: 1356-1362.
    CrossRef
  25. Santos MHS. 1996. Biogenic amines: their importance in foods. Int. J. Food Microbiol. 29: 213-231.
    CrossRef
  26. Shalaby AR. 1996. Significance of biogenic amines to food safety and human health. Food Res. Int. 29: 675-690.
    CrossRef
  27. Spano G, Russo P, Lonvaud-Funel A, Lucas P, Alexandre H, Grandvalet C, et al. 2010. Biogenic amines in fermented foods. Eur. J. Clin. Nutr. 64 (Suppl 3): S95-S100.
    Pubmed CrossRef
  28. Thomas CM, Hong T, van Pijkeren JP, Hemarajata P, Trinh DV, Hu W, et al. 2012. Histamine derived from probiotic Lactobacillus reuteri suppresses TNF via modulation of PKA and ERK signaling. PloS One 7: e31951.
    Pubmed PMC CrossRef
  29. Zaman MZ, Abu Bakar F, Selamat J, Bakar J. 2010. Occurrence of biogenic amines and amines degrading bacteria in fish sauce. Czech. J. Food Sci. 28: 440-449.

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Article

Research article

J. Microbiol. Biotechnol. 2015; 25(9): 1519-1527

Published online September 28, 2015 https://doi.org/10.4014/jmb.1506.06006

Copyright © The Korean Society for Microbiology and Biotechnology.

Biogenic Amine Degradation by Bacillus Species Isolated from Traditional Fermented Soybean Food and Detection of Decarboxylase-Related Genes

Jeong Seon Eom 1, Bo Young Seo 1 and Hye Sun Choi 1*

Department of Agro-Food Resources, National Academy of Agricultural Science, Jeollabuk-do 565-851, Republic of Korea

Received: June 4, 2015; Accepted: July 3, 2015

Abstract

Biogenic amines in some food products present considerable toxicological risks as potential
human carcinogens when consumed in excess concentrations. In this study, we investigated
the degradation of the biogenic amines histamine and tyramine and the presence of genes
encoding histidine and tyrosine decarboxylases and amine oxidase in Bacillus species isolated
from fermented soybean food. No expression of histidine and tyrosine decarboxylase genes
(hdc and tydc) were detected in the Bacillus species isolated (B. subtilis HJ0-6, B. subtilis D'J53-4,
and B. idriensis RD13-10), although substantial levels of amine oxidase gene (yobN) expression
were observed. We also found that the three selected strains, as non-biogenic amineproducing
bacteria, were significantly able to degrade the biogenic amines histamine and
tyramine. These results indicated that the selected Bacillus species could be used as a starter
culture for the control of biogenic amine accumulation and degradation in food. Our study
findings also provided the basis for the development of potential biological control agents
against these biogenic amines for use in the food preservation and food safety sectors.

Keywords: Bacillus spp., Biogenic amines, Degradation, Fermented soybean pastes, Histamine, Tyramine

References

  1. Bover-Cid S, Holzapfel WH. 1999. Improved screening procedure for biogenic amine production by lactic acid bacteria. Int. J. Food Microbiol. 53: 33-41.
    CrossRef
  2. Burdychova R, Komprda T. 2007. Biogenic amine-forming microbial communities in cheese. FEMS Microbiol. Lett. 276:149-155.
    Pubmed CrossRef
  3. Calzad a J, d el O lmo A, P icon A , Gaya P , Nunez M. 2 013. Reducing biogenic-amine-producing bacteria, decarboxylase activity, and biogenic amines in raw milk cheese by highpressure treatments. Appl. Environ. Microbiol. 79: 1277-1283.
    Pubmed KoreaMed CrossRef
  4. Choi JY, Hong SW, Chung KS. 2012. Selection of biogenic amine-reducing microorganisms from a traditional Koreanstyle fermented food, cheonggukjang. Korean J. Food Sci. Technol. 44: 196-201.
    CrossRef
  5. Coton E, Coton M. 2005. Multiplex PCR for colony direct detection of gram-positive histamine- and tyramine-producing bacteria. J. Microb. Methods 63: 296-304.
    Pubmed CrossRef
  6. Coton M, Coton E, Lucas P, Lonvaud A. 2004. Identification of the gene encoding a putative tyrosine decarboxylase of Carnobacterium divergens 508. Development of molecular tools for the detection of tyramine-producing bacteria. Food Microbiol. 21: 125-130.
    CrossRef
  7. Garcia-Ruiz A, Gonzalez-Rompinelli EM, Bartolome B, Moreno-Arribas MV. 2011. Potential of wine-associated lactic acid bacteria to degrade biogenic amines. Int. J. Food Microbiol. 148: 115-120.
    Pubmed CrossRef
  8. Gardini F, Zaccarelli A, Belletti N, Faustini F, Cavazza A, Martuscelli M, et al. 2005. Factors influencing biogenic amine production by a strain of Oenococcus oeni in a mod el system. Food Control 16: 609-616.
    CrossRef
  9. Haak-Frendscho M, Darvas Z, Hegyesi H, Karpati S, Hoffman RL, Laszlo V, et al. 2000. Histidine decarboxylase expression in human melanoma. J. Invest. Dermatol. 115: 345352.
  10. Hagel JM, Facchini PJ. 2005. Elevated tyrosine decarboxylase and tyramine hydroxycinnamoyltransferase levels increase wound-induced tyramine-derived hydroxycinnamic acid amide accumulation in transgenic tobacco leaves. Planta 221:904-914.
    Pubmed CrossRef
  11. Hemarajata P, Gao C, Pflughoeft KJ, Thomas CM, Saulnier DM, Spinler JK, Versalovic J. 2013. Lactobacillus reuterispecific immunoregulatory gene rsiR modulates histamine production and immunomodulation by Lactobacillus reuteri. J. Bacteriol. 195: 5567-5576.
    Pubmed KoreaMed CrossRef
  12. Hwang DF, Chang SH, Shiua CY, Chai T. 1997. Highperformance liquid chromatographic determination of biogenic amines in fish implicated in food poisoning. J. Chromatogr. Biomed. 693: 23-29.
    CrossRef
  13. Kim YS, Cho SH, Jeong DY, Uhm TB. 2012. Isolation of biogenic amines-degrading strains of Bacillus subtilis and Bacillus amyloliquefaciens from traditionally fermented soybean products. Korean J. Microbiol. 48: 220-224.
    CrossRef
  14. Largeron M, Neudorffer A, Fleury MB. 2003. Oxidation of unactivated primary aliphatic amines catalyzed by an electrogenerated 3,4-azaquinone species: a small-molecule mimic of amine oxidases. Angew. Chem. 42: 1026-1029.
    Pubmed CrossRef
  15. Latorre-Moratalla ML, Bover-Cid S, Aymerich T, Marcos B, Vidal-Carou MC, Garriga M. 2007. Aminogenesis control in fermented sausages manufactured with pressurized meat batter and starter culture. Meat Sci. 75: 460-469.
    Pubmed CrossRef
  16. Lee JI, Kim YW. 2013. Characterization of amine oxidases from Arthrobacter aurescens and application for determination of biogenic amines. World J. Microbiol. Biotechnol. 29: 673-682.
    Pubmed CrossRef
  17. Maintz L, Novak N. 2007. Histamine and histamine intolerance. Am. J. Clin. Nutr. 85: 1185-1196.
    Pubmed
  18. Masini E, Fabbroni V, Giannini L, Vannacci A, Messerini L, Perna F, et al. 2005. Histamine and histidine decarboxylase up-regulation in colorectal cancer: correlation with tumor stage. Inflamm. Res. 54(Suppl 1): S80-S81.
    Pubmed CrossRef
  19. Mbarki R, Sadok S, Barkallah I. 2008. Influence of gamma irradiation on microbiological, biochemical, and textural properties of bonito (sarda sarda) during chilled storage. Food Sci. Technol. Int. 14: 367-373.
    CrossRef
  20. Naila A, Flint S, Fletcher G, Bremer P, and Meerdink G. 2010. Control of biogenic amines in food - existing and emerging approaches. J. Food Sci. 75: R139-R150.
    Pubmed KoreaMed CrossRef
  21. Nieto-Arribas P, Poveda JM, Sesena S, Palop L, Cabezas L. 2009. Technological characterization of Lactobacillus isolates from traditional Manchego cheese for potential use as adjunct starter cultures. Food Control 20: 1092-1098.
    CrossRef
  22. Ozd estan O, U ren A. 2 009. A m ethod for benzoyl c hloride derivatization of biogenic amines for high performance liquid chromatography. Talanta 78: 1321-1326.
    Pubmed CrossRef
  23. Rodriguez-Jerez JJ, Mora-Ventura MT, Lopez-Sabater EI, Hernandez-Herrero M. 1994. Histidine, lysine and ornithine decarboxylase bacteria in Spanish salted semipreserved anchovies. J. Food Protect. 57: 784-787.
  24. Saaid M, Saad B, Hashim NH, Ali ASM, and Saleh MI. 2009. Determination of biogenic amines in selected Malaysian food. Food Chem. 113: 1356-1362.
    CrossRef
  25. Santos MHS. 1996. Biogenic amines: their importance in foods. Int. J. Food Microbiol. 29: 213-231.
    CrossRef
  26. Shalaby AR. 1996. Significance of biogenic amines to food safety and human health. Food Res. Int. 29: 675-690.
    CrossRef
  27. Spano G, Russo P, Lonvaud-Funel A, Lucas P, Alexandre H, Grandvalet C, et al. 2010. Biogenic amines in fermented foods. Eur. J. Clin. Nutr. 64 (Suppl 3): S95-S100.
    Pubmed CrossRef
  28. Thomas CM, Hong T, van Pijkeren JP, Hemarajata P, Trinh DV, Hu W, et al. 2012. Histamine derived from probiotic Lactobacillus reuteri suppresses TNF via modulation of PKA and ERK signaling. PloS One 7: e31951.
    Pubmed KoreaMed CrossRef
  29. Zaman MZ, Abu Bakar F, Selamat J, Bakar J. 2010. Occurrence of biogenic amines and amines degrading bacteria in fish sauce. Czech. J. Food Sci. 28: 440-449.