Abstract
This study was carried out to find a method to control tyrosine decarboxylase activity (TDC) of a strain of Enterococcus faecium capable of producing high levels of tyramine. To select a TDC inhibitor, enzyme assay was first performed using purified TDC enzyme and 0.1% of TDC inhibiting chemicals. When 0.23% of nicotinic acid was added, tyramine content (363 ug/mL) was lower than that of the control group (873 ug/mL). At the same time, bacterial growth was decreased 1 log cycle from 8.62 to 7.56 log CFU/mL. TDC expression level in E. faecium was measured by using RT-qPCR. Lower expression level (below 0.7) was observed after the addition of 0.23% nicotinic acid (in vitro). When cheonggukjang was manufactured with addition of nicotinic acid, tyramine contents were decreased from 698.67 to 117.27 mg/kg when the concentration of nicotinic acid added was increased from 0.10 to 0.30%. These results suggest that nicotinic acid could be used as an agent (TDC inhibitor) to reduce tyramine content in cheonggukjang.
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Eitenmiller RR, Koehler PE, Reagan JO. Tyramine in fermented sausages: factors affecting formation of tyramine and tyrosine decarboxylase. J. Food Sci. 43: 689–693 (1978)
Joosten H.M.L.J. The biogenic amine contents of Dutch cheese and their toxicological significance. Neth. Milk Dairy J. 42: 25–42 (1988)
Oh SJ, Mah JH, Kim JH, Kim YW, Hwang HJ. Reduction of Tyramine by Addition of Schizandra chinensis Baillon in Cheonggukjang. J. Med. Food 15: 1109–1115 (2012)
Bodmer S, Imark C, Kneubühl M. Biogenic amines in foods: histamine and food processing. Inflamm. Res. 48: 296–300 (1999)
Shalaby AR. Significance of biogenic amines to food safety and human health. Food Res. Int. 29: 675–690 (1996)
Brink B, Damirik C, Joosten HMLJ, Huis in’t Veld JHJ. Occurrence and formation of biologically active amines in foods. Int. J. Food Microbiol. 11: 73–84 (1990)
Marcobal Á, Martín-Álvarez PJ, Polo MC, Muñoz R, Moreno-Arribas M. Formation of biogenic amines throughout the industrial manufacture of red wine. J. Food Prot. 69: 397–404 (2006)
Coton E, Coton M. Evidence of horizontal transfer as origin of strain to strain variation of the tyramine production trait in Lactobacillus brevis. Food Microbiol. 26: 52–57 (2009)
Mah JH. Evaluation and Reduction of Biogenic Amines in Korean Traditional Fermented Foods. Korea University, Seoul, Korea. (2003)
Lee YL. Reduction effect of biogenic amines in Doenjang by combined application of microorganisms and plant extracts. Korea University, Seoul, Korea. (2017)
Sarantinopoulos P, Andrighetto C, Georgalaki MD, Rea MC, Lombardi A, Cogan TM, Kalantzopoulos G, Tsakalidou E. Biochemical properties of enterococci relevant to their technological performance. Int. Dairy J. 11: 621–647 (2001)
Marcobal Á, de las Rivas B, García-Moruno E, Muñoz R. The tyrosine decarboxylation test does not differentiate Enterococcus faecalis from Enterococcus faecium. System. Appl.Microbiol. 27: 423–426 (2004)
Zhang K, and Ni Y. Tyrosine decarboxylase from Lactobacillus brevis: Soluble expression and characterization. Protein Expres. Purify. 94: 33–39 (2014)
Gale E.F. The bacterial amino acid decarboxylases. Adv. Enzymol. Relat. Area Mol. Biol. NY. vol. 6: 1–32 (1946)
Fernández M, Linares DM, Rodríguez A, Alvarez MA. Factors affecting tyramine production in Enterococcus durans IPLA 655. Appl. Microbiol. Biotech. 73: 1400–1406 (2007)
Landete JM. Pardo I. Ferrer S. Regulation of hdc expression and HDC activity by enological factors in lactic acid bacteria. J. Appl. Microbiol. 105: 1544–1551 (2008)
Lee BN. Reduction of Biogenic Amines by Application of Degradation Strains and Chemical Compounds to Cheonggukjang. Korea University, Seoul, Korea. (2011)
Ben-Giglrey B, Vieites Baptista de Sousa, Juan M, Villa Tomas G. Changes in biogenic amines and microbiological analysis in albacore (Thunnus alalunga) muscle during frozen storage. J. Food Protec. 61: 608–615 (1998)
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25: 402–408 (2001)
Bover-Cid S, Holzapfel, WH. Improved screening procedure for biogenic amine production by lactic acid bacteria. Int. J. Food Microbiol. 53: 33–41 (1999)
Ladero V, Martínez N, Martín MC, Fernández M, Alvarez MA. qPCR for quantitative detection of tyramine-producing bacteria in dairy products. Food Res. Int. 43: 289–295 (2010)
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This research was supported by the High Value-added Food Technology Development Program (314057-032-SB020) funded by Korea Institute of Planning and Evaluation for Technology in Ministry of Agriculture, Food and Rural Affairs, Republic of Korea.
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Kang, HR., Kim, HS., Mah, JH. et al. Tyramine reduction by tyrosine decarboxylase inhibitor in Enterococcus faecium for tyramine controlled cheonggukjang . Food Sci Biotechnol 27, 87–93 (2018). https://doi.org/10.1007/s10068-017-0205-0
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DOI: https://doi.org/10.1007/s10068-017-0205-0