SpringerLink
Log in

Identification of an alcohol tolerant multicopper oxidase for reduction of biogenic amines in fermented foods

  • Original Article
  • Published:
Systems Microbiology and Biomanufacturing Aims and scope Submit manuscript

Abstract

Biogenic amines are a group of microbial metabolites detected in fermented foods that have potential health risk. Reduction of biogenic amines in fermented foods by enzymes is an effective and safe approach as it has less influences on food flavor and fermentation process. In this work, a multicopper oxidase named as MCOP from Lactobacillus paracasei XJ02 was successfully expressed in E. coli BL21 (DE3). The Km and Vmax of MCOP were detected to be 4.34 mmol/L and 5.61 mmol/ (L· min), respectively. MCOP was resistant to acidic condition and was stable at a wide temperature range (4oC−65oC). Activity of MCOP was significantly inhibited by 5−20% NaCl, whereas it was dramatically increased in the presence of 5−20% ethanol. This enzyme significantly degraded putrescine and cadaverine in soy sauce with a degradation rate of 10.3% of total BAs. Moreover, addition of MCOP efficiently reduced the content of histamine and putrescine in huangjiu by 41.1% and 19.8%, respectively. The degradation rate for total biogenic amines in huangjiu was 20.5%. The results demonstrated the good performance of an ethanol tolerant multicopper oxidase in reduction of biogenic amines in alcohol beverages. This provides potential enzyme candidates for being used in food safety control.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Durak-Dados A, Michalski M, Osek J. Histamine and other biogenic amines in food. J Vet Res. 2020;64(2):281–88. https://doi.org/10.2478/jvetres-2020-0029.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Ruiz-Capillas C, Herrero AM. Impact of biogenic amines on food quality and safety. Foods. 2019;8(2):62. https://doi.org/10.3390/foods8020062.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. **a XL, Zhang QW, Zhang B, Zhang WJ, Wang W. Insights into the biogenic amine metabolic landscape during industrial semidry Chinese rice wine fermentation. J Agric Food Chem. 2016;64(39):7385–93. https://doi.org/10.1021/acs.jafc.6b01523.

    Article  CAS  PubMed  Google Scholar 

  4. Gao XL, Li C, He R, Zhang Y, Wang B, Zhang Z, Ho C. Research advances on biogenic amines in traditional fermented foods: emphasis on formation mechanism, detection and control methods. Food Chem. 2023;405:134911. https://doi.org/10.1016/j.foodchem.2022.134911.

    Article  CAS  Google Scholar 

  5. Li BB, Xu Y, Niu SH, Zhang N, Li W, Song GS, Zhang RY, Yang Y. Research progress on biogenic amine content and biogenic amine oxidase in food. Food Sci. 2019;40(01):341–47. https://doi.org/10.7506/spkx1002-6630-20171205-054.

    Article  Google Scholar 

  6. Klementová L, Purevdorj K, Butor I, Jancová P, Bábková D, Bunka F, Bunková L. Reduction of histamine, putrescine and cadaverine by the bacteria Lacticaseibacillus casei depending on selected factors in the real condition of the dairy product. Food Microbiol. 2024;117:104391. https://doi.org/10.1016/j.fm.2023.104391.

    Article  CAS  PubMed  Google Scholar 

  7. Lee JI, Kim YW. Characterization of amine oxidases from Arthrobacter aurescens and application for determination of biogenic amines. World J Microbiol Biotechnol. 2013;29(4):673–82. https://doi.org/10.1007/s11274-012-1223-y.

    Article  CAS  PubMed  Google Scholar 

  8. Ni XM, Yang T, Fang F. Biogenic amines-degrading enzymes and their applications: a review. Microbiol China. 2021;48(11):4398–411. https://doi.org/10.13344/j.microbiol.china.210201.

    Article  CAS  Google Scholar 

  9. Pintus F, Sabatucci A, Maccarrone M, Dainese E, Medda R. Amine oxidase from Euphorbia characias: kinetic and structural characterization. Biotechnol Appl Biochem. 2018;65(1):81–8. https://doi.org/10.1002/bab.1612.

    Article  CAS  PubMed  Google Scholar 

  10. Chauhan PS, Goradia B, Saxena A. Bacterial laccase: recent update on production, properties and industrial applications. 3 Biotech. 2017;7:323. https://doi.org/10.1007/s13205-017-0955-7.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Callejon S, Sendra R, Ferrer S, Pardo I. Cloning and characterization of a new laccase from Lactobacillus plantarum J16 CECT 8944 catalyzing biogenic amines degradation. Appl Microbiol Biotechnol. 2016;100(7):3113–24. https://doi.org/10.1007/s00253-015-7158-0.

    Article  CAS  PubMed  Google Scholar 

  12. Callejon S, Sendra R, Ferrer S, Pardo I. Recombinant laccase from Pediococcus acidilactici CECT 5930 with ability to degrade tyramine. PLoS One. 2017;12(10):e0186019. https://doi.org/10.1371/journal.pone.0186019.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Xu J. Characterization and heterologus expression of multicopper oxidases for degradation of biogenic amines. Wuxi: Jiangnan University; 2019.

    Google Scholar 

  14. Olmeda I, Casino P, Collins RE, Sendra R, Callejon S, Huesa J, Soares AS, Ferrer S, Pardo I. Structural analysis and biochemical properties of laccase enzymes from two Pediococcus species. Microb Biotechnol. 2021;14(3):1026–43. https://doi.org/10.1111/1751-7915.13751.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Li T, Huang L, Li Y, Xu Z, Ge X, Zhang Y, Wang N, Wang S, Yang W, Lu F, Liu Y. The heterologous expression, characterization, and application of a novel laccase from Bacillus velezensis. Sci Total Environ. 2020;713:136713. https://doi.org/10.1016/j.scitotenv.2020.136713.

    Article  CAS  PubMed  Google Scholar 

  16. Yang QH, Zhang ML, Zhang MM, Wang CQ, Liu YY, Fan XJ, Li H. Characterization of a novel, cold-adapted, and thermostable laccase-like enzyme with high tolerance for organic solvents and salt and potent dye decolorization ability, derived from a marine metagenomic library. Front Microbiol. 2018;9:2998. https://doi.org/10.3389/fmicb.2018.02998.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Wang XF, Zhao YS, Zhang SF, Lin XP, Liang HP, Chen YX, Ji CF. Heterologous expression of the Lactobacillus sakei multiple copper oxidase to degrade histamine and tyramine at different environmental conditions. Foods. 2022;11(20):3306. https://doi.org/10.3390/foods11203306.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Guo X, Zhou S, Wang YW, Song JL, Wang HM, Kong DL, Zhu J, Dong WW, He MX, Hu GQ, Ruan ZY. Characterization of a highly thermostable and organic solvent-tolerant copper-containing polyphenol oxidase with dye-decolorizing ability from Kurthia Huakuii LAM0618T. PLoS One. 2016;11(10):e0164810. https://doi.org/10.1371/journal.pone.0164810.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Callejón S, Sendra R, Ferrer S, Pardo I. Identification of a novel enzymatic activity from lactic acid bacteria able to degrade biogenic amines in wine. Appl Microbiol Biotechnol. 2014;98(1):185–98. https://doi.org/10.1007/s00253-013-4829-6.

    Article  CAS  PubMed  Google Scholar 

  20. Yang S, Long Y, Yan H, Cai HW, Li YD, Wang XG. Gene cloning, identification, and characterization of the multicopper oxidase CumA from Pseudomonas sp. 593. Biotechnol Appl Biochem. 2017;64(3):347–55. https://doi.org/10.1002/bab.1501.

    Article  CAS  PubMed  Google Scholar 

  21. Bian YQ, Xu GC, Ni Y. Optimization of fermentation conditions for production of diacetyl reductase using recombinant Escherichia coli. J Food Sci Biotechnol. 2017;36(09):944–50. https://doi.org/10.3969/j.issn.1673-1689.2017.09.009.

    Article  Google Scholar 

  22. Agbo P, Heath JR, Gray HB. Modeling dioxygen reduction at multicopper oxidase cathodes. J Am Chem Soc. 2014;136(39):13882–87. https://doi.org/10.1021/ja5077519.

    Article  CAS  PubMed  Google Scholar 

  23. Li L, Zou D, Ruan LY, Wen ZY, Chen SW, Xu L, Wei X. Evaluation of the biogenic amines and microbial contribution in traditional Chinese sausages. Front Microbiol. 2019;10:872. https://doi.org/10.3389/fmicb.2019.00872.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Luo QQ, Shi RY, Gong PF, Liu YT, Chen W, Wang CT. Biogenic amines in huangjiu (Chinese rice wine): formation, hazard, detection, and reduction. LWT-Food Sci Technol. 2022;168:113952. https://doi.org/10.1016/j.lwt.2022.113952.

    Article  CAS  Google Scholar 

  25. Yang J, Li WJ, Ng TB, Deng XZ, Lin J, Ye XY. Laccases: production, expression regulation, and applications in pharmaceutical biodegradation. Front Microbiol. 2017;8:832. https://doi.org/10.3389/fmicb.2017.00832.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Reiss R, Ihssen J, Thöny-Meyer L. Bacillus pumilus laccase: a heat stable enzyme with a wide substrate spectrum. BMC Biotechnol. 2011;11:9. https://doi.org/10.1186/1472-6750-11-9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Koschorreck K, Richter SM, Ene AB, Roduner E, Schmid RD, Urlacher VB. Cloning and characterization of a new laccase from Bacillus licheniformis catalyzing dimerization of phenolic acids. Appl Microbiol Biotechnol. 2008;79(2):217–24. https://doi.org/10.1007/s00253-008-1417-2.

    Article  CAS  PubMed  Google Scholar 

  28. Huy ND, Le NTM, Chew KW, Park SM, Show PL. Characterization of a recombinant laccase from Fusarium oxysporum HUIB02 for biochemical application on dyes removal. Biochem Eng J. 2021;168:107958. https://doi.org/10.1016/j.bej.2021.107958.

    Article  CAS  Google Scholar 

  29. Martins LO, Soares CM, Pereira MM, Teixeira M, Costa T, Jones GH, Henriques AO. Molecular and biochemical characterization of a highly stable bacterial laccase that occurs as a structural component of the Bacillus subtilis endospore coat. J Biol Chem. 2002;277(21):18849–59. https://doi.org/10.1074/jbc.M200827200.

    Article  CAS  PubMed  Google Scholar 

  30. Sondhi S, Sharma P, Saini S, Puri N, Gupta N. Purification and characterization of an extracellular, thermo-alkali-stable, metal tolerant laccase from Bacillus tequilensis SN4. PLoS One. 2014;9(5):e96951. https://doi.org/10.1371/journal.pone.0096951.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Brander S, Mikkelsen JD, Kepp KP. Characterization of an alkali- and halide-resistant laccase expressed in E. coli: CotA from Bacillus clausii. PLoS One. 2014;9(6):e99402. https://doi.org/10.1371/journal.pone.0099402.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Jimenez-Juarez N, Roman-Miranda R, Baeza A, Sánchez-Amat A, Vazquez-Duhalt R, Valderrama B. Alkali and halide-resistant catalysis by the multipotent oxidase from Marinomonas mediterranea. J Biotechnol. 2005;117(1):73–82. https://doi.org/10.1016/j.jbiotec.2005.01.002.

    Article  CAS  PubMed  Google Scholar 

  33. Ruijssenaars HJ, Hartmans S. A cloned Bacillus halodurans multicopper oxidase exhibiting alkaline laccase activity. Appl Microbiol Biotechnol. 2004;65(2):177–82. https://doi.org/10.1007/s00253-004-1571-0.

    Article  CAS  PubMed  Google Scholar 

  34. Fang F, Yang T, Zhou JW, Chen J, Du GC, Xu J. Multicopper oxidase mutant with improved salt tolerance. US. 2021;11008552:B2.

    Google Scholar 

  35. García-Ruiz A, González-Rompinelli EM, Bartolomé B, Moreno-Arribas MV. Potential of wine-associated lactic acid bacteria to degrade biogenic amines. Int J Food Microbiol. 2011;148(2):115–20. https://doi.org/10.1016/j.ijfoodmicro.2011.05.009.

    Article  CAS  PubMed  Google Scholar 

  36. Liu SP, Yu JX, Wei XL, Ji ZW, Zhou ZL, Meng XY, Mao J. Sequencing-based screening of functional microorganism to decrease the formation of biogenic amines in Chinese rice wine. Food Control. 2016;64:98–104. https://doi.org/10.1016/j.foodcont.2015.12.013.

    Article  CAS  Google Scholar 

  37. Cheng SM, Xu Y, Lan X. Isolation, characterization, and application of biogenic amines-degrading strains from fermented food. J Food Saf. 2020;40(1):e12716. https://doi.org/10.1111/jfs.12716.

    Article  Google Scholar 

Download references

Funding

This work was supported by the National Natural Science Foundation of China (32172182).

Author information

Author notes

  1. Linyan Wei and **aoxuan **a contributed equally to this work.

Authors and Affiliations

  1. Science Center for Future Foods, Jiangnan University, Wuxi, 214122, China

    Linyan Wei & Fang Fang

  2. Key Laboratory of Industrial Biotechnology, School of Biotechnology, Ministry of Education, Jiangnan University, Wuxi, 214122, China

    Linyan Wei & Fang Fang

  3. Engineering Research Center of Ministry of Education on Food Synthetic Biotechnology, Jiangnan University, Wuxi, 214122, China

    Linyan Wei & Fang Fang

  4. State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Bei**g, 100193, China

    **aoxuan **a

Authors
  1. Linyan Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. **aoxuan **a
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fang Fang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fang Fang.

Ethics declarations

Conflict of interest

The authors declare that there are no conflicts of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wei, L., **a, X. & Fang, F. Identification of an alcohol tolerant multicopper oxidase for reduction of biogenic amines in fermented foods. Syst Microbiol and Biomanuf 4, 699–707 (2024). https://doi.org/10.1007/s43393-024-00246-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s43393-024-00246-y

Keywords

Search

Navigation