Biogenic amines degradation by microorganisms isolated from cheese
Keywords:biogenic amines, Bacillus, degradation, cheese
The aim of this study was the isolation and characterization of microorganisms able to degrade biogenic amines and their identification. Individual microorganisms were obtained by isolation from commercially available foodstuffs and food produced in the technological laboratories of Faculty of Technology, Tomas Bata University in Zlín and subsequently identified by MALDI-TOF MS. The results of MALDI-TOF MS identification were verified by 16S rRNA sequenation. In this work was studied the ability of 5 bacterial strains positive to biogenic amines degradation isolated from dairy products to decrease biogenic amines content in vitro and quantified reduction in the concentration of biogenic amines tryptamine, β-phenylethylamine, putrescine, cadaverine, histamine and tyramine. The level of degradation (decrease of biogenic amines) was determined on the base of the ability to grow in media with biogenic amines as the sole source carbon and nitrogen. The isolated strains with the ability of degradation of one or more biogenic amines were cultured in medium supplemented with relevant biogenic amines, the media derivatized with dansyl chloride and these amines separated by HPLC at a wavelength of 254 nm. From five tested strains identified as Bacillus subtilis, Bacillus pumilus, Enterobacter cloacae, Rhizobium radiobacter and Acinetobacter pitii, isolated from gouda type cheese, the greatest ability of degradation was observed in Bacillus subtilis, which was capable to degrade almost all amount of histamine, cadaverine and putrescine. Other four strains showed a lower rate of degradation than Bacillus subtilis, but the ability to degrade biogenic amines with these microorganisms was still significant.
Alvarez, M. A., Moreno-Arribas, M. V. 2014. The problem of biogenic amines in fermented foods and the use of potential biogenic amine-degrading microorganisms as a solution. Trends in Food Science and Technology, vol. 39, no. 2, p. 146-155. https://doi.org/10.1016/j.tifs.2014.07.007
Askar, A., Treptow, H. 1986. Biogene amine in Lebensmitteln - Vorkommen, Bedeutung und Bestimmung. Molecular Nutrition Food Reasearch, vol. 32, no. 4, p. 420.
Arnold, S. H., Brown, W. D. 1978. Histamine toxicity from fish products. Advances in Food Research, vol. 34, p. 113-154. https://doi.org/10.1016/S0065-2628(08)60157-3
Bardócz, S., Grant, G., Brow, D. S., Ralph, A. and Pusztai, A. 1993. Polyamines in food - implications for growth and health. The Journal of Nutritional Biochemistry, vol. 4, no. 2, p. 66-71. https://doi.org/10.1016/0955-2863(93)90001-D
Bodmer, S., Imark, C., Kneubühl, M. 1999. Biogenic amines in foods: histamine and food processing. Inflammatory Research, vol. 48, no. 6, p. 296-300. https://doi.org/10.1007/s000110050463
Buňková, L., Buňka, F., Hlobilová, M., Vaňátková, Z., Nováková, D., Dráb, V. 2009. Tyramine production of technological important strains of Lactobacillus, Lactococcus and Streptococcus. European Food Research and Technology, vol. 229, p. 533-538. https://doi.org/10.1007/s00217-009-1075-3
Buňková, L., Adamcová, G., Hudcová, K., Velichová, H., Pachlová, V., Lorencová, E., Buňka, F. 2013. Monitoring of biogenic amines in cheeses manufactured at small-scale farms and in fermented dairy products in the Czech Republic. Food Chemistry, vol. 141, no. 1, p. 548-551. https://doi.org/10.1016/j.foodchem.2013.03.036
Dadáková, E., Křížek, M., Pelikánová, T. 2009. Determination of biogenic amines in foods using ultra-performance liquid chromatography (UPLC). Food Chemistry, vol. 116, no. 1, p. 365-370. https://doi.org/10.1016/j.foodchem.2009.02.018
Degheidi, M. A., Effat, B. A., Shalaby, A. R. 1992. Development of some biogenic amines during Ras cheese ripening with special reference to different starters. In Proceedings 5th Egyptian Conference for Dairy Science and Technology. Cairo, Egypt, p. 205-217.
El-Sayed, M. M. 1997. Biogenic amines in processed cheese available in Egypt. International Journal of Dairy Science, vol. 6, no. 11-12, p. 1079-1086. https://doi.org/10.1016/S0958-6946(96)00031-3
Eom, J. S., Seo, B. Y., Choi, H. S. 2015. Biogenic Amine Degradation by Bacillus Species Isolated from Traditional Fermented Soybean Food and Detection of Decarboxylase-Related Genes. Journal of Microbiology and Biotechnology, vol. 25, no. 9, p. 1519-1527. https://doi.org/10.4014/jmb.1506.06006
European Food Safety Authority (EFSA), 2011. Scientific opinion on risk based control of biogenic amine formation in fermented foods. EFSA Journal, vol. 9, no. 10, p. 1-93. https://doi.org/10.2903/j.efsa.2011.2393
Fadda, S., Vignolo, G., Oliver, G. 2001. Tyramine degradation and tyramine/histamine production by lactic acid bacteria and Kocuria strains. Biotechnology Letters, vol. 23, no. 24, p. 2015-2019. https://doi.org/10.1023/A:1013783030276
Fernández, M., Linares, D. M., Rodríguez, A., Alvarez. M. A. 2007. Factors affecting tyramine production in Enterococcus durans IPLA655. Apllied Microbiology and Biotechnology, vol. 73, no. 6, p. 1400-1406.
Foster, J. W., Hall, H. K. 1991. Inducible pH homeostasis, and the acid tolerance response to Salmonella typhimurium. Journal of Bacteriology, vol. 173, no. 16, p. 5129-5135. https://doi.org/10.1128/jb.173.16.5129-5135.1991
Gregová, G., Kmetová, M., Kmet, V., Venglovský, J., Feher, A. 2012. Antibiotic resistance of Escherichia coli isolated from a poultry slaughterhouse. Annals of Agricultural and Environental Medicine, vol. 19, no. 1, p. 75-77. PMid:22462449
Gücüglu, A, Küpülü, Ö. 2010. The effect of different starter cultures and ripening temperatures on formation of biogenic amine in Turkish fermented sausages. European Food Research and Technology, vol. 230, p. 875-884. https://doi.org/10.1007/s00217-010-1220-z
Halász, A., Baráth, A., Simon-Sarkadi, L., Holzapfel, W. 1994. Biogenic amines and their production by micro-organisms in food-review. Trends in Food Science and Technology, vol. 5, no. 2, p. 49. https://doi.org/10.1016/0924-2244(94)90070-1
Hernandez-Jover, T., Izquierdo-Pulido, M., Veciana-Nogues, M. T., Marine-Font, A., Vidal-Carou, M. C. 1997. Biogenic amine and polyamine contents in meat and meat products. Journal of Agricultural and Food Chemistry, vol. 45, no. 6, p. 2098-102. https://doi.org/10.1021/jf960790p
Herrero-Fresno, A., Martínez, N., Sánchez-Llana, E., Díaz, M., Fernández, M., Martin, M. C., Ladero, V., Alvarez, M. A. 2012. Lactobacillus casei strains isolated from cheese reduce biogenic amine accumulation in an experimental model. International Journal of Food Microbiology, vol. 157, no. 2, p. 297-304. https://doi.org/10.1016/j.ijfoodmicro.2012.06.002
Christensen, H., Bisgaard, M. 2010. Molecular classification and its impact on diagnostics and understanding the phylogeny and epidemiology of selected member of Pasteurellaceae of veterinary importance. Berliner und Münchener Tierärztliche Wochenschrift, vol. 123, no. 1-2, p. 20-30.
Joosten, H. M. L. G., Olieman, C. 1986. Determination of biogenic amines in cheese and some other food products by high-performance liquid chromatography in wmbination with thermo-sensitized reaction detection. Journal of Chromatography, vol. 356, no. 2, p. 311-319. https://doi.org/10.1016/S0021-9673(00)91491-2
Joosten, H. M. L. G., Stadhouders, J. 1987. Conditions allowing the formation of biogenic amines in cheese. 1. Decarboxylative properties of starter bacteria. Netherlands Milk Dairy Journal, vol. 41, p. 247-259.
Joosten, H. M. L. G. 1988. Conditions allowing the formation of biogenic amines in cheese. 3. Factors influencing the amounts formed. Netherlands Milk Dairy Journal, vol. 41, p. 329-357.
Ladero, V., Calles-Enríquez, M., Fernández, M., Alvarez, M. A. 2010. Toxicological effects of dietary biogenic amines. Current Nutrition and Food Science, vol. 6, p. 145-156. https://doi.org/10.2174/157340110791233256
Latorre-Moratalla, M. L., Bover-Cid, S., Aymerich, T., Marcos, B., Vidal-Carou, M. C., Garriga, M. 2007. Aminogenesis control in fermented sausages manufactured with pressurized meat batter and starter culture. Meat Science, vol. 75, no. 3, p. 460-469. https://doi.org/10.1016/j.meatsci.2006.07.020
Latorre-Moratalla, M., Bover-Cid, S., Talon, R., Garriga, M., Zanardi, E., Ianieri, A., Fraqueza, M., Elias, M., Drosinos, E., Vidal-Carou, M. 2010. Strategies to reduce biogenic amine accumulation in traditional sausage manufacturing. Food Science and Technology, vol. 43, no. 1, p. 20-25. https://doi.org/10.1016/j.lwt.2009.06.018
Lee, Y. C., Lin, C. S., Liu, F. L., Huang, T. Z. 2015. Degradation of histamine by Bacillus polymyxa isolated from salted fish products. Journal of Food and Drug Analysis, vol. 23, no. 4, p. 836-844. https://doi.org/10.1016/j.jfda.2015.02.003
Linares, D. M., del Río, B., Ladero, V., Martínez, N., Fernández, M., Cruz Martín, M., Álvarez, M. A. 2011. Factors influencing biogenic amines accumulation in dairy products. Frontiers in Microbiology, vol. 3, p. 180. https://doi.org/10.3389/fmicb.2012.00180
Lovenberg, W. 1973. Some vaso- and psychoactive substances in food: amines stimulates depressants and hallucinogens. In Toxicants Occurring Naturally in Foods, Washington, DC : National Academy of Science.
Maijala, R. L. 1993. Formation of histamine and tyramine by some lactic acid bacteria in MRS-broth and modified decarboxylation agar. Letters in Applied Microbiology, vol. 17, no. 1, p. 40-43. https://doi.org/10.1111/j.1472-765X.1993.tb01431.x
Mariné-Font, A., Vidal-Carou, M. C., Izquierdo-Pulido, M., Veciana-Nogués, M. T., Hernández-Jover T. 1995. Les amines biogènes dans les aliments: leur signification, leur analyse. Annales des Falsifications et de l'Expertise Chimique et Toxicologique, vol. 88, p. 119-140.
Martinez, N., Cruz Martin, M., Herrero, A., Fernandez, M., Alvarez, M., Ladero, V. 2011. qPCR as a powerful tool for microbial food spoilage quantification: significante for food quality. Trends in Food Science and Technology, vol. 22, no. 7, p. 367-376. https://doi.org/10.1016/j.tifs.2011.04.004
Postollec, F., Falentin, H., Pavan, S., Combrisson, J., Sohier, D. 2011. Recent advances in quantitative PCR (qPCR) applications in food microbiology. Food Microbiology, vol. 28, no. 5, p. 848-861. https://doi.org/10.1016/j.fm.2011.02.008
Shalaby, A. R. 1996. Significance of biogenic amines in food safety and human health. Food Research International, vol. 29, no. 7, p. 675-690. https://doi.org/10.1016/S0963-9969(96)00066-X
Silla Santos, H. M. 1996. Biogenic amines: their importance in foods. International Journal of Food Microbiology, vol. 29, no. 2-3, p. 213-231. https://doi.org/10.1016/0168-1605(95)00032-1
Simmon, K. E., Croft, A. C., Petti, C. A. 2006. Application of SmartGene IDNS Software to partial 16S rRNA gene sequences for a diverse group of bacteria in a clinical laboratory. Journal of Clinical Microbiology, vol. 44, no. 12, p. 4400-4406. https://doi.org/10.1128/JCM.01364-06
Smělá, D., Pechová, P., Komprda, T., Klejdus, B., Kubáň, V. 2004. Chromatografické stanovení biogenních aminů v trvanlivých salámech během fermentace a skladování (Chromatographic determination of biogenic amines in durable salami during fermentation and storage). Chemické listy, vol. 98, p. 432-437.
Stratton, J. E., Hutkins, R. W., Taylor, S. L. 1991. Biogenic amines in cheese and other fermented foods: a review. Journal of Food Protection, vol. 54, p. 460-470. https://doi.org/10.4315/0362-028X-54.6.460
Tawfik, N. F., Shalaby, A. R., Effat, B. A. 1992. Biogenic amine contents of ras cheese and incidence of their bacterial producers. Egyptian Journal of Dairy Science, vol. 20, p. 219-225.
ten Brink, B., Damink, C., Joosten, H. M., Huis in't Veld, J. H. 1990. Occurrence and formation of biologically active amines in foods. International Journal of Food Microbiology, vol. 11, no. 1, p. 73-84. https://doi.org/10.1016/0168-1605(90)90040-C
Valsamaki, K., Michaelidou, A., Polychroniadou, A. 2000. Biogenic amine production in Feta cheese. Food chemistry, vol. 71, no. 2, p. 259-266. https://doi.org/10.1016/S0308-8146(00)00168-0
Vítková, L. 2016. Izolace mikroorganismů degradujících biogenní aminy (Isolation of microorganisms degrading biogenic amines) : Diploma theses. Zlin : UTB, p. 85.
Voigt, M. N., Eitenmiller, R. R. 1978. Role of histidine and tyrosine decarboxylases and mono-diamine oxidases in amine on build-up in cheese. Journal of Food Protection, vol. 41, p. 182-186. https://doi.org/10.4315/0362-028X-41.3.182
Yongmei, L., Xiaohong, C., Mei, J., Xin, L., Rahman, N., Mingsheng, D., Yan, G. 2009. Biogenic amines in Chinese soy sauce. Food Control, vol. 20, no. 6, p. 593-597. https://doi.org/10.1016/j.foodcont.2008.08.020
Zaman, M. Z., Bakar, F. A., Selamat, J., Bakar, J. 2010. Occurrence of Biogenic Amines and Ami-nes Degrading Bacteria in Fish Sauce. Czech Journal of Food Sciences, vol. 28, p. 440-449.
Zaman, M. Z., Bakar, F. A., Jinap, S., Bakar, J. 2011. Novel starter cultures to inhibit biogenic amines accumulation during fish sauce fermentation. International Journal of Food Microbiology, vol. 145, no. 1, p. 84-91. https://doi.org/10.1016/j.ijfoodmicro.2010.11.031
Zaman, M. Z., Bakar, F. A., Selamat, J., Bakar, J., Ang, S. S., Chong, C. Y. 2014. Degradation of histamine by the halotolerant Staphylococcus carnosus FS19 isolate obtained from fish sauce. Food Control, vol. 40, p. 58-63. https://doi.org/10.1016/j.foodcont.2013.11.031
Zhao, X., Yyng, L., Yu, Z., Peng, N., Xiao, L., Yin, D., Qin, B. 2008. Characterization of depth-related microbial communities in lake sediment by denaturing gradient gel electrophoresis of amplified 16S rRNA fragments. Journal of Environmental Sciences, vol. 20, no. 2, p. 224-230. https://doi.org/10.1016/S1001-0742(08)60035-2
How to Cite
LicenseAuthors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).