Isolation and molecular characterization of Enterococcus strains producing biogenic amines from traditional cheese samples
Main Article Content
Keywords
biogenic amines; Enterococcus; traditional cheeses; Türkiye
Abstract
Traditional fermented cheese is widely consumed in Türkiye because of its distinctive flavor and nutritional value. This study aimed to isolate and characterize Enterococcus species from traditional cheese samples and to evaluate their ability to produce biogenic amines (BAs). A total of 186 cheese samples were screened for the presence of Enterococcus spp., yielding 135 isolates, of which 92 were identified as E. faecium and 43 as E. faecalis. Phenotypic identification was performed using standard biochemical tests, while molecular characterization was achieved through 16S rDNA gene sequencing. The decarboxylase activity of the isolates was assessed using modified decarboxylase media, and the concentrations of four BAs, named histamine, tyramine, putrescine, and cadaverine, were quantified using high-performance liquid chromatography. In addition, polymerase chain reaction analysis was employed to detect BA-encoding genes. Gel electrophoresis results showed that 25, 24, 21, and 13 strains harbored genes responsible for the production of histamine, tyramine, putrescine, and cadaverine, respectively. Among the 25 BA-producing isolates, 18 were E. faecium and 7 were E. faecalis. The BA concentrations in cheese samples ranged from ND to 97.36 mg/L, with putrescine being the most abundant BA. Specifically, histamine, tyramine, putrescine, and cadaverine were produced in the ranges of 14.87–26.24, 2.9–33.47, 0.91–97.36, and 1.18–57.84 mg/L, respectively. No statistically significant differences in BA levels were observed between bacterial groups. These findings highlight that BA-producing Enterococcus strains are present in traditional cheeses, posing potential safety concerns, as BAs are heat-stable compounds that cannot be eliminated by common thermal food-processing techniques. Their presence may reflect both quality of raw materials and hygienic conditions during production of cheese.
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Barbieri, F., Montanari, C., Gardini, F. and Tabanelli, G. 2019. Biogenic amine production by lactic acid bacteria: a review. Foods. 8(1):17. https://doi.org/10.3390/foods8010017
Beasley, S.S. and Saris, P.E.J. 2004. Nisin-producing Lactococcus lactis strains isolated from human milk. Appl Environ Microbiol. 70(8):5051–5053. https://doi.org/10.1128/AEM.70.8.5051–5053
Benkerroum, N. 2016. Biogenic amines in dairy products: origin, incidence, and control means. Compr Rev Food Sci Food Saf. 15(4):801–826. https://doi.org/10.1111/1541-4337.12212
Bogdanovi´c, T., Petriˇcevi´c, S., Brkljaˇca, M., Listeš, I. and Pleadin, J. 2020. Biogenic amines in selected foods of animal origin obtained from the Croatian retail market. Food Addit Contam A. 37(5):815–830. https://doi.org/10.1080/19440049.2020.1726503
Botello-Morte, L., Moniente, M., Gil-Ramírez, Y., Virto, R., García-Gonzalo, D. and Pagán, R. 2022. Identification by means of molecular tools of the microbiota responsible for the formation of histamine accumulated in commercial cheeses in Spain. Food Control. 133:108595. https://doi.org/10.1016/j.foodcont.2021.108595
Bover-Cid, S. and Holzapfel, W.H. 1999. Improved screening procedure for biogenic amine production by lactic acid bacteria. Int J Food Microbiol. 53(1):33–41. https://doi.org/10.1016/S0168-1605(99) 00152-X
Burdychova, R. and Komprda, T. 2007. Biogenic amine-forming microbial communities in cheese. FEMS Microbiol Lett. 276(2):149–155. https://doi.org/10.1111/j.1574-6968.2007.00922.x
Combarros‐Fuertes, P., Fernández, D., Arenas, R., Diezhandino, I., Tornadijo, M.E. and Fresno, J.M. 2016. Biogenic amines in Zamorano cheese: factors involved in their accumulation. J Sci Food Agric. 96(1):295–305.https://doi.org/10.1002/jsfa.7093
Coton, E., Rollan, G., Bertrand, A. and Lonvaud-Funel, A. 1998. Histamine-producing lactic acid bacteria in wines: early detection, frequency, and distribution. Am J Enol Vitic. 49(2):199–204. https://doi.org/10.5344/ajev.1998.49.2.199
Dabadé, D.S., Jacxsens, L., Miclotte, L., Abatih, E., Devlieghere, F. and De Meulenaer, B. 2021. Survey of multiple biogenic amines and correlation to microbiological quality and free amino acids in foods. Food Control.120:107497. https://doi.org/10.1016/j.foodcont.2020.107497
de las Rivas, B., Marcobal, A., Carrascosa, A.V. and Munoz, R. 2006. PCR detection of foodborne bacteria producing the biogenic amines histamine, tyramine, putrescine, and cadaverine. J Food Prot. 69(10):2509–2514. http://doi.org/10.13039/100007652
EFSA Panel on Biological Hazards (BIOHAZ). 2011. Scientific opinion on risk-based control of biogenic amine formation in fermented foods. EFSA J. 9(10):2393. https://doi.org/10.2903/j.efsa.2011.2393
Ferchichi, M., Sebei, K., Boukerb, A.M., Karray-Bouraoui, N., Chevalier, S., Feuilloley, M.G.J., Connil, N. and Zommiti, M. 2021. Enterococcus spp.: is it a bad choice for a good use—a conundrum to solve? Microorganisms. 9(11):2222. https://doi.org/10.3390/microorganisms9112222
Fernández-Garcı́a, E., Carbonell, M., Gaya, P. and Nuñez, M. 2004. Evolution of the volatile components of ewes raw milk Zamorano cheese. Seasonal variation. Int Dairy J. 14(8):701–711. https://doi.org/10.1016/j.idairyj.2003.12.011
Geraldes, C., Tavares, L., Gil, S. and Oliveira, M. 2022. Enterococcus virulence and resistant traits associated with its permanence in the hospital environment. Antibiotics (Basel). 11(7):857. https://doi.org/10.3390/antibiotics11070857
Ghazvinian, M., Asgharzadeh Marghmalek, S., Gholami, S.A., Amiri, E. and Goli, H.R. 2024. Antimicrobial resistance patterns, virulence genes, and biofilm formation in enterococci strains collected from different sources. BMC Infect Dis. 24(1):274. https://doi.org/10.1186/s12879-024-09117-2
Gök, Ş.M., Türk Dağı, H., Kara, F., Arslan, U. and Fındık, D. 2020. Investigation of antibiotic resistance and virulence factors of Enterococcus faecium and Enterococcus faecalis strains isolated from clinical samples. Microbiol Bul. 54(1):26–39. https://doi.org/10.5578/mb.68810
Gökmen, M. and Ektik, N. 2022. Determination of virulence factors and antibiotic resistances of Enterococcus spp. identified from different stages of ripened (classical) white cheese production. Kocatepe Vet J. 15(1):120–127. https://doi.org/10.30607/kvj.1048982
Hajikhani, R., Onal Darilmaz, D., Yuksekdag, Z.N. and Beyatli, Y. 2021. Assessment of some metabolic activities and potential probiotic properties of eight Enterococcus bacteria isolated from white cheese microbiota. Antonie Van Leeuwenhoek. 114(8):1259–1274. https://doi.org/10.1007/s10482-021-01599-3
Hu, M., Dong, J., Tan, G., Li, X., Zheng, Z. and Li, M. 2021. Metagenomic insights into the bacteria responsible for producing biogenic amines in sufu. Food Microbiol. 98:103762. https://doi.org/10.1016/j.fm.2021.103762
Jahansepas, A., Aghazadeh, M., Rezaee, M.A., Heidarzadeh, S., Mardaneh, J., Mohammadzadeh, A. and Pouresmaeil, O. 2022. Prevalence, antibiotic resistance and virulence of Enterococcus spp. isolated from traditional cheese types. Ethiop J Health Sci. 32(4):799–808. https://doi.org/10.4314/ejhs.v32i4.17
Kandasamy, S., Yoo, J., Yun, J., Kang, H.B., Seol, K.-H. and Ham, J.-S. 2021. Quantitative analysis of biogenic amines in different cheese varieties obtained from the Korean domestic and retail markets. Metabolites. 11(1):31. https://doi.org/10.3390/metabo11010031
Kročko, M., Čanigová, M., Ducková, V., Artimová, A., Bezeková, J. and Poston, J. 2011. Antibiotic resistance of Enterococcus species isolated from raw foods of animal origin in south west part of Slovakia. Czech J Food Sci. 29(6):654–659. https://doi.org/10.17221/246/2010-CJFS
Li, Y., Zhao, N., Li, Y., Zhang, D., Sun, T. and Li, J. 2023. Dynamics and diversity of microbial community in salmon slices during refrigerated storage and identification of biogenic amine-producing bacteria. Food Biosci. 52:102441. https://doi.org/10.1016/j.fbio.2023.102441
Ma, J.-K., Raslan, A.A., Elbadry, S., El-Ghareeb, W.R., Mulla, Z.S., Bin-Jumah, M., Abdel-Daim, M.M. and Darwish, W.S. 2020. Levels of biogenic amines in cheese: correlation to microbial status, dietary intakes, and their health risk assessment. Environ Sci Pollut Res Int. 27(35):44452–44459. https://doi.org/10.1007/s11356-020-10401-2
Maijala, R.L. 1993. Formation of histamine and tyramine by some lactic acid bacteria in MRS‐broth and modified decarboxylation agar. Lett Appl Microbiol. 17(1):40–43. https://doi.org/10.1111/j.1472-765X.1993.tb01431.x
Marcobal, Á., de las Rivas, B., García-Moruno, E. and Muñoz, R. 2004. The tyrosine decarboxylation test does not differentiate Enterococcus faecalis from Enterococcus faecium. Syst Appl Microbiol. 27(4):423–426. https://doi.org/10.1078/0723202041438428
Merabti, R., Madec, M.N., Chuat, V., Becila, F.Z., Boussekine, R., Bekhouche, F. and Valence, F. 2019. First insight into the technological features of lactic acid bacteria isolated from Algerian fermented wheat Lemzeiet. Curr Microbiol. 76(10):1095-1104. https://doi.org/10.1007/s00284-019-01727-3
Montanari, C., Barbieri, F., Lorenzini, S., Gottardi, D., Šimat, V., Özogul, F., Gardini, F. and Tabanelli, G. 2023. Survival, growth, and biogenic amine production of Enterococcus faecium FC12 in response to extracts and essential oils of Rubus fruticosus and Juniperus oxycedrus. Front Nutr. 9:1092172. https://doi.org/10.3389/fnut.2022.109217
Natrella, G., Vacca, M., Minervini, F., Faccia, M. and De Angelis, M.A. 2024. Comprehensive review on the biogenic amines in cheeses: their origin, chemical characteristics, hazard and reduction strategies. Foods. 13(16):2583. https://doi.org/10.3390/foods1316258
Oruc, O., Cetin, O., Darilmaz, D.O. and Yüsekdag, Z.N. 2021. Determination of the biosafety of potential probiotic Enterococcus faecalis and Enterococcus faecium strains isolated from traditional white cheeses. Food Sci Technol (LWT). 148:111741. https://doi.org/10.1016/j.lwt.2021.111741
O’Sullivan, D.J., Fallico, V., O’Sullivan, O., McSweeney, P.L., Sheehan, J.J., Cotter, P.D. and Giblin L. 2015. High-throughput DNA sequencing to survey bacterial histidine and tyrosine decarboxylases in raw milk cheeses. BMC Microbiol. 15(1):266. https://doi.org/10.1186/s12866-015-0596-0
Raafat, S.A., Abo-Elmagd, E.K., Awad, R.A. and Hassan, E.M. 2016. Prevalence of vancomycin resistant enterococci in different food samples. Egypt J Med Microbiol. 25(4):47–55.
Rauscher-Gabernig, E., Gabernig, R., Brueller, W., Grossgut, R., Bauer, F. and Paulsen, P. 2012. Dietary exposure assessment of putrescine and cadaverine and derivation of tolerable levels in selected foods consumed in Austria. Eur Food Res Technol. 235(2):209–220. https://doi.org/10.1007/s00217-012-1748-1
Sang, X., Li, K., Zhu, Y., Ma, X. and Hou, H. 2020. The impact of microbial diversity on biogenic amines formation in grasshopper sub shrimp paste during the fermentation. Front Microbiol. 11:782. https://doi.org/10.3389/fmicb.2020.00782
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How to Cite
Aktop, S., & Şanlıbaba, P. (n.d.). Isolation and molecular characterization of Enterococcus strains producing biogenic amines from traditional cheese samples. Italian Journal of Food Science, 38(1). https://doi.org/10.15586/
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How to Cite
Aktop, S., & Şanlıbaba, P. (n.d.). Isolation and molecular characterization of Enterococcus strains producing biogenic amines from traditional cheese samples. Italian Journal of Food Science, 38(1). https://doi.org/10.15586/