BACKGROUND: The objective of the study was to determine sensitivity of Enterococcus faecium strains from rabbit meat to enterocins. RESULTS: Twenty-five decarboxylase-positive strains (from rabbit meat) allotted to the species E. faecium by genotypization and by MALDI TOF MS spectrometry identification (evaluation score value range 2.104-2.359; in the range for highly probable species identification-score value 2.300-3.000 and secure probable species identification/probable species identification-2.000-2.299) were studied. Seventeen strains were gelatinase positive. Although they did not produce histamine (HIS), spermidine, and spermine, they produce at least one among seven tested biogenic amines (BAs) in small amounts (2-10 mg/L) or up to very high amounts (>1000 mg/L). Putrescine was produced by two strains. These decarboxylase-positive strains were sensitive to enterocins (Ents). All strains were sensitive to Ent 2019 and Ent 55 (inhibitory activity from 200 to 819 200 AU/mL). Twenty-two strains were inhibited by Ent A(P) and Ent 4231; 20 strains were sensitive to Ent M. CONCLUSION: Our results have spread the basic knowledge related to inhibitory spectrum of enterocins showing sensitivity of decarboxylase-positive strains to enterocins. Protective possibilities of enterocins in meat processing were also indicated.

Department of Environmental Protection Engineering Faculty of Technology Tomáš Bat'a University in Zlín T G Masaryka 5555 Zlín 760 01 Czech Republic

Department of Nutrition National Agricultural and Food Centre Hlohovecká 2 Nitra Lužianky 7949 41 Slovakia

Institute of Animal Physiology Slovak Academy of Sciences Šoltésovej 4 6 Košice 040 01 Slovakia

University of Veterinary Medicine and Pharmacy Komenského 73 Košice 041 83 Slovakia

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Alatoom, A. A. , Cunningham S. A., Ihde S. M., Mandrekar J., and Patel R.. 2011. Comparison of direct colony method versus extraction method for identification of Gram‐positive cocci by use of Bruker Biotyper Matrix‐assisted laser desorption ionization‐time of flight mass spectrometry. J. Clin. Microbiol. 49:2868–2873. PubMed PMC

Belguesmia, Y. , Choiset Y., Prévost H., Dalgalarrondo M., Chobert J. M., and Drider D.. 2010. Partial purification and characterization of the mode of action of Enterocin S37: a bacteriocin produced by Enterococcus faecalis S37 isolated from poultry feces. J. Environ. Public Health. doi:10.1155/2010/986460. PubMed DOI PMC

Bover‐Cid, S. , Hugas M., Izquierdo‐Pulido M., and Vidal‐Carou M. C.. 2001. Amino acid‐decarboxylase activity of bacteria isolated from fermented pork sausages. Int. J. Food Microbiol. 66:185–189. PubMed

Buňková, L. , Buňka F., Hlobilová M., Vaňátková Z., Nováková D., and Dráb V.. 2009a. Tyramine production of technological important strains of Lactobacillus, Lactococcus and Streptococcus. Eur. Food Res. Technol. 220:533–538.

Buňková, L. , Buňka F., Pollaková E., Podešvová T., and Dráb V.. 2011. The effect of lactose, NaCl and an aero/anaerobic environment on the tyrosine decarboxylase activity of Lactococcus lactis subsp. cremoris and Lactococcus lactis subsp. lactis . Int. J. Food Microbiol. 147:11–119. PubMed

Cleveland, J. , Montville T. J., Nes I. F., and Chikindas M. L.. 2001. Bacteriocins: safe, natural antimicrobials for food preservation. Int. J. Food Microbiol. 71:1–20. PubMed

Dadáková, E. , Krˇížek M., and Pelikánová T.. 2009. Determination of biogenic amines in foods using ultra performance liquid chromatography (UPLC). Food Chem. 116:365–370.

Dalle Zotte, A. 2004. Dietary advantages: rabbit must tame consumers. Viandes Produits Carnés 23:161–167.

De Vos, P. , Garrity G., Jones D., Krieg N. R., Ludwig W., Rainey F. A., et al. 2009. Bergeys manual of systematic bacteriology. 2nd ed. Vol. 3 Springer, New York, ISBN 0‐ 387‐ 95041‐ 9.

De Vuyst, L. , Callewaert R., and Pot B.. 1996. Characterization of antagonistic activity of Lactobacillus amylovorus DCE471 and large scale isolation of its bacteriocin amylovorin L471. Syst. Appl. Microbiol. 19:9–20.

Foulquié Moreno, M. R. , Sarantopoulos P., Tsakalidou E., and De Vuyst L.. 2006. The role and application of enterococci in food health. Int. J. Food Microbiol. 106:1–24. PubMed

Franz, C. M. , van Belkum M. J., Holzapfel W. H., Abriuel H., and Gálvéz A.. 2007. Diversity of enterococcal bacteriocins and their grouping in a new classification scheme. FEMS Microbiol. Rev. 31:293–310. PubMed

Franz, C. M. , Huch M., Abriouel H., Holzapfel W., and Gálvez A.. 2011. Enterococci as probiotics and their implications in food safety. Int. J. Food Microbiol. 151:125–140. PubMed

Giraffa, G. 2003. Functionality of enterococci in dairy products. Int. J. Food Microbiol. 88:215–222. PubMed

Héchard, Y. , and Sahl H. G.. 2002. Mode of action of modified and unmodified bacteriocins from Gram‐positive bacteria. Biochimie 84:545–557. PubMed

Hernández, P. , and Gondret F.. 2006. Rabbit meat quality Pp. 269–290 in Maertens C. D., Coudert P., eds. Recent advances in rabbit sciences. COST and ILVO Publication, Melle, Belgium.

Klaenhammer, T. R. 1993. Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol. Rev. 12:39–86. PubMed

Koutsoumanis, K. , Tassou C., and Nychas G. J. E.. 2010. Biogenic amines in food Pp. 248–274 in Juneja V. K. and Sofos J. N., eds. Pathogens and toxins in foods: challenges and interventions. ASM Press, Washington, D.C.

Ladero, V. , Férnandéz M., Calles‐Enríquez M., Sánchez‐Lana E., Canedo E., Cruz Martín M., et al. 2012. Is the production of the biogenic amines tyramine and putrescine a species‐level trait in enterococci? Food Microbiol. 30:132–138. PubMed

Lauková, A. , and Mareková M.. 2002. A bacteriocin‐mediated antagonism by Enterococcus faecium EK13 against Listeria innocua in tofu. Arch. Lebensmittelhyg. 53:25–48.

Lauková, A. , Mareková M., and Javorský P.. 1993. Detection and antimicrobial spectrum of a bacteriocin‐like substances produced by Enterococcus faecium CCM 4231. Lett. Appl. Microbiol. 16:257–260.

Lauková, A. , Czikková S., Vasilková Z., Juriš P., and Mareková M.. 1998a. Occurrence of bacteriocin production among environmental enterococci. Lett. Appl. Microbiol. 27:178–182. PubMed

Lauková, A. , Czikková S., Vasilková Z., Juriš P., and Krupicer I.. 1998b. Antimicrobial effect of enterocin CCM4231 in the cattle slurry environment. Cytobios 94:73–79. PubMed

Lauková, A. , Czikková S., Dobránsky T., and Burdová O.. 1999a. Inhibition of Listeria monocytogenes and Staphylococcus aureus by enterocin CCM4231 in milk products. Food Microbiol. 16:93–99.

Lauková, A. , Czikková S., Laczková S., and Turek P.. 1999b. Use of enterocin CCM 4231 to control Listeria monocytogenes in experimentally contaminated dry fermented Hornád salami. Int. J. Food Microbiol. 52:115–119. PubMed

Lauková, A. , Vlaemynck G., and Czikková S.. 2001. Effect of enterocin CCM 4231 on Listeria monocytogenes in Saint‐Paulin Cheese. Folia Microbiol. 46:157–160. PubMed

Lauková, A. , Guba P., Nemcová R., and Vasilková Z.. 2003a. Reduction of Salmonella in gnotobiotic Japanese quails caused by the enterocin A‐producing EK13 strain of Enterococcus faecium . Vet. Res. Com. 27:275–280. PubMed

Lauková, A. , Turek P., Mareková M., and Nagy P.. 2003b. Use of ent M, new variant of ent P to control Listeria innocua in experimentally contaminated Gombasek sausage. Arch. Lebensmittelhyg. 54:46–48.

Lauková, A. , Fraqueza M. J., Strompfová V., Pogány Simonová M., Elias M., and Barreto A.. 2011. Bacteriocinogenic activity of Enterococcus faecalis strains from chourico, traditional sausage produced in Southern Portugal. Afr. J. Microbiol. Res. 5:334–339.

Lauková, A. , Chrastinová L., Pogány Simonová M., Strompfová V., Plachá I., Cobanová K., et al. 2012. Enterococcus faecium AL41, its Enterocin M and their beneficial use in rabbits husbandry. Probiotics Antimicrob. Proteins 4:243–249. PubMed

Mareková, M. , Lauková A., De Vuyst L., Skaugen M., and Nes I. F.. 2003. Partial characterization of bacteriocins produced by environmental strain Enterococcus faecium EK13. J. Appl. Microbiol. 94:523–530. PubMed

Mareková, M. , Lauková A., Skaugen M., and Nes I. F.. 2007. Isolation and characterization of a new bacteriocin, termed enterocin M, produced by environmental isolate Enterococcus faecium AL41. J. Ind. Microbiol. Biotechnol. 34:533–537. PubMed

Nes, I. F. , Diep D. B., and Ike Y. 2014. Enterococcal bacteriocins and antimicrobial proteins that contribute to niche control. Enterococci from commensals to leading of drug resistant infection. 1–34. PubMed

Pleva, P. , Buňková L., Lauková A., Lorencová E., Kubáň V., and Buňka F.. 2012a. Factors affected decarboxylase activity of Enterococcus faecium isolated from rabbit. Potravinárstvo 6:46–49.

Pleva, P. , Buňková L., Lauková A., Lorencová E., Kubáň V., and Buňka F.. 2012b. Decarboxylation activity of enterococci from rabbit meat and staphylococci isolated from trout intestines. Vet. Microbiol. 159:438–442. PubMed

Pogány Simonová, M. , Lauková A., Chrastinová L., Strompfová V., Faix Š., Vasilková Z., et al. 2009. Enterococcus faecium CCM7420, bacteriocin PPB CCM7420 and their effect in the digestive tract of rabbits. Czech J. Anim. Sci. 54:376–386.

Pogány Simonová, M. , Lauková A., Žitnan R., and Chrastinová L.. 2015. Effect of rabbit‐origin enterocin‐producing probiotic strain Enterococcus faecium CCM7420 application on growth performance and gut morphometry in rabbits. Czech J. Anim. Sci. 60:509–512.

Rehaiem, A. , Belgacem B. Y., Edalatian M. R., Martínez B., Rodríguez A., Manai M., et al. 2014. Assessment of potential probiotic properties and multiple bacteriocin encoding‐genes of the technological performing strain Enterococcus faecium MMRA. Food Control 37:343–350.

Ribeiro, T. , Oliviera M., Fraqueza M. J., Lauková A., Elias M., Tenreiro R., et al. 2011. Antimicrobial resistance and virulence factors among enterococci isolated from chourico, a traditional Portuguese dry fermented sausage. J. Food Prot. 74:465–469. PubMed

Rodríguez‐Calleja, J. M. , Santos J. A., Otero A., and García‐López M. L.. 2004. Microbiological quality of rabbit meat. J. Food Prot. 67:966–971. PubMed

Silla Santos, M. H. 1996. Biogenic amines:their importance in food. Int. J. Food Microbiol. 29:213–231. PubMed

Simonová, M. , and Lauková A.. 2007. Bacteriocin activity of enterococci from rabbits. Vet. Res. Com. 31:143–152. PubMed

Smelá, D. , Pechová P., Komprda T., Klejdus B., and Kubán V.. 2004. Chromatographic determination of biogenic amines in meat products during fermentation and long term storage. Chemické Listy 98:432–437 (in Czech).

Strompfová, V. , and Lauková A.. 2007. In vitro study on bacteriocin production of Enterococci associated with chickens. Anaerobe 13:228–237. PubMed

Strompfová, V. , Lauková A., and Mudroňová D.. 2003. Effect of bacteriocin‐like substance produced by Enterococcus faecium EF55 on the composition of avian gastrointestinal microflora. Acta Vet. Brno 72:559–564.

Szabóová, R. , Lauková A., Pogány Simonová M., Strompfová V., and Chrastinová L.. 2012. Bacteriocin‐producing enterococci from rabbit meat. Mal. J. Microbiol. 8:211–218.

Zhang, J. , Liu Y., Hu Y., Fang Y., Chen J., Wu D., et al. 2011. Effect of sucrose on the generation of free amino acids and biogenic amines in Chinese traditional dry‐cured fish during processing and storage. Int. J. Food Sci. Technol. 48:69–75. PubMed PMC

Occurrence of Enterococci in the Process of Artisanal Cheesemaking and Their Antimicrobial Resistance