Virulence factor genes possessing Enterococcus faecalis strains from rabbits and their sensitivity to enterocins


  • M. Pogány Simonová Slovak Academy of Sciences
  • A. Lauková Slovak Academy of Sciences



Information concerning the virulence factor genes and antibiotic resistance of rabbit enterococci is limited, so in this study we tested the virulence factor genes in Enterococcus faecalis strains from rabbits. Moreover, their resistance/sensitivity to antibiotics and sensitivity to enterocins was also tested, with the aim of contributing to our enterocin spectra study and to indicate the possibility of enterocin application in prevention or contaminant elimination in rabbit husbandry. A total of 144 rabbit samples were treated using a standard microbiological method. Thirty-one pure colonies of the species Enterococcus faecalis were identified, using the MALDI-TOF identification system and confirmed using phenotyping, among which 15 strains were virulence factor gene absent. The gelE gene was the most detected (42%); however, the expression of gelatinase phenotype did not always correlate with the detection of gelE. Strains did not show ß-haemolysis and were mostly resistant to tested antibiotics, but sensitive to enterocins (Ent), mainly to Ents EK13=A (P), 2019 and Ent M. Rabbit E. faecalis strains displayed antibiotic resistant traits and the presence of expressed and silent virulence genes, but they showed high levels of sensitivity to natural antimicrobials-enterocins, which indicates the possible prevention of multidrug and virulent enterococcal contaminants by enterocins.


Download data is not yet available.

Author Biographies

M. Pogány Simonová, Slovak Academy of Sciences

Institute of Animal Physiology

A. Lauková, Slovak Academy of Sciences

Institute of Animal Physiology


Baele M., Chiers K., Devriese L.A., Smith H.E., Wisselink H.J., Vaneechoutte M., Haesebrouck F. 2001. The gram-positive tonsillar and nasal flora of piglets before and after weaning. J. Appl. Microbiol., 91: 997-1003.


Bessède E., Angla-gre M., Delagarde Y., Sep Hieng S., Ménard A., Mégraud F. 2011. Matrix assisted laser desorption/ionization BIOTYPER: experience in the routine of a University hospital. Clin. Microbiol. Infect., 17: 533-538. doi:10.1111/j.1469-0691.2010.03274.x

De Vuyst L., Foulqiue Moreno M.R., Revets H. 2003. Screening for enterocins and detection of hemolysin and vancomycin resistance in enterococci of different origins. Int. J. Food Microbiol., 84: 299-318. doi:10.1016/S0168-1605(02)00425-7

Devriese L.A., Hommez J., Wijfels R., Haesebrouck E. 1991. Composition of the enterococcal and streptococcal intestinal flora of poultry. J. Appl. Bacteriol., 71: 46-50. doi:10.1111/j.1365-2672.1991.tb04661.x

Eaton T.J. Gasson M.J. 2001. Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Appl. Environ. Microbiol., 67: 1628-1635.


Fisher K., Philips C. 2009. The ecology, epidemiology and virulence of Enterococcus. Review Microbiol., 155: 1749-1757. doi:10.1099/mic.0.026385-0

Foulquie Moreno M.R., Sarantinopoulos P., Tsakalidou E., De Vuyst L. 2006. The role and application of enterococci in food and health. Review. Int. J. Food Microbiol., 106: 1-24. doi:10.1016/j.ijfoodmicro.2005.06.026

Franz Ch.A.M.P., Holzapfel W.H., Stiles M.E. 1999. Enterococci at the crossroads of food safety? Int. J. Food Microbiol., 47: 1-24.

Franz Ch.M.A.P., Huch M., Abriouel H., Holzapfel W., Gálvez A. 2011. Enterococci as probiotics and their implications in food safety. In J. Food Microbiol., 151: 125-140. doi:10.1016/j.ijfoodmicro.2011.08.014

Garrity G.M. 2009. Bergey’s Manual of Systematic Bacteriology: The Firmicutes. In: Whitman et al. (Eds.), Bergey’s Manual of Systematic Bacteriology, Vol. 3, Springer, New York, 269-295.

Gilmore M.S., Clewell D.B., Courvalin P., Dunny G.M., Murray B.E., Rice L.B. 2002. The Enterococci: Pathogenesis, Molecular Biology and Antibiotic Resistance. ASM Press, Washington, DC, 1-383.

Giraffa G. 2006. Enterococci from foods. FEMS Microbiol. Rev., 26: 163-171. doi.10.1111/j.1574-6976.2002.tb00608.x

Gülhan T., Aksakal A., Ekin I.H., Savaşan S., Boynukara B. 2006. Virulence factors of Enterococcus faecium and Enterococcus faecalis strains isolated from humans and pets. Turk. J. Vet. Anim. Sci., 30: 477-482.

Iseppi R., Messi P., Anacarso I., Bondi M., Sabia C., Condò C., de Niederhausen S. 2015. Antimicrobial resistance and virulence traits in Enterococcus strains isolated from dogs and cats. New Microbiol., 38: 369-378.

Kanemitsu K., Nishino T., Kurushima H., Okamura N., Takemura H., Yamamoto H., Kahu M. 2001. Quantitative detection of gelatinase activity among enterococci. J. Microbiol. Meth. 47: 11-16.


Lauková A., Mareková M., Štyriak I. 2003. Inhibitory effect of different enterocins against fecal bacterial isolates. Berl. Münch. Tierärztl. Wschr., 116: 37-40. ISSN 0341-6593

Lauková A., Strompfová V., Kandričáková A., Ščerbová J., Semedo-Laemsaddek T., Miltko R., Belzecki G. 2015. Virulence factors genes in enterococci isolated from beavers (Castor fiber). Folia Microbiol., 60: 151-154. doi:10.1007/s12223-014-0357-8

Linaje R., Coloma M.D., Pérez-Martínez G., Zúñiga M. 2004. Characterization of faecal enterococci from rabbits for the selection of probiotic strains. J. Appl. Microbiol., 96: 761-771. doi:10.1111/j.1365-2672.2004.02191.x

Manero A., Blanch A.R. 1999. Identification of Enterococcus spp. with biochemical key. Appl. Environ. Microbiol., 65: 4425-

Medeiros A.W., Pereira R.I., Oliveira D., Martins P,D., d´Azavedo P.A., van der Sand S., Frazzon J., Frazzon A.P.G. 2014. Molecular detection of virulence factors among food and

clinical Enterococcus faecalis strains in South Brazil. Braz. J. Microbiol., 45: 327-332.


National Committee for Clinical Laboratory Standards. 2012. Approved standard M2-A8. Performance standards for antimicrobial disk susceptibility tests, 8th ed. NCCLS, Wayne, Pa.

Nes I.F., Holo H. 2000. Class II antimicrobial peptides from lactic acid bacteria. Biopolymers, 55: 50-61. doi:10.1002/1097-0282(2000)55:1<50::AID-BIP50>3.0.CO;2-3

Özmen Toğay S., Çelebi Keskin A., Açik L., Temiz A. 2010. Virulence genes, antibiotic resistance and plasmid profiles of Enterococcus faecalis and Enterococcus faecium from naturally fermented Turkish foods. J. Appl. Microbiol., 109: 1084-1092. doi:10.1111/j.1365-2672.2010.04763.x

Peeters J., Mac K., Wichmann-Schauer H., Klein G., Ellerbroek L. 2003. Species distribution and antibiotic resistance isolated from food of animal origin in Germany. Int. J. Food Microbiol., 88: 311-314. doi:10.1016/S0168-1605(03)00193-4.

Poeta P., Costa D., Igrejas A., Rodrigues J., Torres C. 2007. Phenotypic and genotypic characterization of antimicrobial resistance in faecal enterococci from wild boars (Sus scrofa). Vet. Microbiol., 125: 368-374. doi:10.1016/j.vetmic.2007.06.003

Pogány Simonová M., Lauková A., Chrastinová Ľ., Stompfová V., Faix Š., Vasilková Z.,Ondruška Ľ., Jurčík R., Rafay J. 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., Haviarová M. 2010. Pseudomonads from rabbits and their sensitivity to antibiotics and natural antimicrobials. Res. Vet. Sci., 88: 203-207. doi:10.1016/j.rvsc.2009.07.010

Ribeiro T., Oliveira M., Fraqueza M.J., Lauková A., Elias M., Tenreiro R., Barreto A.S., Semedo-Lemsaddek T. 2011. Antibiotic resistance and virulence factors among enterococci isolated from chouriço, a traditional Portuguese dry fermented sausage. J. Food Prot., 74: 465-469. Accession 60385401.

Semedo-Lemsaddek T., Santos M.A., Martins P., Lopes M.F.S., Marques J.F., Tenreiro R., Crespo M.T.B. 2003. Comparative study using type strains and clinical and Food isolates to examine hemolytic activity and occurence of the cyl operon in enterococci. J. Clin. Microbiol., 41: 2569-2576. doi:10.1128/


Semedo-Lemsaddek T., Silva Nóbrega C., Ribeiro T., Pedroso N.M., Sales-Luis T., Lemsaddek A., Tenreiro R., Tavares L., Vilela C.L., Oliveira M. 2013. Virulence traits and antibiotic resistance among enterococci isolated from Eurasian otter (Lutra lutra). Vet. Microbiol., 163: 378-382. doi:10.1016/j.vetmic.2012.12.032

Simonová M., Lauková A., Štyriak I. 2005. Enterococci from rabbits – potential feed additive. Czech J. Anim. Sci., 50: 416-421.

Simonová M., Lauková A. 2007. Bacteriocin activity of enterococci from rabbits. Vet. Res. Com., 31: 143-152. doi:10.1007/s11259-006-3411-4

Smith-Palmer A., Stewart J., Fyfe L. 1998. Antimicrobial properties of plant essential oils and essences against five important food-borne pathogens. Lett. Appl. Microbiol., 26: 118-122. doi:10.1046/j.1472-765X.1998.00303.x

Strompfová V., Marciňáková M., Simonová M., Gancarčíková S., Jonecová Z., Sciranková Ľ., Koščová J., Buleca V., Čobanová K., Lauková A. 2006. Enterococcus faecium EK13-an enterocin A-producing strain with probiotic character and its effect in piglets. Anaerobe, 12: 242-248. doi:10.1016/j.anaerobe.2006.09.003

Upadhyaya P.M., Ravikumar K.L., Umapathy B.L. 2009. Review of virulence factors of Enterococcus: an emerging nosocomial pathogens. Ind. J. Med. Microbiol., 27: 301-305. doi:10.4103/0255-0857.55437