Screening of virulence genes in Staphylococcus aureus isolates from rabbits
DOI:
https://doi.org/10.4995/wrs.2015.3961Keywords:
Staphylococcus aureus, rabbit, virulence factors, genotype, MLSTAbstract
Staphylococcus aureus is a versatile pathogen able to cause disease in both humans and animals. In rabbits, this bacterium infects animals of different ages, producing several purulent lesions. The ability of S. aureus to cause disease depends on a combination of virulence factors. The aim of this study was therefore to investigate the distribution of bacterial virulence determinants in 69 S. aureus isolates from rabbits. Some virulence factors (7 adhesins, 1 toxin and 1 protease) were positive in all rabbit S. aureus isolates analysed, while others (1 adhesin and 10 toxins) were always negative. The remaining virulence factors were more variable among isolates. An association between genotype and the different profiles of virulence factors was observed, but not with the type of lesion (P<0.05). One strain of each genotype was further analysed by multilocus sequence typing, generating ST121, ST96 and ST2951, determining a greater number of enterotoxins in ST121 isolates compared to ST96 and ST2951 isolates, which could justify the different pathogenicity between strains.
Downloads
References
Agnoletti F., Mazzolini E., Bacchin C., Bano L., Berto G., Rigoli R., Muffato G., Coato P., Tonon E., Drigo I. 2014. First reporting of methicillin-resistant Staphylococcus aureus (MRSA) ST398 in an industrial rabbit holding and in farmrelated people. Vet. Microbiol., 170: 172-177. doi:10.1016/j.vetmic.2014.01.035
Akineden O., Annemuller C., Hassan A.A., Lammler C., Wolter W., Zschock M. 2001. Toxin genes and other characteristics of Staphylococcus aureus isolates from milk of cows with mastitis. Clin. Vaccine Immunol., 8: 959-964. doi:10.1128/cdli.8.5.959-964.2001
Arciola C.R., Baldassarri L., Montanaro L. 2001. Presence of icaA and icaD genes and slime production in a collection of staphylococcal strains from catheter-associated infections. J. Clin. Microbiol., 39: 2151-2156. doi:10.1128/JCM.39.6.2151-2156.2001
Blaiotta G., Fusco V., von Eiff C., Villani F., Becker K. 2006. Biotyping of enterotoxigenic Staphylococcus aureus by enterotoxin gene cluster (egc) polymorphism and spa typing analyses. Appl. Environ. Microbiol., 72: 6117-6123. doi:10.1128/AEM.00773-06
Boden Wastfelt M.K., Flock J.I. 1995. Incidence of the highly conserved fib gene and expression of the fibrinogen-binding (Fib) protein among clinical isolates of Staphylococcus aureus. J. Clin. Microbiol., 33: 2347-2352.
Buzzola F.R., Alvarez L.P., Tuchscherr L.P., Barbagelata M.S., Lattar S.M., Calvinho L., Sordelli D.O. 2007. Differential abilities of capsulated and noncapsulated Staphylococcus aureus isolates from diverse agr groups to invade mammary epithelial cells. Infect. Immun., 75: 886-891. doi:10.1128/IAI.01215-06
Corpa, J.M., Hermans, K., Haesebrouck, F. 2009. Main Pathologies associated with Staphylococcus aureus infections in rabbits: a review. World Rabbit Sci., 17: 115-125. doi:10.4995/wrs.2009.651
Cucarella C., Solano C., Valle J., Amorena B., Lasa I., Penadés J.R. 2001. Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J. Bacteriol., 183: 2888-2896. doi:10.1128/JB.183.9.2888-2896.2001
Enright M.C., Day N.P., Davies C.E., Peacock S.J., Spratt B.G. 2000. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J. Clin. Microbiol., 38: 1008-1015.
Fitzgerald J.R., Hartigan P.J., Meaney W.J., Smyth C.J. 2000. Molecular population and virulence factor analysis of Staphylococcus aureus from bovine intramammary infection. J. Appl. Microbiol., 88: 1028-1037. doi:10.1046/j.1365-2672.2000.01071.x
Gordon R.J., Lowy F.D. 2008. Pathogenesis of methicillin- resistant Staphylococcus aureus infection. Clin. Infect. Dis., 46 Suppl 5: S350-359. doi:10.1086/533591
Guerrero I., Ferrian S., Penadés M., García-Quirós A., Pascual J.J., Selva L., Viana D., Corpa J.M. 2015. Host responses associated with chronic staphylococcal mastitis in rabbits. Vet. J., 204: 338-344. doi:10.1016/j.tvjl.2015.03.020
Haveri M., Hovinen M., Roslöf A., Pyörälä S. 2008. Molecular types and genetic profiles of Staphylococcus aureus strains isolated from bovine intramammary infections and extramammary sites. J. Clin. Microbiol., 46: 3728-3735. doi:10.1128/JCM.00769-08
Herron-Olson L., Fitzgerald J.R., Musser J.M., Kapur V. 2007. Molecular correlates of host specialization in Staphylococcus aureus. PLoS ONE, 2: e1120. doi:10.1371/journal.pone.0001120
Holtfreter S., Bauer K., Thomas D., Feig C., Lorenz V., Roschack K., Friebe E., Selleng K., Lövenich S., Greve T., Greinacher A., Panzig B., Engelmann S., Lina G., Bröker B.M. 2004. egc-Encoded superantigens from Staphylococcus aureus are neutralized by human sera much less efficiently than are classical staphylococcal enterotoxins or toxic shock syndrome toxin. Infect. Immun., 72: 4061-4071. doi:10.1128/IAI.72.7.4061-4071.2004
Holtfreter S., Grumann D., Schmudde M., Nguyen H.T., Eichler P., Strommenger B., Kopron K., Kolata J., Giedrys-Kalemba S., Steinmetz I., Witte W., Bröker B.M. 2007. Clonal distribution of superantigen genes in clinical Staphylococcus aureus isolates. J. Clin. Microbiol., 45: 2669-2680. doi:10.1128/JCM.00204-07
Hussain M., von Eiff C., Sinha B., Joost I., Herrmann M., Peters G., Becker K. 2008. eap gene as novel target for specific identification of Staphylococcus aureus. J. Clin. Microbiol., 46,: 470-476. doi:10.1128/JCM.01425-07
Jarraud S., Lyon G.J., Figueiredo A.M., Gérard L., Vandenesch F., Etienne J., Muir T.W., Novick R.P. 2000. Exfoliatin-producing strains define a fourth agr specificity group in Staphylococcus aureus. J. Bacteriol., 182: 6517-6522. doi:10.1128/JB.182.22.6517-6522.2000
Jarraud S., Peyrat M.A., Lim A., Tristan A., Bes M., Mougel C., Etienne J., Vandenesch F., Bonneville M., Lina G. 2001. egc, a highly prevalent operon of enterotoxin gene, forms a putative nursery of superantigens in Staphylococcus aureus. J. Immunol., 166: 669-677. doi:10.4049/jimmunol.166.1.669
Jarraud S., Mougel C., Thioulouse J., Lina G., Meugnier H., Forey F., Nesme X., Etienne J., Vandenesch F. 2002. Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect. Immun., 70: 631-641. doi:10.1128/IAI.70.2.631-641.2002
Ji G., Beavis R., Novick R.P. 1997. Bacterial interference caused by autoinducing peptide variants. Science, 276: 2027-2030. doi:10.1126/science.276.5321.2027
Josefsson E., McCrea K.W., Ni Eidhin D., O’Connell D., Cox J., Hook M., Foster T.J. 1998. Three new members of the serine-aspartate repeat protein multigene family of Staphylococcus aureus. Microbiology, 144: 3387-3395. doi:10.1099/00221287-144-12-3387
Larsen H.D., Aarestrup F.M., Jensen N.E. 2002. Geographical variation in the presence of genes encoding superantigenic exotoxins and beta-hemolysin among Staphylococcus aureus isolated from bovine mastitis in Europe and USA. Vet. Microbiol., 85: 61-67. doi:10.1016/S0378-1135(01)00478-3
Letertre C., Perelle S., Dilasser F., Fach P. 2003. Identification of a new putative enterotoxin SEU encoded by the egc cluster of Staphylococcus aureus. J. Appl. Microbiol., 95: 38-43. doi:10.1046/j.1365-2672.2003.01957.x
Lina G., Piémont Y., Godail-Gamot F., Bes M., Peter M.O., Gauduchon V., Vandenesch F., Etienne J. 1999. Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin. Infect. Dis., 29: 1128-1132. doi:10.1086/313461
Luczak-Kadlubowska A., Krzyszton-Russjan J., Hryniewicz W. 2006. Characteristics of Staphylococcus aureus strains isolated in Poland in 1996 to 2004 that were deficient in species-specific proteins. J. Clin. Microbiol., 44: 4018-4024. doi:10.1128/JCM.01164-06
Nashev D., Toshkova K., Salasia S.I., Hassan A.A., Lämmler C., Zschöck M. 2004. Distribution of virulence genes of Staphylococcus aureus isolated from stable nasal carriers. FEMS Microbiol. Lett., 233: 45-52. doi:10.1016/j.femsle.2004.01.032
O’Riordan K., Lee J.C. 2004. Staphylococcus aureus capsular polysaccharides. Clin. Microbiol. Rev., 17: 218-234. doi:10.1128/CMR.17.1.218-234.2004
Okerman L., Devriese L.A., Maertens L., Okerman F., Godard C. 1984. Cutaneous staphylococcosis in rabbits. Vet. Rec., 114: 313-315. doi:10.1136/vr.114.13.313
Ote I., Taminiau B., Duprez J.N., Dizier I., Mainil J.G. 2011. Genotypic characterization by polymerase chain reaction of Staphylococcus aureus isolates associated with bovine mastitis. Vet. Microbiol., 153: 285-292. doi:10.1016/j.vetmic.2011.05.042
Peacock S.J., Moore C.E., Justice A., Kantzanou M., Story L., Mackie K., O’Neill G., Day N.P. 2002. Virulent combinations of adhesin and toxin genes in natural populations of Staphylococcus aureus. Infect. Immun., 70: 4987-4996. doi:10.1128/IAI.70.9.4987-4996.2002
Prevost G., Couppie P., Prevost P., Gayet S., Petiau P., Cribier B., Monteil H., Piemont Y. 1995. Epidemiological data on Staphylococcus aureus strains producing synergohymenotropic toxins. J. Med. Microbiol., 42: 237-245. doi:10.1099/00222615-42-4-237
Projan S.J., Novick R.P. 1997. The molecular basis of pathogenesis, In: Crossley, K.B., Archer, G.L. (ed). The staphylococci in human disease. Churchill Livingstone, New York.
Sabat A., Melles D.C., Martirosian G., Grundmann H., van Belkum A., Hryniewicz W. 2006. Distribution of the serine-aspartate repeat protein-encoding sdr genes among nasal-carriage and invasive Staphylococcus aureus strains. J. Clin. Microbiol., 44: 1135-1138. doi:10.1128/JCM.44.3.1135-1138.2006
Smyth D.S., Hartigan P.J., Meaney W.J., Fitzgerald J.R., Deobald C.F., Bohach G.A., Smyth C.J. 2005. Superantigen genes encoded by the egc cluster and SaPIbov are predominant among Staphylococcus aureus isolates from cows, goats, sheep, rabbits and poultry. J. Med. Microbiol., 54: 401-411. doi:10.1099/jmm.0.45863-0
Smyth D.S., Feil E.J., Meaney W.J., Hartigan P.J., Tollersrud T., Fitzgerald J.R., Enright M.C., Smyth C.J. 2009. Molecular genetic typing reveals further insights into the diversity of animal-associated Staphylococcus aureus. J. Med. Microbiol., 58: 1343-1353. doi:10.1099/jmm.0.009837-0
Strommenger B., Cuny C., Werner G., Witte W. 2004. Obvious lack of association between dynamics of epidemic methicillinresistant Staphylococcus aureus in central Europe and agr specificity groups. Eur. J. Clin. Microbiol. Infect. Dis., 23: 15-19. doi:10.1007/s10096-003-1046-8
Tristan A., Ying L., Bes M., Etienne J., Vandenesch F., Lina G. 2003. Use of multiplex PCR to identify Staphylococcus aureus adhesins involved in human hematogenous infections. J. Clin. Microbiol., 41: 4465-4467. doi:10.1128/JCM.41.9.4465-4467.2003
Trotonda M.P., Manna A.C., Cheung A.L., Lasa I., Penadés J.R. 2005. SarA positively controls bap-dependent biofilm formation in Staphylococcus aureus. J. Bacteriol., 187: 5790-5798. doi:10.1128/JB.187.16.5790-5798.2005
van Leeuwen W.B., Melles D.C., Alaidan A., Al-Ahdal M., Boelens H.A., Snijders S.V., Wertheim H., van Duijkeren E., Peeters J.K., van der Spek P.J., Gorkink R., Simons G., Verbrugh H.A., van Belkum A. 2005. Host- and tissue-specific pathogenic traits of Staphylococcus aureus. J. Bacteriol., 187: 4584-4591. doi:10.1128/JB.187.13.4584-4591.2005
Vancraeynest D., Hermans K., Haesebrouck F. 2004. Genotypic and phenotypic screening of high and low virulence Staphylococcus aureus isolates from rabbits for biofilm formation and MSCRAMMs. Vet. Microbiol., 103: 241-247.
doi:10.1016/j.vetmic.2004.09.002
Vancraeynest D., Haesebrouck F., Deplano A., Denis O., Godard C. Wildemauwe C., Hermans K. 2006. International dissemination of a high virulence rabbit Staphylococcus aureus clone. J. Vet. Med. B, 103: 241-247. doi:10.1111/j.1439-0450.2006.01025.x
Vautor E., Magnone V., Rios G., Le Brigand K., Bergonier D., Lina G., Meugnier H., Barbry P., Thiery R., Pepin M. 2009. Genetic differences among Staphylococcus aureus isolates from dairy ruminant species: a single-dye DNA microarray approach. Vet. Microbiol., 133: 105-114. doi:10.1016/j.vetmic.2008.06.006
Viana D., Selva L., Segura P., Penadés, J.R., Corpa J.M. 2007. Genotypic characterization of Staphylococcus aureus strains isolated from rabbit lesions. Vet. Microbiol., 121: 288-298. doi:10.1016/j.vetmic.2006.12.003
Viana D., Comos M., McAdam P.R., Ward M.J., Selva L., Guinane C.M., González-Muñoz B.M., Tristan A., Foster S.J., Fitzgerald J.R., Penadés J.R. 2015. A single natural nucleotide mutation alters bacterial pathogen host tropism. Nat. Genet., 47: 361-366. doi:10.1038/ng.3219
Wang S.C., Wu C.M., Xia S.C., Qi Y.H., Xia L.N., Shen J.Z. 2009. Distribution of superantigenic toxin genes in Staphylococcus aureus isolates from milk samples of bovine subclinical mastitis cases in two major diary production regions of China. Vet. Microbiol., 137: 276-281. doi:10.1016/j.vetmic.2009.01.007
Zecconi A., Cesaris L., Liandris E., Daprà V., Piccinini R. 2006. Role of several Staphylococcus aureus virulence factors on the inflammatory response in bovine mammary gland. Microb. Pathog., 40: 177-183. doi:10.1016/j.micpath.2006.01.001
Downloads
Published
Issue
Section
License
This journal is licensed under a "Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)".