Characterisation of Staphylococcus aureus strain causing severe respiratory disease in rabbits

Jinxiang Wang, Lei Sang, Yanfeng Chen, Shikun Sun, Dongjin Chen, Xiping Xie
DOI: https://doi.org/10.4995/wrs.2019.10454

Abstract

Staphylococcus aureus is acknowledged as one of the important pathogens isolated from humans and animals. However, the S. aureus causing severe respiratory diseases in rabbits have not been well characterised. A S. aureus named FZHW001, isolated from the lungs of dead rabbits with severe respiratory disease, was characterised by artificial infection of rabbits, detection of virulence factors, multi-locus sequencing typing and antimicrobial susceptibility test. The FZHW001 infected rabbits showed identical respiratory symptoms to those of naturally infected ones, and the isolate could spread through directed contact among rabbits. The isolate was typed into clonal complex 121 and carried 7 of 13 tested virulence factors. Furthermore, the isolate was identified to be methicillin-susceptible S. aureus and was susceptible to 7 of 12 tested antibiotics. This study first describes the characteristics of S. aureus isolated from rabbits causing severe respiratory disease, which will help in further understanding the pathogenic mechanisms of S. aureus in rabbits.

Keywords

Staphylococcus aureus; rabbit; respiratory disease; virulence factors; multi-locus sequencing typing

Full Text:

PDF

References

Angen O., Feld L., Larsen J., Rostgaard K., Skov R., Madsen A.M., Larsen A.R. 2017. Transmission of methicillin-resistant Staphylococcus aureus to human volunteers visiting a swine farm. Appl. Environ. Microbiol., 23:e01489-17. https://doi.org/10.1128/AEM.01489-17

Argudin M.A., Cariou N., Salandre O., Le Guennec J., Nemeghaire S., Butaye P. 2013. Genotyping and antimicrobial resistance of Staphylococcus aureus isolates from diseased turkeys. Avian Pathol., 6: 572-580. https://doi.org/10.1080/03079457.2013.854308.

Brady R.A., Mocca C.P., Plaut R.D., Takeda K., Burns D.L. 2018. Comparison of the immune response during acute and chronic Staphylococcus aureus infection. PLoS One, 3:e0195342. https://doi.org/10.1371/journal.pone.0195342

Brakstad O.G., Aasbakk K., Maeland J.A. 1992. Detection of Staphylococcus aureus by polymerase chain reaction amplification of the nuc gene. J. Clin. Microbiol., 7: 1654-1660.

CLSI (Clinical and Laboratory Standards Institute). 2013. Performance standards for antimicrobial susceptibility testing, twenty-second informational supplement, CLSI document M100-S22. Wayne, PA, USA.

Crowley E.J., King J.M., Wilkinson T., Worgan H.J., Huson K.M., Rose M.T., McEwan N.R. 2017. Comparison of the microbial population in rabbits and guinea pigs by next generation sequencing. PLoS One, 2: e0165779. https://doi.org/10.1371/journal.pone.0165779

Denayer S., Delbrassinne L., Nia Y., Botteldoorn N. 2017. Food-Borne outbreak investigation and molecular typing: high diversity of Staphylococcus aureus strains and importance of toxin detection. Toxins (Basel), 12: E407. https://doi.org/10.3390/toxins9120407

Doudoulakakis A., Spiliopoulou I., Spyridis N., Giormezis N., Kopsidas J., Militsopoulou M., Lebessi E., Tsolia M. 2017. Emergence of a Staphylococcus aureus clone resistant to mupirocin and fusidic acid carrying exotoxin genes and causing mainly skin infections. J. Clin. Microbiol., 8: 2529-2537. https://doi.org/10.1128/JCM.00406-17

Edwards A.M., Potts J.R., Josefsson E., Massey R.C. 2010. Staphylococcus aureus host cell invasion and virulence in sepsis is facilitated by the multiple repeats within FnBPA. PLoS Pathog., 6: e1000964. https://doi.org/10.1371/journal.ppat.1000964

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., 3: 1008-1015.

Gomez-Sanz E., Torres C., Ceballos S., Lozano C., Zarazaga M. 2013. Clonal dynamics of nasal Staphylococcus aureus and Staphylococcus pseudintermedius in dog-owning household members. Detection of MSSA ST(398). PLoS One, 7: e69337. https://doi.org/10.1371/journal.pone.0069337

Haenni M., Chatre P., Dupieux-Chabert C., Metayer V., Bes M., Madec J.Y., Laurent F. 2017. Molecular epidemiology of methicillin-resistant Staphylococcus aureus in horses, cats, and dogs over a 5-year period in france. Front. Microbiol., 8: 2493.

https://doi.org/10.3389/fmicb.2017.02493

Hecker M., Mader U., Volker U. 2018. From the genome sequence via the proteome to cell physiology - pathoproteomics and pathophysiology of Staphylococcus aureus. Int. J. Med. Microbiol., 308: 545-557. https://doi.org/10.1016/j.ijmm.2018.01.002

Hermans K., Devriese L.A., Haesebrouck F. 2003. Rabbit staphylococcosis: difficult solutions for serious problems. Vet. Microbiol., 1: 57-64. https://doi.org/10.1016/S0378-1135(02)00260-2

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., 2: 631-641. https://doi.org/10.1128/IAI.70.2.631-641.2002

Kurt K., Rasigade J.P., Laurent F., Goering R.V., Zemlickova H., Machova I., Struelens M.J., Zautner A.E., Holtfreter S., Broker B., Ritchie S., Reaksmey S., Limmathurotaskul D., Peacock S.J., Cuny C., Layer F., Witte W., Nubel U. 2013. Subpopulations of Staphylococcus aureus clonal complex 121 are associated with distinct clinical entities. PLoS One., 3:

e58155. https://doi.org/10.1371/journal.pone.0058155

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. https://doi.org/10.1086/313461

Merz A., Stephan R., Johler S. 2016. Genotyping and DNA microarray based characterization of Staphylococcus aureus isolates from rabbit carcasses. Meat Sci., 112: 86-89. https://doi.org/10.1016/j.meatsci.2015.11.002

Moreno-Grúa E., Pérez-Fuentes S., Muñoz-Silvestre A., Viana D., Fernández-Ros A., Sanz-Tejero C., Corpa J., Selva L. 2018. Characterization of livestock-associated methicillin-resistant Staphylococcus aureus isolates obtained from commercial rabbitries located in the Iberian Peninsula. Front. Microbiol., 9: 1812. https://doi.org/10.3389/fmicb.2018.01812

Murakami K., Minamide W., Wada K., Nakamura E., Teraoka H., Watanabe S. 1991. Identification of methicillin-resistant strains of staphylococci by polymerase chain reaction. J. Clin. Microbiol., 10: 2240-2244.

Paterson G.K., Larsen A.R., Robb A., Edwards G.E., Pennycott T.W., Foster G., Mot D., Hermans K., Baert K., Peacock S.J., Parkhill J., Zadoks R.N., Holmes M.A. 2012. The newly described mecA homologue, mecALGA251, is present in methicillinresistant Staphylococcus aureus isolates from a diverse range of host species. J. Antimicrob. Chemother., 67: 2809-2813. https://doi.org/10.1093/jac/dks329

Que Y.A., Haefliger J.A., Piroth L., Francois P., Widmer E., Entenza J.M., Sinha B., Herrmann M., Francioli P., Vaudaux P., Moreillon P. 2005. Fibrinogen and fibronectin binding cooperate for valve infection and invasion in Staphylococcus aureus experimental endocarditis. J. Exp. Med., 10: 1627-1635. https://doi.org/10.1084/jem.20050125

Robinson D.A., Enright M.C. 2004. Multilocus sequence typing and the evolution of methicillin-resistant Staphylococcus aureus. Clin. Microbiol. Infect., 2: 92-97. https://doi.org/10.1111/j.1469-0691.2004.00768.x

Sato T., Usui M., Konishi N., Kai A., Matsui H., Hanaki H., Tamura Y. 2017. Closely related methicillin-resistant Staphylococcus aureus isolates from retail meat, cows with mastitis, and humans in Japan. PLoS One, 10: e0187319. https://doi.org/10.1371/journal.pone.0187319

Schmidt T., Kock M.M., Ehlers M.M. 2017. Molecular Characterization of Staphylococcus aureus isolated from bovine mastitis and close human contacts in South African dairy herds: genetic diversity and interspecies

host transmission. Front. Microbiol., 8: 511. https://doi.org/10.3389/fmicb.2017.00511

Sicot N., Khanafer N., Meyssonnier V., Dumitrescu O., Tristan A., Bes M., Lina G., Vandenesch F., Vanhems P., Etienne J., Gillet Y. 2013. Methicillin resistance is not a predictor of severity in community acquired Staphylococcus aureus necrotizing pneumonia-results of a prospective

observational study. Clin. Microbiol. Infect., 19: E142-148. https://doi.org/10.1111/1469-0691.12022

Srinivasan V., Sawant A.A., Gillespie B.E., Headrick S.J., Ceasaris L., Oliver S.P. 2006. Prevalence of enterotoxin and toxic shock syndrome toxin genes in Staphylococcus aureus isolated from milk of cows with mastitis. Foodborne Pathog. Dis., 3: 274-283. https://doi.org/10.1089/fpd.2006.3.274

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., 9: 418-422. https://doi.org/10.1111/j.1439-0450.2006.00977.x

Verkade E., Kluytmans J. 2014. Livestock-associated Staphylococcus aureus CC398: animal reservoirs and human infections. Infect. Genet. Evol., 21: 523-530. https://doi.org/10.1016/j.meegid.2013.02.013

Viana D., Selva L., Penadés M., Corpa J.M. 2015. Screening of virulence genes in Staphylococcus aureus isolates from rabbits. World Rabbit Sci., 23: 185-195. https://doi.org/10.4995/wrs.2015.3961

Weisburg W.G., Barns S.M., Pelletier D.A., Lane D.J. 1991. 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol., 2: 697-703. https://doi.org/10.1128/jb.173.2.697-703.1991

Xie Y., He Y., Gehring A, Hu Y, Li Q., Tu SI., Shi X. 2011. Genotypes and toxin gene profiles of Staphylococcus aureus clinical isolates from China. PLoS One, 12: e28276. https://doi.org/10.1371/journal.pone.0028276

Abstract Views

896
Metrics Loading ...

Metrics powered by PLOS ALM


Bookmark and Share

 

Cited-By (articles included in Crossref)

This journal is a Crossref Cited-by Linking member. This list shows the references that citing the article automatically, if there are. For more information about the system please visit Crossref site

1. Staphylococcus aureus in Agriculture: Lessons in Evolution from a Multispecies Pathogen
Soyoun Park, Jennifer Ronholm
Clinical Microbiology Reviews  vol: 34  issue: 2  year: 2021  
doi: 10.1128/CMR.00182-20



 

 Universitat Politècnica de València

 

Official journal of the World Rabbit Science Association (WRSA)

 

e-ISSN: 1989-8886     ISSN: 1257-5011   https://doi.org/10.4995/wrs