Analyze Diet
Antibiotics (Basel, Switzerland)2025; 14(11); 1082; doi: 10.3390/antibiotics14111082

Characterization of Staphylococcus aureus CC1 and CC1660 of Human and Equine Origin.

Abstract: : isolates from humans and horses of the equine-associated clonal complexes (CCs) CC1 and CC1660 were comparatively investigated for their genomic relationships. : A total of 91 isolates (64 human, 27 equine) were subjected to whole-genome sequencing (WGS), sequence analysis, and antimicrobial susceptibility testing. : WGS confirmed 75 CC1 and 16 CC1660 isolates, comprising nine sequence types (STs) in CC1 and four STs in CC1660. Ten types were present in CC1 and five in CC1660. In the gene of three CC1 isolates, a 285 bp deletion was detected, and a nucleotide deletion causing a premature stop codon was found in one CC1660 isolate. Core genome (cg) MLST revealed a minimum difference of 1398/1492 alleles between the two CCs. All CC1 isolates harbored group III and capsule type 8 alleles, whereas all CC1660 isolates had group II and capsule type 5 alleles. Antimicrobial susceptibility testing revealed 18 phenotypic and 19 genotypic resistance patterns. All isolates were susceptible to vancomycin, linezolid and quinupristin-dalfopristin. Several virulence genes were detected in different combinations. The equine leukocidin genes were found in 22 isolates from horses and 38 isolates from humans, of which 35 had confirmed contact with horses. No Panton-Valentine leukocidin genes were found. Three human CC1660 isolates carried the toxic shock syndrome toxin-1 gene . : The analysis of the 91 isolates might suggest intra- and interspecies transmission among and between humans and horses, which should be monitored in the future.
Publication Date: 2025-10-27 PubMed ID: 41301578PubMed Central: PMC12649262DOI: 10.3390/antibiotics14111082Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

Overview

  • This study compares the genetic characteristics and antimicrobial resistance of Staphylococcus aureus clonal complexes CC1 and CC1660 isolated from humans and horses.
  • The research investigates the genomic relationships between human- and equine-associated strains to understand potential transmission and differences in virulence and resistance.

Background and Objectives

  • Staphylococcus aureus is a bacterium that can infect both humans and animals, including horses.
  • The study focuses on two specific clonal complexes (CC1 and CC1660) of S. aureus that are associated with horses.
  • The goal was to compare the isolates collected from humans and horses to see how genetically related they are and to study their antibiotic resistance and virulence properties.

Methods

  • A total of 91 S. aureus isolates were collected: 64 from humans and 27 from horses.
  • Whole-genome sequencing (WGS) was performed to analyze the genetic material of these isolates.
  • Sequence typing identified nine different sequence types within CC1 and four within CC1660.
  • Antimicrobial susceptibility testing was conducted to determine which antibiotics the bacteria were resistant or susceptible to.
  • Analysis included looking at specific genes related to virulence (ability to cause disease) and resistance to antibiotics.

Key Findings: Genomic Relationships

  • WGS confirmed 75 isolates belonged to CC1 and 16 to CC1660.
  • The allele difference (genetic variation) between CC1 and CC1660 was large, indicating clear genetic distinction between these complexes.
  • Different groups (allotypes) of genes related to capsule formation and immune evasion were found:
    • All CC1 isolates had group III immune evasion genes and capsule type 8 alleles.
    • All CC1660 isolates had group II immune evasion genes and capsule type 5 alleles.
  • Specific deletions and mutations were detected in some isolates’ immune evasion genes, potentially affecting their function.

Antimicrobial Resistance Patterns

  • Antimicrobial susceptibility testing revealed 18 different phenotypic resistance patterns and 19 genotypic resistance patterns among the isolates.
  • All isolates remained susceptible to vancomycin, linezolid, and quinupristin-dalfopristin, which are important antibiotics for treating resistant infections.
  • This information highlights which antibiotics may still be effective against these S. aureus strains.

Virulence Factors and Transmission Insights

  • Several virulence genes were detected in various combinations across isolates.
  • Equine leukocidin genes (toxins potentially involved in infection severity) were found in 22 horse isolates and 38 human isolates.
  • Among the human isolates with equine leukocidin genes, 35 had confirmed contact with horses, suggesting possible cross-species transmission.
  • No Panton-Valentine leukocidin (PVL) genes, commonly associated with severe human infections, were detected.
  • Three human CC1660 isolates carried the toxic shock syndrome toxin-1 gene, indicating potential for severe toxin-mediated disease.

Conclusions and Implications

  • The study supports the idea that S. aureus strains from horses and humans, particularly those with contact to horses, might be exchanged between species (intra- and interspecies transmission).
  • Monitoring of such transmissions is important for infection control in both human and veterinary medicine.
  • Understanding the genetic differences and resistance profiles can better inform treatment strategies and prevent the spread of resistant or particularly virulent strains.

Cite This Article

APA
(2025). Characterization of Staphylococcus aureus CC1 and CC1660 of Human and Equine Origin. Antibiotics (Basel), 14(11), 1082. https://doi.org/10.3390/antibiotics14111082

Publication

ISSN: 2079-6382
NlmUniqueID: 101637404
Country: Switzerland
Language: English
Volume: 14
Issue: 11
PII: 1082

Researcher Affiliations

Conflict of Interest Statement

The authors declare no conflicts of interest.

References

This article includes 76 references
  1. Rasquel-Oliveira FS, Ribeiro JM, Martelossi-Cebinelli G, Costa FB, Nakazato G, Casagrande R, Verri WA. Staphylococcus aureus in Inflammation and Pain: Update on Pathologic Mechanisms. Pathogens 2025;14:185.
    doi: 10.3390/pathogens14020185pmc: PMC11858194pubmed: 40005560google scholar: lookup
  2. Holmes MA, Zadoks RN. Methicillin resistant S. aureus in human and bovine mastitis. J. Mammary Gland Biol. Neoplasia 2011;16:373–382.
    doi: 10.1007/s10911-011-9237-xpubmed: 21984431google scholar: lookup
  3. Cuny C, Friedrich A, Kozytska S, Layer F, Nübel U, Ohlsen K, Strommenger B, Walther B, Wieler L, Witte W. Emergence of methicillin-resistant Staphylococcus aureus (MRSA) in different animal species. Int. J. Med. Microbiol. 2010;300:109–117.
    doi: 10.1016/j.ijmm.2009.11.002pubmed: 20005777google scholar: lookup
  4. Marshall K, Marsella R. Evolution of the Prevalence of Antibiotic Resistance to Staphylococcus spp. Isolated from Horses in Florida over a 10-Year Period. Vet. Sci. 2023;10:71.
    doi: 10.3390/vetsci10020071pmc: PMC9959586pubmed: 36851375google scholar: lookup
  5. Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J. Clin. Microbiol. 2000;38:1008–1015.
  6. Feil EJ, Cooper JE, Grundmann H, Robinson DA, Enright MC, Berendt T, Peacock SJ, Smith JM, Murphy M, Spratt BG. How clonal is Staphylococcus aureus?. J. Bacteriol. 2003;185:3307–3316.
  7. Lindsay JA, Moore CE, Day NP, Peacock SJ, Witney AA, Stabler RA, Husain SE, Butcher PD, Hinds J. Microarrays reveal that each of the ten dominant lineages of Staphylococcus aureus has a unique combination of surface-associated and regulatory genes. J. Bacteriol. 2006;188:669–676.
  8. Jolley K, Bray J, Maiden M. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res. 2018;3:124.
  9. Monecke S, Luedicke C, Slickers P, Ehricht R. Molecular epidemiology of Staphylococcus aureus in asymptomatic carriers. Eur. J. Clin. Microbiol. Infect. Dis. 2009;28:1159–1165.
    doi: 10.1007/s10096-009-0752-2pubmed: 19434432google scholar: lookup
  10. Holtfreter S, Grumann D, Balau V, Barwich A, Kolata J, Goehler A, Weiss S, Holtfreter B, Bauerfeind SS, Döring P. Molecular Epidemiology of Staphylococcus aureus in the General Population in Northeast Germany: Results of the Study of Health in Pomerania (SHIP-TREND-0). J. Clin. Microbiol. 2016;54:2774–2785.
    doi: 10.1128/JCM.00312-16pmc: PMC5078557pubmed: 27605711google scholar: lookup
  11. Rao Q, Shang W, Hu X, Rao X. Staphylococcus aureus ST121: A globally disseminated hypervirulent clone. J. Med. Microbiol. 2015;64:1462–1473.
    doi: 10.1099/jmm.0.000185pubmed: 26445995google scholar: lookup
  12. Monecke S, Feßler AT, Burgold-Voigt S, Krüger H, Mühldorfer K, Wibbelt G, Liebler-Tenorio EM, Reinicke M, Braun SD, Hanke D. Staphylococcus aureus isolates from Eurasian Beavers (Castor fiber) carry a novel phage-borne bicomponent leukocidin related to the Panton-Valentine leukocidin. Sci. Rep. 2021;11:24394.
    doi: 10.1038/s41598-021-03823-6pmc: PMC8695587pubmed: 34937862google scholar: lookup
  13. Moon DC, Kim BY, Tamang MD, Nam HM, Jang GC, Jung SC, Lee HS, Park YH, Lim SK. Genome Sequence of a Unique t2247-ST692-III Livestock-Associated Methicillin-Resistant Staphylococcus aureus Strain from Chicken Carcass. Genome Announc. 2016;4:e00026-16.
    doi: 10.1128/genomeA.00026-16pmc: PMC4767913pubmed: 26950323google scholar: lookup
  14. Monecke S, Gavier-Widén D, Hotzel H, Peters M, Guenther S, Lazaris A, Loncaric I, Müller E, Reissig A, Ruppelt-Lorz A. Diversity of Staphylococcus aureus Isolates in European Wildlife. PLoS ONE 2016;11:e0168433.
  15. García-Álvarez L, Holden MT, Lindsay H, Webb CR, Brown DF, Curran MD, Walpole E, Brooks K, Pickard DJ, Teale C. Meticillin-resistant Staphylococcus aureus with a novel mecA homologue in human and bovine populations in the UK and Denmark: A descriptive study. Lancet Infect. Dis. 2011;11:595–603.
  16. Vancraeynest D., Haesebrouck F., Deplano A., Denis O., Godard C., Wildemauwe C., Hermans K. International dissemination of a high virulence rabbit Staphylococcus aureus clone. J. Vet. Med. B Infect. Dis. Vet. Public Health. 2006;53:418–422. doi: 10.1111/j.1439-0450.2006.00977.x.
  17. Burgold-Voigt S., Monecke S., Busch A., Bocklisch H., Braun S.D., Diezel C., Hotzel H., Liebler-Tenorio E.M., Müller E., Reinicke M., et al. Characterisation of a Staphylococcus aureus Isolate Carrying Phage-Borne Enterotoxin E from a European Badger (Meles meles) Pathogens. 2023;12:704. doi: 10.3390/pathogens12050704.
    doi: 10.3390/pathogens12050704pmc: PMC10220527pubmed: 37242375google scholar: lookup
  18. Bar-Gal G.K., Blum S.E., Hadas L., Ehricht R., Monecke S., Leitner G. Host-specificity of Staphylococcus aureus causing intramammary infections in dairy animals assessed by genotyping and virulence genes. Vet. Microbiol. 2015;176:143–154. doi: 10.1016/j.vetmic.2015.01.007.
    doi: 10.1016/j.vetmic.2015.01.007pubmed: 25631254google scholar: lookup
  19. Smyth D.S., Feil E.J., Meaney W.J., Hartigan P.J., Tollersrud T., Fitzgerald J.R., Enright M.C., Smyth C.J. Molecular genetic typing reveals further insights into the diversity of animal-associated Staphylococcus aureus. J. Med. Microbiol. 2009;58:1343–1353. doi: 10.1099/jmm.0.009837-0.
    doi: 10.1099/jmm.0.009837-0pubmed: 19528163google scholar: lookup
  20. Schlotter K., Ehricht R., Hotzel H., Monecke S., Pfeffer M., Donat K. Leukocidin genes lukF-P83 and lukM are associated with Staphylococcus aureus clonal complexes 151, 479 and 133 isolated from bovine udder infections in Thuringia, Germany. Vet. Res. 2012;43:42. doi: 10.1186/1297-9716-43-42.
    doi: 10.1186/1297-9716-43-42pmc: PMC3416645pubmed: 22587484google scholar: lookup
  21. Richardson E.J., Bacigalupe R., Harrison E.M., Weinert L.A., Lycett S., Vrieling M., Robb K., Hoskisson P.A., Holden M.T.G., Feil E.J., et al. Gene exchange drives the ecological success of a multi-host bacterial pathogen. Nat. Ecol. Evol. 2018;2:1468–1478. doi: 10.1038/s41559-018-0617-0.
    doi: 10.1038/s41559-018-0617-0pmc: PMC7610605pubmed: 30038246google scholar: lookup
  22. Voss A., Loeffen F., Bakker J., Klaassen C., Wulf M. Methicillin-resistant Staphylococcus aureus in pig farming. Emerg. Infect. Dis. 2005;11:1965–1966. doi: 10.3201/eid1112.050428.
    doi: 10.3201/eid1112.050428pmc: PMC3367632pubmed: 16485492google scholar: lookup
  23. Monecke S., Kuhnert P., Hotzel H., Slickers P., Ehricht R. Microarray based study on virulence-associated genes and resistance determinants of Staphylococcus aureus isolates from cattle. Vet. Microbiol. 2007;125:128–140. doi: 10.1016/j.vetmic.2007.05.016.
    doi: 10.1016/j.vetmic.2007.05.016pubmed: 17614219google scholar: lookup
  24. Witte W., Strommenger B., Stanek C., Cuny C. Methicillin-resistant Staphylococcus aureus ST398 in humans and animals, Central Europe. Emerg. Infect. Dis. 2007;13:255–258. doi: 10.3201/eid1302.060924.
    doi: 10.3201/eid1302.060924pmc: PMC2725865pubmed: 17479888google scholar: lookup
  25. Nemati M., Hermans K., Lipinska U., Denis O., Deplano A., Struelens M., Devriese L.A., Pasmans F., Haesebrouck F. Antimicrobial resistance of old and recent Staphylococcus aureus isolates from poultry: First detection of livestock-associated methicillin-resistant strain ST398. Antimicrob. Agents Chemother. 2008;52:3817–3819. doi: 10.1128/AAC.00613-08.
    doi: 10.1128/AAC.00613-08pmc: PMC2565892pubmed: 18663024google scholar: lookup
  26. Cuny C., Abdelbary M.M.H., Köck R., Layer F., Scheidemann W., Werner G., Witte W. Methicillin-resistant Staphylococcus aureus from infections in horses in Germany are frequent colonizers of veterinarians but rare among MRSA from infections in humans. One Health. 2016;2:11–17. doi: 10.1016/j.onehlt.2015.11.004.
  27. Murphy R.J.T., Ramsay J.P., Lee Y.T., Pang S., O’Dea M.A., Pearson J.C., Axon J.E., Raby E., Abdulgader S.M., Whitelaw A., et al. Multiple introductions of methicillin-resistant Staphylococcus aureus ST612 into Western Australia associated both with human and equine reservoirs. Int. J. Antimicrob. Agents. 2019;54:681–685. doi: 10.1016/j.ijantimicag.2019.08.022.
  28. Cuny C., Witte W. MRSA in equine hospitals and its significance for infections in humans. Vet. Microbiol. 2017;200:59–64. doi: 10.1016/j.vetmic.2016.01.013.
    doi: 10.1016/j.vetmic.2016.01.013pubmed: 26869097google scholar: lookup
  29. Albrecht N., Jatzwauk L., Slickers P., Ehricht R., Monecke S. Clonal replacement of epidemic methicillin-resistant Staphylococcus aureus strains in a German university hospital over a period of eleven years. PLoS ONE. 2011;6:e28189. doi: 10.1371/journal.pone.0028189.
  30. Merz A., Stephan R., Johler S. Staphylococcus aureus Isolates from Goat and Sheep Milk Seem to Be Closely Related and Differ from Isolates Detected from Bovine Milk. Front. Microbiol. 2016;7:319. doi: 10.3389/fmicb.2016.00319.
    doi: 10.3389/fmicb.2016.00319pmc: PMC4789554pubmed: 27014240google scholar: lookup
  31. Azara E., Piras M.G., Parisi A., Tola S. Antimicrobial susceptibility and genotyping of Staphylococcus aureus isolates collected between 1986 and 2015 from ovine mastitis. Vet. Microbiol. 2017;205:53–56. doi: 10.1016/j.vetmic.2017.05.006.
    doi: 10.1016/j.vetmic.2017.05.006pubmed: 28622861google scholar: lookup
  32. Carfora V., Giacinti G., Sagrafoli D., Marri N., Giangolini G., Alba P., Feltrin F., Sorbara L., Amoruso R., Caprioli A., et al. Methicillin-resistant and methicillin-susceptible Staphylococcus aureus in dairy sheep and in-contact humans: An intra-farm study. J. Dairy Sci. 2016;99:4251–4258. doi: 10.3168/jds.2016-10912.
    doi: 10.3168/jds.2016-10912pubmed: 27060817google scholar: lookup
  33. Monecke S., Burgold-Voigt S., Feßler A.T., Krapf M., Loncaric I., Liebler-Tenorio E.M., Braun S.D., Diezel C., Müller E., Reinicke M., et al. Characterisation of Staphylococcus aureus Strains and Their Prophages That Carry Horse-Specific Leukocidin Genes lukP/Q. Toxins. 2025;17:20. doi: 10.3390/toxins17010020.
    doi: 10.3390/toxins17010020pmc: PMC11769447pubmed: 39852974google scholar: lookup
  34. Sieber S., Gerber V., Jandova V., Rossano A., Evison J.M., Perreten V. Evolution of multidrug-resistant Staphylococcus aureus infections in horses and colonized personnel in an equine clinic between 2005 and 2010. Microb. Drug Resist. 2011;17:471–478. doi: 10.1089/mdr.2010.0188.
    doi: 10.1089/mdr.2010.0188pubmed: 21875361google scholar: lookup
  35. Islam M.Z., Espinosa-Gongora C., Damborg P., Sieber R.N., Munk R., Husted L., Moodley A., Skov R., Larsen J., Guardabassi L. Horses in Denmark Are a Reservoir of Diverse Clones of Methicillin-Resistant and -Susceptible Staphylococcus aureus. Front. Microbiol. 2017;8:543. doi: 10.3389/fmicb.2017.00543.
    doi: 10.3389/fmicb.2017.00543pmc: PMC5376617pubmed: 28421046google scholar: lookup
  36. Sung J.M., Lloyd D.H., Lindsay J.A. Staphylococcus aureus host specificity: Comparative genomics of human versus animal isolates by multi-strain microarray. Microbiology. 2008;154:1949–1959. doi: 10.1099/mic.0.2007/015289-0.
    doi: 10.1099/mic.0.2007/015289-0pubmed: 18599823google scholar: lookup
  37. Monecke S., Coombs G., Shore A.C., Coleman D.C., Akpaka P., Borg M., Chow H., Ip M., Jatzwauk L., Jonas D., et al. A field guide to pandemic, epidemic and sporadic clones of methicillin-resistant Staphylococcus aureus. PLoS ONE. 2011;6:e17936. doi: 10.1371/journal.pone.0017936.
  38. Lawal O.U., Ayobami O., Abouelfetouh A., Mourabit N., Kaba M., Egyir B., Abdulgader S.M., Shittu A.O. A 6-Year Update on the Diversity of Methicillin-Resistant Staphylococcus aureus Clones in Africa: A Systematic Review. Front. Microbiol. 2022;13:860436. doi: 10.3389/fmicb.2022.860436.
    doi: 10.3389/fmicb.2022.860436pmc: PMC9113548pubmed: 35591993google scholar: lookup
  39. Williamson D.A., Monecke S., Heffernan H., Ritchie S.R., Roberts S.A., Upton A., Thomas M.G., Fraser J.D. High usage of topical fusidic acid and rapid clonal expansion of fusidic acid-resistant Staphylococcus aureus: A cautionary tale. Clin. Infect. Dis. 2014;59:1451–1454. doi: 10.1093/cid/ciu658.
    doi: 10.1093/cid/ciu658pubmed: 25139961google scholar: lookup
  40. Alba P., Feltrin F., Cordaro G., Porrero M.C., Kraushaar B., Argudín M.A., Nykäsenoja S., Monaco M., Stegger M., Aarestrup F.M., et al. Livestock-Associated Methicillin Resistant and Methicillin Susceptible Staphylococcus aureus Sequence Type (CC)1 in European Farmed Animals: High Genetic Relatedness of Isolates from Italian Cattle Herds and Humans. PLoS ONE. 2015;10:e0137143. doi: 10.1371/journal.pone.0137143.
  41. Leopold S.R., Goering R.V., Witten A., Harmsen D., Mellmann A. Bacterial whole-genome sequencing revisited: Portable, scalable, and standardized analysis for typing and detection of virulence and antibiotic resistance genes. J. Clin. Microbiol. 2014;52:2365–2370. doi: 10.1128/JCM.00262-14.
    doi: 10.1128/JCM.00262-14pmc: PMC4097726pubmed: 24759713google scholar: lookup
  42. Cunningham S.A., Chia N., Jeraldo P.R., Quest D.J., Johnson J.A., Boxrud D.J., Taylor A.J., Chen J., Jenkins G.D., Drucker T.M., et al. Comparison of Whole-Genome Sequencing Methods for Analysis of Three Methicillin-Resistant Staphylococcus aureus Outbreaks. J. Clin. Microbiol. 2017;55:1946–1953. doi: 10.1128/JCM.00029-17.
    doi: 10.1128/JCM.00029-17pmc: PMC5442552pubmed: 28404677google scholar: lookup
  43. Graveland H., Wagenaar J.A., Bergs K., Heesterbeek H., Heederik D. Persistence of livestock associated MRSA CC398 in humans is dependent on intensity of animal contact. PLoS ONE. 2011;6:e16830. doi: 10.1371/journal.pone.0016830.
  44. Ramón-Maiques S., Marina A., Guinot A., Gil-Ortiz F., Uriarte M., Fita I., Rubio V. Substrate binding and catalysis in carbamate kinase ascertained by crystallographic and site-directed mutagenesis studies: Movements and significance of a unique globular subdomain of this key enzyme for fermentative ATP production in bacteria. J. Mol. Biol. 2010;397:1261–1275. doi: 10.1016/j.jmb.2010.02.038.
    doi: 10.1016/j.jmb.2010.02.038pubmed: 20188742google scholar: lookup
  45. Zhang L., Thomas J.C., Didelot X., Robinson D.A. Molecular signatures identify a candidate target of balancing selection in an arcD-like gene of Staphylococcus epidermidis. J. Mol. Evol. 2012;75:43–54. doi: 10.1007/s00239-012-9520-5.
    doi: 10.1007/s00239-012-9520-5pmc: PMC3493253pubmed: 23053194google scholar: lookup
  46. Lodder G., Werckenthin C., Schwarz S., Dyke K. Molecular analysis of naturally occuring ermC-encoding plasmids in staphylococci isolated from animals with and without previous contact with macrolide/lincosamide antibiotics. FEMS Immunol. Med. Microbiol. 1997;18:7–15. doi: 10.1111/j.1574-695X.1997.tb01022.x.
  47. EMA (European Medicines Agency) Categorisation of Antibiotics in the European Union. EMA; Amsterdam, The Netherlands: 2019.
  48. CLSI . Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals. 7th ed. Clinical and Laboratory Standards Institute; Wayne, PA, USA: 2024. CLSI Supplement VET01S.
  49. CLSI . Performance Standards for Antimicrobial Susceptibility Testing. 35th ed. Clinical and Laboratory Standards Institute; Wayne, PA, USA: 2025. CLSI Supplement M100.
  50. Guignard B., Entenza J.M., Moreillon P. Beta-lactams against methicillin-resistant Staphylococcus aureus. Curr. Opin. Pharmacol. 2005;5:479–489. doi: 10.1016/j.coph.2005.06.002.
    doi: 10.1016/j.coph.2005.06.002pubmed: 16095969google scholar: lookup
  51. Scholtzek A.D., Hanke D., Walther B., Eichhorn I., Stöckle S.D., Klein K.S., Gehlen H., Lübke-Becker A., Schwarz S., Feßler A.T. Molecular Characterization of Equine Staphylococcus aureus Isolates Exhibiting Reduced Oxacillin Susceptibility. Toxins. 2019;11:535. doi: 10.3390/toxins11090535.
    doi: 10.3390/toxins11090535pmc: PMC6783909pubmed: 31540335google scholar: lookup
  52. Feßler A., Scott C., Kadlec K., Ehricht R., Monecke S., Schwarz S. Characterization of methicillin-resistant Staphylococcus aureus ST398 from cases of bovine mastitis. J. Antimicrob. Chemother. 2010;65:619–625. doi: 10.1093/jac/dkq021.
    doi: 10.1093/jac/dkq021pubmed: 20164198google scholar: lookup
  53. Brennan G.I., Abbott Y., Burns A., Leonard F., McManus B.A., O’Connell B., Coleman D.C., Shore A.C. The Emergence and Spread of Multiple Livestock-Associated Clonal Complex 398 Methicillin-Resistant and Methicillin-Susceptible Staphylococcus aureus Strains among Animals and Humans in the Republic of Ireland, 2010–2014. PLoS ONE. 2016;11:e0149396. doi: 10.1371/journal.pone.0149396.
  54. Scholtzek A.D., Hanke D., Eichhorn I., Walther B., Lübke-Becker A., van Duijkeren E., Köck R., Schwarz S., Feßler A.T. Heterogeneity of antimicrobial susceptibility testing results for sulfamethoxazole/trimethoprim obtained from clinical equine Staphylococcus aureus isolates using different methods. Vet. Microbiol. 2020;242:108600. doi: 10.1016/j.vetmic.2020.108600.
    doi: 10.1016/j.vetmic.2020.108600pubmed: 32122605google scholar: lookup
  55. Kehrenberg C., Schwarz S. fexA, a novel Staphylococcus lentus gene encoding resistance to florfenicol and chloramphenicol. Antimicrob. Agents Chemother. 2004;48:615–618. doi: 10.1128/AAC.48.2.615-618.2004.
  56. Goering R.V., Morrison D., Al-Doori Z., Edwards G.F., Gemmell C.G. Usefulness of mec-associated direct repeat unit (dru) typing in the epidemiological analysis of highly clonal methicillin-resistant Staphylococcus aureus in Scotland. Clin. Microbiol. Infect. 2008;14:964–969. doi: 10.1111/j.1469-0691.2008.02073.x.
  57. Monecke S., König E., Earls M.R., Leitner E., Müller E., Wagner G.E., Poitz D.M., Jatzwauk L., Vremerǎ T., Dorneanu O.S., et al. An epidemic CC1-MRSA-IV clone yields false-negative test results in molecular MRSA identification assays: A note of caution, Austria, Germany, Ireland, 2020. Euro Surveill. 2020;25:2000929. doi: 10.2807/1560-7917.ES.2020.25.25.2000929.
  58. Cuny C., Strommenger B., Witte W., Stanek C. Clusters of infections in horses with MRSA ST1, ST254, and ST398 in a veterinary hospital. Microb. Drug Resist. 2008;14:307–310. doi: 10.1089/mdr.2008.0845.
    doi: 10.1089/mdr.2008.0845pubmed: 19025385google scholar: lookup
  59. Wick R.R., Judd L.M., Gorrie C.L., Holt K.E. Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput. Biol. 2017;13:e1005595. doi: 10.1371/journal.pcbi.1005595.
  60. Prjibelski A., Antipov D., Meleshko D., Lapidus A., Korobeynikov A. Using SPAdes De Novo Assembler. Curr. Protoc. Bioinform. 2020;70:e102. doi: 10.1002/cpbi.102.
    doi: 10.1002/cpbi.102pubmed: 32559359google scholar: lookup
  61. Seemann T. mlst. Github. [(accessed on 1 September 2025)]. Available online: https://github.com/tseemann/mlst.
  62. Bartels M.D., Petersen A., Worning P., Nielsen J.B., Larner-Svensson H., Johansen H.K., Andersen L.P., Jarløv J.O., Boye K., Larsen A.R., et al. Comparing whole-genome sequencing with Sanger sequencing for spa typing of methicillin-resistant Staphylococcus aureus. J. Clin. Microbiol. 2014;52:4305–4308. doi: 10.1128/JCM.01979-14.
    doi: 10.1128/JCM.01979-14pmc: PMC4313303pubmed: 25297335google scholar: lookup
  63. Silva M., Machado M.P., Silva D.N., Rossi M., Moran-Gilad J., Santos S., Ramirez M., Carriço J.A. chewBBACA: A complete suite for gene-by-gene schema creation and strain identification. Microb. Genom. 2018;4:e000166. doi: 10.1099/mgen.0.000166.
    doi: 10.1099/mgen.0.000166pmc: PMC5885018pubmed: 29543149google scholar: lookup
  64. Zhou Z., Alikhan N.F., Sergeant M.J., Luhmann N., Vaz C., Francisco A.P., Carriço J.A., Achtman M. GrapeTree: Visualization of core genomic relationships among 100,000 bacterial pathogens. Genome Res. 2018;28:1395–1404. doi: 10.1101/gr.232397.117.
    doi: 10.1101/gr.232397.117pmc: PMC6120633pubmed: 30049790google scholar: lookup
  65. CLSI . Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals. 6th ed. Clinical and Laboratory Standards Institute; Wayne, PA, USA: 2024. CLSI Standard VET01.
  66. BVL . BVL-Report 14.6 Bericht zur Resistenzmonitoringstudie 2018 [BVL-Report 14.6 Report on the Resistance Monitoring Study 2018] BVL; Berlin, Germany: 2020.
  67. Feldgarden M., Brover V., Haft D.H., Prasad A.B., Slotta D.J., Tolstoy I., Tyson G.H., Zhao S., Hsu C.H., McDermott P.F., et al. Validating the AMRFinder Tool and Resistance Gene Database by Using Antimicrobial Resistance Genotype-Phenotype Correlations in a Collection of Isolates. Antimicrob. Agents Chemother. 2019;63:e00483-19. doi: 10.1128/AAC.00483-19.
    doi: 10.1128/AAC.00483-19pmc: PMC6811410pubmed: 31427293google scholar: lookup
  68. Bortolaia V., Kaas R.S., Ruppe E., Roberts M.C., Schwarz S., Cattoir V., Philippon A., Allesoe R.L., Rebelo A.R., Florensa A.F., et al. ResFinder 4.0 for predictions of phenotypes from genotypes. J. Antimicrob. Chemother. 2020;75:3491–3500. doi: 10.1093/jac/dkaa345.
    doi: 10.1093/jac/dkaa345pmc: PMC7662176pubmed: 32780112google scholar: lookup
  69. Zankari E., Allesøe R., Joensen K.G., Cavaco L.M., Lund O., Aarestrup F.M. PointFinder: A novel web tool for WGS-based detection of antimicrobial resistance associated with chromosomal point mutations in bacterial pathogens. J. Antimicrob. Chemother. 2017;72:2764–2768. doi: 10.1093/jac/dkx217.
    doi: 10.1093/jac/dkx217pmc: PMC5890747pubmed: 29091202google scholar: lookup
  70. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990;215:403–410. doi: 10.1016/S0022-2836(05)80360-2.
    doi: 10.1016/S0022-2836(05)80360-2pubmed: 2231712google scholar: lookup
  71. Consortium T.U. UniProt: The Universal Protein Knowledgebase in 2025. Nucleic Acids Res. 2024;53:D609–D617. doi: 10.1093/nar/gkae1010.
    doi: 10.1093/nar/gkae1010pmc: PMC11701636pubmed: 39552041google scholar: lookup
  72. Chen L., Yang J., Yu J., Yao Z., Sun L., Shen Y., Jin Q. VFDB: A reference database for bacterial virulence factors. Nucleic Acids Res. 2005;33:D325–D328. doi: 10.1093/nar/gki008.
    doi: 10.1093/nar/gki008pmc: PMC539962pubmed: 15608208google scholar: lookup
  73. Monecke S., Gavier-Widen D., Mattsson R., Rangstrup-Christensen L., Lazaris A., Coleman D.C., Shore A.C., Ehricht R. Detection of mecC-positive Staphylococcus aureus (CC130-MRSA-XI) in diseased European hedgehogs (Erinaceus europaeus) in Sweden. PLoS ONE. 2013;8:e66166. doi: 10.1371/journal.pone.0066166.
  74. Monecke S., Jatzwauk L., Müller E., Nitschke H., Pfohl K., Slickers P., Reissig A., Ruppelt-Lorz A., Ehricht R. Diversity of SCCmec Elements in Staphylococcus aureus as Observed in South-Eastern Germany. PLoS ONE. 2016;11:e0162654. doi: 10.1371/journal.pone.0162654.
  75. Coleman D., Knights J., Russell R., Shanley D., Birkbeck T.H., Dougan G., Charles I. Insertional inactivation of the Staphylococcus aureus beta-toxin by bacteriophage phi 13 occurs by site- and orientation-specific integration of the phi 13 genome. Mol. Microbiol. 1991;5:933–939. doi: 10.1111/j.1365-2958.1991.tb00768.x.
  76. Coleman D.C., Sullivan D.J., Russell R.J., Arbuthnott J.P., Carey B.F., Pomeroy H.M. Staphylococcus aureus Bacteriophages Mediating the Simultaneous Lysogenic Conversion of β-Lysin, Staphylokinase and Enterotoxin A: Molecular Mechanism of Triple Conversion. J. Gen. Microbiol. 1989;135:1679–1697. doi: 10.1099/00221287-135-6-1679.
    doi: 10.1099/00221287-135-6-1679pubmed: 2533245google scholar: lookup

Citations

This article has been cited 0 times.