1887

Abstract

(formerly subsp. ) is a common commensal and opportunistic pathogen of companion dogs. It carries a range of antimicrobial resistance genes and is an occasional zoonotic pathogen.

Despite the potential insight offered by genome sequencing into the biology of , few genomes are currently available for study.

To sequence and analyse genomes to improve understanding of this organism’s molecular epidemiology, antimicrobial resistance and bacterium–host interactions.

Twenty-five genomes of clinical isolates collected at a veterinary referral hospital in Scotland, UK, were sequenced with Illumina technology. These genomes were analysed by a series of bioinformatics tools along with 16 previously sequenced genomes.

Phylogenetic comparison of the 41 genomes shows that the current phylogeny is dominated by clades of closely related isolates, at least one of which has spread internationally. Ten of the 11 methicillin-resistant genomes in this collection of 41 encoded the promoter and gene mutations that are predicted to render the isolates susceptible to penicillins in the presence of clavulanic acid, a feature only described to date in methicillin-resistant . Seven such isolates were from the current study and, in line with the genome-based prediction, all were susceptible to amoxicillin/clavulanic acid shared very few highly conserved virulence-associated genes with , another common commensal and opportunistic canine pathogen.

The availability of a further 25 genome sequences from clinical isolates will aid in better understanding the epidemiology, bacterial–host interactions and antimicrobial resistance of this opportunistic pathogen.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2021-08-25
2024-04-19
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References

  1. Igimi S, Takahashi E, Mitsuoka T. Staphylococcus schleiferi subsp. coagulans subsp. nov., isolated from the external auditory meatus of dogs with external ear otitis. Int J Syst Bacteriol 1990; 40:409–411 [View Article] [PubMed]
    [Google Scholar]
  2. Madhaiyan M, Wirth JS, Saravanan VS. Phylogenomic analyses of the Staphylococcaceae family suggest the reclassification of five species within the genus Staphylococcus as heterotypic synonyms, the promotion of five subspecies to novel species, the taxonomic reassignment of five Staphylococcus species to Mammaliicoccus gen. nov., and the formal assignment of Nosocomiicoccus to the family Staphylococcaceae. Int J Syst Evol Microbiol 2020; 70:5926–5936 [View Article] [PubMed]
    [Google Scholar]
  3. Yamashita K, Shimizu A, Kawano J, Uchida E, Haruna A et al. Isolation and characterization of staphylococci from external auditory meatus of dogs with or without otitis externa with special reference to Staphylococcus schleiferi subsp coagulans isolates. J Vet Med Sci 2005; 67:263–268 [View Article] [PubMed]
    [Google Scholar]
  4. May ER, Hnilica KA, Frank LA, Jones RD, Bemis DA. Isolation of Staphylococcus schleiferi from healthy dogs and dogs with otitis, pyoderma, or both. J Am Vet Med Assoc 2005; 227:928–931 [View Article]
    [Google Scholar]
  5. Foster G, Barley J. Staphylococcus schleiferi subspecies coagulans in dogs. Vet Rec 2007; 161:496 [View Article] [PubMed]
    [Google Scholar]
  6. Hariharan H, Gibson K, Peterson R, Frankie M, Matthew V et al. Staphylococcus pseudintermedius and Staphylococcus schleiferi Subspecies coagulans from Canine Pyoderma Cases in Grenada, West Indies, and Their Susceptibility to Beta-Lactam Drugs. Vet Med Int 2014; 2014:850126 [View Article] [PubMed]
    [Google Scholar]
  7. Kawakami T, Shibata S, Murayama N, Nagata M, Nishifuji K et al. Antimicrobial susceptibility and methicillin resistance in Staphylococcus pseudintermedius and Staphylococcus schleiferi subsp. coagulans isolated from dogs with pyoderma in Japan. J Vet Med Sci 2010; 72:1615–1619 [View Article] [PubMed]
    [Google Scholar]
  8. Griffeth GC, Morris DO, Abraham JL, Shofer FS, Rankin SC. Screening for skin carriage of methicillin-resistant coagulase-positive staphylococci and Staphylococcus schleiferi in dogs with healthy and inflamed skin. Vet Dermatol 2008; 19:142–149 [View Article] [PubMed]
    [Google Scholar]
  9. Vandenesch F, Lebeau C, Bes M, Lina G, Lina B et al. Clotting activity in Staphylococcus schleiferi subspecies from human patients. J Clin Microbiol 1994; 32:388–392 [View Article] [PubMed]
    [Google Scholar]
  10. Kumar D, Cawley JJ, Irizarry-Alvarado JM, Alvarez A, Alvarez S. Case of Staphylococcus schleiferi subspecies coagulans endocarditis and metastatic infection in an immune compromised host. Transpl Infect Dis 2007; 9:336–338 [View Article] [PubMed]
    [Google Scholar]
  11. Thibodeau E, Boucher H, DeNofrio D, Pham DT, Snydman D. First report of a left ventricular assist device infection caused by Staphylococcus schleiferi subspecies coagulans: a coagulase-positive organism. Diagn Microbiol Infect Dis 2012; 74:68–69 [View Article] [PubMed]
    [Google Scholar]
  12. Tzamalis A, Chalvatzis N, Anastasopoulos E, Tzetzi D, Dimitrakos S. Acute postoperative Staphylococcus schleiferi endophthalmitis following uncomplicated cataract surgery: First report in the literature. Eur J Ophthalmol 2013; 23:427–430 [View Article] [PubMed]
    [Google Scholar]
  13. Yarbrough ML, Hamad Y, Burnham CA, George IA, McAdam AJ. The brief case: Bacteremia and vertebral osteomyelitis due to Staphylococcus schleiferi. J Clin Microbiol 2017; 55:3157–3161 [View Article] [PubMed]
    [Google Scholar]
  14. Abraham JL, Morris DO, Griffeth GC, Shofer FS, Rankin SC. Surveillance of healthy cats and cats with inflammatory skin disease for colonization of the skin by methicillin-resistant coagulase-positive staphylococci and Staphylococcus schleiferi ssp. schleiferi. Vet Dermatol 2007; 18:252–259 [View Article] [PubMed]
    [Google Scholar]
  15. Martins PD, de Almeida TT, Basso AP, de Moura TM, Frazzon J et al. Coagulase-positive staphylococci isolated from chicken meat: Pathogenic potential and vancomycin resistance. Foodborne Pathog Dis 2013; 10:771–776 [View Article] [PubMed]
    [Google Scholar]
  16. Sergelidis D, Abrahim A, Papadopoulos T, Soultos N, Martziou E et al. Isolation of methicillin-resistant Staphylococcus spp. from ready-to-eat fish products. Lett Appl Microbiol 2014; 59:500–506 [View Article] [PubMed]
    [Google Scholar]
  17. Kizerwetter-Swida M, Chrobak-Chmiel D, Rzewuska M, Antosiewicz A, Dolka B et al. Genetic characterization of coagulase-positive staphylococci isolated from healthy pigeons. Pol J Vet Sci 2015; 18:627–634 [View Article] [PubMed]
    [Google Scholar]
  18. Vrbovska V, Sedlacek I, Zeman M, Svec P, Kovarovic V et al. Characterization of Staphylococcus intermedius group isolates associated with animals from Antarctica and emended description of Staphylococcus delphini. Microorganisms 2020; 8: [View Article] [PubMed]
    [Google Scholar]
  19. Foster G, Robb A, Paterson GK. Isolation and genome sequencing of Staphylococcus schleiferi subspecies coagulans from antarctic and North Sea seals. Access Microbiol 2020; 2:acmi000162 [View Article]
    [Google Scholar]
  20. Peacock SJ, Paterson GK. Mechanisms of methicillin resistance in Staphylococcus aureus. Annu Rev Biochem 2015; 84:577–601 [View Article] [PubMed]
    [Google Scholar]
  21. Huse HK, Miller SA, Chandrasekaran S, Hindler JA, Lawhon SD et al. Evaluation of oxacillin and cefoxitin disk diffusion and MIC breakpoints established by the Clinical and Laboratory Standards Institute for detection of meca-mediated oxacillin resistance in Staphylococcus schleiferi. J Clin Microbiol 2018; 56:e01653–17 [View Article]
    [Google Scholar]
  22. Roberts S, O’Shea K, Morris D, Robb A, Morrison D et al. A real-time PCR assay to detect the Panton Valentine Leukocidin toxin in staphylococci: screening Staphylococcus schleiferi subspecies coagulans strains from companion animals. Vet Microbiol 2005; 107:139–144 [View Article] [PubMed]
    [Google Scholar]
  23. Chanchaithong P, Perreten V, Schwendener S, Tribuddharat C, Chongthaleong A et al. Strain typing and antimicrobial susceptibility of methicillin-resistant coagulase-positive staphylococcal species in dogs and people associated with dogs in Thailand. J Appl Microbiol 2014; 117:572–586 [View Article] [PubMed]
    [Google Scholar]
  24. Costa SS, Oliveira V, Serrano M, Pomba C, Couto I. Phenotypic and molecular traits of Staphylococcus coagulans associated with canine skin infections in Portugal. Antibiotics (Basel) 2021; 10: [View Article] [PubMed]
    [Google Scholar]
  25. Detwiler A, Bloom P, Petersen A, Rosser EJ. Multi-drug and methicillin resistance of staphylococci from canine patients at a veterinary teaching hospital (2006-2011. Vet Q 2013; 33:60–67 [View Article] [PubMed]
    [Google Scholar]
  26. Penna B, Varges R, Medeiros L, Martins GM, Martins RR et al. Species distribution and antimicrobial susceptibility of staphylococci isolated from canine otitis externa. Vet Dermatol 2010; 21:292–296 [View Article] [PubMed]
    [Google Scholar]
  27. Rossi CC, Pereira MF, Giambiagi-deMarval M. Underrated Staphylococcus species and their role in antimicrobial resistance spreading. Genet Mol Biol 2020; 43:e20190065 [View Article] [PubMed]
    [Google Scholar]
  28. Haaber J, Penadés JR, Ingmer H. Transfer of antibiotic resistance in Staphylococcus aureus. Trends Microbiol 2017; 25:893–905 [View Article] [PubMed]
    [Google Scholar]
  29. Frosini SM, Bond R, McCarthy AJ, Feudi C, Schwarz S et al. Genes on the move: in vitro transduction of antimicrobial resistance genes between human and canine staphylococcal pathogens. Microorganisms 2020; 8:12 [View Article]
    [Google Scholar]
  30. Méric G, Miragaia M, de Been M, Yahara K, Pascoe B et al. Ecological overlap and horizontal gene transfer in Staphylococcus aureus and Staphylococcus epidermidis. Genome Biol Evol 2015; 7:1313–1328 [View Article] [PubMed]
    [Google Scholar]
  31. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
    [Google Scholar]
  32. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
    [Google Scholar]
  33. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  34. Meier-Kolthoff JP, Göker M. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 2019; 10:2182 [View Article] [PubMed]
    [Google Scholar]
  35. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S et al. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 2012; 67:2640–2644 [View Article]
    [Google Scholar]
  36. Zukancic A, Khan MA, Gurmen SJ, Gliniecki QM, Moritz-Kinkade DL et al. Staphylococcal Protein A (spa) locus is a hot spot for recombination and horizontal gene transfer in Staphylococcus pseudintermedius. mSphere 2020; 5: [View Article] [PubMed]
    [Google Scholar]
  37. Kaya H, Hasman H, Larsen J, Stegger M, Johannesen TB et al. Sccmecfinder, a web-based tool for typing of staphylococcal cassette chromosome MEC in Staphylococcus aureus using whole-genome sequence data. mSphere 2018; 3: [View Article] [PubMed]
    [Google Scholar]
  38. Cole K, Foster D, Russell JE, Golubchik T, Llewelyn M et al. Draft genome sequences of 64 type strains of 50 species and 25 subspecies of the genus Staphylococcus Rosenbach 1884. Microbiol Resour Announc 2019; 8:e00062–19 [View Article]
    [Google Scholar]
  39. Lee GY, Yang SJ. Complete genome sequence of a methicillin-resistant Staphylococcus schleiferi strain from canine otitis externa in Korea. J Vet Sci 2020; 21:e11 [View Article]
    [Google Scholar]
  40. Misic AM, Cain CL, Morris DO, Rankin SC, Beiting DP. Complete genome sequence and methylome of Staphylococcus schleiferi, an important cause of skin and ear infections in veterinary medicine. Genome Announc 2015; 3:e01011–15 [View Article]
    [Google Scholar]
  41. Sasaki T, Tsubakishita S, Kuwahara-Arai K, Matsuo M, Lu YJ et al. Complete genome sequence of methicillin-resistant Staphylococcus schleiferi strain TSCC54 of canine origin. Genome Announc 2015; 3:e01268–15 [View Article]
    [Google Scholar]
  42. Kaas RS, Leekitcharoenphon P, Aarestrup FM, Lund O. Solving the problem of comparing whole bacterial genomes across different sequencing platforms. PLoS One 2014; 9:e104984 [View Article]
    [Google Scholar]
  43. Letunic I, Bork P. Interactive Tree of Life (iTOL) v4: Recent updates and new developments. Nucleic Acids Res 2019; 47:W256–W259 [View Article]
    [Google Scholar]
  44. Feßler AT, Wang Y, Wu C, Schwarz S. Mobile lincosamide resistance genes in staphylococci. Plasmid 2018; 99:22–31 [View Article] [PubMed]
    [Google Scholar]
  45. Harrison EM, Ba X, Coll F, Blane B, Restif O et al. Genomic identification of cryptic susceptibility to penicillins and β-lactamase inhibitors in methicillin-resistant Staphylococcus aureus. Nat Microbiol 2019; 4:1680–1691 [View Article] [PubMed]
    [Google Scholar]
  46. Descloux S, Rossano A, Perreten V. Characterization of New Staphylococcal Cassette Chromosome mec (SCCmec) and topoisomerase genes in fluoroquinolone- and methicillin-resistant Staphylococcus pseudintermedius. J Clin Microbiol 2008; 46:1818–1823 [View Article] [PubMed]
    [Google Scholar]
  47. Yamagishi J, Kojima T, Oyamada Y, Fujimoto K, Hattori H et al. Alterations in the DNA topoisomerase IV grlA gene responsible for quinolone resistance in Staphylococcus aureus. Antimicrob Agents Chemother 1996; 40:1157–1163 [View Article] [PubMed]
    [Google Scholar]
  48. Wladyka B, Piejko M, Bzowska M, Pieta P, Krzysik M et al. A peptide factor secreted by Staphylococcus pseudintermedius exhibits properties of both bacteriocins and virulence factors. Sci Rep 2015; 5:14569 [View Article] [PubMed]
    [Google Scholar]
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