1887

Abstract

Reports on the commensal organism and opportunistic pathogen have largely considered isolates from humans and companion dogs. Two subspecies are recognized: the coagulase-negative ssp. , typically seen in humans, and the coagulase-positive ssp. , typically seen in dogs. In this study, we report the isolation, genome sequencing and comparative genomics of three ssp. isolates from mouth samples from two species of healthy, free-living Antarctic seals, southern elephant seals () and Antarctic fur seals (), in the South Orkney Islands, Antarctica, and three isolates from post-mortem samples from grey seals () in Scotland, UK. This is the first report of ssp. isolation from Antarctic fur seal and grey seal. The Antarctic fur seal represents the first isolation of ssp. from the family , while the grey seal represents the first isolation from a pinniped in the Northern Hemisphere. We compare seal, dog and human isolates from both subspecies in the first genome-based phylogenetic analysis of the species.

  • 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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2020-08-21
2024-04-20
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References

  1. Freney J, Brun Y, Bes M, Meugnier H, Grimont F et al. Staphylococcus lugdunensis sp. nov. and Staphylococcus schleiferi sp. nov., two Species from Human Clinical Specimens. Int J Syst Evol Microbiol 1988; 38:168–172
    [Google Scholar]
  2. Igimi S, Takahashi E, Mitsuoka T, subsp Sschleiferi. 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]
  3. Assumpção YdeM, Teixeira IM, Paletta ACC, Ferreira EdeO, Pinto TCA et al. Matrix-assisted laser desorption ionization-time of flight mass spectrometry-based method for accurate discrimination of Staphylococcus schleiferi subspecies. Vet Microbiol 2020; 240:108472 [View Article][PubMed]
    [Google Scholar]
  4. Cain CL, Morris DO, O'Shea K, Rankin SC. Genotypic relatedness and phenotypic characterization of Staphylococcus schleiferi subspecies in clinical samples from dogs. Am J Vet Res 2011; 72:96–102 [View Article][PubMed]
    [Google Scholar]
  5. 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]
  6. Ghosh A, Singh Y, Kapil A, Dhawan B. Staphylococcal Cassette Chromosome mec (SCCmec) typing of clinical isolates of coagulase-negative staphylocci (CoNS) from a tertiary care hospital in New Delhi, India. Indian J Med Res 2016; 143:365–370 [View Article][PubMed]
    [Google Scholar]
  7. 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]
  8. 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][PubMed]
    [Google Scholar]
  9. Arnold AR, Burnham C-AD, Ford BA, Lawhon SD, McAllister SK et al. Evaluation of an immunochromatographic assay for rapid detection of penicillin-binding protein 2a in human and animal Staphylococcus intermedius group, Staphylococcus lugdunensis, and Staphylococcus schleiferi clinical isolates. J Clin Microbiol 2016; 54:745–748 [View Article][PubMed]
    [Google Scholar]
  10. Célard M, Vandenesch F, Darbas H, Grando J, Jean-Pierre H et al. Pacemaker infection caused by Staphylococcus schleiferi, a member of the human preaxillary flora: four case reports. Clin Infect Dis 1997; 24:1014–1015 [View Article][PubMed]
    [Google Scholar]
  11. Da Costa A, Lelièvre H, Kirkorian G, Célard M, Chevalier P et al. Role of the preaxillary flora in pacemaker infections: a prospective study. Circulation 1998; 97:1791–1795 [View Article][PubMed]
    [Google Scholar]
  12. Iravani Mohammad Abadi M, Moniri R, Khorshidi A, Piroozmand A, Mousavi SGA et al. Molecular characteristics of nasal carriage methicillin-resistant coagulase negative staphylococci in school students. Jundishapur J Microbiol 2015; 8:e18591 [View Article][PubMed]
    [Google Scholar]
  13. Oztürkeri H, Kocabeyoğlu O, Yergök YZ, Koşan E, Yenen OS et al. Distribution of coagulase-negative staphylococci, including the newly described species Staphylococcus schleiferi, in nosocomial and community acquired urinary tract infections. Eur J Clin Microbiol Infect Dis 1994; 13:1076–1079 [View Article][PubMed]
    [Google Scholar]
  14. Grattard F, Etienne J, Pozzetto B, Tardy F, Gaudin OG et al. Characterization of unrelated strains of Staphylococcus schleiferi by using ribosomal DNA fingerprinting, DNA restriction patterns, and plasmid profiles. J Clin Microbiol 1993; 31:812–818 [View Article][PubMed]
    [Google Scholar]
  15. Kluytmans J, Berg H, Steegh P, Vandenesch F, Etienne J et al. Outbreak of Staphylococcus schleiferi wound infections: strain characterization by randomly amplified polymorphic DNA analysis, PCR ribotyping, conventional ribotyping, and pulsed-field gel electrophoresis. J Clin Microbiol 1998; 36:2214–2219 [View Article][PubMed]
    [Google Scholar]
  16. Leung MJ, Nuttall N, Mazur M, Taddei TL, McComish M et al. Case of Staphylococcus schleiferi endocarditis and a simple scheme to identify clumping factor-positive staphylococci. J Clin Microbiol 1999; 37:3353–3356 [View Article][PubMed]
    [Google Scholar]
  17. 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]
  18. 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]
  19. 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][PubMed]
    [Google Scholar]
  20. Foster G, Barley J. Staphylococcus schleiferi subspecies coagulans in dogs. Vet Rec 2007; 161:496 [View Article][PubMed]
    [Google Scholar]
  21. 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; 2014:8501267 [View Article][PubMed]
    [Google Scholar]
  22. 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]
  23. 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]
  24. 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]
  25. 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]
  26. Kizerwetter-Świda 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]
  27. Nikolaisen NK, Lassen DCK, Chriél M, Larsen G, Jensen VF et al. Antimicrobial resistance among pathogenic bacteria from mink (Neovison vison) in Denmark. Acta Vet Scand 2017; 59:60 [View Article][PubMed]
    [Google Scholar]
  28. Vrbovská V, Sedláček I, Zeman M, Švec P, Kovařovic V et al. Characterization of Staphylococcus intermedius group isolates associated with animals from antarctica and emended description of Staphylococcus delphini . Microorganisms 2020; 8:E204204 [View Article][PubMed]
    [Google Scholar]
  29. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article][PubMed]
    [Google Scholar]
  30. 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]
  31. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article][PubMed]
    [Google Scholar]
  32. Yoon S-H, Ha S-M, Lim J, Kwon S, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek 2017; 110:1281–1286 [View Article][PubMed]
    [Google Scholar]
  33. 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][PubMed]
    [Google Scholar]
  34. 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][PubMed]
    [Google Scholar]
  35. 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][PubMed]
    [Google Scholar]
  36. 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:e01011–01015 [View Article][PubMed]
    [Google Scholar]
  37. 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][PubMed]
    [Google Scholar]
  38. 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][PubMed]
    [Google Scholar]
  39. Letunic I, Bork P. Interactive tree of life (iTOL) V4: recent updates and new developments. Nucleic Acids Res 2019; 47:W256–W259 [View Article][PubMed]
    [Google Scholar]
  40. Matuszewska M, Murray GGR, Harrison EM, Holmes MA, Weinert LA. The evolutionary genomics of host specificity in Staphylococcus aureus . Trends Microbiol 2020; 28:465–477 [View Article][PubMed]
    [Google Scholar]
  41. Richardson EJ, Bacigalupe R, Harrison EM, Weinert LA, Lycett S et al. Gene exchange drives the ecological success of a multi-host bacterial pathogen. Nat Ecol Evol 2018; 2:1468–1478 [View Article][PubMed]
    [Google Scholar]
  42. Fravel V, Van Bonn W, Rios C, Gulland F. Meticillin-resistant Staphylococcus aureus in a harbour seal (Phoca vitulina). Vet Rec 2011; 169:155 [View Article][PubMed]
    [Google Scholar]
  43. Paterson GK, Larsen AR, Robb A, Edwards GE, Pennycott TW et al. The newly described mecA homologue, mecALGA251, is present in methicillin-resistant Staphylococcus aureus isolates from a diverse range of host species. J Antimicrob Chemother 2012; 67:2809–2813 [View Article][PubMed]
    [Google Scholar]
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