Skip to main content
NCBI home page
Access Microbiology logoLink to Access Microbiology
. 2020 Aug 21;2(10):acmi000162. doi: 10.1099/acmi.0.000162

Isolation and genome sequencing of Staphylococcus schleiferi subspecies coagulans from Antarctic and North Sea seals

Geoff Foster 1,*, Andrew Robb 2, Gavin K Paterson 3,*
PMCID: PMC7660238  PMID: 33195976

Abstract

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

Keywords: bacterial genomics, coagulase-positive staphylococci, otariid, seals, Staphylococcus schleiferi

Introduction

Staphylococcus schleiferi appears primarily to be a commensal and opportunistic pathogen of humans and domestic dogs. Two subspecies are recognized, S. schleiferi ssp. schleiferi [1] and S. schleiferi ssp. coagulans [2]. S. schleiferi ssp. coagulans is identified phenotypically on the basis of free coagulase production (tube test), urease production and the ability to ferment ribose, which are properties that S. schleiferi ssp. schleiferi typically lacks [2]. The two subspecies are also differentiated based on DNA–DNA hybridization [2] and matrix-assisted laser desorption/ionization time-of-flight mass spectrometry [3]. However, not all studies differentiate the two subspecies and some authors have highlighted potential difficulties with their separation [4, 5]. Both subspecies can encode methicillin resistance, as well as other antimicrobial resistance, heightening their potential clinical significance [6–9].

S. schleiferi ssp. schleiferi can be isolated from human preaxillary skin [10, 11] and nares [12] and is associated with a range of nosocomial infections, including urinary tract infections [13], brain abscess and cerebrospinal fluid culture [14], pacemaker- and catheter-related infections [10, 14], surgical wound infections [14, 15] and endocarditis [16]. In contrast, S. schleiferi ssp. coagulans is rarely found in humans [5], but is frequently isolated from healthy dogs from the skin [17] and the external ear canal [18], as well as being associated with external ear otitis [2, 18–20] and pyoderma [19, 21, 22]. S. schleiferi ssp. schleiferi has also been reported from dogs [19] and both subspecies have been isolated from cats [23]. In addition, S. schleiferi ssp. coagulans has been reported from chicken meat [24], ready-to-eat retail fish [25] and the posterior nares and cloaca of healthy feral and domestic pigeons (family Columbidae) [26]. S. schleiferi , not delineated to subspecies level, has been isolated from clinical material in farmed mink [27]. Finally, S. schleiferi ssp. coagulans has been isolated in Antarctica from the cloaca and beaks of Adélie penguins (Pygoscelis adeliae), from South Polar skua (Stercorarius maccormicki) droppings, and the anus of two species of seals from the family Phocidae: Weddell seals (Leptonychotes weddellii) and southern elephant seals (Mirounga leonina) [28]. Thus the host range of S. schleiferi extends beyond humans and dogs and likely includes a range of hitherto unreported host species.

In this study, we report the isolation and genome sequencing of three S. schleiferi ssp. coagulans isolates from three Antarctic seals; two southern elephant seals (M. leonina) and an Antarctic fur seal (Arctocephalus gazella) and three isolates from grey seals (Halichoerus grypus) in the North Sea. To the best of our knowledge, isolates from these three host species have not been genome sequenced previously and this report represents the first isolation of S. schleiferi from a member of the family Otaridae, an Antarctic fur seal (A. gazella) and the first from grey seal (H. grypus). To place these seal isolates into the context of the S. schleiferi population we present the first genome-based phylogenetic analysis of the species comparing both subspecies and including isolates from humans, dogs and three seal species.

Material and methods

Bacterial isolation

Healthy, free-living Antarctic seals were sampled by the British Antarctic Survey at two separate sites on Signy Island in the South Orkney Islands, Antarctica in 1993. A swab on the end of a broomstick was used to collect an oral sample when a male (territorial) seal yawned. The samples were freeze-dried and subsequently examined by microbiological culture at Scotland’s Rural College (SRUC) Veterinary Services, Inverness. Three further isolates were collected post-mortem from three grey seals found dead on the North Sea shoreline in Fife, eastern Scotland between 2002 and 2016 and reported under the Scottish Marine Animals Strandings Scheme (SMASS). Carcases were transported to SRUC Veterinary Services, Inverness for a post-mortem examination and selected tissues and gross lesions were sampled for microbiological and histopathological diagnoses. The animals likely died from phocine distemper virus, emphysema and necrotizing haemorrhagic gastro-enteritis, respectively. S. schleiferi ssp. coagulans was isolated from several organs from these grey seals; the isolates subjected to further study here were collected from the lungs. Isolation was made on Columbia agar supplemented with 5 % sheep blood (CSBA) (Oxoid, Basingstoke, UK) incubated in air plus 5 % CO2 at 37 °C for 18–24 h. Sub-cultures were made to CSBA for characterization tests. Initial identification to species was made by API ID 32Staph (bioMérieux, Basingstoke, UK). Antimicrobial sensitivity testing was performed using Vitek 2 (bioMérieux, Basingstoke, UK) following the manufacturer’s instructions. Using the AST-P634 Staphylococcus card the antimicrobials tested were: cefoxitin screen, benylpenicillin, oxacillin, gentamicin, ciprofloxacin, inducible clindamycin resistance, erythromycin, clindamycin, linezolid, daptomycin, teicoplanin, vancomycin, tetracycline, nitrofurantoin, fuscidic acid, chloramphenicol, rifampicin and trimethorprim, with interpretation performed using the Clinical and Laboratory Standards Institute (CLSI) criteria (2015). Clumping factor and free coagulase were tested with lyophilized rabbit plasma with EDTA (Oxoid).

Whole-genome sequencing

Whole-genome sequencing was performed by Microbes NG (University of Birmingham, UK) using Illumina technology with 2×250 bp paired-end reads. Genomic DNA libraries were prepared using the Nextera XT Library Prep kit (Illumina, San Diego, USA) following the manufacturer’s protocol with the following modifications: 2 ng of DNA instead of 1 were used as input, and the PCR elongation time was increased to 1 min from 30 s. Reads were trimmed using Trimmomatic version 0.30 [29] and a sliding window quality cut-off of 15. Genome assembly was performed de novo using SPAdes version 3.7, with default parameters for 250 bp Illumina reads [30], and annotated by the National Center for Biotechnology Information (NCBI) Prokaryotic Genome Annotation Pipeline [31].

Genome analysis

Average nucleotide identity (ANI) was calculated using the EZBioCloud ANI Calculator (https://www.ezbiocloud.net/tools/ani) [32]. Acquired resistance genes were identified using ResFinder-3.1 employing the threshold of 60 % for percentage identity and minimum length of 60 % [33].

Phylogenetic relationships between study isolates and previously sequenced, assembled and annotated S. schleiferi isolates [34–37] was inferred using CSI Phylogeny 1.4 (Call SNPs and Infer Phylogeny) [38] with S. schleiferi ssp. schleiferi ATCC43808T (GCA_900458895.1) as the reference genome and applying default settings [minimum depth at single-nucleotide polymorphism (SNP) positions: 10×; minimum relative depth at SNP positions: 10 %; minimum distance between SNPs (prune): 10 bp; minimum SNP quality: 30; minimum read mapping quality: 25; and minimum Z score: 1.96]. We found 2 115 918 positions in all analysed genomes. The resultant tree was annotated using the Interactive Tree of Life (iTOL) [39]. Two further, hitherto unpublished, S. schleiferi ssp. coagulans canine isolates from the Royal (Dick) School of Veterinary Studies were also included for comparison (Table S1, available in the online version of the article).

Isolate and data availability

Isolates metadata and nucleotide accessions are provided in Table S1. The genome sequenced isolates A/G14/99/8, A/G16/00/1, A/W41/99/1 and M615/02/4 have been deposited with the Culture Collection University of Gothenburg as CCUG52137, CCUG52138, CCUG53690 and CCUG 52139, respectively.

Results

Isolation of Antarctic and North Sea seal S. schleiferi

In the course of British Antarctic Survey bacteriological investigations of mouth samples collected from seals at Signy Island, South Orkneys in Antarctica, four isolates of S. schleiferi were isolated from three animals. Isolates A/G14/99/8 and A/G16/00/1 and AG16/00/7 were recovered from two southern elephant seals (M. leonina) sampled at the Gourlay Peninsula at the south-easternmost end of the island and A/W41/99/1 was recovered from an Antarctic fur seal (A. gazella) sampled at the Wallows in the north-east. With isolates A/G16/00/1 and A/G16/00/7 having been isolated from the same animal, only A/G16/00/1 from these two was taken forward for further study. Isolates M615/02/4, M31/11/1, M611545/16/1 were collected post-mortem from the lungs of grey seals that had stranded in different parts of Fife (North Sea coast), Scotland in 2002, 2011 and 2016, respectively. The three North Sea isolates were tube coagulase- and urease-positive, clumping factor-negative and unable to ferment trehalose, phenotypes indicative of S. schleiferi ssp. coagulans. The three Antarctic seal isolates shared these features, with the exception that they were each able to ferment trehalose.

Genome sequencing and genomic-based identification

To investigate these six isolates further they were genome sequenced using HiSeq technology. The genome sizes and GC % content were as follows: A/G14/99/8, 2 402 027 bp, 35.8 %; A/G16/00/1, 2 374 021 bp, 35.9 %; A/W41/99/1, 2 402 964 bp, 35.8 %; M615/02/4, 2 590 557 bp, 35.9 %; M31/11/1, 2 471 374 bp, 35.9 %; and M611545/16/1, 2 399 198 bp, 36.1 %. To confirm the identity of the six seal isolates to species and subspecies levels on the basis of genome sequence, a comparison with the two genome-sequenced S. schleiferi subspecies type strains (accessions in Table S1) was performed using ANI. In each case the ANI was closer to S. schleiferi ssp. coagulans (97.47 %–98.89 %) than to S. schleiferi ssp. schleiferi (95.09–95.68 %), consistent with all six seal isolates belonging to S. schleiferi ssp. coagulans (Table S1).

Phylogenetic relationships among S. schleiferi

To compare the relationships between the six seal isolates and other genome-sequenced S. schleiferi isolates, a phylogenetic tree was constructed based on SNPs across the core genome (Fig. 1). The phylogeny clearly delineated the two S. schleiferi subspecies, with the six seal isolates belonging to S. schleiferi ssp. coagulans. The six seal isolates were split between three clades, indicating that diverse S. schleiferi ssp. coagulans lineages are present in seals. The Antarctic seal isolates A/G14/98/1 and A/W41/99/1 are identical and most closely related to the third Antarctic seal isolate, A/G16/00/1 (separated by 4289 SNPs). Likewise, the two North Sea grey seal isolates M31/11/1 and M615/02/4 are closely related, being separated by 150 SNPs. These two clusters of seal isolates are, however, distinct, being separated by at least 14 621 SNPs. In contrast, the final North Sea grey seal isolate (M611545/16/1) is not closely related to any other analysed isolate, with its closest relative differing by 22661 SNPs and the closest seal isolate being separated from it by 23 316 SNPs. There were two other closely related clusters of S. schleiferi ssp. coagulans isolates. Isolates 2142, 2317, 5909 and OT-1 are separated by a mean pairwise SNP difference of 187, while 1360 and 6124 are separated by 142 SNPs (Fig. 1).

Fig. 1.

Fig. 1.

Open in a new tab

Phylogenetic tree of sequenced S. schleiferi isolates. Generated from SNPs across 2 093 618 positions in the core genome using CSI Phylogeny 1.4(38) with S. schleiferi ssp. schleiferi ATCC43808T (GCA_002901995.1) as the reference genome and the tree root. Seal isolates from this study are highlighted in bold. Host and country of origin indicated, where known. Genome accessions are provided in Table S1. Subspecies assigned based on ANI to type strains of S. schleiferi ssp. coagulans (DSM6628T) and S. schleiferi ssp. schleiferi (ATCC43808T).

Antimicrobial resistance

None of the six seal isolates, A/G14/99/8, A/G16/00/1, A/W41/99/1, M615/02/4, M31/11/1and M611545/16/1, displayed phenotypic resistance against the antimicrobials tested. Consistent with that finding, no acquired antimicrobial resistance genes were identified in their genome sequences.

Discussion

We describe here the isolation and whole-genome sequencing of six isolates of S. schleiferi ssp. coagulans from three species of pinniped, namely southern elephant seal, Antarctic fur seal and grey seal. While S. schleiferi ssp. coagulans has been isolated from Antarctic seals previously [28], those isolates have not been characterized further than identification using partial 16S rRNA gene sequencing and to the best of our knowledge this study represents the first isolation of S. schleiferi from Antarctic fur seal and grey seal. This finding enhances our understanding of the distribution of this commensal and opportunistic pathogen and extends the known host range of S. schleiferi ssp. coagulans to now include dogs, humans, feral and domestic pigeons, southern elephant seals, Antarctic fur seal, grey seals, Weddell seal, Adélie penguins, South Polar skua and possibly chicken and fish. This diverse range of host species suggests that S. schleiferi ssp. coagulans may have a broad host range comprising other as yet unrecognized host species. Veterinary diagnostic laboratories should therefore consider the possible diagnosis of S. schleiferi ssp. coagulans among coagulase-positive staphylococci isolated from any host species. In the case of the Antarctic seal isolates in this study, they were recovered from mouth swabs from apparently healthy animals, suggesting that S. schleiferi ssp. coagulans is an oral commensal in this setting. The grey seal isolates in this study were isolated post-mortem from dead seals with underlying diseases, but may also have carried commensal S. schleiferi ssp. coagulans that disseminated to the lungs and other organs during ill health or following death. While no link to infection is apparent from these current data, it would be reasonable, based on its epidemiology in dogs, to consider that S. schleiferi ssp. coagulans may also act as a commensal and opportunistic pathogen in seals and other hosts.

The three Antarctic seal isolates in this study were able to ferment trehalose, which is considered to be a feature of S. schleiferi ssp. schleiferi but not typical of S. schleiferi ssp. coagulans [2]. The isolates therefore represent further phenotypic diversity among S. schleiferi ssp. coagulans and highlight the potential difficulty of relying on any single phenotype to differentiate closely related bacterial species or subspecies.

The phylogenetic analysis clearly differentiated the two S. schleiferi subspecies, and in agreement with ANI data, showed that all six seal isolates belonged to the subspecies S. schleiferi ssp. coagulans. While some of the seal isolates were closely related to each other, distinct strains are nonetheless present in seal species. Interestingly, A/G14/99/8 and A/W41/99/1 were identical across all 2 093 618 positions, despite being isolated at different sites and being from different host species, which is suggestive of transmission between individual Antarctic seals or exposure to a common source.

While the number of sequenced isolates is small for both S. schleiferi subspecies, the phylogenetic analysis does indicate rather limited diversity among the S. schleiferi ssp. schleiferi isolates sequenced to date compared to S. schleiferi ssp. coagulans (mean pairwise SNP distance 816 versus 14 189). This may be partly caused by the wider range of host species and country of origin among the currently sequenced S. schleiferi ssp. coagulans isolates.

In addition to cases of related seal isolates, two other clusters of related S. schleiferi ssp. coagulans are also apparent in the phylogenetic analysis. These were all canine isolates, but in each case these included isolates from distant countries, the USA and the UK in one instance and the USA and the Republic of Korea in the other. This suggests the international dissemination of these clones and such apparent clonal expansion may represent particularly successful or virulent clones that may merit further investigation. Of course, the phylogenetic tree is limited to a rather small number of available genome sequenced isolates and the sequencing of further isolates from different geographical areas, host species, isolation sites, carriage and disease will greatly improve our knowledge of S. schleiferi biology. For instance, certain strains of S. schleiferi ssp. coagulans may show host specificity, as seen among Staphylococcus aureus lineages [40, 41].

None of the isolates showed phenotypic or genotypic resistance to antimicrobials, although it is worth noting that methicillin-resistant S. aureus (MRSA) has been isolated from wild harbour seals (Phoca vitulina) previously, including one animal inhabiting Scottish waters [42, 43].

In conclusion, we report the isolation and genome sequencing of six S. schleiferi ssp. coagulans isolates from three species of seal, including Antarctic fur seal, which represents the first report from an otariid species, and the first report from grey seal, which represents the only isolation from a species of seal resident in the Northern Hemisphere to date. We present the first genome-based phylogeny for the S. schleiferi species, showing that the two currently recognized subspecies are clearly defined. In addition, while this phylogenetic analysis is limited by the availability of sequenced isolates, it does highlight the international dissemination of canine isolates, which may be linked to the clonal expansion of particularly fit or virulent lineages and should be investigated further.

Supplementary Data

Supplementary material 1
Click here for additional data file. (14.3KB, xlsx)

Funding information

Culture of Antarctic seals was funded by the British Antarctic Survey. Grey seal post-mortems were carried out under the Scottish Marine Animals Stranding Scheme, which receives funding from the Scottish Government Marine Directorate and the UK Department of Environment, Farming and Rural Affairs (Defra). Internal funding to G. K. P. at the University of Edinburgh.

Acknowledgements

We are grateful to Lesley F Thomson, formerly of British Antarctic Survey Plymouth, UK for provision of seal samples. Genome sequencing was provided by MicrobesNG (http://www.microbesng.uk). The excellent technical assistance of Jennifer Harris and Sarah Goodbrand at the Royal (Dick) School of Veterinary Studies, University of Edinburgh is gratefully acknowledged.

Conflicts of interest

The authors declare that there are no conflicts of interest.

Ethical statement

The Antarctic seal samples were collected by a third party with no extant records of the ethical approval given at the time of their collection in 1993. However, it was determined that sampling was minimally invasive with brief oral swabbing at a distance when the free-living animals yawned naturally. The three North Sea isolates were collected from wild seals found dead by natural causes and post-mortem examined to determine their cause of death under the Scottish Marine Mammals Strandings Scheme funded by the Scottish and UK Governments. In these circumstances, no ethical approval was deemed necessary.

Footnotes

Abbreviations: ANI, average nucleotide identity; ATCC, American Type Culture Collection; CSI Phylogeny, Call SNPs and Infer Phylogeny; MRSA, methicillin-resistant Staphylococcus aureus; NCTC, National Collection of Type Cultures; SMMSS, Scottish Marine Mammals Strandings Scheme; SNP, single nucleotide polymorphism; SRUC, Scotland's Rural College.

One supplementary table is available with the online version of this article.

Sequencing reads and genome assemblies from this study have been deposited with GenBank under the following accessions: A/G14/99/8 SRR10919442 and JAABPD000000000; A/G16/00/1 SRR10919444 and JAABPB000000000; A/W41/99/1 SRR10919443 and JAABPC000000000; 66170 SRR10919441 and JAABPE000000000; 65195 SRR10919440 and JAABPF000000000; M615/02/4 SRR11842963 and JABTCN000000000; M31/11/1 SRR11842962 and JABTCO000000000; M611545/16/1 SRR11842961 and JABTCP000000000.

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. doi: 10.1099/00207713-40-4-409. [DOI] [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. doi: 10.1016/j.vetmic.2019.108472. [DOI] [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. doi: 10.2460/ajvr.72.1.96. [DOI] [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. doi: 10.1128/JCM.32.2.388-392.1994. [DOI] [PMC free 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. doi: 10.4103/0971-5916.182629. [DOI] [PMC free 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. doi: 10.1016/j.vetmic.2005.01.002. [DOI] [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. doi: 10.1128/JCM.01653-17. [DOI] [PMC free 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. doi: 10.1128/JCM.02869-15. [DOI] [PMC free 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. doi: 10.1093/clinids/24.5.1014. [DOI] [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. doi: 10.1161/01.cir.97.18.1791. [DOI] [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. doi: 10.5812/jjm.18591v2. [DOI] [PMC free 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. doi: 10.1007/BF02111833. [DOI] [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. doi: 10.1128/JCM.31.4.812-818.1993. [DOI] [PMC free 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. doi: 10.1128/JCM.36.8.2214-2219.1998. [DOI] [PMC free 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. doi: 10.1128/JCM.37.10.3353-3356.1999. [DOI] [PMC free 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. doi: 10.1111/jam.12545. [DOI] [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. doi: 10.1292/jvms.67.263. [DOI] [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. doi: 10.2460/javma.2005.227.928. [DOI] [PubMed] [Google Scholar]
  • 20.Foster G, Barley J. Staphylococcus schleiferi subspecies coagulans in dogs. Vet Rec. 2007;161:496. doi: 10.1136/vr.161.14.496. [DOI] [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;2014:850126. doi: 10.1155/2014/850126. [DOI] [PMC free 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. doi: 10.1292/jvms.10-0172. [DOI] [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. doi: 10.1111/j.1365-3164.2007.00604.x. [DOI] [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. doi: 10.1089/fpd.2013.1492. [DOI] [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. doi: 10.1111/lam.12304. [DOI] [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. doi: 10.1515/pjvs-2015-0081. [DOI] [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. doi: 10.1186/s13028-017-0328-6. [DOI] [PMC free 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;8:204.:E204. doi: 10.3390/microorganisms8020204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–2120. doi: 10.1093/bioinformatics/btu170. [DOI] [PMC free 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. doi: 10.1089/cmb.2012.0021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30:2068–2069. doi: 10.1093/bioinformatics/btu153. [DOI] [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. doi: 10.1007/s10482-017-0844-4. [DOI] [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. doi: 10.1093/jac/dks261. [DOI] [PMC free 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. doi: 10.1128/MRA.00062-19. [DOI] [PMC free 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. doi: 10.4142/jvs.2020.21.e11. [DOI] [PMC free 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. doi: 10.1128/genomeA.01011-15. [DOI] [PMC free 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. doi: 10.1128/genomeA.01268-15. [DOI] [PMC free 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. doi: 10.1371/journal.pone.0104984. [DOI] [PMC free 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. doi: 10.1093/nar/gkz239. [DOI] [PMC free 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. doi: 10.1016/j.tim.2019.12.007. [DOI] [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. doi: 10.1038/s41559-018-0617-0. [DOI] [PMC free 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. doi: 10.1136/vr.d4199. [DOI] [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. doi: 10.1093/jac/dks329. [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplementary material 1
Click here for additional data file. (14.3KB, xlsx)

Articles from Access Microbiology are provided here courtesy of Microbiology Society

RESOURCES