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Staphylococcus Debuckii Sp. Nov., a Coagulase-Negative Species from Bovine Milk

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Staphylococcus Debuckii Sp. Nov., a Coagulase-Negative Species from Bovine Milk TAXONOMIC DESCRIPTION Naushad et al., Int J Syst Evol Microbiol DOI 10.1099/ijsem.0.003457 Staphylococcus debuckii sp. nov., a coagulase-negative species from bovine milk Sohail Naushad,1,2,* Uliana Kanevets,1 Diego Nobrega,1,2 Domonique Carson,1,2 Simon Dufour,2,3 Jean-Philippe Roy,2,4 P. Jeffrey Lewis2,5 and Herman W. Barkema1,2 Abstract A novel type strain, designated SDB 2975T (=CECT 9737T=DSM 105892T), of the novel species Staphylococcus debuckii sp. nov. isolated from bovine milk is described. The novel species belongs to the genus Staphylococcus and showed resistance to tetracycline and was oxidase- and coagulase-negative, catalase-positive, and Gram-stain-positive. Phylogenetic relationships of Staphylococcus debuckii SDB 2975T to other staphylococcal species were inferred from 16S rRNA gene and whole- genome-based phylogenetic reconstruction. The 16S rRNA gene comparisons showed that the strain is closely related to Staphylococcus condimenti (99.73 %), Staphylococcus piscifermentans (99.66 %), Staphylococcus carnosus (99.59 %) and Staphylococcus simulans (98.03 %). Average nucleotide identity (ANI) values between S.taphylococcus debuckii SDB 2975T and its closely related Staphylococcus species were 83.96, 94.5, 84.03 and 78.09 %, respectively, and digital DNA–DNA hybridization (dDDH) values were 27.70, 58.02, 27.70 and 22.00 %, respectively. The genome of Staphylococcus debuckii SDB 2975T was sequenced with PacBio and Illumina technologies and is 2 691 850 bp long, has a G+C content of 36.6 mol% and contains 2678 genes and 80 RNAs, including six copies of each5S rRNA, 16S rRNA and 23S rRNA genes. Biochemical profiling and a newly developed PCR assay enabled differentiation of Staphylococcus debuckii SDB 2975T and three other SDB strains from its closest staphylococcal species. Differentiation was also achieved by matrix-assisted laser desorption/ ionization time-of-flight mass spectrometry (MALDI-TOF). Genes unique to Staphylococcus debuckii were identified and a PCR- based assay was developed to differentiate Staphylococcus debuckii from other staphylococcal species. In conclusion, the results of phylogenetic analysis along with the ANI values <95 %, and dDDH values <70 % from closely related species along with the phenotypic and biochemical characteristics and specific MALDI-TOF profiles demonstrated that Staphylococcus debuckii SDB 2975T represents a novel species within the genus Staphylococcus, named Staphylococcus debuckii sp. nov. (SDB 2975T=CECT 9737T=DSM 105892T). Non-aureus staphylococci (NAS), commonly known as genus Staphylococcus are Gram-positive cocci that occur coagulase-negative staphylococci (CNS), are the most fre- singly, in pairs, short chains and irregular grape-like clusters quently isolated organisms from bovine mastitis milk [9]. Since its description, classification of the genus Staphy- worldwide [1–4]. NAS belong to the genus Staphylococcus, lococcus has been under active revisions [10–12]. Many new first described in 1884 [5], and currently (as of September Staphylococcus species have been described in the last 2018) consists of 51 species and 28 subspecies (www.bac- decade [13–16]. However, in the past, description of novel terio.net/staphylococcus.html), out of which 25 NAS species staphylococcal species was solely based upon morphological are most commonly identified from bovine milk in Canada, and biochemical characteristics [9, 17]. However, these the phylogeny, distribution, virulence and antimicrobial methods do not always identify Staphylococcus species reli- resistance profiles of those 25 NAS species were described ably [15, 18, 19]. Many new rules of genome-based classifi- recently [2, 6–8]. Morphologically, the members of the cation and methods of identification have been published in Author affiliations: 1Department of Production Animal Health, Faculty of Veterinary Medicine, University of Calgary, 3330 Hospital Drive NW, Calgary AB, Canada; 2Canadian Bovine Mastitis and Milk Quality Research Network, St-Hyacinthe, QC, Canada; 3Department of Pathology and Microbiology, Faculty of Veterinary Medicine, University of Montreal, Saint-Hyacinthe QC, Canada; 4Department of Clinical Sciences, Faculte de medecine vet erinaire, Universite de Montreal, 3200 Rue Sicotte, St-Hyacinthe, Quebec, Canada; 5Department of Pathology and Microbiology, Atlantic Veterinary College, University of Prince Edward Island, Charlottetown, PE, Canada. *Correspondence: Sohail Naushad, [email protected] Keywords: novel species; coagulase-negative staphylococci; bovine intramammary infection; whole-genome sequencing; virulence factors; antimicrobial resistance. Abbreviations: ANI, average nucleotide identity; ARG, antimicrobial resistant gene; CAS, coagulase-negative staphylococci; dDDH, digital DNA–DNA hybridization; GGDC, Genome-to-Genome Distance Calculator; ML, maximum-likelihood; MSA, multiple sequence alignment; NAS, non-aureus staphy- lococci; OGRI, overall genome related index; WGS, whole-genome sequencing. One supplementary table is available with the online version of this article. 003457 ã 2019 The Authors Downloaded from www.microbiologyresearch.org by This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. IP: 54.70.40.11 1 On: Sat, 22 Jun 2019 10:18:51 Naushad et al., Int J Syst Evol Microbiol the last decade [20–24]. With the advent of next-generation Each of them was originally assigned as Staphylococcus pisci- sequencing technologies, bacterial species are currently fermentans with scores of 1.757, 1.831 and 1.864, respec- being recognized based on whole-genome sequences, aug- tively. These scores are within the ‘probable genus mented with matrix-assisted laser desorption/ionization identification’ only, with insufficiently reliable species time-of-flight mass spectrometry (MALDI-TOF MS) demarcation. Following more analyses, we eventually and phenotypic and chemotypic characterization [23–26]. named them Staphylococcus debuckii SDB 3462 (MQM ID Two prokaryotic bacteria are typically regarded as different 3462) isolated from fourth quarter (right rear) of a cow 15 species if genomic DNA exhibits a DNA–DNA hybridiza- days after calving and Staphylococcus debuckii SDB 5244 tion (DDH) value <70 % [27, 28], with the DDH value (MQM ID 5244) and Staphylococcus debuckii SDB 5264 reflecting relatedness or similarity between two genomes. (MQM ID 5264), both isolated from the same second quar- However, after several studies proposed the replacement of ter (left rear) of a cow 5 and 13 days after calving, DDH with pairwise genome-sequence derived similarity respectively. indices, the overall genome related index (OGRI) has become an alternative (to DDH) accepted standard for pro- PHYLOGENY karyotic speciation [20, 23, 24]. Like DDH, OGRI can be Core genome (Fig. 1) and 16S rRNA gene (Fig. 2) trees of used to check if a strain belongs to a known species by cal- T culating the relatedness between genome sequences of novel staphylococcal species showed that strain SDB 2975 was strains and type strain of a species [24]. Recently, average most closely related to Staphylococcus condimenti (99.73 %), nucleotide identity (ANI) and digital DDH (dDDH) have S. piscifermentans (99.66 %), S. carnosus (99.59 %) and S. been most widely used for bacterial species demarcation simulans (98.03 %), with percentage similarity (16S – rRNA gene) for each species shown in parentheses. How- [13, 26, 29 31]. The proposed and generally accepted spe- T cies boundary for ANI and dDDH values are 95~96 and ever, apart from distinct branching of strain SDB 2975 in 70 %, respectively [24]. the phylogenetic trees, the 16S rRNA gene sequences simi- larities were not distinct enough for determining the species. Following recommended guidelines [17, 32] and the new Traditionally, newly discovered bacterial strains in most rules of classification [20, 24], herein we describe strain SDB T T T cases have been defined as members of the same species if 2975 (=CECT 9737 =DSM 105892 ) as the type strain of they share 97 % or greater 16S rRNA gene sequence similar- the novel species Staphylococcus debuckii sp. nov. We also ity [23, 34, 35]. However, many studies have pointed out report the phenotypic and chemotypic characterization of S. limitations in 16S rRNA gene-based classification of prokar- debuckii, along with the whole-genome sequencing (WGS), yotes, and in many cases bacteria have been misclassified as genome annotation and characterization and phylogenetic members of incorrect taxonomic groups [36–39]. The avail- characteristics. We also generated MALDI-TOF profiles to ability of the whole genomes has enabled resolving many distinguish Staphylococcus debuckii from other closely incorrect taxonomical relationships [40, 41]. In order to related staphylococcal species. compute the core genome phylogeny of Staphylococcus debuckii, complete genomes of S. carnosus LTH 3730 ISOLATION AND HOME HABITAT (CP016760.1), S. condimenti DSM 11674T (NZ_CP015114), Strain SDB 2975T was isolated from the milk of the right S. simulans FDAARGOS_124 (NZ_CP014016.1) and S. pis- fore quarter of an eighth lactation cow at 35 days-in-milk cifermentans NCTC13836 (NZ_LT906447.1) were down- housed in a tie-stall herd in Quebec, Canada. The cow pro- loaded from the NCBI. Genome sequences of 25 other bovine duced on average 29 kg of milk per day on a preceding dairy NAS species were
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