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Brumpt 1922 Sp. Nov., Nom. Rev., Isolated from Bovine Digital Dermatitis

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Brumpt 1922 Sp. Nov., Nom. Rev., Isolated from Bovine Digital Dermatitis TAXONOMIC DESCRIPTION Kuhnert et al., Int. J. Syst. Evol. Microbiol. DOI 10.1099/ijsem.0.004027 Treponema phagedenis (ex Noguchi 1912) Brumpt 1922 sp. nov., nom. rev., isolated from bovine digital dermatitis Peter Kuhnert1,*, Isabelle Brodard1, Maher Alsaaod1,2, Adrian Steiner2, Michael H. Stoffel3 and Joerg Jores1 Abstract ‘Treponema phagedenis’ was originally described in 1912 by Noguchi but the name was not validly published and no type strain was designated. The taxon was not included in the Approved Lists of Bacterial Names and hence has no standing in nomen- clature. Six Treponema strains positive in a ‘T. phagedenis’ phylogroup-specific PCR test were isolated from digital dermatitis (DD) lesions of cattle and further characterized and compared with the human strain ‘T. phagedenis’ ATCC 27087. Results of phenotypic and genotypic analyses including API ZYM, VITEK2, MALDI- TOF and electron microscopy, as well as whole genome sequence data, respectively, showed that they form a cluster of species identity. Moreover, this species identity was shared with ‘T. phagedenis’-like strains reported in the literature to be regularly isolated from bovine DD. High average nucleotide identity values between the genomes of bovine and human ‘T. phagedenis’ were observed. Slight genomic as well as phenotypic vari- ations allowed us to differentiate bovine from human isolates, indicating host adaptation. Based on the fact that this species is regularly isolated from bovine DD and that the name is well dispersed in the literature, we propose the species Treponema phagedenis sp. nov., nom. rev. The species can phenotypically and genetically be identified and is clearly separated from other Treponema species. The valid species designation will allow to further explore its role in bovine DD. The type strain for Treponema phagedenis sp. nov., nom. rev. is B43.1T (=DSM 110455T=NCTC 14362T) isolated from a bovine DD lesion in Switzerland. Species of the genus Treponema are spiral- shaped, strictly designated and deposited in at least two culture collections in anaerobic or microaerophilic Gram-negative bacteria. They different countries [3]. None of these criteria have been met are often associated with specific hosts and a fraction of them for ‘T. phagedenis’. are well- recognized pathogens. The genus currently comprises 28 validated species names according to the List of Prokary- The fact that ‘T. phagedenis’ till this day has not been validly otic Names with Standing in Nomenclature [1]. However, published is somehow surprising. The species has been known although on this list, type strains and their corresponding for more than 100 years and the isolation and partial charac- 16S rRNA gene sequences are not available for Treponema terization of ‘T. phagedenis’ or ‘T. phagedenis’-like bacteria from minutum, Treponema paraluiscuniculi, Treponema pertenue bovine digital dermatitis (DD), a globally leading form of foot and Treponema pallidum, even though the latter is the type disease- related lameness in cattle [4], has been reported many species of the genus. The list does not include ‘Treponema times over the years [5–14]. A possible reason might be the fact, phagedenis’ and this name has not been validly published until that ‘T. phagedenis’ was originally isolated from a woman [15] today. To be validly published, a bacterial name must be (i) contained in the Approved List of Bacterial Names [2] or after and that the only ‘T. phagedenis’ strain deposited at a culture 1980 (ii) be published in the IJSB/IJSEM or (iii) if published collection, strain ATCC 27087, is also of human origin and was outside IJSEM be included in a validation list published in isolated from a case of syphilis [16]. This strain has originally there and, finally, (iv) the type strain of the species must be been deposited as T. pallidum Kazan 8. Author affiliations: 1Institute of Veterinary Bacteriology, Vetsuisse Faculty, University of Bern, Bern, Switzerland; 2Clinic for Ruminants, Vetsuisse Faculty, University of Bern, Bern, Switzerland; 3Division of Veterinary Anatomy, Vetsuisse Faculty, University of Bern, Bern, Switzerland. *Correspondence: Peter Kuhnert, peter. kuhnert@ vetsuisse. unibe. ch Keywords: cattle; lameness; digital dermatitis; hoof disease; Treponema. Abbreviations: ANI, average nucleotide identity; DD, digital dermatitis; MALDI- TOF, matrix assisted laser desorption ionization- time of flight; MLST, multi locus sequence typing; MSP, MALDI- TOF reference spectra; TSA, tryptic soy agar. The GenBank accession number for the 16S rRNA gene of T. phagedenis B43.1T is MN396624. The genome sequences of T. phagedenis strains have been deposited under accession numbers CP042818 (B43.1T), CP042817 (B36.5), CP042816 (B31.4), CP042815 (S2.3), CP042814 (S8.5), CP042813 (S11.1), and VOQA00000000 (ATCC 27087). One supplementary table is available with the online version of this article. 004027 © 2020 The Authors 1 Kuhnert et al., Int. J. Syst. Evol. Microbiol. 2020 Table 1. Treponema phagedenis strains characterized in this study ISOLation AND strains Designation Year Origin Feet from animals with DD lesions were collected at the T slaughterhouse in Langnau (Canton of Bern) and St. Gallen B43.1 2018 Bovine DD lesion, Switzerland (Canton of St. Gallen) and further processed in the labora- B36.5 2018 Bovine DD lesion, Switzerland tory on the same day. Lesions were cleared mechanically B31.4 2018 Bovine DD lesion, Switzerland from dirt and a swab was taken for nested-PCR analyses [13]. Strain isolation from samples being PCR-positive for the T. S2.3 2019 Bovine DD lesion, Switzerland phagedenis phylogroup was done according to Evans et al. S8.5 2019 Bovine DD lesion, Switzerland [13] from a punch biopsy cut into pieces in an anaerobic work station (Don Whitley Scientific). Six isolates from different S11.1 2019 Bovine DD lesion, Switzerland animals were obtained and preserved at −80 %. Three isolates T ATCC 27087 1965 Human syphilis, Kazan, Russia were obtained from Canton of Bern (B43.1 , B36.5 and B31.4) and another three from the Canton of St. Gallen (S2.3, S8.5 and S11.1). If needed, strains were grown from stocks in oteb (Anaerob Systems) supplemented with 10 % rabbit serum In 1912, Noguchi [15] first described'Spirochaeta phagedenis' (Sigma- Aldrich) or on tripticase soy agar (TSA)–blood plates isolated from a phagedenic lesion on the external genitalia (Oxoid) under anaerobic conditions at 37 °C. The human of a woman for which later the name ‘T. phagedenis’ was T. phagedenis ATCC 27087 as well as the type strains of used [17, 18]. The first report of bovine isolates similar to T. medium ATCC 700293T and T. pedis DSM 18691T were ‘T. phagedenis’ was in 1997 when Choi et al. [12] described obtained from their corresponding culture collections. a strain which was isolated from a bovine DD lesion and which was related to human ‘T. phagedenis’ based as on 16S rRNA gene sequences. This was later confirmed by other PHenotYPIC AND CHemotaxonomic studies using biochemical and genetic comparisons [10, 19]. CHaracteriZation Bovine DD has emerged worldwide since its first descrip- The API ZYM strips (bioMérieux) were used to determine tion in 1974 [20] and has become the most common and enzyme profiles of isolates according to the manufacturer's most important infectious foot disease causing lameness in recommendations. Table 2 shows the enzyme profiles of cattle. Three different Treponema phylogroups were isolated T. phagedenis isolates in comparison to other Treponema and characterized from DD lesions, i.e. T. medium phylo- species. Treponema phagedenis showed consistent results group, T. pedis phylogroup and ‘T. phagedenis’ phylogroup for all reactions except for leucine arylamidase, naphthol- [19, 21]. While the former two are recognized species, the AS- BI- phosphohydrolase and β-glucuronidase. Therefore, latter still awaits taxonomic appraisal [22]. Moreover, several T. phagedenis can be separated from all other Treponema authors have shown that human and bovine ‘T. phagedenis’ species by two or more characters used on the API ZYM strains showed a low level of diversity and should actually system. Conflicting results compared to published data were be described as the same species [10, 19]. A complete taxo- repeatedly obtained with the type strains of T. pedis (acid nomic description would help to investigate the role of this phosphatase) and T. medium (alkaline phosphatase, C8 species in pathogenicity and host–pathogen interaction. It esterase lipase and acid phosphatase) [24]. This may be due is of utmost importance to decipher the causative pathogens to the subjective interpretation of reactions on a scale from 0 of DD, to develop diagnostic assays and to conduct epide- to 5, whereby 0, 1, 2 are considered negative while 3, 4 and 5 miological studies related to DD. We, therefore, propose the are positive according to the supplier. validation of the taxon name Treponema phagedenis sp. nov., In order to gain objective and extended enzyme profiles, we nom. rev. generated data on the automated system VITEK2 using ANC For this purpose, we analysed six Swiss strains isolated from cards (bioMérieux). The T. phagedenis isolates were thereby bovine DD lesions in the framework of a prevalence study [23] compared to type strains of T. pedis and T. medium (Table 3). as well as the human strain ATCC 27087 (Table 1). These strains This way, it was possible to unambiguously identify and separate were first compared to each other using 16SrRNA gene analysis. T. phagedenis by five and four stable characters from T. pedis and Afterwards they were phenotypically characterized by using the T. medium, respectively. Interestingly, the human T. phagedenis API ZYM and VITEK2 microbiological identification systems, ATCC 27087 showed different reactions for LeuA, TyrA, PheA MALDI- TOF and scanning electron microscopy. Afterwards, and OPS compared to all six bovine isolates (Table 3). These next generation sequencing was used to characterize and markers allowed to phenotypically differentiate the human compare the genome sequences. Results of the phenotypic and strain from bovine T. phagedenis isolates.
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