Toward a Novel Multilocus Phylogenetic Taxonomy for the Dermatophytes

Abstract

Type and reference strains of members of the onygenalean family Arthrodermataceae have been sequenced for rDNA ITS and partial LSU, the ribosomal 60S protein, and fragments of β-tubulin and translation elongation factor 3. The resulting phylogenetic trees showed a large degree of correspondence, and topologies matched those of earlier published phylogenies demonstrating that the phylogenetic representation of dermatophytes and dermatophyte-like fungi has reached an acceptable level of stability. All trees showed Trichophyton to be polyphyletic. In the present paper, Trichophyton is restricted to mainly the derived clade, resulting in classification of nearly all anthropophilic dermatophytes in Trichophyton and Epidermophyton, along with some zoophilic species that regularly infect humans. Microsporum is restricted to some species around M. canis, while the geophilic species and zoophilic species that are more remote from the human sphere are divided over Arthroderma, Lophophyton and Nannizzia. A new genus Guarromyces is proposed for Keratinomyces ceretanicus. Thirteen new combinations are proposed; in an overview of all described species it is noted that the largest number of novelties was introduced during the decades 1920-1940, when morphological characters were used in addition to clinical features. Species are neo- or epi-typified where necessary, which was the case in Arthroderma curreyi, Epidermophyton floccosum, Lophophyton gallinae, Trichophyton equinum, T. mentagrophytes, T. quinckeanum, T. schoenleinii, T. soudanense, and T. verrucosum. In the newly proposed taxonomy, Trichophyton contains 16 species, Epidermophyton one species, Nannizzia 9 species, Microsporum 3 species, Lophophyton 1 species, Arthroderma 21 species and Ctenomyces 1 species, but more detailed studies remain needed to establish species borderlines. Each species now has a single valid name. Two new genera are introduced: Guarromyces and Paraphyton. The number of genera has increased, but species that are relevant to routine diagnostics now belong to smaller groups, which enhances their identification.

Keywords: Arthrodermataceae; Dermatophytes; Phylogeny; Taxonomy; Trichophyton.

Fig. 1

Number of name changes of members of Arthrodermataceae during the period 1840–2015, with 5-year increments. The largest number of new names was created when morphology was added to clinical data as criteria for species distinction. The period 1960–1995 is marked by the addition of teleomorph names, leading to dual nomenclature of the dermatophytes. The bar at the right shows the approximate number of existing anthropophilic species (n = 10), the number of times these have been described (basionyms: n = 103) and the total number of name changes for these 10 species (n = 242). Possible [7] and proven synonyms of Trichophyton rubrum are listed in ocher (n = 48), of which (n = 24) were basionyms, in red

Fig. 2

Overview of changing taxonomic principles during the period 1840–2015. Of the oldest species, no original material has been preserved; the rare ones are discarded as being doubtful; the widely used names are neotypified. Latin diagnoses were required between 1937 and 2013. Pleomorphic naming with separate typification of ana- and teleomorph has been relevant between 1957 and 2013. The generic and specific nomenclatural system proposed in the present article is valid from the situation per January 1, 2013 onwards

Fig. 3

Maximum likelihood phylogenetic tree (RAxML v.8.0.0) based on ITS and partial LSU, TUB and 60S L10 sequences of Arthrodermataceae species using GTRCAT as model, with 1000 bootstrap replications, shown when >70 %, where genera were collapsed. Guarromyces ceretanicus was selected as outgroup

Fig. 4

Maximum likelihood phylogenetic tree (RAxML v.8.0.0) based on ITS and partial LSU, TUB and 60S L10 sequences of Trichophyton species using GTR + GI as model, with 1000 bootstrap replications, shown when >70 %. Microsporum gypseum was selected as outgroup

Fig. 5

Maximum likelihood phylogenetic tree (RAxML v.8.0.0) based on ITS and partial LSU, TUB and 60S L10 sequences of Microsporum species using T92 + G as model, with 1000 bootstrap replications, shown when >70 %. Arthroderma grubyi was selected as outgroup