Resolving the taxonomy of emerging zoonotic pathogens in the Trichophyton benhamiae complex

Species of the Trichophyton benhamiae complex are predominantly zoophilic pathogens with a worldwide distribution. These pathogens have recently become important due to their epidemic spread in pets and pet owners. Considerable genetic and phenotypic variability has been revealed in these emerging pathogens, but the species limits and host spectra have not been clearly elucidated. In this study, we used an approach combining phylogenetic analysis based on four loci, population-genetic data, phenotypic and physiological analysis, mating type gene characterization and ecological data to resolve the taxonomy of these pathogens. This approach supported the inclusion of nine species in the complex, including three new species and one new variety. Trichophyton benhamiae var. luteum var. nov. (“yellow phenotype” strains) is currently a major cause of zoonotic tinea corporis and capitis in Europe (mostly transmitted from guinea pigs). This variety exhibits unique phenotypic and ecological characteristics compared to T. benhamiae var. benhamiae and is distinguishable by using microsatellite markers but not with the conventional DNA sequence markers used here. We demonstrated that isolates of the “white phenotype” do not form a monophyletic group and are segregated into T. benhamiae var. benhamiae (mostly from North America; dogs), T. europaeum sp. nov. (mostly from Europe; guinea pigs), and T. japonicum sp. nov. (the major cause of zoonotic infections in Japan but also found in Europe; rabbits and guinea pigs). The name T. africanum sp. nov. is proposed for the “African” race of T. benhamiae. The extinction of one mating type gene and adaptation to different hosts have played important roles in the evolution of pathogens from the T. benhamiae complex. A microsatellite typing scheme consisting of ten markers was developed for the purpose of the epidemiological surveillance of these emerging pathogens. MALDI-TOF MS was able to discriminate between the newly proposed species and varieties, suggesting that this method is useful for identification in clinical practice.