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

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Abstract

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 taxa 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). The isolates of the “white phenotype” do not form a monophyletic group and are segregated into three taxa, T. benhamiae var. benhamiae (mostly North America; dogs), T. europaeum sp. nov. (mostly Europe; guinea pigs), and T. japonicum sp. nov. (predominant in East Asia but also found in Europe; rabbits and guinea pigs). The new species T. africanum sp. nov. is proposed for the “African” race of T. benhamiae. The introduction to new geographic areas and host jump followed by extinction of one mating type gene have played important roles in the evolution of these pathogens. Due to considerable phenotypic similarity of many dermatophytes and phenomena such as incomplete lineage sorting or occasional hybridization and introgression, we demonstrate the need to follow polyphasic approach in species delimitation. Neutrally evolving and noncoding DNA regions showed significantly higher discriminatory power compared to conventional protein-coding loci. Diagnostic options for species identification in practice based on molecular markers, phenotype and MALDI-TOF spectra are presented. A microsatellite typing scheme developed in this study is a powerful tool for the epidemiological surveillance of these emerging pathogens.

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Data availability

The important fungal isolate used for experiments are publically available in the internationally recognized culture collections; newly generated DNA sequences are available in European Nucleotide Archive (ENA) database; alignments are available in the Supplementary material.

Change history

  • 07 January 2021

    The original version of this article has been revised: Missing supplementary material has been added and the captions to supplementary files 5-7 have been corrected.

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Acknowledgements

We are very grateful to Jan Karhan and Lukáš Vít Rýdl for the concept of data visualization and help with graphical adjustments of analysis outputs. We thank Milada Chudíčkova, Petra Seifertová and Adéla Kovaříčková for their invaluable assistance in the laboratory and Peter Mikula for research support. We thank Jiřina Stará, Magdalena Skořepová, Stanislava Dobiášová and Jana Hanzlíčková for providing some of the strains used in this study. The research reported in this publication was part of the long-term goals of the ISHAM working group Onygenales.

Funding

Charles University Grant Agency (GAUK 600217): A. Čmoková; Czech Ministry of Health (AZV 17-31269A): M. Kolařík, R. Dobiáš, H. Janouškovcová, I. Kuklová, N. Mallátová, K. Mencl, T. Větrovský, V. Hubka; BIOCEV (CZ.1.05/1.1.00/02.0109) provided by the Ministry of Education, Youth and Sports of the Czech Republic and ERDF: V. Hubka; Charles University Research Centre program no. 204069: V. Hubka; Czech Academy of Sciences (Project RVO 67985939): M. Man.

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Supplementary file1 Fig. S1 Legend for the host icons used in this study (PDF 559 KB)

13225_2020_465_MOESM2_ESM.pdf

Supplementary file2 Fig. S2 Maximum likelihood tree based on ITS region sequences. Maximum likelihood bootstrap values are appended to the nodes; only support values higher than 70% are shown; the ex-type strains are designated with a superscripted T; Trichophyton rubrum CBS 202.88 was used as the outgroup. Clades with >5 identical sequences are collapsed; *positions refer to the alignment available in the Supplementary material (PDF 76 KB)

13225_2020_465_MOESM3_ESM.pdf

Supplementary file3 Fig. S3 Maximum likelihood tree based on gapdh gene sequences. Maximum likelihood bootstrap values are appended to the nodes; only support values higher than 70% are shown; the ex-type strains are designated with a superscripted T; Trichophyton rubrum CBS 202.88 was used as the outgroup. Clades with >5 identical sequences are collapsed; *positions refer to the alignment available in the Supplementary material (PDF 63 KB)

13225_2020_465_MOESM4_ESM.pdf

Supplementary file4 Fig. S4 Maximum likelihood tree based on tef1-α gene sequences. Maximum likelihood bootstrap values are appended to the nodes; only support values higher than 70% are shown; the ex-type strains are designated with a superscripted T; Trichophyton rubrumTrichophyton rubrum CBS 202.88 was used as the outgroup. Clades with >5 identical sequences are collapsed; *positions refer to the alignment available in the Supplementary material (PDF 80 KB)

13225_2020_465_MOESM5_ESM.pdf

Supplementary file5 Fig. S5 Maximum likelihood tree based on tubb gene sequences. Maximum likelihood bootstrap values are appended to the nodes; only support values higher than 70% are shown; the ex-type strains are designated with a superscripted T; Trichophyton rubrum CBS 202.88 was used as the outgroup. Clades with >5 identical sequences are collapsed (PDF 54 KB)

13225_2020_465_MOESM6_ESM.png

Supplementary file6 Fig. S6 Phylogenetic tree of the Trichophyton benhamiae clade revealed by the analysis of ten microsatellite loci in 318 strains constructed in FAMD software using a Jaccard index-based distance matrix. Coloured circles display the genotype diversity of the ITS, gapdh and tef1-α loci and the distribution of MAT gene idiomorphs across Trichophyton benhamiae clade species (PNG 915 KB)

Supplementary file 7. Supplementary Tables S1–S11 (XLSX 358 KB)

Supplementary file 8. Alignment of the ITS rDNA region sequences (FAS 237 KB)

Supplementary file 9. Alignment of the gapdh gene sequences (FAS 201 KB)

Supplementary file 10. Alignment of the tef1-α gene sequences (FAS 235 KB)

Supplementary file 11. Alignment of the tubb (β-tubulin) gene sequences (FAS 173 KB)

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Čmoková, A., Kolařík, M., Dobiáš, R. et al. Resolving the taxonomy of emerging zoonotic pathogens in the Trichophyton benhamiae complex. Fungal Diversity 104, 333–387 (2020). https://doi.org/10.1007/s13225-020-00465-3

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Keywords

  • Epizootic fungal infections
  • Microsatellite typing scheme
  • Multigene phylogeny
  • Population genetic structure
  • Superficial skin infections
  • Zoophilic dermatophytes