Taxonomy of the Trichophyton mentagrophytes/T. interdigitale Species Complex Harboring the Highly Virulent, Multiresistant Genotype T. indotineae

Abstract

A severe outbreak of highly virulent and multi-resistant dermatophytosis by species in the Trichophyton mentagrophytes/T. interdigitale complex is ongoing in India. The correct identity of the etiologic agent is a much-debated issue. In order to define species limits, a taxonomic study was undertaken combining molecular, morphological, and physiological characteristics as evidence of classification. Molecular characteristics show that T. mentagrophytes s. str. and T. interdigitale s. str. can be distinguished with difficulty from each other, but are unambiguously different from the Indian genotype, T. indotineae by sequences of the HMG gene. The entities were confirmed by multilocus analysis using tanglegrams. Phenotypic characters of morphology and physiology are not diagnostic, but statistically significant differences are observed between the molecular siblings. These properties may be drivers of separate evolutionary trends. Trichophyton mentagrophytes represents the ancestral, homothallic cloud of genotypes with a probable geophilic lifestyle, while T. indotineae and T. interdigitale behave as anthropophilic, clonal offshoots. The origin of T. indotineae, which currently causes a significant public health problem, is zoonotic, and its emergence is likely due to widespread misuse of antifungals.

Keywords: Dermatophytosis; India; Multiresistance; Outbreak; Trichophyton indotineae.

Fig. 1

Tanglegram of 113 strains generated from Tef1-α (left) tree, ITS (central) tree, HMG tree (right)

Fig. 2

Maximum Likelihood tree generated from Tef1-α, ITS, and HMG sequences of 113 strains, combined with the source data of the strains

Fig. 3

Maximum likelihood tree constructed using HMG sequences and General Time Reversible model in MEGA7; combined with morphology and physiology results T. Trichophyton

Fig. 4

Phenotypic methodology followed in the study. a Tween-80 opacity negative result b Tween-80 opacity positive result. c Hair perforation test positive result. d Hair perforation test negative result e Keratin azure agar evaluation from left to right; positive, weakly positive, negative. f Evaluation of urease activity; from left to right; negative, weakly positive and positive

Fig. 5

Summary of the hypothesis proposed in the current study. Terrestrial ancestral species harboring both mating types and able to infect burrowing animals is producing populations which are clonal and highly adapted to the human host