The origin of human pathogenicity and biological interactions in Chaetothyriales

Abstract

Fungi in the order Chaetothyriales are renowned for their ability to cause human infections. Nevertheless, they are not regarded as primary pathogens, but rather as opportunists with a natural habitat in the environment. Extremotolerance is a major trend in the order, but quite different from black yeasts in Capnodiales which focus on endurance, an important additional parameter is advancing toxin management. In the ancestral ecology of rock colonization, the association with metabolite-producing lichens is significant. Ant-association, dealing with pheromones and repellents, is another mainstay in the order. The phylogenetically derived family, Herpotrichiellaceae, shows dual ecology in monoaromatic hydrocarbon assimilation and the ability to cause disease in humans and cold-blooded vertebrates. In this study, data on ecology, phylogeny, and genomics were collected and analyzed in order to support this hypothesis on the evolutionary route of the species of Chaetothyriales. Comparing the ribosomal tree with that of enzymes involved in toluene degradation, a significant expansion of cytochromes is observed and the toluene catabolism is found to be complete in some of the Herpotrichiellaceae. This might enhance human systemic infection. However, since most species have to be traumatically inoculated in order to cause disease, their invasive potential is categorized as opportunism. Only in chromoblastomycosis, true pathogenicity might be surmised. The criterion would be the possible escape of agents of vertebrate disease from the host, enabling dispersal of adapted genotypes to subsequent generations.

Development of PCR-Multiplex Assays for Identification of the Herpotrichiellaceae Family and Agents Causing Chromoblastomycosis

“…Determining the family is clinically important as it excludes a series of other agents causing FEO [5,9], limiting the species to specific known agents. In the context of surveillance and research, identifying species within the Herpotrichiellaceae family aids in the development of studies and the monitoring of the diversity and occurrence of these agents in the environment [2,3,41].…”

“…The identification of these pathogens not only aids in the management of associated infections [13,14] but is also essential for the development of fundamental research to enhance the epidemiological understanding of both PHM and CBM, thus improving the comprehension of the biological diversity within this family and its environmental and parasitic relationships [2,3].…”

Sugarcane: an unexpected habitat for black yeasts in Chaetothyriales

“…In Herpotrichiellaceae , morphological features are highly variable within species, and are polyphyletic within the order Chaetothyriales (Quan et al 2020 ). For this reason, description of phenotypes is significant to understand the ecology of the fungus at hand, but provides no reliable diagnostic features (Quan et al 2023 ). Although the new species are morphologically hardly distinguishable from other species of the genera Cladophialophora and Exophiala , the multilocus analysis revealed a robust phylogenetic distance.…”

Fungi as mutualistic partners in ant-plant interactions

“…In contrast, most domatia-associated Chaetothyriales cluster close to Cyphellophoraceae and Paracladophialophoraceae ( Quan et al., 2023 ) in a monophyletic clade that is composed of domatia-associated species only (“domatia symbiont clade”) and that could potentially constitute a distinct family ( Voglmayr et al., 2011 ; Vasse et al., 2017 ; Quan et al., 2020 ). The substantial genome (and gene) reduction reported for species in the domatia symbiont clade ( Moreno et al., 2019 ) suggests a long evolutionary specialization.…”

“…In addition, the closest relatives of these clades are the families Cyphellophoraceae and Phaeosaccardinulaceae, mostly composed of plant-associated species ( Quan et al., 2020 ). Domatia species also occur in Cyphellophoraceae, but also in Herpotrichiellaceae and Trichomeriaceae which have many epiphyllous ones ( Quan et al., 2020 ; Quan et al., 2023 ). The scraping of leaf surfaces by arboreal ants — most probably to collect epiphylls for larval feeding, as observed today ( Davidson et al., 2003 ; Davidson et al., 2016 ) — may have provided many opportunities over time for epiphyllous Chaetothyriales and Capnodiales to adapt and colonize in the environment of newly emerging domatia, where their tolerance to different chemical compounds would give them an advantage over competitors.…”