The origin of human pathogenicity and biological interactions in Chaetothyriales
Yu Quan, Shuwen Deng, Francesc X. Prenafeta‐Boldú, Veronika Mayer, Lucía Muggia, Agnese Cometto, Vânia Aparecida Vicente, Nickolas Menezes da Silva, Maria Eduarda Grisolia, Yinggai Song, Sarah Ahmed, Xueke Niu, Bruna Jacomel Favoreto de Souza Lima, Peiying Feng, Roxana G. Vitale, Marcus de Melo Teixeira, Montarop Sudhadham, Conceicao Pedrozo e Silva de Azevedo, Anamélia Lorenzetti Bocca, Gerhard Haase, Laura Selbmann, Dongmei Shi, Yingqian Kang, Sybren de Hoog
Abstract
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.