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Fungi are ubiquitous and inhabit every known terrestrial habitat. Pathogenic fungi are highly diverse, and recent years have seen an uprise in the emergence of new pathogens on crops, animals and humans. The order Trichosporonales (Tremellomycetes, Agaricomycotina, Basidiomycota) harbours saprobic and a few opportunistic human pathogenic species. These emerging pathogens cause superficial skin irritations, as well as invasive life-threatening infections. Yet, little is known about their evolution, ecology, virulence mechanisms and transition to pathogenic lifestyles. In this study we aimed to determine genomic signatures associated with lifestyle transitions, virulence and host/substrate specialization among 30 Trichosporonales species from a total of 41 genome sequences. We used comparative analyses of genome content, including gene functional categories, repetitive element content and tRNA composition among saprotrophic and reported opportunistic human pathogens. A genome-scale phylogenetic reconstruction revealed that even though the different genera are monophyletic, opportunistic pathogenic species are present in distantly-related clades. Statistical analyses showed that differences in genome structure among species did not correlate with predicted lifestyles. Intriguingly, we found that tRNA content varied widely across species (from 51 to 1455 manually curated tRNA genes). The expansion was independent from the phylogenetic structure. Opportunistic pathogenic species showed an overall increased efficiency in the translation of genes associated with host colonization (i.e. lipid metabolism), while exclusively saprotrophic species showed an increase translation efficiency for genes associated with a saprotrophic lifestyle (i.e. carbohydrate metabolism). This pattern was consistent among distantly-related saprotrophic and pathogenic Cryptococcus species (order Tremellales). In conclusion, our analyses link genomic information with ecology and fungal lifestyles across an entire order. We find evidence for an evolutionary scenario where distinct habitats select for an optimized translation of genes involved in successful proliferation in the respective habitat. We predict that lifestyles are not strictly defined by gene repertoires, but also by expression profiles in fungal pathogens.
