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Linking genome evolution and physiological adaptations to understand lifestyle transition and emergence of pathogenicity in the Trichosporonales (Agaricomycotina)

Subject Area Evolution and Systematics of Plants and Fungi
Medical Microbiology and Mycology, Hygiene, Molecular Infection Biology
Microbial Ecology and Applied Microbiology
Metabolism, Biochemistry and Genetics of Microorganisms
Term from 2021 to 2024
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 460261834
 
Final Report Year 2024

Final Report Abstract

In recent years, the emergence of new fungal pathogens for humans has posed significant health threats. Fungal pathogens are known for their diversity and rapid adaptation to host defenses. Despite the growing threat of fungal pathogens, little is known about their transition from saprotrophic to pathogenic lifestyles. To gain insights into fungal lifestyle transitions, we studied the Trichosporonales order, which includes both saprotrophic species and opportunistic human pathogens, as a system to reveal evolutionary adaptations leading to virulence in fungi. The study focused on multiple areas of fungal biology, particularly how the adaptive translation of metabolic pathways influences physiology and ecology of these fungi. We found that distinct molecular mechanisms have evolved to support these different ecological strategies. Namely, opportunistic pathogens show tRNA profiles and codon usage bias that facilitate the translation of proteins essential for rapid host colonization, while allowing them to remain competitive in natural environments. In contrast, saprotrophic fungi display translational adaptations that enhance the breakdown of organic matter present in the environment. The predicted genomic signatures associated with these adaptations and lifestyles are supported by in vitro experimental assays. These findings provide insights into how tRNA molecules, in combination with codon usage bias, regulate rapid adaptation to new ecological niches. This project links genomic data to fungal physiology and ecology, while providing insights into fungal lifestyle evolution and pathogenesis. Additionally, this project contributed to the identification and classification of a new fungal class, Peribolosporomycetes. Members of this new lineage are osmotolerant and heat-resistant basidiomycetes adapted to extreme conditions, such as saline or high-temperature habitats. The description of this new class highlights the ecological diversity within fungal habitats and survival strategies. In summary, this project provides evolutionary and physiological insights into how fungi adapt to different environments, either as decomposers or opportunistic human pathogens. It also provides the basis for developing tools to predict fungal lifestyles based on genomic and physiological data. These findings have practical implications for medical mycology, environmental conservation, biotechnology and predictive biology. Understanding the evolutionary, genetic, molecular, and physiological adaptations that enable fungi to colonize various environments may promote future progresses in fungicides, fungal-derived enzymes and sustainability efforts.

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