Fungi are mostly investigated for their impact on agriculture, food and technology, and even in these cases these organisms are neglected, compared with bacteria, viruses and other eukaryotes. Yet, fungal diseases kill more than 1.6 million people each year. This evidence requires urgent attention, also because new fungal pathogens are expected to emerge with climate change and environmental pollution. Most human fungal pathogens are opportunistic: their ecological success is not dependent on host infection and their growth in the human body is occasional. Therefore, their genetic traits are shaped by pressures other than those present in the human body, and a connection may be drawn between extremophilic and pathogenic lifestyles. We focused on the genus Scedosporium (Microascaceae), a group of life-threatening fungi with outstanding degradative skills. Since the genomic data is fragmentary for the genus, we sequenced the genomes of S. aurantiacum MUT6114 and S. minutisporum MUT6113, isolated from tannery wastewater and a Polyciclic Aromatic Hydrocarbons (PAHs)-contaminated soil, respectively. We characterized the publicly available Microascaceae genomes, most of which lacked annotation, and provided the first comparative framework for this family. By comparing Microascaceae with other pathogenic and non-pathogenic ascomycetes, we found that quantitative traits are not sufficient to outline a common pathogenic genomic asset and that, from a phylogenomics perspective, there is a lack of convergence of putative pathogenicity traits. We investigated the role of point mutations and transposons insertions in pathogenicity and resistance to drugs, and found that these roles might have both ancient and recent roots. We also use RNA-seq to describe the response of the two isolates to voriconazole, confirming the involvement of previously identified genomic traits. Our results highlight the strengths and limitations of genomics applied to opportunistic human pathogens, the high multifactoriality of pathogenicity and resistance to drugs, and suggest a scenario where pressures other than anthropic ones shaped pathogenic lifestyle in filamentous fungi.
A genomic perspective on filamentous fungal human pathogens: the Scedosporium case.
Francesco Venice;Federica Spina;Stefano Ghignone;Giovanna Cristina Varese
2023-01-01
Abstract
Fungi are mostly investigated for their impact on agriculture, food and technology, and even in these cases these organisms are neglected, compared with bacteria, viruses and other eukaryotes. Yet, fungal diseases kill more than 1.6 million people each year. This evidence requires urgent attention, also because new fungal pathogens are expected to emerge with climate change and environmental pollution. Most human fungal pathogens are opportunistic: their ecological success is not dependent on host infection and their growth in the human body is occasional. Therefore, their genetic traits are shaped by pressures other than those present in the human body, and a connection may be drawn between extremophilic and pathogenic lifestyles. We focused on the genus Scedosporium (Microascaceae), a group of life-threatening fungi with outstanding degradative skills. Since the genomic data is fragmentary for the genus, we sequenced the genomes of S. aurantiacum MUT6114 and S. minutisporum MUT6113, isolated from tannery wastewater and a Polyciclic Aromatic Hydrocarbons (PAHs)-contaminated soil, respectively. We characterized the publicly available Microascaceae genomes, most of which lacked annotation, and provided the first comparative framework for this family. By comparing Microascaceae with other pathogenic and non-pathogenic ascomycetes, we found that quantitative traits are not sufficient to outline a common pathogenic genomic asset and that, from a phylogenomics perspective, there is a lack of convergence of putative pathogenicity traits. We investigated the role of point mutations and transposons insertions in pathogenicity and resistance to drugs, and found that these roles might have both ancient and recent roots. We also use RNA-seq to describe the response of the two isolates to voriconazole, confirming the involvement of previously identified genomic traits. Our results highlight the strengths and limitations of genomics applied to opportunistic human pathogens, the high multifactoriality of pathogenicity and resistance to drugs, and suggest a scenario where pressures other than anthropic ones shaped pathogenic lifestyle in filamentous fungi.
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