Extensive horizontal transfer of transposable elements shapes fungal mobilomes

Abstract

Transposons impact eukaryotic genome size and evolution. Horizontal transfer of transposable elements (HTT) is important for their long-term persistence, but it has only been systematically studied in animals, and thus the abundance, impact, and factors that shape HTTs in lineages outside animals are unknown. Fungi are at least as ancient and diverse as animals and are characterized by extensive genome size variation caused by transposons. Here, we screened 1,348 genomes across fungal biodiversity, genome sizes, and lifestyles to detect extensive HTTs, which generated on average 7%-but up to 70%-of the transposon content in some taxa. We in total identified at least 5,906 independent HTTs, mostly involving Tc1/Mariner DNA transposons. While the majority of HTTs occur between closely related taxa, irrespective of their lifestyles, HTTs were particularly common in Mucoromycotina, Sordariomycetes, Dothideomycetes, and Leotiomycetes. Importantly, species lacking fungal-specific defense mechanisms against transposons, and those with gene-sparse and repeat-rich genomic compartments, are involved in a significantly higher number of HTTs, unveiling ecological and genomic factors shaping HTTs. Our findings thus illuminate the dynamic landscape of HTTs in fungi, providing the framework to further study the impact of HTTs on genome evolution and the processes that mediate transposon transfers within and between eukaryotic lineages.