Gene acquisition by giant transposons primes eukaryotes for rapid evolution via horizontal gene transfer

Horizontal gene transfer (HGT) disseminates genetic information between species and is a powerful mechanism of adaptation. Yet, we know little about its underlying drivers in eukaryotes. Giant <i>Starship</i> transposons have been implicated as agents of fungal HGT, providing an unprecedented opportunity to reveal the evolutionary parameters behind this process. Here, we characterize the <i>ssf</i> gene cluster, which contributes to formaldehyde resistance, and use it to demonstrate how mobile element evolution shapes fungal adaptation. We found that <i>ssf</i> clusters have been acquired by various distantly related <i>Starships</i>, which each exhibit multiple instances of horizontal transfer across fungal species (at least nine events, including between different taxonomic orders). Many <i>ssf</i> clusters have subsequently integrated into their host's genome, illustrating how <i>Starships</i> shape the evolutionary trajectory of fungal hosts beyond any single transfer. Our results demonstrate the key role <i>Starships</i> play in mediating rapid and repeated adaptation via HGT, elevating the importance of mobile element evolution in eukaryotic biology.