Transposable elements in eukaryotic organisms have historically been considered “selfish,” at best conferring indirect benefits to their host organisms. The Starships are a recently discovered feature in fungal genomes that are, in some cases, predicted to confer beneficial traits to their hosts and also have hallmarks of being transposable elements. Here, we provide experimental evidence that Starships are indeed autonomous transposons, using the model Paecilomyces variotii , and identify the HhpA “Captain” tyrosine recombinase as essential for their mobilization into genomic sites with a specific target site consensus sequence. Furthermore, we identify multiple recent horizontal gene transfers of Starships , implying that they jump between species. Fungal genomes have mechanisms to defend against mobile elements, which are frequently detrimental to the host. We discover that Starships are also vulnerable to repeat-induced point mutation defense, thereby having implications on the evolutionary stability of such elements.

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 Starship 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 ssf gene cluster, which contributes to formaldehyde resistance, and use it to demonstrate how mobile element evolution shapes fungal adaptation. We found that ssf clusters have been acquired by various distantly related Starships , which each exhibit multiple instances of horizontal transfer across fungal species (at least nine events, including between different taxonomic orders). Many ssf clusters have subsequently integrated into their host’s genome, illustrating how Starships shape the evolutionary trajectory of fungal hosts beyond any single transfer. Our results demonstrate the key role Starships play in mediating rapid and repeated adaptation via HGT, elevating the importance of mobile element evolution in eukaryotic biology.

Natural gene drives have shaped the genomes of many eukaryotes and recently have been considered for applications to control undesirable species. In fungi, these loci are called spore killers.

Whole genome sequencing is rapidly increasing phylogenetic resolution across many groups of fungi. To improve sequencing coverage in the genus Paecilomyces (Eurotiales), we report nine new Paecilomyces genomes representing five different species. Phylogenetic comparison between these genomes and those reported previously showed that Paecilomyces paravariotii is a distinct species from its close relative P. variotii. The independence of P. paravariotii is supported by analysis of overall gene identify (via BLAST), differences in secondary metabolism and an inability to form ascomata when paired with a fertile P. variotii strain of opposite mating type. Furthermore, whole genome sequencing resolves the P. formosus clade into three separate species, one of which lacked a valid name that is now provided.

Horizontal gene transfer (HGT) is an important and potentially frequent process impacting the evolutionary trajectory of eukaryotic species. Yet to date, the mechanism of HGT among eukaryotes has remained a mystery. Here, we demonstrate that Starships, a newly discovered group of cargo-mobilizing transposable elements, are active vectors of horizontally transferred DNA among eukaryotic species. We find that multiple Starships simultaneously transfer themselves and their cargo within and between fungal genera separated by upwards of 100 million years of evolution. Transferred Starships are recovered in strains with and without selection for particular Starship-encoded phenotypes. Using whole genome sequencing, we exclude alternative hypotheses such as heterokaryosis, parasex or the random uptake of exogenous DNA by showing that only Starship DNA is precisely transferred. Furthermore, we demonstrate that the introduction of the Hephaestus Starship into a new species increases metal resistance due to the genes carried by this element. Between 18-27% of all Starships in our focal genus, Paecilomyces, have evidence of horizontal transfer under natural conditions, including to other fungal genera, revealing Starship-mediated HGT to be a widespread and frequent phenomenon across filamentous fungi. This study identifies the first active genetic mechanism for HGT between eukaryotic species.