The <i>Enterprise</i> , a massive transposon carrying <i>Spok</i> meiotic drive genes

Abstract

The genomes of eukaryotes are full of parasitic sequences known as transposable elements (TEs). Here, we report the discovery of a putative giant tyrosine-recombinase-mobilized DNA transposon, <i>Enterprise</i>, from the model fungus <i>Podospora anserina</i> Previously, we described a large genomic feature called the <i>Spok</i> block which is notable due to the presence of meiotic drive genes of the <i>Spok</i> gene family. The <i>Spok</i> block ranges from 110 kb to 247 kb and can be present in at least four different genomic locations within <i>P. anserina</i>, despite what is an otherwise highly conserved genome structure. We propose that the reason for its varying positions is that the <i>Spok</i> block is not only capable of meiotic drive but is also capable of transposition. More precisely, the <i>Spok</i> block represents a unique case where the <i>Enterprise</i> has captured the <i>Spok</i>s, thereby parasitizing a resident genomic parasite to become a genomic hyperparasite. Furthermore, we demonstrate that <i>Enterprise</i> (without the <i>Spoks</i>) is found in other fungal lineages, where it can be as large as 70 kb. Lastly, we provide experimental evidence that the <i>Spok</i> block is deleterious, with detrimental effects on spore production in strains which carry it. This union of meiotic drivers and a transposon has created a selfish element of impressive size in <i>Podospora</i>, challenging our perception of how TEs influence genome evolution and broadening the horizons in terms of what the upper limit of transposition may be.