Systematic identification of cargo-carrying genetic elements reveals new dimensions of eukaryotic diversity

Abstract

Cargo-carrying mobile elements (CCEs) are genetic entities that transpose diverse protein coding sequences. Although common in bacteria, we know little about the biology of eukaryotic CCEs because no appropriate tools exist for their annotation. For example, Starships are fungal CCEs whose functions are largely unknown because they require time-intensive manual curation. To address this knowledge gap, we developed starfish, a computational workflow for high-throughput eukaryotic CCE annotation. We applied starfish to 2, 899 genomes of 1, 649 fungal species and found that starfish recovers known Starships with >95% precision and accuracy while expanding the number of annotated elements ten-fold. Extant Starship diversity is partitioned into 11 families that differ in their enrichment patterns across fungal classes. Starship cargo changes rapidly such that elements from the same family differ substantially in their functional repertoires, which are predicted to contribute to diverse biological processes such as metabolism. Many elements have convergently evolved to insert into 5S rDNA and AT-rich sequence while others integrate into random locations, revealing both specialist and generalist strategies for persistence. Our work establishes a framework for advancing mobile element biology and provides the means to investigate an emerging dimension of eukaryotic genetic diversity, that of genomes within genomes.