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.

Evolutionary genomics reveals variation in structure and genetic content implicated in virulence and lifestyle in the genusGaeumannomyces

“…All nine Gaeumannomyces strains were found to contain at least one giant TE belonging to the Starship superfamily of giant cargo-carrying TEs (Gluck-Thaler et al 2022), identified using the tool starfish (Gluck-Thaler and Vogan 2023). Currently the most reliable identifying feature of Starships is a single ‘captain’ gene – a tyrosine recombinase gene containing a DUF3435 domain which is found in the first position of each Starship and directs the mobilisation of the element (Urquhart et al 2023b).…”

“…These two genes were then used for a local blastp v2.13.0 search against all nine Gaeumannomyces assemblies reported here, which identified 33 full length hits (>95% identity) that were associated with insertions when visualised in Circos plots. This manual approach was then compared to Starship element identification using starfish v1.0 (Gluck-Thaler and Vogan 2023). One element identified by starfish was discounted as it consisted solely of a single predicted captain gene with no cargo or flanking repeats.…”