Starships are active eukaryotic transposable elements mobilized by a new family of tyrosine recombinases

Abstract

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 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 transfer of Starships, implying that they frequency 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 defence, thereby having implications on the evolutionary stability of such elements.

A Polyphasic Approach including Whole Genome Sequencing Reveals Paecilomyces paravariotii sp. nov. as a Cryptic Sister Species to P. variotii

“…We previously demonstrated the presence of a large transposable element called hephaestus in strains assigned as P. variotii and, in one strain of P. lecythidis [ 20 , 24 ], an element that increases resistance to at least five toxic metal ions. Subsequently, we have shown evidence to support HGT of hephaestus between P. variotii and P. lecythidis [ 24 ].…”

“…We previously demonstrated the presence of a large transposable element called hephaestus in strains assigned as P. variotii and, in one strain of P. lecythidis [ 20 , 24 ], an element that increases resistance to at least five toxic metal ions. Subsequently, we have shown evidence to support HGT of hephaestus between P. variotii and P. lecythidis [ 24 ]. In the P. variotii CBS 144490 and P. paravariotii FRR 5287 comparison, a set of genes (highlighted in blue) were 100% identical in nucleotide sequence between P. variotii and P. paravariotii .…”

Replitrons: a new group of eukaryotic transposons encoding HUH endonuclease

“…At the turn of the century, the rising availability of whole-genome assemblies led to the discovery of several new eukaryotic TE groups, including three major groups of DNA transposons: Helitrons (Kapitonov and Jurka 2001), the tyrosine recombinase-encoding Cryptons (Goodwin et al 2003), and the self-synthesising Polintons/Mavericks (Kapitonov and Jurka 2006; Pritham et al 2007). New TEs continue to be unearthed as genomic data from previously understudied clades is produced, including new superfamilies of DD(E/D) DNA transposons such as KDZ (Böhne et al 2012; Iyer et al 2014), major clades of retrotransposons such as the Naiad / Chlamys Penelope -like elements (Craig et al 2021), and giant transposons such as Starships (Gluck-Thaler et al 2022; Urquhart et al 2022). Here, I have presented Replitrons, a major new group of eukaryotic DNA transposons that encode a previously uncharacterised Rep HUH endonuclease.…”

That's no moon, it's a Starship: Giant transposons driving fungal horizontal gene transfer

“…Over 100 Starship transposons have now been identified in dozens of Pezizomycetes species, a fungal class within the filamentous Ascomycete phylum (Gluck‐Thaler et al, 2022). Many of these Starships have been observed with exceptionally high sequence identity in very distantly related fungi (Gluck‐Thaler et al, 2022; Urquhart et al, 2023, McDonald, unpublished data). The observation of highly identical transposons within distantly related species is suggestive that Starship transposons encode all the genetic machinery required to move themselves between different species.…”