The evolutionary history of mariner elements in stalk-eyed flies reveals the horizontal transfer of transposons from insects into the genome of the cnidarian Hydra vulgaris.

C Alastair Grace,Martin Carr,Ruslan Kalendar

doi:10.1371/journal.pone.0235984

Abstract

The stalk-eyed flies (Diopsidae, Diptera) are a family of approximately 100 species of calypterate dipterans, characterised by extended head capsules. Species within the family have previously been shown to possess six subfamilies of mariner transposons, with nucleotide substitution patterns suggesting that at least two subfamilies are currently active. The vertumnana subfamily has been shown to have been involved in a horizontal transfer event involving Diopsidae and a second dipteran family in the Tephritidae. Presented here are cloned and sequenced mariner elements from three further diopsid species, in addition to a bioinformatic analysis of mariner elements identified in transcriptomic and genomic data from the genus Teleopsis. The newly identified mariner elements predominantly fall into previously recognised subfamilies, however the publicly available Teleopsis data also revealed a novel subfamily. Three of the seven identified subfamilies are shown to have undergone horizontal transfer, two of which appear to involve diopsid donor species. One recipient group of a diopsid mariner is the Bactrocera genus of tephritid flies, the transfer of which was previously proposed in an earlier study of diopsid mariner elements. The second horizontal transfer, of the mauritiana subfamily, can be traced from the Teleopsis genus to the cnidarian Hydra vulgaris. The mauritiana elements are shown to be active in the recipient H. vulgaris and transposase expression is observed in all body tissues examined in both species. The increased diversity of diopsid mariner elements points to a minimum of four subfamilies being present in the ancestral genome. Both vertical inheritance and stochastic loss of TEs have subsequently occurred within the diopsid radiation. The TE complement of H. vulgaris contains at least two mariner subfamilies of insect origin. Despite the phylogenetic distance between donor and recipient species, both subfamilies are shown to be active and proliferating within H. vulgaris.

Highlights

Transposable elements (TEs) are almost universal components of eukaryotic genomes [1], that are capable of driving their own replication and movement within their host genome
Cloned PCR products amplified from genomic DNA extractions of Diasemopsis aethiopica, Diopsis apicalis and Teloglabrus entabensis were subject to BLASTn similarity searching, which resulted in 26 partial mariner sequences being identified (S1 Table)
The genome of the centrioncid Te. entabensis harbours a minimum of four subfamilies, with the capitata, irritans, mellifera and vertumnana subfamilies all amplified in the PCR screen

Summary

Introduction

Transposable elements (TEs) are almost universal components of eukaryotic genomes [1], that are capable of driving their own replication and movement within their host genome. They are divided into two classes, based upon their transposition mechanism. The Tnpase binds to the inverted terminal repeats (ITRs) that flank the transposon and generates double stranded DNA breaks in order to excise the parental element and integrate the element into a new genomic location. Daughter elements may be generated during transposition if the double stranded break created to excise the parental element is repaired using a copy of the transposon as a template (reviewed in [2]). Within Metazoa, one of the most widespread forms of DNA transposon is the Tc1/ mariner superfamily, named after elements originally discovered in Caenorhabditis elegans [3] and Drosophila mauritiana [4]

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