Horizontal transfer of a non-autonomous Helitron among insect and viral genomes.

Brad S Coates

doi:10.1186/s12864-015-1318-6

Abstract

BackgroundThe movement of mobile elements among species by horizontal transposon transfer (HTT) influences the evolution of genomes through the modification of structure and function. Helitrons are a relatively new lineage of DNA-based (class II) transposable elements (TEs) that propagate by rolling-circle replication, and are capable of acquiring host DNA. The rapid spread of Helitrons among animal lineages by HTT is facilitated by shuttling in viral particles or by unknown mechanisms mediated by close organism associations (e.g. between hosts and parasites).ResultsA non-autonomous Helitron independently annotated as BmHel-2 from Bombyx mori and the MITE01 element from Ostrinia nubilalis was predicted in the genomes of 24 species in the insect Order Lepidoptera. Integrated Helitrons retained ≥ 65% sequence identity over a 250 bp consensus, and were predicted to retain secondary structures inclusive of a 3′-hairpin and a 5′-subterminal inverted repeat. Highly similar Hel-2 copies were predicted in the genomes of insects and associated viruses, which along with a previous documented case of real-time virus-insect cell line transposition suggests that this Helitron has likely propagated by HTT.ConclusionsThese findings provide evidence that insect virus may mediate the HTT of Helitron-like TEs. This movement may facilitate the shuttling of DNA elements among insect genomes. Further sampling is required to determine the putative role of HTT in insect genome evolution.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1318-6) contains supplementary material, which is available to authorized users.

Highlights

The movement of mobile elements among species by horizontal transposon transfer (HTT) influences the evolution of genomes through the modification of structure and function
The alignment of two previously annotated Transposable element (TE), a miniature inverted repeat transposable element from Ostrinia nubilalis, OnMITE01 [32], and a Helitron element from B. mori, BmHel-2 [5], generated a 339 bp consensus that showed 66.2% sequence similarity and 77.55% similarity between 50 bp at the 5′-end (Additional file 1) despite these nonprotein coding sequences being from species that have estimated divergence times of > 100 mya [33]
In conjunction with prior research outlined above, the comparative genomic data in this study indicate that viral genomes likely have acquired mobile elements from their insect hosts, with the assumption that cross-infection of related species by the virus and subsequent re-mobilization of the TE can result in HTT

Summary

Introduction

The movement of mobile elements among species by horizontal transposon transfer (HTT) influences the evolution of genomes through the modification of structure and function. Helitrons are a relatively new lineage of DNA-based (class II) transposable elements (TEs) that propagate by rolling-circle replication, and are capable of acquiring host DNA. In contrast to the cut-and-paste propagation of other class II TEs, Helitrons transpose in a conservative fashion where original integrations are retained due to the synthesis of daughter TEs by rolling circle replication (RCR) [1]. This type of replication is similar to that used by ssDNA viruses, bacteria, and plasmids, and involves the enzymatic activity of Replicase/Helicase (RepHel) proteins. Helitrons have been implicated in exon shuffling [10], transcription readthrough [11], and the mobilization of acquired host genome regions [5,12,13]

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