Next-Generation Sequencing Reveals Recent Horizontal Transfer of a DNA Transposon between Divergent Mosquitoes

Yupu Diao,Erjun Ling,Ai Xia,Yajun Ma,Zhijian Jake Tu,Igor Sharakhov,Yumin Qi,Xiaoguang Chen,Jim Biedler

doi:10.1371/journal.pone.0016743

Abstract

Horizontal transfer of genetic material between complex organisms often involves transposable elements (TEs). For example, a DNA transposon mariner has been shown to undergo horizontal transfer between different orders of insects and between different phyla of animals. Here we report the discovery and characterization of an ITmD37D transposon, MJ1, in Anopheles sinensis. We show that some MJ1 elements in Aedes aegypti and An. sinensis contain intact open reading frames and share nearly 99% nucleotide identity over the entire transposon, which is unexpectedly high given that these two genera had diverged 145–200 million years ago. Chromosomal hybridization and TE-display showed that MJ1 copy number is low in An. sinensis. Among 24 mosquito species surveyed, MJ1 is only found in Ae. aegypti and the hyrcanus group of anopheline mosquitoes to which An. sinensis belongs. Phylogenetic analysis is consistent with horizontal transfer and provides the basis for inference of its timing and direction. Although report of horizontal transfer of DNA transposons between higher eukaryotes is accumulating, our analysis is one of a small number of cases in which horizontal transfer of nearly identical TEs among highly divergent species has been thoroughly investigated and strongly supported. Horizontal transfer involving mosquitoes is of particular interest because there are ongoing investigations of the possibility of spreading pathogen-resistant genes into mosquito populations to control malaria and other infectious diseases. The initial indication of horizontal transfer of MJ1 came from comparisons between a 0.4x coverage An. sinensis 454 sequence database and available TEs in mosquito genomes. Therefore we have shown that it is feasible to use low coverage sequencing to systematically uncover horizontal transfer events. Expanding such efforts across a wide range of species will generate novel insights into the relative frequency of horizontal transfer of different TEs and provide the evolutionary context of these lateral transfer events.

Highlights

Horizontal transfer is the transfer of genetic material between reproductively isolated species, which is common among prokaryotes [1]
The average length of the An. sinensis 454 shotgun sequences is 230 bp and the matches to Aae_MJ1 were 100–300 bp in length. Two of these hits were near the termini of MJ1 and had flanking sequences that were specific to An. sinensis
A few well supported clades consist of MJ1 from different Anopheles species, which may either reflect horizontal transfer or introgression [21] between these species within the hyrcanus group

Summary

Introduction

Horizontal transfer is the transfer of genetic material between reproductively isolated species, which is common among prokaryotes [1]. A DNA transposon originally discovered in Drosophila mauritiana [4], has been shown to undergo horizontal transfer across different orders of insects and even across different phyla of animals [5,6]. Members of the IS630-Tc1-mariner (ITm) superfamily share a transposase that contains a conserved D(Asp)DE(Glu) or DDD catalytic triad [9,10]. The IS630-Tc1-mariner superfamily can be organized in several families including Tc1, mariner, ITmD37E and ITmD37D, which are characterized by unique catalytic motifs of DD34E, DD34D, DD37E, and DD37D, respectively [10]. The numbering, which is conserved within each family, refers to the distance between the second D and the third D or E residues of the catalytic triad

Methods

Results

Conclusion