Widespread distribution and evolutionary patterns of mariner-like elements among various spiders and insects

Abstract

Transposable elements (TEs) are present in the genomes of almost all organisms. TEs are classified as either class I or II depending on their mobility mechanism. Class I TEs are retrotransposons that move via a copy– paste mechanism with an RNA intermediate, whereas class II TEs are DNA transposons that move via a cut– paste mechanism as a DNA fragment. Mariner, also referred to as Mos1, is a DNA transposon that was first reported in Drosophila mauritiana (Jacobson et al., 1986; Medhora et al., 1991). It carries a gene encoding a transposase that facilitates self-transposition. Mariner is also present in closely related Drosophila species but is clearly absent from D. melanogaster. A sequence homologous to mariner (Hcmar1) was isolated from the moth Hyalophora cecropia and designated as a mariner-like element (MLE) (Lidholm et al., 1991). At present, MLEs have been isolated from a vast range of phylogenetically distant organisms, such as protozoa (Silva et al., 2005), insects (Robertson, 1993), marine invertebrates (Halaimia-Toumi et al., 2004), and mammals (Auge-Gouillou et al., 1995). According to the current classification, MLEs belong to the Tc1-mariner family, which is a member of the larger IS630-Tc1-mariner superfamily (Shao and Tu, 2001). MLEs can be divided further into five subfamilies: mauritiana, cecropia, mellifera/capitata, irritans, and elegans/briggsae (Robertson and MacLeod, 1993) or into 15 subfamilies (Rouault et al., 2009). The full length of an MLE is approximately 1300 base pairs (bp). This transposon contains one intronless open reading frame (ORF) that encodes a transposase of approximately 340 amino acids, and it is flanked by terminal inverted repeats (TIRs) of approximately 30 bp (Jacobson et al., 1986; Hartl, 1989). MLE transposases that catalyze the transpositional reaction comprise an N-terminal TIR-binding domain with a helix– turn–helix (HTH) motif and a C-terminal catalytic domain with a unique DD(34)D catalytic motif (Shao and Tu, 2001; Plasterk and van Luenen, 2002). In addition, two highly conserved amino acid motifs, WVPHEL and YSPDLAP, are present in the mariner family (Robertson, 1993; Robertson and MacLeod, 1993). In particular, WVPHEL may participate in the formation of the mariner transposase dimer interface (Auge-Gouillou et al., 2005; Liu and Chalmers, 2013). The high sequence similarity of MLEs and their nonuniform distribution, both within genomes and among taxa, strongly suggest that horizontal transfer (HT) has occurred among species (Robertson, 1993; Lohe et al., 1995; Lampe et al., 2003; Rouleux-Bonnin et al., 2005; Casse et al., 2006). The general model of the MLE lifecycle and that of other DNA transposons suggests that a single copy initially invades a genome, which produces multiple copies via duplicative transposition or an unMariner-like elements (MLEs) are DNA transposons that are prevalent in a wide range of eukaryotic genomes and are considered to be inserted into their host genomes via horizontal transfer. In this study, we performed a phylogenetic analysis to compare MLEs obtained from 18 species of three orders, Araneae, Hymenoptera, and Lepidoptera, with previously reported MLEs, which were classified into the mellifera subfamily. These MLEs shared high sequence similarity (92.78%). Furthermore, MLEs obtained from four distinct species contained an intact or almost intact open reading frame that encoded a putative transposase. The phylogenetic differences between these MLEs and their respective host species as well as the high sequence similarity of MLEs clearly suggests that horizontal transfer has recently occurred among species than previously reported MLEs. We discuss their possible modes of horizontal transfer based on the analysis of this study.