Intruder (DD38E), a recently evolved sibling family of DD34E/Tc1 transposons in animals

Abstract

Background A family of Tc1/mariner transposons with a characteristic DD38E triad of catalytic amino acid residues, named Intruder (IT), was previously discovered in sturgeon genomes, but their evolutionary landscapes remain largely unknown. Results Here, we comprehensively investigated the evolutionary profiles of ITs, and evaluated their cut-and-paste activities in cells. ITs exhibited a narrow taxonomic distribution pattern in the animal kingdom, with invasions into two invertebrate phyla (Arthropoda and Cnidaria) and three vertebrate lineages (Actinopterygii, Agnatha, and Anura): very similar to that of the DD36E/IC family. Some animal orders and species seem to be more hospitable to Tc1/mariner transposons, one order of Amphibia and seven Actinopterygian orders are the most common orders with horizontal transfer events and have been invaded by all four families (DD38E/IT, DD35E/TR, DD36E/IC and DD37E/TRT) of Tc1/mariner transposons, and eight Actinopterygii species were identified as the major hosts of these families. Intact ITs have a total length of 1.5–1.7 kb containing a transposase gene flanked by terminal inverted repeats (TIRs). The phylogenetic tree and sequence identity showed that IT transposases were most closely related to DD34E/Tc1. ITs have been involved in multiple events of horizontal transfer in vertebrates and have invaded most lineages recently (< 5 million years ago) based on insertion age analysis. Accordingly, ITs presented high average sequence identity (86–95%) across most vertebrate species, suggesting that some are putatively active. ITs can transpose in human HeLa cells, and the transposition efficiency of consensus TIRs was higher than that of the TIRs of natural isolates. Conclusions We conclude that DD38E/IT originated from DD34E/Tc1 and can be detected in two invertebrate phyla (Arthropoda and Cnidaria), and in three vertebrate lineages (Actinopterygii, Agnatha and Anura). IT has experienced multiple HT events in animals, dominated by recent amplifications in most species and has high identity among vertebrate taxa. Our reconstructed IT transposon vector designed according to the sequence from the “cat” genome showed high cut-and-paste activity. The data suggest that IT has been acquired recently and is active in many species. This study is meaningful for understanding the evolution of the Tc1/mariner superfamily members and their hosts.

Prokaryotic and Eukaryotic Horizontal Transfer of Sailor (DD82E), a New Superfamily of IS630-Tc1-Mariner DNA Transposons

“…Then, these transposase sequences were used as a query to search the genomes deposited in the National Center for Biotechnology Information (NCBI) genome project database (https://blast.ncbi.nlm.nih.gov/Blast, accessed on 25 October 2020) using TBLASTN with an E-value of 1e-100. Subsequently, the best hits were extracted with 2-kb flanking sequences, since most ITm families contain TIRs (including untranslated region) less than 2 kb as previous studies reported, such as DD35E/TR [20], DD36E/IC [21], DD38E/IT [22], DD37D/maT [23], DD39D/GT [23]. The presence of TIRs and TSDs was manually screened in the resulting sequences, to identify potential DNA transposons.…”

“…The MAFFT program was used to perform multiple alignments of DDE domains [36]. Reference transposase sequences were obtained from GenBank and the references of DD35E/TR [20], DD36E/IC [21], DD37E/TRT [27], DD38E/IT [22], Zator and TP36 [32]. Bacterial transposases from insertion sequence 256 (IS256) were chosen as the outgroup.…”

“…The most striking difference was undoubtedly the DDE signature. Tc1/mariner elements are characterized by the presence of the DD34-41E/D signature [20][21][22][23][24][27][28][29][30]. Although the Sailor superfamily was shown to contain the DD82E catalytic domain, this characteristic varied widely across Sailor members (DD78-111E) (Figure 4C).…”

“…The second half contains the DDE/D domain, which possesses the catalytic activity required for the excision and insertion of the TE. The GRPR-like motif is located between the two HTH motifs of the paired domain and is supposed to mediate the binding of the paired domain to the target site duplication (TSD), the TA dinucleotide [19], which has been identified in most Tc1/mariner superfamilies, such as DD35E/TR [20], DD36E/IC [21], DD38E/IT [22], DD37D/maT [23], DD39D/GT [23] and DD41D/VS [24]. The classification of ITm transposons is reliably associated with the length of the peptide chain between the second "D" and the third "E/D" amino acid residues (aa) of the catalytic domain, the so-called DDE/D signature.…”

“…The classification of ITm transposons is reliably associated with the length of the peptide chain between the second "D" and the third "E/D" amino acid residues (aa) of the catalytic domain, the so-called DDE/D signature. Nine families are classically considered, and most of their phylogenetic relationships have been updated and are well defined: DD34E/Tc1 [25], DD34D/mariner [26], DD37D/maT [23], DD39D/GT [23], DD41D/VS [24], DD35E/TR [20], DD36E/IC [21], DD37E/TRT [27] and DD38E/IT [22]. However, until recently, studies have shown that many groups of ITm transposons carry the same DDE/D signatures but have different phylogenetic origins [28][29][30].…”