Multiple Invasions of Visitor, a DD41D Family of Tc1/mariner Transposons, throughout the Evolution of Vertebrates

Abstract

Although the DD41D (named as Visitor, VS) family of Tc1/mariner transposons was discovered in Arthropods, Mollusca and Ctenophora, the evolution profile of this family is still largely unknown. We found that VS is widespread in the animal kingdom, including 140 species of 18 orders in invertebrates and 30 species of 12 orders in vertebrates, and one land plant species. Our data revealed multiple horizontal transfer (HT) events in both invertebrates and vertebrates and invasion into multiple lineages of mammals, including Chiroptera (seven species), Dasyuromorphia/Marsupialia (one species), Didelphimorphia/Marsupialia (one species), Diprotodontia/Marsupialia (two species) and Primates (one species). Phylogenetic analysis revealed a close relationship of VSs to DD37D/maT and DD34D/mariner and confirmed that VSs with the DD40D signature identified previously is not a distinct family, but originated from DD41D/VS. Age analysis revealed that the most recent invasion of VSs was found in ray-finned fishes and a toad, followed by relatively young invasions in bats and marsupials, whereas VSs in mammals, jawless fishes and lizards were mainly represented by ancient copies, suggesting old age. phylogenetic analyses and comparison of pairwise distances between VSs and recombination-activating gene 1 (RAG1) support HT events of VSs in vertebrates. The intact VSs from bats were non-functional as determined by the transposition activity assay. Some vertebrate lineages and species were identified as the hot hosts of Tc1/mariner transposons. Overall, our study presents the evolution profile of VSs and suggests that VSs play roles in diversifying and shaping the genomes of diverse animal lineages.

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

“…On the other hand, the taxonomic distributions of Tc1/mariner families ( IT , TR , IC , and TRT ) in animals also revealed that they share some common hosts. Thus, some orders and species seem to be more hospitable to Tc1/mariner transposons than others, which has also been noted in a recent study [ 23 ]. The Actinopterygii and Anura tend to be more susceptible to the invasions of Tc1/mariner transposons, as all well-defined close sibling families of DD34E/ Tc1 ( IT , TR , IC and TRT ) were detected in these lineages.…”

“…To assess the distribution of IT among species, a TBLASTN search against all the available prokaryotic (archaea and bacteria) and eukaryotic (chromista, plantae, animalia, protozoa, and fungi) genomes placed at the NCBI database was performed using the sturgeon IT transposase sequence as the query. This revealed that IT has a restricted taxonomic distribution compared with the families of DD41D/VS [ 23 ] and DD37E/ TRT [ 20 ] of Tc1/mariner transposons, for which the taxonomic breadth has been well defined. Considerable hits encoding the preserved DD38E motifs were identified only in the animalia among eukaryotes, where ITs were present in 40 species of Arthropoda and one of the Cnidaria in invertebrates, one Agnathan species, one Anuran species, and 98 species in the Actinopterygii in vertebrates (Fig.…”

“…Although diverse Tc1/mariner transposons families have been discovered and known for decades, the evolutionary landscapes of some of them are not well characterized, and knowledge of their taxonomic distribution, intra-family diversity and evolutionary dynamics are still fragmented because of the limited historical availability of genome information, such as for DD34D/ mariner , DD34E/ Tc1 , DD × D/ pogo , DD37D/ maT , and DD39D [ 19 , 38 ]. With increases in genome sequencing data, the whole evolutionary profiles of these DNA transposons can now be well defined and more informative data are available, such as for DD37E/ TRT [ 20 ], DD36E/ IC [ 21 ], DD35E/ TR [ 22 ], DD41D/VS [ 23 ] and DD38E/ IT reported here. However, we still found that Tc1/mariner transposons have experienced significantly different evolutionary profiles across families in terms of the complexity of intra-family structure, taxonomic breadth, and evolutionary dynamics.…”

“…DD37E/ TRT transposons also occur widely in eukaryotes and are present in protozoans, fungi and animals [ 20 ]. By contrast, the DD36E/ IC [ 21 ], DD35E/ TR [ 22 ], DD41D/VS [ 23 ], and DD38E/ IT families exhibit relatively narrow distributions and are mainly restricted to the animal kingdom, and DD35E/ TR is only detected in vertebrates [ 22 ]. In addition, analyses of evolutionary dynamics have suggested that DD37E/ TRT [ 20 ], DD36E/ IC [ 21 ], DD35E/ TR [ 22 ], and DD38E/ IT seem to be recently evolved families, and more active and intact copies of these families can be detected in many species across multiple lineages.…”

“…They seek “TA” sequences to be inserted into the host genome, as a consequence “TA” target site duplications flanking the inserted transposon [ 19 ]. At least four families of Tc1/mariner transposons, including DD41D/VS, DD37E/ TRT, DD36E/ IC , and DD35E/ TR have been well-described recently [ 20 – 23 ]. While DD34E/ Tc1 [ 17 ], DD × D/ pogo [ 24 ], and DD34D/ mariner [ 18 ] were discovered very early and have been reported extensively, and DD × D/ pogo has been suggested as a separate superfamily of IS630-Tc1-mariner transposon group very recently [ 25 ].…”