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Simple Summary: Transposable elements, including DNA transposons, play a significant role in genetic material exchanges between prokaryotes and eukaryotes. Comparative profiling of the evolution pattern of DNA transposons between prokaryotes and eukaryotes may identify potential genetic material exchanges between them and provide insights into the evolutionary history of prokaryotic and eukaryotic genomes. The members of the IS630-Tc1-mariner (ITm) group may represent the most diverse and widely distributed DNA transposons in nature, and the discovery of new members of this group is highly expected based on the increasing availability of genome sequencing data. We discovered a new superfamily (termed Sailor) belonging to the ITm hyperfamily, which differed from the known superfamilies of Tc1/mariner, DDxD/pogo and DD34E/Gambol, regarding phylogenetic position and catalytic domain. Our data revealed that Sailor was distributed in both prokaryotes and eukaryotes and suggested that horizontal transfer (HT) events of Sailor may occur from prokaryotic to eukaryotic genomes. Finally, internal transmissions of Sailor in prokaryotes and eukaryotes were also detected. Here, a new superfamily of IS630-Tc1-mariner (ITm) DNA transposons, termed Sailor, is identified, that is characterized by a DD82E catalytic domain and is distinct from all previously known superfamilies of the ITm group. Phylogenetic analyses revealed that Sailor forms a monophyletic clade with a more intimate link to the clades of Tc1/mariner and DD34E/Gambol. Sailor was detected in both prokaryotes and eukaryotes and invaded a total of 256 species across six kingdoms. Sailor is present in nine species of bacteria, two species of plantae, four species of protozoa, 23 species of Chromista, 12 species of Fungi and 206 species of animals. Moreover, Sailor is extensively distributed in invertebrates (a total of 206 species from six phyla) but is absent in vertebrates. Sailor transposons are 1.38–6.98 kb in total length and encoded transposases of ~676 aa flanked by TIRs with lengths between 18, 1362 and 4 bp (TATA) target-site duplications. Furthermore, our analysis provided strong evidence of Sailor transmissions from prokaryotes to eukaryotes and internal transmissions in both. These data update the classification of the ITm group and will contribute to the understanding of the evolution of ITm transposons and that of their hosts. [ABSTRACT FROM AUTHOR]

[Display omitted] • maTs , GTs and VSs showed differential evolution patterns in eukaryotes. • DD37D and DD39D family composed an independent clade, with close to DD41D and DD34D. • HT might exist a lower rate of maTs between invertebrates and GTs between land plant. • Most of maTs and GTs might encoded active transposases possess intact characters. DNA transposons play a significant role in shaping the size and structure of eukaryotic genomes. The Tc1/mariner transposons are the most diverse and widely distributed superfamily of DNA transposons and the structure and distribution of several Tc1/mariner families, such as DD35E/ TR , DD36E/ IC , DD37E/ TRT , and DD41D/ VS, have been well studied. Nonetheless, a greater understanding of the structure and diversity of Tc1/mariner transposons will provide insight into the evolutionary history of eukaryotic genomes. Here, we conducted further analysis of DD37D/ maT and DD39D (named Guest , GT), which were identified by the specific catalytic domains DD37D and DD39D. Most transposons of the maT family have a total length of approximately 1.3 kb and harbor a single open reading frame encoding a ~ 346 amino acid (range 302–398 aa) transposase protein, flanked by short terminal inverted repeats (TIRs) (13–48 base pairs, bp). In contrast, GT s transposons were longer (2.0–5.8 kb), encoded a transposase protein of ~400 aa (range 140–592 aa), and were flanked by short TIRs (19–41 bp). Several conserved motifs, including two helix–turn–helix (HTH) motifs, a GRPR (GRKR) motif, a nuclear localization sequence, and a DDD domain, were also identified in maT and GT transposases. Phylogenetic analyses of the DDD domain showed that the maT and GT families each belong to a monophyletic clade and appear to be closely related to DD41D/ VS and DD34D/ mariner. In addition, maT s are mainly distributed in invertebrates (144 species), whereas GT s are mainly distributed in land plants through a small number of GT s are present in Chromista and animals. Sequence identity and phylogenetic analysis revealed that horizontal transfer (HT) events of maT and GT might occur between kingdoms and phyla of eukaryotes; however, pairwise distance comparisons between host genes and transposons indicated that HT events involving maT s might be less frequent between invertebrate species and HT events involving GT s may be less frequent between land plant species. Overall, the DD37D/ maT and DD39D/ GT families display significantly different distribution and tend to be identified in more ancient evolutionary families. The discovery of intact transposases, perfect TIRs, and target site duplications (TSD) of maT s and GT s illustrates that the DD37D/ maT and DD39D/ GT families may be active. Together, these findings improve our understanding of the diversity of Tc1 / mariner transposons and their impact on eukaryotic genome evolution. [ABSTRACT FROM AUTHOR]