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Simple Summary: Transposable elements (TEs) are mobile genetic elements that play vital role in defining and contributing to the size, shape and structure of both prokaryotic and eukaryotic genomes in nature. The piggyBac (PB), a superfamily of DNA transposons, has been isolated over the years from various organisms including insects, fungi and plants. These piggyBac transposon systems have high efficiency with a wide usage in the study of gene therapies, mutagenesis and transgenesis. Currently, there is limited information available on DNA transposons in small (compact) genomes of animals. Therefore, this study aims to annotate the PB transposons in small genomes of animals, revealing their evolution profiles in both vertebrate and invertebrate genomes. TEs, including DNA transposons, are major contributors of genome expansions, and have played a very significant role in shaping the evolution of animal genomes, due to their capacity to jump from one genomic position to the other. In this study, we investigated the evolution landscapes of PB transposons, including their distribution, diversity, activity and structure organization in 79 species of small (compact) genomes of animals comprising both vertebrate and invertebrates. Overall, 212 PB transposon types were detected from almost half (37) of the total number of the small genome species (79) investigated. The detected PB transposon types, which were unevenly distributed in various genera and phyla, have been classified into seven distinct clades or families with good bootstrap support (>80%). The PB transposon types that were identified have a length ranging from 1.23 kb to 9.51 kb. They encode transposases of approximately ≥500 amino acids in length, and possess terminal inverted repeats (TIRs) ranging from 4 bp to 24 bp. Though some of the transposon types have long TIRs (528 bp), they still maintain the consistent and reliable 4 bp target site duplication (TSD) of TTAA. However, PiggyBac-2_Cvir transposon originating from the Crassostrea virginica species exhibits a unique TSD of TATG. The TIRs of the transposons in all the seven families display high divergence, with a highly conserved 5′ end motif. The core transposase domains (DDD) were better conserved among the seven different families compared to the other protein domains, which were less prevalent in the vertebrate genome. The divergent evolution dynamics analysis also indicated that the majority of the PB transposon types identified in this study are either relatively young or old, with some being active. Additionally, numerous invasions of PB transposons were found in the genomes of both vertebrate and invertebrate animals. The data reveals that the PB superfamily is widely distributed in these species. PB transposons exhibit high diversity and activity in the small genomes of animals, and might play a crucial role in shaping the evolution of these small genomes of animals. [ABSTRACT FROM AUTHOR]

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]