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Some families of mobile elements in bacterial genomes encode not only a transposase but also an accessory TnpB gene. This gene has been shown to encode an RNA-guided DNA endonuclease, co-evolving with Y1 transposase and serine recombinase in mobile elements IS605 and IS607. In this paper, we reveal the evolutionary relationships among TnpB-containing mobile elements (TCMEs) in well-assembled genomes of six bacterial species: Bacillus cereus, Clostridioides difficile, Deinococcus radiodurans, Escherichia coli, Helicobacter pylori and Salmonella enterica. In total, 9996 TCMEs were identified in 4594 genomes. They belonged to 39 different insertion sequences (ISs). Based on their genetic structures and sequence identities, the 39 TCMEs were classified into three main groups and six subgroups. According to our phylogenetic analysis, TnpBs include two main branches (TnpB-A and TnpB-B) and two minor branches (TnpB-C and TnpB-D). The key TnpB motifs and the associated Y1 and serine recombinases were highly conserved across species, even though their overall sequence identities were low. Substantial variation was observed for the rate of invasion across bacterial species and strains. Over 80% of the genomes of B. cereus, C. difficile, D. radiodurans and E. coli contained TCMEs; however, only 64% of the genomes of H. pylori and 44% of S. enterica genomes contained TCMEs. IS605 showed the largest rate of invasion in these species, while IS607 and IS1341 had a relatively narrow distribution. Co-invasions of IS605, IS607 and IS1341 elements were observed in various genomes. The largest average copy number was observed for IS605b elements in C. difficile. The average copy numbers of most other TCMEs were smaller than four. Our findings have important implications for understanding the co-evolution of TnpB-containing mobile elements and their biological roles in host genome evolution. [ABSTRACT FROM AUTHOR]

Simple Summary: Despite the discovery of the Tigger family of pogo transposons in the mammalian genome, the evolution profile of this family is still incomplete. Here, we conducted a systematic evolution analysis for Tigger in nature. The data revealed that Tigger was found in a broad variety of animals, and extensive invasion of Tigger was observed in mammal genomes. Common horizontal transfer events of Tigger elements were observed across different lineages of animals, including mammals, that may have led to their widespread distribution, while parasites and invasive species may have promoted Tigger HT events. Our results also indicate that the activity of Tigger transposons tends to be low in vertebrates; only one mammalian genome and fish genome may harbor active Tigger. The data of this study revealed that Tigger was found in a wide variety of animal genomes, including 180 species from 36 orders of invertebrates and 145 species from 29 orders of vertebrates. An extensive invasion of Tigger was observed in mammals, with a high copy number. Almost 61% of those species contain more than 50 copies of Tigger; however, 46% harbor intact Tigger elements, although the number of these intact elements is very low. Common HT events of Tigger elements were discovered across different lineages of animals, including mammals, that may have led to their widespread distribution, whereas Helogale parvula and arthropods may have aided Tigger HT incidences. The activity of Tigger seems to be low in the kingdom of animals, most copies were truncated in the mammal genomes and lost their transposition activity, and Tigger transposons only display signs of recent and current activities in a few species of animals. The findings suggest that the Tigger family is important in structuring mammal genomes. [ABSTRACT FROM AUTHOR]