Phylogenetic Relationships among TnpB-Containing Mobile Elements in Six Bacterial Species
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 <i>IS605</i> and <i>IS60...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2023-02-01
|
| Series: | Genes |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2073-4425/14/2/523 |
| _version_ | 1797620779348656128 |
|---|---|
| author | Yali Wang Mengke Guo Naisu Yang Zhongxia Guan Han Wu Numan Ullah Emmanuel Asare Shasha Shi Bo Gao Chengyi Song |
| author_facet | Yali Wang Mengke Guo Naisu Yang Zhongxia Guan Han Wu Numan Ullah Emmanuel Asare Shasha Shi Bo Gao Chengyi Song |
| author_sort | Yali Wang |
| collection | DOAJ |
| description | 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 <i>IS605</i> and <i>IS607</i>. In this paper, we reveal the evolutionary relationships among TnpB-containing mobile elements (TCMEs) in well-assembled genomes of six bacterial species: <i>Bacillus cereus</i>, <i>Clostridioides difficile</i>, <i>Deinococcus radiodurans</i>, <i>Escherichia coli</i>, <i>Helicobacter pylori</i> and <i>Salmonella enterica</i>. 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 <i>B. cereus</i>, <i>C. difficile</i>, <i>D. radiodurans</i> and <i>E. coli</i> contained TCMEs; however, only 64% of the genomes of <i>H. pylori</i> and 44% of <i>S. enterica</i> genomes contained TCMEs. <i>IS605</i> showed the largest rate of invasion in these species, while <i>IS607</i> and <i>IS1341</i> had a relatively narrow distribution. Co-invasions of <i>IS605</i>, <i>IS607</i> and <i>IS1341</i> elements were observed in various genomes. The largest average copy number was observed for <i>IS605b</i> elements in <i>C. difficile</i>. 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. |
| first_indexed | 2024-03-11T08:47:28Z |
| format | Article |
| id | doaj.art-fd752faea98e45fe80eece8e38b32fda |
| institution | Directory Open Access Journal |
| issn | 2073-4425 |
| language | English |
| last_indexed | 2024-03-11T08:47:28Z |
| publishDate | 2023-02-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Genes |
| spelling | doaj.art-fd752faea98e45fe80eece8e38b32fda2023-11-16T20:44:08ZengMDPI AGGenes2073-44252023-02-0114252310.3390/genes14020523Phylogenetic Relationships among TnpB-Containing Mobile Elements in Six Bacterial SpeciesYali Wang0Mengke Guo1Naisu Yang2Zhongxia Guan3Han Wu4Numan Ullah5Emmanuel Asare6Shasha Shi7Bo Gao8Chengyi Song9College of Animal Science and Technology, Yangzhou University, Yangzhou 225009, ChinaCollege of Animal Science and Technology, Yangzhou University, Yangzhou 225009, ChinaCollege of Animal Science and Technology, Yangzhou University, Yangzhou 225009, ChinaCollege of Animal Science and Technology, Yangzhou University, Yangzhou 225009, ChinaDepartment of Immunology, School of Medicine, Shenzhen University, Shenzhen 518060, ChinaCollege of Animal Science and Technology, Yangzhou University, Yangzhou 225009, ChinaCollege of Animal Science and Technology, Yangzhou University, Yangzhou 225009, ChinaCollege of Animal Science and Technology, Yangzhou University, Yangzhou 225009, ChinaCollege of Animal Science and Technology, Yangzhou University, Yangzhou 225009, ChinaCollege of Animal Science and Technology, Yangzhou University, Yangzhou 225009, ChinaSome 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 <i>IS605</i> and <i>IS607</i>. In this paper, we reveal the evolutionary relationships among TnpB-containing mobile elements (TCMEs) in well-assembled genomes of six bacterial species: <i>Bacillus cereus</i>, <i>Clostridioides difficile</i>, <i>Deinococcus radiodurans</i>, <i>Escherichia coli</i>, <i>Helicobacter pylori</i> and <i>Salmonella enterica</i>. 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 <i>B. cereus</i>, <i>C. difficile</i>, <i>D. radiodurans</i> and <i>E. coli</i> contained TCMEs; however, only 64% of the genomes of <i>H. pylori</i> and 44% of <i>S. enterica</i> genomes contained TCMEs. <i>IS605</i> showed the largest rate of invasion in these species, while <i>IS607</i> and <i>IS1341</i> had a relatively narrow distribution. Co-invasions of <i>IS605</i>, <i>IS607</i> and <i>IS1341</i> elements were observed in various genomes. The largest average copy number was observed for <i>IS605b</i> elements in <i>C. difficile</i>. 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.https://www.mdpi.com/2073-4425/14/2/523TnpBtransposable elements<i>IS605</i><i>IS607</i><i>IS1341</i> |
| spellingShingle | Yali Wang Mengke Guo Naisu Yang Zhongxia Guan Han Wu Numan Ullah Emmanuel Asare Shasha Shi Bo Gao Chengyi Song Phylogenetic Relationships among TnpB-Containing Mobile Elements in Six Bacterial Species Genes TnpB transposable elements <i>IS605</i> <i>IS607</i> <i>IS1341</i> |
| title | Phylogenetic Relationships among TnpB-Containing Mobile Elements in Six Bacterial Species |
| title_full | Phylogenetic Relationships among TnpB-Containing Mobile Elements in Six Bacterial Species |
| title_fullStr | Phylogenetic Relationships among TnpB-Containing Mobile Elements in Six Bacterial Species |
| title_full_unstemmed | Phylogenetic Relationships among TnpB-Containing Mobile Elements in Six Bacterial Species |
| title_short | Phylogenetic Relationships among TnpB-Containing Mobile Elements in Six Bacterial Species |
| title_sort | phylogenetic relationships among tnpb containing mobile elements in six bacterial species |
| topic | TnpB transposable elements <i>IS605</i> <i>IS607</i> <i>IS1341</i> |
| url | https://www.mdpi.com/2073-4425/14/2/523 |
| work_keys_str_mv | AT yaliwang phylogeneticrelationshipsamongtnpbcontainingmobileelementsinsixbacterialspecies AT mengkeguo phylogeneticrelationshipsamongtnpbcontainingmobileelementsinsixbacterialspecies AT naisuyang phylogeneticrelationshipsamongtnpbcontainingmobileelementsinsixbacterialspecies AT zhongxiaguan phylogeneticrelationshipsamongtnpbcontainingmobileelementsinsixbacterialspecies AT hanwu phylogeneticrelationshipsamongtnpbcontainingmobileelementsinsixbacterialspecies AT numanullah phylogeneticrelationshipsamongtnpbcontainingmobileelementsinsixbacterialspecies AT emmanuelasare phylogeneticrelationshipsamongtnpbcontainingmobileelementsinsixbacterialspecies AT shashashi phylogeneticrelationshipsamongtnpbcontainingmobileelementsinsixbacterialspecies AT bogao phylogeneticrelationshipsamongtnpbcontainingmobileelementsinsixbacterialspecies AT chengyisong phylogeneticrelationshipsamongtnpbcontainingmobileelementsinsixbacterialspecies |