Intruder (DD38E), a recently evolved sibling family of DD34E/Tc1 transposons in animals
Abstract Background A family of Tc1/mariner transposons with a characteristic DD38E triad of catalytic amino acid residues, named Intruder (IT), was previously discovered in sturgeon genomes, but their evolutionary landscapes remain largely unknown. Results Here, we comprehensively investigated the...
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doaj-9ead1fbe935b4efc8d2eb344161e30c62020-12-13T12:13:56ZengBMCMobile DNA1759-87532020-12-0111111510.1186/s13100-020-00227-7Intruder (DD38E), a recently evolved sibling family of DD34E/Tc1 transposons in animalsBo Gao0Wencheng Zong1Csaba Miskey2Numan Ullah3Mohamed Diaby4Cai Chen5Xiaoyan Wang6Zoltán Ivics7Chengyi Song8College of Animal Science & Technology, Yangzhou UniversityCollege of Animal Science & Technology, Yangzhou UniversityDivision of Medical Biotechnology, Paul Ehrlich InstituteCollege of Animal Science & Technology, Yangzhou UniversityCollege of Animal Science & Technology, Yangzhou UniversityCollege of Animal Science & Technology, Yangzhou UniversityCollege of Animal Science & Technology, Yangzhou UniversityDivision of Medical Biotechnology, Paul Ehrlich InstituteCollege of Animal Science & Technology, Yangzhou UniversityAbstract Background A family of Tc1/mariner transposons with a characteristic DD38E triad of catalytic amino acid residues, named Intruder (IT), was previously discovered in sturgeon genomes, but their evolutionary landscapes remain largely unknown. Results Here, we comprehensively investigated the evolutionary profiles of ITs, and evaluated their cut-and-paste activities in cells. ITs exhibited a narrow taxonomic distribution pattern in the animal kingdom, with invasions into two invertebrate phyla (Arthropoda and Cnidaria) and three vertebrate lineages (Actinopterygii, Agnatha, and Anura): very similar to that of the DD36E/IC family. Some animal orders and species seem to be more hospitable to Tc1/mariner transposons, one order of Amphibia and seven Actinopterygian orders are the most common orders with horizontal transfer events and have been invaded by all four families (DD38E/IT, DD35E/TR, DD36E/IC and DD37E/TRT) of Tc1/mariner transposons, and eight Actinopterygii species were identified as the major hosts of these families. Intact ITs have a total length of 1.5–1.7 kb containing a transposase gene flanked by terminal inverted repeats (TIRs). The phylogenetic tree and sequence identity showed that IT transposases were most closely related to DD34E/Tc1. ITs have been involved in multiple events of horizontal transfer in vertebrates and have invaded most lineages recently (< 5 million years ago) based on insertion age analysis. Accordingly, ITs presented high average sequence identity (86–95%) across most vertebrate species, suggesting that some are putatively active. ITs can transpose in human HeLa cells, and the transposition efficiency of consensus TIRs was higher than that of the TIRs of natural isolates. Conclusions We conclude that DD38E/IT originated from DD34E/Tc1 and can be detected in two invertebrate phyla (Arthropoda and Cnidaria), and in three vertebrate lineages (Actinopterygii, Agnatha and Anura). IT has experienced multiple HT events in animals, dominated by recent amplifications in most species and has high identity among vertebrate taxa. Our reconstructed IT transposon vector designed according to the sequence from the “cat” genome showed high cut-and-paste activity. The data suggest that IT has been acquired recently and is active in many species. This study is meaningful for understanding the evolution of the Tc1/mariner superfamily members and their hosts.https://doi.org/10.1186/s13100-020-00227-7IntruderTc1/mariner transposonsDD38EHorizontal transferEvolution |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Bo Gao Wencheng Zong Csaba Miskey Numan Ullah Mohamed Diaby Cai Chen Xiaoyan Wang Zoltán Ivics Chengyi Song |
spellingShingle |
Bo Gao Wencheng Zong Csaba Miskey Numan Ullah Mohamed Diaby Cai Chen Xiaoyan Wang Zoltán Ivics Chengyi Song Intruder (DD38E), a recently evolved sibling family of DD34E/Tc1 transposons in animals Mobile DNA Intruder Tc1/mariner transposons DD38E Horizontal transfer Evolution |
author_facet |
Bo Gao Wencheng Zong Csaba Miskey Numan Ullah Mohamed Diaby Cai Chen Xiaoyan Wang Zoltán Ivics Chengyi Song |
author_sort |
Bo Gao |
title |
Intruder (DD38E), a recently evolved sibling family of DD34E/Tc1 transposons in animals |
title_short |
Intruder (DD38E), a recently evolved sibling family of DD34E/Tc1 transposons in animals |
title_full |
Intruder (DD38E), a recently evolved sibling family of DD34E/Tc1 transposons in animals |
title_fullStr |
Intruder (DD38E), a recently evolved sibling family of DD34E/Tc1 transposons in animals |
title_full_unstemmed |
Intruder (DD38E), a recently evolved sibling family of DD34E/Tc1 transposons in animals |
title_sort |
intruder (dd38e), a recently evolved sibling family of dd34e/tc1 transposons in animals |
publisher |
BMC |
series |
Mobile DNA |
issn |
1759-8753 |
publishDate |
2020-12-01 |
description |
Abstract Background A family of Tc1/mariner transposons with a characteristic DD38E triad of catalytic amino acid residues, named Intruder (IT), was previously discovered in sturgeon genomes, but their evolutionary landscapes remain largely unknown. Results Here, we comprehensively investigated the evolutionary profiles of ITs, and evaluated their cut-and-paste activities in cells. ITs exhibited a narrow taxonomic distribution pattern in the animal kingdom, with invasions into two invertebrate phyla (Arthropoda and Cnidaria) and three vertebrate lineages (Actinopterygii, Agnatha, and Anura): very similar to that of the DD36E/IC family. Some animal orders and species seem to be more hospitable to Tc1/mariner transposons, one order of Amphibia and seven Actinopterygian orders are the most common orders with horizontal transfer events and have been invaded by all four families (DD38E/IT, DD35E/TR, DD36E/IC and DD37E/TRT) of Tc1/mariner transposons, and eight Actinopterygii species were identified as the major hosts of these families. Intact ITs have a total length of 1.5–1.7 kb containing a transposase gene flanked by terminal inverted repeats (TIRs). The phylogenetic tree and sequence identity showed that IT transposases were most closely related to DD34E/Tc1. ITs have been involved in multiple events of horizontal transfer in vertebrates and have invaded most lineages recently (< 5 million years ago) based on insertion age analysis. Accordingly, ITs presented high average sequence identity (86–95%) across most vertebrate species, suggesting that some are putatively active. ITs can transpose in human HeLa cells, and the transposition efficiency of consensus TIRs was higher than that of the TIRs of natural isolates. Conclusions We conclude that DD38E/IT originated from DD34E/Tc1 and can be detected in two invertebrate phyla (Arthropoda and Cnidaria), and in three vertebrate lineages (Actinopterygii, Agnatha and Anura). IT has experienced multiple HT events in animals, dominated by recent amplifications in most species and has high identity among vertebrate taxa. Our reconstructed IT transposon vector designed according to the sequence from the “cat” genome showed high cut-and-paste activity. The data suggest that IT has been acquired recently and is active in many species. This study is meaningful for understanding the evolution of the Tc1/mariner superfamily members and their hosts. |
topic |
Intruder Tc1/mariner transposons DD38E Horizontal transfer Evolution |
url |
https://doi.org/10.1186/s13100-020-00227-7 |
work_keys_str_mv |
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