Repeated horizontal transfer of a DNA transposon in mammals and other tetrapods

Horizontal transfer (HT) is central to the evolution of prokaryotic species. Selfish and mobile genetic elements, such as phages, plasmids, and transposons, are the primary vehicles for HT among prokaryotes. In multicellular eukaryotes, the prevalence and evolutionary significance of HT remain uncle...

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Bibliographic Details
Published in:Proceedings of the National Academy of Sciences - PNAS 2008-11, Vol.105 (44), p.17023-17028
Main Authors: Pace, John K. II, Gilbert, Clément, Clark, Marlena S, Feschotte, Cédric
Format: Article
Language:English
Subjects:
Animals
Anura
Base Sequence
Bats
Biological Sciences
Biological taxonomies
Databases, Genetic
Deoxyribonucleic acid
DNA
DNA Transposable Elements - genetics
Eukaryotes
Evolution
Evolution, Molecular
Gene Transfer, Horizontal
Genetic transposition
Genome
Genomes
Genomics
Humans
Lacertilia
Mammals
Mammals - genetics
Mice
Mites
Molecular Sequence Data
Myotis lucifugus
Phylogeny
Primates
Rats
Rodents
Transposons
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Summary:Horizontal transfer (HT) is central to the evolution of prokaryotic species. Selfish and mobile genetic elements, such as phages, plasmids, and transposons, are the primary vehicles for HT among prokaryotes. In multicellular eukaryotes, the prevalence and evolutionary significance of HT remain unclear. Here, we identified a set of DNA transposon families dubbed SPACE INVADERS (or SPIN) whose consensus sequences are [almost equal to]96% identical over their entire length (2.9 kb) in the genomes of murine rodents (rat/mouse), bushbaby (prosimian primate), little brown bat (laurasiatherian), tenrec (afrotherian), opossum (marsupial), and two non-mammalian tetrapods (anole lizard and African clawed frog). In contrast, SPIN elements were undetectable in other species represented in the sequence databases, including 19 other mammals with draft whole-genome assemblies. This patchy distribution, coupled with the extreme level of SPIN identity in widely divergent tetrapods and the overall lack of selective constraint acting on these elements, is incompatible with vertical inheritance, but strongly indicative of multiple horizontal introductions. We show that these germline infiltrations likely occurred around the same evolutionary time (15-46 mya) and spawned some of the largest bursts of DNA transposon activity ever recorded in any species lineage (nearly 100,000 SPIN copies per haploid genome in tenrec). The process also led to the emergence of a new gene in the murine lineage derived from a SPIN transposase. In summary, HT of DNA transposons has contributed significantly to shaping and diversifying the genomes of multiple mammalian and tetrapod species.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.0806548105