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

Abstract

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 Ϸ96% 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. genome evolution ͉ lateral gene transfer ͉ transposable elements ͉ transposase L ateral or horizontal transfer (HT), the transfer of genetic material between reproductively isolated species, is a frequent occurrence in prokaryotes with selfish and mobile genetic elements such as phages, plasmids, and transposons, serving as the primary vehicles for HT of prokaryotic genes (1). In contrast, reports of HT are scarce in eukaryotes and most cases of nuclear acquisition implicate transfers from prokaryotes or endosymbionts (2-6). The best documented instances of HT between the nuclear genomes of multicellular eukaryotes involve mobile genetic elements, and in particular class 2 or DNA mediated transposons (7,8). Thus far, conspicuous cases of HT of DNA transposons have been detected among insects (8-12), fish (13) and, in one example, between plants (14). Germline invasions by retroviruses have been documented for several mammals (15-18), and there is mounting evidence supporting the horizontal introduction of a snake retroposon in ruminants (19,20). However, to our knowledge, there has been no substantiated report of HT of DNA transposons in mammals. Here, we present unequivocal evidence for the repeated HT of a DNA transposon family named SPACE INVADERS in 7 tetrapod lineages, including 5 mammalian orders. ResultsDiscovery of SPIN Transposons. While surveying DNA transposons in the draft...

The Atlantic salmon genome provides insights into rediploidization

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Host RNAs, including transposons, are encapsidated by a eukaryotic single-stranded RNA virus

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