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 approximately 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.

Fig. 1.

Sequence identity and multiple alignment of SPIN elements. (A) Interspecific sequence identity across the entire length of full-length SPIN elements. The plot reflects the average sequence identity in nonoverlapping bins of 50 nt across a multiple alignment of the full-length SPIN consensus sequences from bat, tenrec, and bushbaby, along with single-copy sequences from frog, lizard, and opossum. An average of 98% pairwise nucleotide identity is observed between the bat, tenrec, and bushbaby consensus sequences and an average of 96% between any 2 sequences (range = 84–99%). The transposase ORF is depicted as a black rectangle and the terminal inverted repeats are indicated by arrowheads. (B) Multiple alignment of the 5′ and 3′ ends of full-length and MITE SPIN elements. The 16-bp TIRs are boxed. All SPIN elements share the same imperfection at position 4 in their consensus (black arrowheads). The only exception is SPIN_Xt, the full-length SPIN element in frog, for which we were able to locate only a single partial copy. However, the same TIR imperfection is found in the consensus sequence of SPIN_NA_5_Xt, a MITE subfamily from frog. [Rodent, mouse/rat; Og, Otolemur garnettii (bushbaby); Et, Echinops telfairi (tenrec); Ml, Myotis lucifugus (bat); Xt, Xenopus tropicalis (frog); Ac, Anolis carolinensis (lizard); Md, Monodelphis domestica (opossum)].

Fig. 2.

Experimental verification of the presence or absence of SPIN transposons. PCR fragments of expected sizes were obtained in all species (or a close relative) where SPIN elements were identified computationally. A PCR product of the expected size (data not shown) was also obtained with DNA from the opossum, Monodelphis domestica. DNA sequencing of cloned PCR products for each species confirmed that they represent distinct SPIN family members (see SI Materials and Methods).

Fig. 3.

Species distribution and timing of amplification of SPIN transposons. The tree depicts the phylogenetic relationship and divergence times of the vertebrate species with complete or nearly complete genome sequences currently available (23, 42). The species harboring SPIN transposons are in bold. The timing of SPIN amplification in each species lineage is shown by the red vertical bars above the corresponding branches. Each set of bars represents the age span for all SPIN MITE subfamilies found in the species with each individual bar showing the relative proportion of elements falling within the same, nonoverlapping 3-myr bin (see SI Materials and Methods). The age span is not shown for lizard because the neutral substitution rate is undetermined for this species. However, we note that the level of sequence divergence of SPIN in lizard is similar to those observed in bushbaby and tenrec (see Table 1).