Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution

Abstract

Horizontal transfer is the passage of genetic material between genomes by means other than parent-to-offspring inheritance. Although the transfer of genes is thought to be crucial in prokaryotic evolution, few instances of horizontal gene transfer have been reported in multicellular eukaryotes; instead, most cases involve transposable elements. With over 200 cases now documented, it is possible to assess the importance of horizontal transfer for the evolution of transposable elements and their host genomes. We review criteria for detecting horizontal transfers and examine recent examples of the phenomenon, shedding light on its mechanistic underpinnings, including the role of host-parasite interactions. We argue that the introduction of transposable elements by horizontal transfer in eukaryotic genomes has been a major force propelling genomic variation and biological innovation.

Figure I. (a) Simplified model of the lifecycle of TE families and the importance of horizontal transfer

Grey bars represent chromosomes, colored squares represent TEs (with the original sequence in red, mutated in orange, diversified in yellow, persistent in green, and inactivated by orange and red lines). Arrows represent transitions between stages (not all possibilities are illustrated). (b and c) Expected phylogenetic patterns of TEs found among hosts when HTT is frequent (b) versus rare (c). Hypothetical TE phylogenies are depicted with black lines, black circles at nodes illustrate episodes of HTT, and host species are shown in colored silhouettes on the right of each tree with color similarity indicative of their phylogenetic relatedness.

Figure I. Schematics of the transposition mechanisms for the three major groups of TEs, with special reference to points in the process where the possibility of HTT is especially high

White circles with solid borders are cells, gray circles with dashed borders are nuclei; bold lines indicate host DNA (black = donor site, grey = recipient site); TEs are represented by red boxes (DNA) or squiggly lines (mRNA); protein products are represented by shaded circles and ovals; thick black arrows indicate stage in transposition during which TEs are disassociated from host genomic DNA and thought to be most likely to horizontally transfer.

Figure I. An example of the lines of evidence used to infer the horizontal transfer of a transposable element family, OposCharlie1 (OC1), across 3 phyla and 3 continents

(a) Phylogenetic evidence based on a tree showing the patchy distribution and timing of amplification of OC1 across phyla. Presence indicated with an orange lightning bolt, timing of amplification (mya) estimated for vertebrates based on sequence divergence of copies from the consensus shown below tree. (b) Lack of orthologous insertions among taxa illustrated by an alignment showing empty sites at orthologous positions across taxa sharing recently transferred copies of OC1 (target site duplications of insert shown in yellow). (c) Sequence identity shown by a plot of the percent identity at the nucleotide level across all aligned regions of the OC1 consensus sequence across taxa, including the transposase open-reading frame (indicated by the blue rectangle), using 10 bp window and 3 bp steps. (d) Biogeographical evidence represented by a phylogeny of OC1 elements superimposed on a map to illustrate the presumed distribution of the host species at the inferred time of transfer which shows higher identity among geographically overlapping species. (e) Candidate vectors include i. naked DNA or RNA, ii. TEs, iii. viruses, iv. bacteria (e.g., Wolbachia), v. cellular parasites (e.g., trypanosomes), vi. internal parasites (e.g., schistosomes), vii. obligate endoparasitoids (e.g., parasitoid wasps), viii. ectoparasites (e.g., R. prolixus, the blood sucking triatomine bug, which has OC1 copies 95% similar to those found in its preferred host, the opossum [based on Gilbert et al. 2010]).

Figure I. Schematic of the impact of HTT on the genome

Red chevron represents HTT, yellow and orange circles represent proximate physical effects of HTT, colored arrows represent consequences (purple = beneficial, green = neutral, and light blue = deleterious), and the rectangle represents potential downstream outcomes of effects for which there is a selective benefit.