A role for host–parasite interactions in the horizontal transfer of transposons across phyla

Abstract

Horizontal transfer (HT), or the passage of genetic material between non-mating species, is increasingly recognized as an important force in the evolution of eukaryotic genomes 1, 2. Transposons, with their inherent ability to mobilize and amplify within genomes, may be especially prone to HT3 -7. However, the means by which transposons can spread across widely diverged species remain elusive. Here we present evidence that host-parasite interactions have promoted the HT of four transposon families between invertebrates and vertebrates. We found that Rhodnius prolixus, a triatomine bug feeding on the blood of diverse tetrapods and vector of the Chagas disease in humans, carries in its genome four distinct transposon families that also invaded the genomes of a diverse, but overlapping, set of tetrapods. The bug transposons are ~98% identical and cluster phylogenetically with those of the opossum and squirrel monkey, two of its preferred mammalian hosts in South America. We also identified one of these transposon families in the pond snail Lymnaea stagnalis, a nearly cosmopolitan vector of trematodes infecting diverse vertebrates, whose ancestral sequence is nearly identical and clusters with those found in Old World mammals. Together these data provide evidence for a previously hypothesized role of hostparasite interactions in facilitating HT among animals 3,7 . Furthermore, the large amount of DNA generated by the amplification of the horizontally-transferred transposons supports the idea that the exchange of genetic material between hosts and parasites influence their genomic evolution.In order to examine the factors underlying HT among widely diverged taxa we began our investigation with SPACE INVADERS (or SPIN), a recently described DNA transposon that has undergone repeated episodes of HT across the genomes of seven tetrapod lineages 5 . We first performed a series of BLASTN searches using the SPIN superconsensus sequence 5 as a query against all GenBank databases (see Methods), including 102 species for which whole genome shotgun (WGS) sequences are available. In addition to the vertebrates previously known to harbor SPIN, we found highly significant hits (e-values as low as 0, corresponding here to 86% identity over >1 kb) in the triatomine bug, Rhodnius prolixus, an hemipteran insect that feeds on the blood of mammals, birds, and reptiles and serves as a vector forCorrespondence and requests for materials should be addressed to C.F. (cedric@uta.edu). * These authors contributed equally to this work Supplementary Information is linked to the online version of the paper at www.nature.com/nature. Author Contributions C.G., S.S., and C.F. designed research, performed research, and analyzed data. J.K.P. contributed data and perl scripts. P.J.B. contributed reagents/material. C.G., S.S., and C.F. wrote the paper. Supplementary Fig. 2), a pattern indicative of the accumulation of discrete substitutions in each copy and consistent with neutral evolution of transposons after their integration in the genome...

Chromosomal divergence and evolutionary inferences in Rhodniini based on the chromosomal location of ribosomal genes

“…In many organisms, rDNA clusters behave as mobile genetic elements due to the presence of transposable elements adjacent to the ribosomal genes (Schubert & Wobus 1985, Zhang et al 2008. Several transposable elements have been described in Triatominae (Gilbert et al 2010), including a non-long terminal repeat retrotransposon inserted inside the 28S rDNA sequence of R. prolixus (Jakubczak et al 1991). Thus, we can envisage an rDNA cluster with associated transposable elements moving through genomes, as previously postulated for other insects (Cabrero & Camacho 2008, Nguyen et al 2010, Cabral-de-Mello et al 2011a).…”

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

“…34). Of particular note is the apparent proliferation of transposable elements among organisms that have no vertical lineage, e.g., between Drosophila species (35), among higher plants (36), and among distantly related tetrapods (37,38). These transposable elements show remarkable sequence identity despite host genome variation arising from divergent evolution.…”

Quand les éléments génétiques mobiles bondissent entre espèces animales

“…La seconde est que l'on observe un accroissement constant du nombre de cas de transferts d'ET rapportés chez les opistokontes 1 (métazoaires et champignons) et les plantes, les deux groupes d'eucaryotes multicellulaires représentant la part la plus importante des génomes complètement séquencés. Enfin, à plusieurs reprises, de tels transferts se sont produits sur des distances phylogénétiques considérables, avec par exemple 12 transferts impliquant au moins deux taxons qui appartiennent à des phyla animaux séparés par plus de 500 millions d'années (par exemple entre insectes et mammifères [8]). Le nombre et l'étendue de ces transferts sont d'autant plus remarquables que jusqu'à présent, quasiment aucune étude n'a cherché à caractériser ce phénomène de manière systématique.…”

“…De nombreuses hypothèses impliquant divers vecteurs bactériens et/ou viraux ont été proposées, souvent sur la base d'expériences conduites en laboratoire, sans qu'aucune n'ait été entièrement validée dans la nature. Récemment, nous avons découvert que les génomes de dix vertébrés, dont huit mammifères, un reptile et un amphibien, contiennent entre une et quatre familles d'ET également présentes dans le génome d'une punaise hématophage (Rhodnius prolixus), un insecte vecteur de trypanosomes responsables de la maladie de Chagas [8]. Les ET de la punaise sont quasiment identiques à ceux des vertébrés et forment un groupe phylogénétique avec ceux du singe écu-reuil et de l'opossum (un marsupial), deux de ses hôtes préférés en Amérique du Sud (Figure 1).…”