Pervasive horizontal transfer of rolling-circle transposons among animals

Abstract

Horizontal transfer (HT) of genes is known to be an important mechanism of genetic innovation, especially in prokaryotes. The impact of HT of transposable elements (TEs), however, has only recently begun to receive widespread attention and may be significant due to their mutagenic potential, inherent mobility, and abundance. Helitrons, also known as rolling-circle transposons, are a distinctive subclass of TE with a unique transposition mechanism. Here, we describe the first evidence for the repeated HT of four different families of Helitrons in an unprecedented array of organisms, including mammals, reptiles, fish, invertebrates, and insect viruses. The Helitrons present in these species have a patchy distribution and are closely related (80-98% sequence identity), despite the deep divergence times among hosts. Multiple lines of evidence indicate the extreme conservation of sequence identity is not due to selection, including the highly fragmented nature of the Helitrons identified and the lack of any signatures of selection at the nucleotide level. The presence of horizontally transferred Helitrons in insect viruses, in particular, suggests that this may represent a potential mechanism of transfer in some taxa. Unlike genes, Helitrons that have horizontally transferred into new host genomes can amplify, in some cases reaching up to several hundred copies and representing a substantial fraction of the genome. Because Helitrons are known to frequently capture and amplify gene fragments, HT of this unique group of DNA transposons could lead to horizontal gene transfer and incur dramatic shifts in the trajectory of genome evolution.

Fig. 1.—

(a) Alignment of 5' and 3' ends (30 bp) of Heligloria (Hg) elements from species into which the element has horizontally transferred (for criteria, see Materials and Methods and supplementary table S1, Supplementary Material online for additional species not included in the analysis). Similarity at the 3' end (>80%) is used to determine family designation (shown in gray with white letters). Similarity at the 5' end (>80%) is used to designate subfamilies (two shown here: A, light gray with black letters and B, black with white letters). Species names denoted with the first letter of the genus and species (Acyrthosiphon pisum [Ap], Anolis carolinensis [Ac], Bombyx mori [Bm], Drosophila willistoni [Dw], D. ananassae [Da], D. yakuba [Dy], Myotis lucifugus [Ml], Petromyzon marinus [Pm], Rhodnius prolixus [Rp], Cotesia plutella Braco Virus [BV]). (b) Sequence identity (%) among copies of HeligloriaAi elements from the six species (table 1) in which they were identified (see supplementary Materials and Methods, Supplementary Material online); sequence identity was calculated using 10 bp windows with 3-bp stepwise increments over the internal region.

FIG. 2.—

Schematic representation of phylogenetic relationships among animal lineages and estimated divergence times (Ma). Presence of horizontally transferred Helitrons from four different families in each lineage are denoted by rectangles (not placed relative to the timescale). Numbers in parentheses on the right indicate the number of species (when >1) for which whole genome sequence data are publicly available in the whole genome shotgun (National Center for Biotechnology Information).

Fig. 3.—

Distribution of Helitron families (Heligloria, Helisimi, Heliminu, and Helianu) across species and their contribution (shown in Kbp) toward the host genome.