Widespread horizontal transfer of retrotransposons

Abstract

In higher organisms such as vertebrates, it is generally believed that lateral transfer of genetic information does not readily occur, with the exception of retroviral infection. However, horizontal transfer (HT) of protein coding repetitive elements is the simplest way to explain the patchy distribution of BovB, a long interspersed element (LINE) about 3.2 kb long, that has been found in ruminants, marsupials, squamates, monotremes, and African mammals. BovB sequences are a major component of some of these genomes. Here we show that HT of BovB is significantly more widespread than believed, and we demonstrate the existence of two plausible arthropod vectors, specifically reptile ticks. A phylogenetic tree built from BovB sequences from species in all of these groups does not conform to expected evolutionary relationships of the species, and our analysis indicates that at least nine HT events are required to explain the observed topology. Our results provide compelling evidence for HT of genetic material that has transformed vertebrate genomes.transposon | interspersed repeat R epetitive DNA is abundant in metazoan genomes and is largely composed of transposable elements (TEs). Retrotransposons are a class of TEs that are able to "copy and paste" themselves within the genome via an RNA intermediate (1). Long interspersed element (LINE) retrotransposons encode an endonuclease that nicks the DNA and allows the reverse transcriptase encoded by the element to copy the RNA produced from the TE back into DNA during repair of the nick, integrating the LINE into a new genomic position (2). However, unlike retroviruses, LINEs and other TEs do not encode an envelope protein and are hence unable to disperse horizontally without a vector between species.Horizontal transfer (HT) of TEs is largely inferred by similarity of DNA sequence; however, where the mechanism of HT has been demonstrated, a vector such as a parasite or virus was involved. For example, both P elements, between species of Drosophila (3), and the Space Invader DNA transposon, between tetrapods (4, 5), are transmitted by arthropod parasites (5, 6). The Sauria short interspersed element (SINE), has been shown to have transferred into a West African rodent poxvirus from the snake, Echis ocellatus, also supporting viruses as mechanisms for retrotransposon HT (7). HT of retrotransposons is significant because conservative estimates of their prevalence indicate that they make up between a third and a half of typical vertebrate genomes. Thus, demonstration of widespread HT for retrotransposons has significant implications for our understanding of genome structure and evolution. In this report we describe a comprehensive analysis of HT of BovB, a LINE about 3.2 kb long, which has previously been described in ruminants, marsupials, squamates, monotremes, and African mammals (8-11). Results and DiscussionTo determine the sequence conservation of BovB across taxa and examine the evidence for HT, we identified BovB sequences in all publicly available genomes and in sev...

Widespread and frequent horizontal transfers of transposable elements in plants

“…However, although horizontal gene transfers are very common in Bacteria (Rocha 2013), evidence of HTTs in eukaryotes remains scarce, although recent reports suggest their potential impact in genome evolution . Three criteria have been defined for the detection of HTTs: patchy distributions of TEs in phylogenies; identification of TEs exhibiting high sequence similarity between distantly related taxa; and phylogenetic incongruence between the host and TEs Kuraku et al 2012;Wallau et al 2012;Walsh et al 2013). An exhaustive search for HTTs that meet these three criteria in a wide taxonomic range thus requires a comprehensive set of genomic resources.…”

Exogenous Transposable Elements Circumvent Identity-Based Silencing, Permitting the Dissection of Expression-Dependent Silencing

“…Although transgenesis might be considered an artificial approach to investigate silencing, evidence suggests that transgenesis can occur naturally (Kyndt et al, 2015). In addition, TEs undergo widespread horizontal transfer into new genomes (Bartolomé et al, 2009;Walsh et al, 2013) akin to transgenesis. For example, the P element TE was horizontally transferred from Drosophila willistoni to Drosophila melanogaster in the early 20th century after >40 million years of divergence between the two species (Daniels et al, 1990).…”

Next-generation sequencing as means to retrieve tick systematic markers, with the focus on Nuttalliella namaqua (Ixodoidea: Nuttalliellidae)

“…Given that transposable elements are abundant in vertebrate genomes, N. namaqua and argasids (which share a similar feeding biology) could have contributed to vertebrate genome evolution since the Permian. In this regard, the BovB LINE gene obtained in this study was proposed to have been widely disseminated among vertebrates via horizontal transfer by tick vectors (Walsh et al 2013). The high coverage of these elements in the present study may be due to their high abundance in vertebrate genomes and tick hosts (Walsh et al 2013).…”

“…In this regard, the BovB LINE gene obtained in this study was proposed to have been widely disseminated among vertebrates via horizontal transfer by tick vectors (Walsh et al 2013). The high coverage of these elements in the present study may be due to their high abundance in vertebrate genomes and tick hosts (Walsh et al 2013). The possibility exists that transposable elements might have been the first "infectious" agent transmitted by ticks.…”

“…Given the ancient proposed origin of Nuttalliella in the Late Carboniferous or Early Permian (Mans et al 2011;Mans et al 2012), its generalist feeding behaviour on reptiles and mammals (Mans et al 2014), the ability to maintain nucleated red blood cells intact over prolonged period between multiple feeding events (Mans et al 2012), with the possibility of blood meal regurgitation, it is a likely vector of vertebrate transposable elements (Walsh et al 2013). Given that transposable elements are abundant in vertebrate genomes, N. namaqua and argasids (which share a similar feeding biology) could have contributed to vertebrate genome evolution since the Permian.…”