New environment, new invaders - repeated horizontal transfer of LINEs to sea snakes

Abstract

While numerous studies have found horizontal transposon transfer (HTT) to be widespread across metazoans, few have focused on HTT in marine ecosystems. To investigate potential recent HTTs into marine species we searched for novel repetitive elements in sea snakes, a group of elapids which transitioned to a marine habitat at most 18 Mya. Our analysis uncovered repeated HTTs into sea snakes following their marine transition. Such major shifts in habitat should require significant genomic changes.The six subfamilies of LINE retrotransposons identified in the olive sea snake ( Aipysurus laevis ) are transcribed, and hence are likely still active and expanding across the genome. A search of 600 metazoan genomes found all six were absent from other amniotes, including terrestrial elapids, with the most similar transposons present in fish and marine invertebrates. The one exception was a similar transposon found in sea kraits, a lineage of amphibious elapids which independently transitioned to a marine environment following their divergence from terrestrial species 25 Mya. Our finding of repeated horizontal transfer events into separate lineages of marine snakes greatly expands past findings of frequent horizontal transfer in the marine environment, suggesting it is ideal for the transfer of transposons.Transposons are drivers of evolution as sources of genomic sequence and hence genomic novelty. This provides evidence of the environment influencing evolution of metazoans not only through specific selection pressures, but also by contributing novel genomic material. Significance StatementRecent research has found horizontal transfer (HT) of transposons between marine animals. We analyzed the olive sea snake ( Aipysurus laevis ) genome, uncovering HT of six novel retrotransposons into sea snakes since their marine transition within the last 18 Mya. All six are absent from terrestrial animals and are most similar to retrotransposons found in fish, corals and the independently marine sea kraits. All six retrotransposons are likely still active and expanding across the genome in A. laevis . Our findings suggest the marine environment is ideal for the HT of transposons; and provide evidence that changing environments can influence evolution not only through novel selective pressures, but also by contributing novel genomic material. Main Text

Multiple ancestral duplications of the red-sensitive opsin gene (LWS) in teleost fishes and convergent spectral shifts to green vision in gobies

“…An alternative explanation for how gobies might have acquired LWS3 is through horizontal gene transfer. While arguably unlikely, horizontal gene transfer has been shown to contribute to genetic diversity in sea-snakes which have several transposable elements that are most like the ones found in teleosts and corals (Galbraith et al 2020). However, based on the vertebrate genomes we surveyed; it is currently not possible to discern a potential hypothetical donor for LWS3 .…”

Horizontal transposon transfer and its implications for the ancestral ecology of hydrophiine snakes

“…At least eleven autonomous TEs have been horizontally transferred into hydrophiines, with most likely from marine organisms. We have previously described the horizontal transfer of the Proto2 to Aipysurus laevis in Galbraith et al (2020) [6] and the PIF-Harbinger to Laticauda in Galbraith et al (2021) [7]…”

“…Of these eleven, three were transferred into the ancestral hydrophiine, five into sea kraits, one into sea snakes and one into the common ancestor of terrestrial hydrophiines and sea snakes (Figure 7). We have previously described 2 of the 11 HT events in detail, that of Proto2-Snek to Aipysurus and Harbinger-Snek toLaticauda, both of which were likely transferred from a marine species (see [6,7]). Three of the four newly identified HT events identified in Laticauda were probably also from an aquatic species, because similar sequences are only found in marine or amphibious species.…”

“…Sea kraits ( Laticauda ) are amphibious and have specialised to hunt various fish including eels and anguilliform-like fish at sea, while digesting prey, mating and shedding on land [5]. Since transitioning to marine environments, both sea snakes and sea kraits have been the recipients of multiple independent horizontal transposon transfer (HTT) events, which may have had adaptive potential [6,7].…”

Genome stability is in the eye of the beholder: recent retrotransposon activity varies significantly across avian diversity

“…Confirmed CR1 CARP consensus sequences were manually curated through a "search, extend, align, trim" method as described in (Galbraith et al 2020) to ensure that the 3' hairpin and microsatellite were intact. Briefly, this curation method involves searching for sequences highly similar to the consensus with BLASTN 2.7.1+ (Zhang et al 2000), extending the coordinates of the sequences found by flanks of 600 bp, aligning these sequences using MAFFT v7.453 (Katoh and Standley 2013) and trimming the discordant regions manually in Geneious Prime v2020.1.…”