LTR-Retrotransposons from Bdelloid Rotifers Capture Additional ORFs Shared between Highly Diverse Retroelement Types

Abstract

Rotifers of the class Bdelloidea, microscopic freshwater invertebrates, possess a highly-diversified repertoire of transposon families, which, however, occupy less than 4% of genomic DNA in the sequenced representative Adineta vaga. We performed a comprehensive analysis of A. vaga retroelements, and found that bdelloid long terminal repeat (LTR)-retrotransposons, in addition to conserved open reading frame (ORF) 1 and ORF2 corresponding to gag and pol genes, code for an unusually high variety of ORF3 sequences. Retrovirus-like LTR families in A. vaga belong to four major lineages, three of which are rotifer-specific and encode a dUTPase domain. However only one lineage contains a canonical env-like fusion glycoprotein acquired from paramyxoviruses (non-segmented negative-strand RNA viruses), although smaller ORFs with transmembrane domains may perform similar roles. A different ORF3 type encodes a GDSL esterase/lipase, which was previously identified as ORF1 in several clades of non-LTR retrotransposons, and implicated in membrane targeting. Yet another ORF3 type appears in unrelated LTR-retrotransposon lineages, and displays strong homology to DEDDy-type exonucleases involved in 3′-end processing of RNA and single-stranded DNA. Unexpectedly, each of the enzymatic ORF3s is also associated with different subsets of Penelope-like Athena retroelement families. The unusual association of the same ORF types with retroelements from different classes reflects their modular structure with a high degree of flexibility, and points to gene sharing between different groups of retroelements.

Giant Reverse Transcriptase-Encoding Transposable Elements at Telomeres

“…DEDDy exonucleases (ExoN) have also been found in nidoviruses, and were hypothesized to have a proofreading function in these large (+)ssRNA viruses ( Ulferts and Ziebuhr 2014 ). Both DEDDy-like and GDSL-like Terminon ORFs exhibit similarity to ORF3’s in bdelloid LTR retrotransposons ( Rodriguez et al 2017 ).…”

Evolutionary dynamics of transposable elements in bdelloid rotifers

“…These early ideas were transformed by more detailed studies of the model bdelloid species Adineta vaga , which used refined methods and genome-scale data to discover a variety of retrotransposon families. These include an endonuclease-deficient Penelope -like element (PLE) designated Athena [57,58], which is itself incorporated within much larger and highly unusual retroelements called Terminons [59]; another PLE that has retained its endonuclease [60], LTR retrotransposons ( Juno , Vesta , TelKA and Mag [61,62]), and LINE-like retrotransposons ( R4 , R9 , Hebe , RTE , Tx1 and Soliton [44,63,64]). In total, TEs accounted for 2.2% of the 217 Mb genome (~4.8 Mb) [44], rising to ~4% on inclusion of the recently discovered giant Terminon elements [59].…”

Using bioinformatic and phylogenetic approaches to classify transposable elements and understand their complex evolutionary histories

“…For RNA-based class I TEs, this dimension is provided by envelope ( env ) genes, which are responsible for interaction with host cell membranes. Their capture by LTR-retrotransposons has occurred independently multiple times in evolution, with the most prominent branch represented by vertebrate retroviruses, supplemented by an impressive diversity of smaller branches in insects, nematodes, and rotifers, with env genes acquired from baculoviruses (dsDNA), herpesviruses (dsDNA), phleboviruses (ssRNA), or paramyxoviruses (−ssRNA) [ 107 , 108 ]. It should be noted that while env genes in LTR retrotransposons appear downstream of pol as ORF3, acquisition of a downstream ORF3 does not automatically imply that it codes for an env gene.…”

“…It should be noted that while env genes in LTR retrotransposons appear downstream of pol as ORF3, acquisition of a downstream ORF3 does not automatically imply that it codes for an env gene. The env -like function of ORF3’s in numerous plant LTR retrotransposons still has not been established, and in rotifers ORF3s were derived from other enzymatic functions, such as DEDDy exonuclease or GDSL esterase/lipase [ 108 – 110 ]. The nucleocapsid ORFs constitute another important component in retroelement replication, whether they proliferate as enveloped viruses, or intragenomically as ribonucleoprotein particles (RNP), which can form nucleoprotein cores and adopt the shape of virus-like particles (VLPs).…”