Yushenova Irina A.
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PreprintGiant reverse transcriptase-encoding transposable elements at telomeres( 2017-05) Arkhipova, Irina R. ; Yushenova, Irina A. ; Rodriguez, FernandoTransposable elements are omnipresent in eukaryotic genomes and have a profound impact on chromosome structure, function and evolution. Their structural and functional diversity is thought to be reasonably well-understood, especially in retroelements, which transpose via an RNA intermediate copied into cDNA by the element-encoded reverse transcriptase, and are characterized by a compact structure. Here we report a novel type of expandable eukaryotic retroelements, which we call Terminons. These elements can attach to G-rich telomeric repeat overhangs at the chromosome ends, in a process apparently facilitated by complementary C-rich repeats at the 3’-end of the RNA template immediately adjacent to a hammerhead ribozyme motif. Terminon units, which can exceed 40 kb in length, display an unusually complex and diverse structure, and can form very long chains, with host genes often captured between units. As the principal polymerizing component, Terminons contain Athena reverse transcriptases previously described in bdelloid rotifers and belonging to the enigmatic group of Penelope-like elements, but can additionally accumulate multiple co-oriented ORFs, including DEDDy 3’-exonucleases, GDSL esterases/lipases, GIY-YIG-like endonucleases, rolling-circle replication initiator (Rep) proteins, and putatively structural ORFs with coiled-coil motifs and transmembrane domains. The extraordinary length and complexity of Terminons and the high degree of inter-family variability in their ORF content challenge the current views on the structural organization of eukaryotic retroelements, and highlight their possible connections with the viral world and the implications for the elevated frequency of gene transfer.
PreprintBiochemical properties of bacterial reverse transcriptase-related (rvt) gene products : multimerization, protein priming, and nucleotide preference( 2018-05) Yushenova, Irina A. ; Arkhipova, Irina R.Cellular reverse transcriptase-related (rvt) genes represent a novel class of reverse transcriptases (RTs), which are only distantly related to RTs of retrotransposons and retroviruses, but, similarly to telomerase RTs, are immobilized in the genome as single-copy genes. They have been preserved by natural selection throughout the evolutionary history of large taxonomic groups, including most fungi, a few plants and invertebrates, and even certain bacteria, being the only RTs present across different domains of life. Bacterial rvt genes are exceptionally rare but phylogenetically related, consistent with common origin of bacterial rvt genes rather than eukaryote-to-bacteria transfer. To investigate biochemical properties of bacterial RVTs, we conducted in vitro studies of recombinant HaRVT protein from the filamentous gliding bacterium Herpetosiphon aurantiacus (Chloroflexi). Although HaRVT does not utilize externally added standard primer-template combinations, in the presence of divalent manganese it can polymerize very short products, using dNTPs rather than NTPs, with a strong preference for dCTP incorporation. Further, we investigated the highly conserved N- and C-terminal domains, which distinguish RVT proteins from other RTs. We show that the N-terminal coiled-coil motif, which is present in nearly all RVTs, is responsible for the ability of HaRVT to multimerize in solution, forming up to octamers. The C-terminal domain may be capable of protein priming, which is abolished by site-directed mutagenesis of the catalytic aspartate and greatly reduced in the absence of the conserved tyrosine residues near the C-terminus. The unusual biochemical properties displayed by RVT in vitro will provide the basis for understanding its biological function in vivo.
ArticleEndonuclease-containing Penelope retrotransposons in the bdelloid rotifer Adineta vaga exhibit unusual structural features and play a role in expansion of host gene families(BioMed Central, 2013-08-27) Arkhipova, Irina R. ; Yushenova, Irina A. ; Rodriguez, FernandoPenelope-like elements (PLEs) are an enigmatic group of retroelements sharing a common ancestor with telomerase reverse transcriptases. In our previous studies, we identified endonuclease-deficient PLEs that are associated with telomeres in bdelloid rotifers, small freshwater invertebrates best known for their long-term asexuality and high foreign DNA content. Completion of the high-quality draft genome sequence of the bdelloid rotifer Adineta vaga provides us with the opportunity to examine its genomic transposable element (TE) content, as well as TE impact on genome function and evolution. We performed an exhaustive search of the A. vaga genome assembly, aimed at identification of canonical PLEs combining both the reverse transcriptase (RT) and the GIY-YIG endonuclease (EN) domains. We find that the RT/EN-containing Penelope families co-exist in the A. vaga genome with the EN-deficient RT-containing Athena retroelements. Canonical PLEs are present at very low copy numbers, often as a single-copy, and there is no evidence that they might preferentially co-mobilize EN-deficient PLEs. We also find that Penelope elements can participate in expansion of A. vaga multigene families via trans-action of their enzymatic machinery, as evidenced by identification of intron-containing host genes framed by the Penelope terminal repeats and characteristic target-site duplications generated upon insertion. In addition, we find that Penelope open reading frames (ORFs) in several families have incorporated long stretches of coding sequence several hundred amino acids (aa) in length that are highly enriched in asparagine residues, a phenomenon not observed in other retrotransposons. Our results show that, despite their low abundance and low transcriptional activity in the A. vaga genome, endonuclease-containing Penelope elements can participate in expansion of host multigene families. We conclude that the terminal repeats represent the cis-acting sequences required for mobilization of the intervening region in trans by the Penelope-encoded enzymatic activities. We also hypothesize that the unusual capture of long N-rich segments by the Penelope ORF occurs as a consequence of peculiarities of its replication mechanism. These findings emphasize the unconventional nature of Penelope retrotransposons, which, in contrast to all other retrotransposon types, are capable of dispersing intron-containing genes, thereby questioning the validity of traditional estimates of gene retrocopies in PLE-containing eukaryotic genomes.
ArticleGenomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga(Nature Publishing Group, 2013-07-21) Flot, Jean-Francois ; Hespeels, Boris ; Li, Xiang ; Noel, Benjamin ; Arkhipova, Irina R. ; Danchin, Etienne G. J. ; Hejno, Andreas ; Henrissat, Bernard ; Koszul, Romain ; Aury, Jean-Marc ; Barbe, Valerie ; Barthelemy, Roxane-Marie ; Bast, Jens ; Bazykin, Georgii A. ; Chabrol, Olivier ; Couloux, Arnaud ; Da Rocha, Martine ; Da Silva, Corinne ; Gladyshev, Eugene A. ; Gouret, Philippe ; Hallatschek, Oskar ; Hecox-Lea, Bette ; Labadie, Karine ; Lejeune, Benjamin ; Piskurek, Oliver ; Poulain, Julie ; Rodriguez, Fernando ; Ryan, Joseph F. ; Vakhrusheva, Olga A. ; Wajnberg, Eric ; Wirth, Benedicte ; Yushenova, Irina A. ; Kellis, Manolis ; Kondrashov, Alexey S. ; Mark Welch, David B. ; Pontarotti, Pierre ; Weissenbach, Jean ; Wincker, Patrick ; Jaillon, Olivier ; Van Doninck, KarineLoss of sexual reproduction is considered an evolutionary dead end for metazoans, but bdelloid rotifers challenge this view as they appear to have persisted asexually for millions of years1. Neither male sex organs nor meiosis have ever been observed in these microscopic animals: oocytes are formed through mitotic divisions, with no reduction of chromosome number and no indication of chromosome pairing2. However, current evidence does not exclude that they may engage in sex on rare, cryptic occasions. Here we report the genome of a bdelloid rotifer, Adineta vaga (Davis, 1873)3, and show that its structure is incompatible with conventional meiosis. At gene scale, the genome of A. vaga is tetraploid and comprises both anciently duplicated segments and less divergent allelic regions. However, in contrast to sexual species, the allelic regions are rearranged and sometimes even found on the same chromosome. Such structure does not allow meiotic pairing; instead, we find abundant evidence of gene conversion, which may limit the accumulation of deleterious mutations in the absence of meiosis. Gene families involved in resistance to oxidation, carbohydrate metabolism and defence against transposons are significantly expanded, which may explain why transposable elements cover only 3% of the assembled sequence. Furthermore, 8% of the genes are likely to be of non-metazoan origin and were probably acquired horizontally. This apparent convergence between bdelloids and prokaryotes sheds new light on the evolutionary significance of sex.