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DNA repair during nonreductional meiosis in the asexual rotifer Adineta vaga.

ABSTRACT: Rotifers of the class Bdelloidea are microscopic animals notorious for their long-term persistence in the apparent absence of sexual reproduction and meiotic recombination. This evolutionary paradox is often counterbalanced by invoking their ability to repair environmentally induced genome breakage. By studying the dynamics of DNA damage response in the bdelloid species Adineta vaga, we found that it occurs rapidly in the soma, producing a partially reassembled genome. By contrast, germline DNA repair is delayed to a specific time window of oogenesis during which homologous chromosomes adopt a meiotic-like juxtaposed configuration, resulting in accurate reconstitution of the genome in the offspring. Our finding that a noncanonical meiosis is the mechanism of germline DNA repair in bdelloid rotifers gives previously unidentified insights on their enigmatic long-term evolution.

SUBMITTER: Terwagne M

PROVIDER: S-EPMC9710870 | biostudies-literature | 2022 Dec

REPOSITORIES: biostudies-literature

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DNA repair during nonreductional meiosis in the asexual rotifer <i>Adineta vaga</i>.

Terwagne Matthieu M Nicolas Emilien E Hespeels Boris B Herter Ludovic L Virgo Julie J Demazy Catherine C Heuskin Anne-Catherine AC Hallet Bernard B Van Doninck Karine K

Science advances 20221130 48

Rotifers of the class Bdelloidea are microscopic animals notorious for their long-term persistence in the apparent absence of sexual reproduction and meiotic recombination. This evolutionary paradox is often counterbalanced by invoking their ability to repair environmentally induced genome breakage. By studying the dynamics of DNA damage response in the bdelloid species <i>Adineta vaga</i>, we found that it occurs rapidly in the soma, producing a partially reassembled genome. By contrast, germli ...[more]

PMID: 36449626

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Project description:Space exposure experiments from the last 15 years have unexpectedly shown that several terrestrial organisms, including some multi-cellular species, are able to survive in open space without protection. The robustness of bdelloid rotifers suggests that these tiny creatures can possibly be added to the still restricted list of animals that can deal with the exposure to harsh condition of space. Bdelloids are one of the smallest animals on Earth. Living all over the world, mostly in semi-terrestrial environments, they appear to be extremely stress tolerant. Their desiccation tolerance at any stage of their life cycle is known to confer tolerance to a variety of stresses including high doses of radiation and freezing. In addition, they constitute a major scandal in evolutionary biology due to the putative absence of sexual reproduction for at least 60 million years. Adineta vaga, with its unique characteristics and a draft genome available, was selected by ESA (European Space Agency) as a model system to study extreme resistance of organisms exposed to space environment. In this manuscript, we documented the resistance of desiccated A. vaga individuals exposed to increasing doses of X-ray, protons and Fe ions. Consequences of exposure to different sources of radiation were investigated in regard to the cellular type including somatic (survival assay) and germinal cells (fertility assay). Then, the capacity of A. vaga individuals to repair DNA DSB induced by different source of radiation was investigated. Bdelloid rotifers represent a promising model in order to investigate damage induced by high or low LET radiation. The possibility of exposure both on hydrated or desiccated specimens may help to decipher contribution of direct and indirect radiation damage on biological processes. Results achieved through this study consolidate our knowledge about the radioresistance of A. vaga and improve our capacity to compare extreme resistance against radiation among living organisms including metazoan.

Project description:BackgroundRotifers of the class Bdelloidea are microscopic freshwater invertebrates best known for: their capacity for anhydrobiosis; the lack of males and meiosis; and for the ability to capture genes from other non-metazoan species. Although genetic exchange between these animals might take place by non-canonical means, the overall lack of meiosis and syngamy should greatly impair the ability of transposable elements (TEs) to spread in bdelloid populations. Previous studies demonstrated that bdelloid chromosome ends, in contrast to gene-rich regions, harbour various kinds of TEs, including specialized telomere-associated retroelements, as well as DNA TEs and retrovirus-like retrotransposons which are prone to horizontal transmission. Vertically-transmitted retrotransposons have not previously been reported in bdelloids and their identification and studies of the patterns of their distribution and evolution could help in the understanding of the high degree of TE compartmentalization within bdelloid genomes.ResultsWe identified and characterized a non-long terminal repeat (LTR) retrotransposon residing primarily in subtelomeric regions of the genome in the bdelloid rotifer Adineta vaga. Contrary to the currently prevailing views on the mode of proliferation of non-LTR retrotransposons, which results in frequent formation of 5'-truncated ('dead-on-arrival') copies due to the premature disengagement of the element-encoded reverse transcriptase from its template, this non-LTR element, Hebe, is represented only by non-5'-truncated copies. Most of these copies, however, were subject to internal deletions associated with microhomologies, a hallmark of non-homologous end-joining events.ConclusionsThe non-LTR retrotransposon Hebe from the bdelloid rotifer A. vaga was found to undergo frequent microhomology-associated deletions, rather than 5'-terminal truncations characteristic of this class of retrotransposons, and to exhibit preference for telomeric localization. These findings represent the first example of a vertically transmitted putatively deleterious TE in bdelloids, and may indicate the involvement of microhomology-mediated non-homologous end-joining in desiccation-induced double-strand break repair at the genome periphery.

Project description:BackgroundPenelope-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.ResultsWe 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.ConclusionsOur 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.

Dataset Information

DNA repair during nonreductional meiosis in the asexual rotifer Adineta vaga.

Publications

DNA repair during nonreductional meiosis in the asexual rotifer <i>Adineta vaga</i>.

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