Ionizing radiation responses appear incidental to desiccation responses in the bdelloid rotifer Adineta vaga.

BACKGROUND: The remarkable resistance to ionizing radiation found in anhydrobiotic organisms, such as some bacteria, tardigrades, and bdelloid rotifers has been hypothesized to be incidental to their desiccation resistance. Both stresses produce reactive oxygen species and cause damage to DNA and other macromolecules. However, this hypothesis has only been investigated in a few species. RESULTS: In this study, we analyzed the transcriptomic response of the bdelloid rotifer Adineta vaga to desiccation and to low- (X-rays) and high- (Fe) LET radiation to highlight the molecular and genetic mechanisms triggered by both stresses. We identified numerous genes encoding antioxidants, but also chaperones, that are constitutively highly expressed, which may contribute to the protection of proteins against oxidative stress during desiccation and ionizing radiation. We also detected a transcriptomic response common to desiccation and ionizing radiation with the over-expression of genes mainly involved in DNA repair and protein modifications but also genes with unknown functions that were bdelloid-specific. A distinct transcriptomic response specific to rehydration was also found, with the over-expression of genes mainly encoding Late Embryogenesis Abundant proteins, specific heat shock proteins, and glucose repressive proteins. CONCLUSIONS: These results suggest that the extreme resistance of bdelloid rotifers to radiation might indeed be a consequence of their capacity to resist complete desiccation. This study paves the way to functional genetic experiments on A. vaga targeting promising candidate proteins playing central roles in radiation and desiccation resistance.

Back to the roots, desiccation and radiation resistances are ancestral characters in bdelloid rotifers.

BACKGROUND: Bdelloid rotifers are micro-invertebrates distributed worldwide, from temperate latitudes to the most extreme areas of the planet like Antarctica or the Atacama Desert. They have colonized any habitat where liquid water is temporarily available, including terrestrial environments such as soils, mosses, and lichens, tolerating desiccation and other types of stress such as high doses of ionizing radiation (IR). It was hypothesized that bdelloid desiccation and radiation resistance may be attributed to their potential ability to repair DNA double-strand breaks (DSBs). Here, these properties are investigated and compared among nine bdelloid species collected from both mild and harsh habitats, addressing the correlation between the ability of bdelloid rotifers to survive desiccation and their capacity to repair massive DNA breakage in a phylogenetically explicit context. Our research includes both specimens isolated from habitats that experience frequent desiccation (at least 1 time per generation), and individuals sampled from habitats that rarely or never experienced desiccation. RESULTS: Our analysis reveals that DNA repair prevails in somatic cells of both desiccation-tolerant and desiccation-sensitive bdelloid species after exposure to X-ray radiation. Species belonging to both categories are able to withstand high doses of ionizing radiation, up to 1000 Gy, without experiencing any negative effects on their survival. However, the fertility of two desiccation-sensitive species, Rotaria macrura and Rotaria rotatoria, was more severely impacted by low doses of radiation than that of desiccation-resistant species. Surprisingly, the radioresistance of desiccation-resistant species is not related to features of their original habitat. Indeed, bdelloids isolated from Atacama Desert or Antarctica were not characterized by a higher radioresistance than species found in more temperate environments. CONCLUSIONS: Tolerance to desiccation and radiation are supported as ancestral features of bdelloid rotifers, with a group of species of the genus Rotaria having lost this trait after colonizing permanent water habitats. Together, our results provide a comprehensive overview of the evolution of desiccation and radiation resistance among bdelloid rotifers.

Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga.

Loss 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 years. 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 pairing. 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), 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.

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

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.

Chromosome-level genome assembly reveals homologous chromosomes and recombination in asexual rotifer Adineta vaga.

Bdelloid rotifers are notorious as a speciose ancient clade comprising only asexual lineages. Thanks to their ability to repair highly fragmented DNA, most bdelloid species also withstand complete desiccation and ionizing radiation. Producing a well-assembled reference genome is a critical step to developing an understanding of the effects of long-term asexuality and DNA breakage on genome evolution. To this end, we present the first high-quality chromosome-level genome assemblies for the bdelloid Adineta vaga, composed of six pairs of homologous (diploid) chromosomes with a footprint of paleotetraploidy. The observed large-scale losses of heterozygosity are signatures of recombination between homologous chromosomes, either during mitotic DNA double-strand break repair or when resolving programmed DNA breaks during a modified meiosis. Dynamic subtelomeric regions harbor more structural diversity (e.g., chromosome rearrangements, transposable elements, and haplotypic divergence). Our results trigger the reappraisal of potential meiotic processes in bdelloid rotifers and help unravel the factors underlying their long-term asexual evolutionary success.

Iron Ladies - How Desiccated Asexual Rotifer Adineta vaga Deal With X-Rays and Heavy Ions?

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.

Genetic Exchange among Bdelloid Rotifers Is More Likely Due to Horizontal Gene Transfer Than to Meiotic Sex.

Although strict asexuality is supposed to be an evolutionary dead end, morphological, cytogenetic, and genomic data suggest that bdelloid rotifers, a clade of microscopic animals, have persisted and diversified for more than 60 Myr in an ameiotic fashion. Moreover, the genome of bdelloids of the genus Adineta comprises 8%-10% of genes of putative non-metazoan origin, indicating that horizontal gene transfers are frequent within this group and suggesting that this mechanism may also promote genetic exchanges among bdelloids as well. To test this hypothesis, we used five independent sequence markers to study the genetic diversity of 576 Adineta vaga individuals from a park in Belgium. Haplowebs and GMYC analyses revealed the existence of six species among our sampled A. vaga individuals, with strong evidence of both intra- and interspecific recombination. Comparison of genomic regions of three allele-sharing individuals further revealed signatures of genetic exchanges scattered among regions evolving asexually. Our findings suggest that bdelloids evolve asexually but exchange DNA horizontally both within and between species.

Against All Odds: Trehalose-6-Phosphate Synthase and Trehalase Genes in the Bdelloid Rotifer Adineta vaga Were Acquired by Horizontal Gene Transfer and Are Upregulated during Desiccation.

The disaccharide sugar trehalose is essential for desiccation resistance in most metazoans that survive dryness; however, neither trehalose nor the enzymes involved in its metabolism have ever been detected in bdelloid rotifers despite their extreme resistance to desiccation. Here we screened the genome of the bdelloid rotifer Adineta vaga for genes involved in trehalose metabolism. We discovered a total of four putative trehalose-6-phosphate synthase (TPS) and seven putative trehalase (TRE) gene copies in the genome of this ameiotic organism; however, no trehalose-6-phosphate phosphatase (TPP) gene or domain was detected. The four TPS copies of A. vaga appear more closely related to plant and fungi proteins, as well as to some protists, whereas the seven TRE copies fall in bacterial clades. Therefore, A. vaga likely acquired its trehalose biosynthesis and hydrolysis genes by horizontal gene transfers. Nearly all residues important for substrate binding in the predicted TPS domains are highly conserved, supporting the hypothesis that several copies of the genes might be functional. Besides, RNAseq library screening showed that trehalase genes were highly expressed compared to TPS genes, explaining probably why trehalose had not been detected in previous studies of bdelloids. A strong overexpression of their TPS genes was observed when bdelloids enter desiccation, suggesting a possible signaling role of trehalose-6-phosphate or trehalose in this process.