No abstract

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.

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 the desiccation resistance. Both stresses produce reactive oxygen species and cause damage to DNA and other macromolecules, including DNA. However, this hypothesis has only been investigated in a few species and it is so far not possible to determine how universal it is. 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 in order to highlight the molecular and genetic mechanisms triggered by both stresses. We detected a transcriptomic response common to desiccation and both radiations with the over-expression of highly expressed genes mainly involved in DNA repair, protein modifications, or coding for Heat Shock Proteins, histones variants, enhancers but also many genes with unknown functions. We also discovered a distinct transcriptomic response specific to rehydration, which involved the over-expression of genes encoding Late Embryogenesis Abundant proteins, Heat Shock Proteins, and glucose repressive proteins. Moreover, we identified numerous genes encoding antioxidants that are constitutively highly expressed, which may contribute to the bdelloid rotifer resistance. Conclusions: These results suggest that the extreme resistance of bdelloid rotifers to radiation might indeed be inherited from and a consequence of their capacity to resist complete desiccation. This study paves the way for functional experiments targeting promising candidate proteins playing central roles in radiation and desiccation resistance.