| 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. |
| Authors | Boris Hespeels, Diego Fontaneto, Valérie Cornet, Sébastien Penninckx, Jérémy Berthe, Lucie Bruneau, James W. Larrick, Eloïse Rapport, Jérémie Bailly, Nicolas Debortoli, Nataliia Iakovenko, Karel Janko, Anne-Catherine Heuskin, Stéphane Lucas, Bernard Hallet & Karine Van Doninck |
| Text | 480101 2023 10.1186/s12915 023 01554 w rotifera Back to the roots, desiccation and radiation resistances are ancestral characters in bdelloid rotifers Boris Hespeels, Diego Fontaneto, Valerie Cornet, Sebastien Penninckx, Jeremy Berthe, Lucie Bruneau, James W. Larrick, Eloise Rapport, Jeremie Bailly, Nicolas Debortoli, Nataliia Iakovenko, Karel Janko, Anne Catherine Heuskin, Stephane Lucas, Bernard Hallet Karine Van Doninck Research Unit in Environmental and Evolutionary Biology URBE , Laboratory of Evolutionary Genetics and Ecology LEGE , NAmur Research Institute for Life Sciences NARILIS , University of Namur, Namur, Belgium Research Unit in Environmental and Evolutionary Biology URBE , Institute of Life, Earth Environment ILEE , University of Namur, Namur, Belgium Molecular Ecology Group MEG , Water Research Institute IRSA , National Research Council of Italy CNR , Verbania Pallanza, Italy Laboratory of Non Mendelian Evolution, Institute of Animal Physiology and Genetics AS CR, Rumburska 89, Lib chov, 277 21, Czech Republic Medical Physics Department, Institut Jules Bordet, Universite Libre de Bruxelles, Brussels, Belgium Research Unit in Molecular Biology and Evolution, DBO, Universite libre de Bruxelles ULB , 1050, Brussels, Belgium Panorama Research Institute, Sunnyvale, CA, USA SETI Institute, Mountain View, CA, USA Faculty of Forestry and Wood Sciences, Czech University of Life Sciences Prague, Kamýcka 129, CZ 165 21 Praha 6, Suchdol, Czech Republic Faculty of Science, University of Ostrava, Chittussiho 10, 71000, Ostrava, Czech Republic Laboratory of Analysis by Nuclear Reactions LARN , Namur Research Institute for Life Sciences Narilis , University of Namur, Namur, Belgium Louvain Institute of Biomolecular Science and Technology, UCLouvain, B 1348, Louvain la Neuve, Belgium 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. 21 Published version https //link.springer.com/article/10.1186/s12915 023 01554 w boris 2023_BMCbiol_Hespeels et al.pdf Articolo in rivista BioMed Central, 1741 7007 BMC biology BMC biology BMC biology Biology BioMed Central biology diego.fontaneto FONTANETO DIEGO |
