DNA Ligases; Ligases; DNA Ligase ATP; Animals; Humans; Phylogeny; DNA Ligases/genetics; DNA Ligases/metabolism; Ligases/metabolism; Proteomics; DNA Damage; DNA Ligase ATP/genetics; DNA Ligase ATP/metabolism; Eukaryota/genetics; Rotifera/genetics; Chemistry (all); Biochemistry, Genetics and Molecular Biology (all); Physics and Astronomy (all); General Physics and Astronomy; General Biochemistry, Genetics and Molecular Biology; General Chemistry; Multidisciplinary
Abstract :
[en] Bdelloid rotifers are part of the restricted circle of multicellular animals that can withstand a wide range of genotoxic stresses at any stage of their life cycle. In this study, bdelloid rotifer Adineta vaga is used as a model to decipher the molecular basis of their extreme tolerance. Proteomic analysis shows that a specific DNA ligase, different from those usually involved in DNA repair in eukaryotes, is strongly over-represented upon ionizing radiation. A phylogenetic analysis reveals its orthology to prokaryotic DNA ligase E, and its horizontal acquisition by bdelloid rotifers and plausibly other eukaryotes. The fungus Mortierella verticillata, having a single copy of this DNA Ligase E homolog, also exhibits an increased radiation tolerance with an over-expression of this DNA ligase E following X-ray exposure. We also provide evidence that A. vaga ligase E is a major contributor of DNA breaks ligation activity, which is a common step of all important DNA repair pathways. Consistently, its heterologous expression in human cell lines significantly improves their radio-tolerance. Overall, this study highlights the potential of horizontal gene transfers in eukaryotes, and their contribution to the adaptation to extreme conditions.
Disciplines :
Environmental sciences & ecology
Author, co-author :
Nicolas, Emilien ; Université Libre de Bruxelles, Molecular Biology and Evolution, Brussels, 1050, Belgium. emilien.nicolas@gmail.com
Simion, Paul ; Université de Namur, Laboratory of Evolutionary Genetics and Ecology, Namur, 5000, Belgium ; Université de Rennes, Ecosystèmes, biodiversité, évolution (ECOBIO UMR 6553), CNRS, Rennes, France
Guérineau, Marc; Université Libre de Bruxelles, Molecular Biology and Evolution, Brussels, 1050, Belgium
Terwagne, Matthieu ; Université de Namur, Laboratory of Evolutionary Genetics and Ecology, Namur, 5000, Belgium
Colinet, Mathilde ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques ; Université de Namur, Laboratory of Evolutionary Genetics and Ecology, Namur, 5000, Belgium
Virgo, Julie; Université de Namur, Laboratory of Evolutionary Genetics and Ecology, Namur, 5000, Belgium
Lingurski, Maxime; Université Libre de Bruxelles, Molecular Biology and Evolution, Brussels, 1050, Belgium
Boutsen, Anaïs ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques ; Université de Namur, Laboratory of Evolutionary Genetics and Ecology, Namur, 5000, Belgium
Dieu, Marc ; Université de Namur, MaSUN-mass spectrometry facility, Namur, 5000, Belgium
Hallet, Bernard ; Université Catholique de Louvain, Louvain Institute of Biomolecular Science and Technology, Louvain-la-Neuve, 1348, Belgium. bernard.hallet@uclouvain.be
Van Doninck, Karine ; Université Libre de Bruxelles, Molecular Biology and Evolution, Brussels, 1050, Belgium. karine.van.doninck@ulb.be ; Université de Namur, Laboratory of Evolutionary Genetics and Ecology, Namur, 5000, Belgium. karine.van.doninck@ulb.be
Language :
English
Title :
Horizontal acquisition of a DNA ligase improves DNA damage tolerance in eukaryotes.
The authors thank Catherine Demazy and Anne-Catherine Wéra for their generous help during the course of this study. The Morphim imaging platform and the Research Unit for Analysis by Nuclear Reactions (LARN) of UNamur are acknowledged for their technical help. This work was supported by the European Research Council (ERC) grant agreement 725998 (RHEA) to K.V.D., and from the Fédération Wallonie-Bruxelles via an’Action de Recherche Concertée’ (ARC) grant to K.V.D. and B.H. E.N. obtained a FSR UNamur fund.
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