Horizontal acquisition of a DNA ligase improves DNA damage tolerance in eukaryotes

Emilien Nicolas (), Paul Simion, Marc Guérineau, Matthieu Terwagne, Mathilde Colinet, Julie Virgo, Maxime Lingurski, Anaïs Boutsen, Marc Dieu, Bernard Hallet () and Karine Doninck ()
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Emilien Nicolas: Université Libre de Bruxelles, Molecular Biology and Evolution
Paul Simion: Université de Namur, Laboratory of Evolutionary Genetics and Ecology
Marc Guérineau: Université Libre de Bruxelles, Molecular Biology and Evolution
Matthieu Terwagne: Université de Namur, Laboratory of Evolutionary Genetics and Ecology
Mathilde Colinet: Université de Namur, Laboratory of Evolutionary Genetics and Ecology
Julie Virgo: Université de Namur, Laboratory of Evolutionary Genetics and Ecology
Maxime Lingurski: Université Libre de Bruxelles, Molecular Biology and Evolution
Anaïs Boutsen: Université de Namur, Laboratory of Evolutionary Genetics and Ecology
Marc Dieu: Université de Namur, MaSUN-mass spectrometry facility
Bernard Hallet: Université Catholique de Louvain, Louvain Institute of Biomolecular Science and Technology
Karine Doninck: Université Libre de Bruxelles, Molecular Biology and Evolution

Nature Communications, 2023, vol. 14, issue 1, 1-14

Abstract: Abstract 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.

Date: 2023
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DOI: 10.1038/s41467-023-43075-8

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