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


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.

SUBMITTER: Nicolas E 

PROVIDER: S-EPMC10665377 | biostudies-literature | 2023 Nov

REPOSITORIES: biostudies-literature

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

Nicolas Emilien E   Simion Paul P   Guérineau Marc M   Terwagne Matthieu M   Colinet Mathilde M   Virgo Julie J   Lingurski Maxime M   Boutsen Anaïs A   Dieu Marc M   Hallet Bernard B   Van Doninck Karine K  

Nature communications 20231122 1


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 o  ...[more]

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