IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-43075-8.html
   My bibliography  Save this article

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

Author

Listed:
  • Emilien Nicolas

    (Université Libre de Bruxelles, Molecular Biology and Evolution)

  • Paul Simion

    (Université de Namur, Laboratory of Evolutionary Genetics and Ecology
    Université de Rennes, Ecosystèmes, biodiversité, évolution (ECOBIO UMR 6553), CNRS)

  • 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
    Université de Namur, Laboratory of Evolutionary Genetics and Ecology)

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.

Suggested Citation

  • Emilien Nicolas & Paul Simion & Marc Guérineau & Matthieu Terwagne & Mathilde Colinet & Julie Virgo & Maxime Lingurski & Anaïs Boutsen & Marc Dieu & Bernard Hallet & Karine Doninck, 2023. "Horizontal acquisition of a DNA ligase improves DNA damage tolerance in eukaryotes," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43075-8
    DOI: 10.1038/s41467-023-43075-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-43075-8
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-43075-8?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Israel Salguero & Rimma Belotserkovskaya & Julia Coates & Matylda Sczaniecka-Clift & Mukerrem Demir & Satpal Jhujh & Marcus D. Wilson & Stephen P. Jackson, 2019. "MDC1 PST-repeat region promotes histone H2AX-independent chromatin association and DNA damage tolerance," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    2. Jean-François Flot & Boris Hespeels & Xiang Li & Benjamin Noel & Irina Arkhipova & Etienne G. J. Danchin & Andreas Hejnol & Bernard Henrissat & Romain Koszul & Jean-Marc Aury & Valérie Barbe & Roxane-, 2013. "Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga," Nature, Nature, vol. 500(7463), pages 453-457, August.
    3. Fernando Rodriguez & Irina A. Yushenova & Daniel DiCorpo & Irina R. Arkhipova, 2022. "Bacterial N4-methylcytosine as an epigenetic mark in eukaryotic DNA," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    4. Li Zheng & Huifang Dai & Mian Zhou & Xiaojin Li & Changwei Liu & Zhigang Guo & Xiwei Wu & Jun Wu & Charles Wang & John Zhong & Qin Huang & Julio Garcia-Aguilar & Gerd P. Pfeifer & Binghui Shen, 2012. "Polyploid cells rewire DNA damage response networks to overcome replication stress-induced barriers for tumour progression," Nature Communications, Nature, vol. 3(1), pages 1-12, January.
    5. Cyriac Kandoth & Michael D. McLellan & Fabio Vandin & Kai Ye & Beifang Niu & Charles Lu & Mingchao Xie & Qunyuan Zhang & Joshua F. McMichael & Matthew A. Wyczalkowski & Mark D. M. Leiserson & Christop, 2013. "Mutational landscape and significance across 12 major cancer types," Nature, Nature, vol. 502(7471), pages 333-339, October.
    6. Takuma Hashimoto & Daiki D. Horikawa & Yuki Saito & Hirokazu Kuwahara & Hiroko Kozuka-Hata & Tadasu Shin-I & Yohei Minakuchi & Kazuko Ohishi & Ayuko Motoyama & Tomoyuki Aizu & Atsushi Enomoto & Koyuki, 2016. "Extremotolerant tardigrade genome and improved radiotolerance of human cultured cells by tardigrade-unique protein," Nature Communications, Nature, vol. 7(1), pages 1-14, November.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Simone Mozzachiodi & Lorenzo Tattini & Agnes Llored & Agurtzane Irizar & Neža Škofljanc & Melania D’Angiolo & Matteo De Chiara & Benjamin P. Barré & Jia-Xing Yue & Angela Lutazi & Sophie Loeillet & Ra, 2021. "Aborting meiosis allows recombination in sterile diploid yeast hybrids," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    2. Irina Ostrovnaya & Audrey Mauguen & Venkatraman E. Seshan & Colin B. Begg, 2021. "Testing tumors from different anatomic sites for clonal relatedness using somatic mutation data," Biometrics, The International Biometric Society, vol. 77(1), pages 283-292, March.
    3. T. Brunoir & C. Mulligan & A. Sistiaga & K. M. Vuu & P. M. Shih & S. S. O’Reilly & R. E. Summons & D. A. Gold, 2023. "Common origin of sterol biosynthesis points to a feeding strategy shift in Neoproterozoic animals," Nature Communications, Nature, vol. 14(1), pages 1-8, December.
    4. Yanling Liu & Jonathon Klein & Richa Bajpai & Li Dong & Quang Tran & Pandurang Kolekar & Jenny L. Smith & Rhonda E. Ries & Benjamin J. Huang & Yi-Cheng Wang & Todd A. Alonzo & Liqing Tian & Heather L., 2023. "Etiology of oncogenic fusions in 5,190 childhood cancers and its clinical and therapeutic implication," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    5. Fernando Rodriguez & Irina A. Yushenova & Daniel DiCorpo & Irina R. Arkhipova, 2022. "Bacterial N4-methylcytosine as an epigenetic mark in eukaryotic DNA," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    6. M. G. Filippone & D. Gaglio & R. Bonfanti & F. A. Tucci & E. Ceccacci & R. Pennisi & M. Bonanomi & G. Jodice & M. Tillhon & F. Montani & G. Bertalot & S. Freddi & M. Vecchi & A. Taglialatela & M. Roma, 2022. "CDK12 promotes tumorigenesis but induces vulnerability to therapies inhibiting folate one-carbon metabolism in breast cancer," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    7. Mu-Kuei Shieu & Hsin-Yu Ho & Shu-Hui Lin & Yu-Sheng Lo & Chia-Chieh Lin & Yi-Ching Chuang & Ming-Ju Hsieh & Mu-Kuan Chen, 2022. "Association of KMT2C Genetic Variants with the Clinicopathologic Development of Oral Cancer," IJERPH, MDPI, vol. 19(7), pages 1-10, March.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43075-8. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.