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Molecular basis for proofreading by the unique exonuclease domain of Family-D DNA polymerases

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  • Leonardo Betancurt-Anzola

    (Architecture and Dynamics of Biological Macromolecules, Institut Pasteur, Université Paris Cité, CNRS
    New England Biolabs Inc.
    New England Biolabs France
    Sorbonne Université, Collège Doctoral, ED 515)

  • Markel Martínez-Carranza

    (Architecture and Dynamics of Biological Macromolecules, Institut Pasteur, Université Paris Cité, CNRS)

  • Marc Delarue

    (Architecture and Dynamics of Biological Macromolecules, Institut Pasteur, Université Paris Cité, CNRS)

  • Kelly M. Zatopek

    (New England Biolabs Inc.)

  • Andrew F. Gardner

    (New England Biolabs Inc.)

  • Ludovic Sauguet

    (Architecture and Dynamics of Biological Macromolecules, Institut Pasteur, Université Paris Cité, CNRS)

Abstract

Replicative DNA polymerases duplicate entire genomes at high fidelity. This feature is shared among the three domains of life and is facilitated by their dual polymerase and exonuclease activities. Family D replicative DNA polymerases (PolD), found exclusively in Archaea, contain an unusual RNA polymerase-like catalytic core, and a unique Mre11-like proofreading active site. Here, we present cryo-EM structures of PolD trapped in a proofreading mode, revealing an unanticipated correction mechanism that extends the repertoire of protein domains known to be involved in DNA proofreading. Based on our experimental structures, mutants of PolD were designed and their contribution to mismatch bypass and exonuclease kinetics was determined. This study sheds light on the convergent evolution of structurally distinct families of DNA polymerases, and the domain acquisition and exchange mechanism that occurred during the evolution of the replisome in the three domains of life.

Suggested Citation

  • Leonardo Betancurt-Anzola & Markel Martínez-Carranza & Marc Delarue & Kelly M. Zatopek & Andrew F. Gardner & Ludovic Sauguet, 2023. "Molecular basis for proofreading by the unique exonuclease domain of Family-D DNA polymerases," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-44125-x
    DOI: 10.1038/s41467-023-44125-x
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    References listed on IDEAS

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    1. Clément Madru & Ghislaine Henneke & Pierre Raia & Inès Hugonneau-Beaufet & Gérard Pehau-Arnaudet & Patrick England & Erik Lindahl & Marc Delarue & Marta Carroni & Ludovic Sauguet, 2020. "Structural basis for the increased processivity of D-family DNA polymerases in complex with PCNA," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    2. Kathryn Tunyasuvunakool & Jonas Adler & Zachary Wu & Tim Green & Michal Zielinski & Augustin Žídek & Alex Bridgland & Andrew Cowie & Clemens Meyer & Agata Laydon & Sameer Velankar & Gerard J. Kleywegt, 2021. "Highly accurate protein structure prediction for the human proteome," Nature, Nature, vol. 596(7873), pages 590-596, August.
    3. John Jumper & Richard Evans & Alexander Pritzel & Tim Green & Michael Figurnov & Olaf Ronneberger & Kathryn Tunyasuvunakool & Russ Bates & Augustin Žídek & Anna Potapenko & Alex Bridgland & Clemens Me, 2021. "Highly accurate protein structure prediction with AlphaFold," Nature, Nature, vol. 596(7873), pages 583-589, August.
    4. Ludovic Sauguet & Pierre Raia & Ghislaine Henneke & Marc Delarue, 2016. "Shared active site architecture between archaeal PolD and multi-subunit RNA polymerases revealed by X-ray crystallography," Nature Communications, Nature, vol. 7(1), pages 1-12, November.
    5. Panchali Goswami & Ferdos Abid Ali & Max E. Douglas & Julia Locke & Andrew Purkiss & Agnieszka Janska & Patrik Eickhoff & Anne Early & Andrea Nans & Alan M. C. Cheung & John F. X. Diffley & Alessandro, 2018. "Structure of DNA-CMG-Pol epsilon elucidates the roles of the non-catalytic polymerase modules in the eukaryotic replisome," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    6. Anja Spang & Jimmy H. Saw & Steffen L. Jørgensen & Katarzyna Zaremba-Niedzwiedzka & Joran Martijn & Anders E. Lind & Roel van Eijk & Christa Schleper & Lionel Guy & Thijs J. G. Ettema, 2015. "Complex archaea that bridge the gap between prokaryotes and eukaryotes," Nature, Nature, vol. 521(7551), pages 173-179, May.
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