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Auxiliary ATP binding sites support DNA unwinding by RecBCD

Author

Listed:
  • Rani Zananiri

    (Faculty of Biology, Technion - Israel Institute of Technology)

  • Sivasubramanyan Mangapuram Venkata

    (Faculty of Biology, Technion - Israel Institute of Technology)

  • Vera Gaydar

    (Faculty of Biology, Technion - Israel Institute of Technology)

  • Dan Yahalom

    (Faculty of Biology, Technion - Israel Institute of Technology)

  • Omri Malik

    (Faculty of Biology, Technion - Israel Institute of Technology
    Russell Berrie Nanotechnology Institute, Technion - Israel Institute of Technology)

  • Sergei Rudnizky

    (Faculty of Biology, Technion - Israel Institute of Technology)

  • Oded Kleifeld

    (Faculty of Biology, Technion - Israel Institute of Technology)

  • Ariel Kaplan

    (Faculty of Biology, Technion - Israel Institute of Technology
    Russell Berrie Nanotechnology Institute, Technion - Israel Institute of Technology)

  • Arnon Henn

    (Faculty of Biology, Technion - Israel Institute of Technology
    Russell Berrie Nanotechnology Institute, Technion - Israel Institute of Technology)

Abstract

The RecBCD helicase initiates double-stranded break repair in bacteria by processively unwinding DNA with a rate approaching ∼1,600 bp·s−1, but the mechanism enabling such a fast rate is unknown. Employing a wide range of methodologies — including equilibrium and time-resolved binding experiments, ensemble and single-molecule unwinding assays, and crosslinking followed by mass spectrometry — we reveal the existence of auxiliary binding sites in the RecC subunit, where ATP binds with lower affinity and distinct chemical interactions as compared to the known catalytic sites. The essentiality and functionality of these sites are demonstrated by their impact on the survival of E.coli after exposure to damage-inducing radiation. We propose a model by which RecBCD achieves its optimized unwinding rate, even when ATP is scarce, by using the auxiliary binding sites to increase the flux of ATP to its catalytic sites.

Suggested Citation

  • Rani Zananiri & Sivasubramanyan Mangapuram Venkata & Vera Gaydar & Dan Yahalom & Omri Malik & Sergei Rudnizky & Oded Kleifeld & Ariel Kaplan & Arnon Henn, 2022. "Auxiliary ATP binding sites support DNA unwinding by RecBCD," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29387-1
    DOI: 10.1038/s41467-022-29387-1
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    References listed on IDEAS

    as
    1. Andrew F. Taylor & Gerald R. Smith, 2003. "RecBCD enzyme is a DNA helicase with fast and slow motors of opposite polarity," Nature, Nature, vol. 423(6942), pages 889-893, June.
    2. Bian Liu & Ronald J. Baskin & Stephen C. Kowalczykowski, 2013. "DNA unwinding heterogeneity by RecBCD results from static molecules able to equilibrate," Nature, Nature, vol. 500(7463), pages 482-485, August.
    3. Martin R. Singleton & Mark S. Dillingham & Martin Gaudier & Stephen C. Kowalczykowski & Dale B. Wigley, 2004. "Crystal structure of RecBCD enzyme reveals a machine for processing DNA breaks," Nature, Nature, vol. 432(7014), pages 187-193, November.
    4. Sergei Rudnizky & Adaiah Bavly & Omri Malik & Lilach Pnueli & Philippa Melamed & Ariel Kaplan, 2016. "H2A.Z controls the stability and mobility of nucleosomes to regulate expression of the LH genes," Nature Communications, Nature, vol. 7(1), pages 1-12, December.
    5. Sangtae Kim & Pavel A. Pevzner, 2014. "MS-GF+ makes progress towards a universal database search tool for proteomics," Nature Communications, Nature, vol. 5(1), pages 1-10, December.
    6. Mark S. Dillingham & Maria Spies & Stephen C. Kowalczykowski, 2003. "RecBCD enzyme is a bipolar DNA helicase," Nature, Nature, vol. 423(6942), pages 893-897, June.
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    Cited by:

    1. Luisa Moretto & Marko Ušaj & Oleg Matusovsky & Dilson E. Rassier & Ran Friedman & Alf Månsson, 2022. "Multistep orthophosphate release tunes actomyosin energy transduction," Nature Communications, Nature, vol. 13(1), pages 1-18, December.

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