IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-29387-1.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-29387-1
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-29387-1?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. 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. 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.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    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.

    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. Zheng Fang & Hongqiang Qin & Jiawei Mao & Zhongyu Wang & Na Zhang & Yan Wang & Luyao Liu & Yongzhan Nie & Mingming Dong & Mingliang Ye, 2022. "Glyco-Decipher enables glycan database-independent peptide matching and in-depth characterization of site-specific N-glycosylation," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Kai Zhou & Chun-Xu Xue & Tingting Xu & Ping Shen & Sha Wei & Kelly L. Wyres & Margaret M. C. Lam & Jinquan Liu & Haoyun Lin & Yunbo Chen & Kathryn E. Holt & Yonghong Xiao, 2023. "A point mutation in recC associated with subclonal replacement of carbapenem-resistant Klebsiella pneumoniae ST11 in China," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    3. Kaiyuan Liu & Yuzhen Ye & Sujun Li & Haixu Tang, 2023. "Accurate de novo peptide sequencing using fully convolutional neural networks," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    4. Shuxiang Li & Tiejun Wei & Anna R. Panchenko, 2023. "Histone variant H2A.Z modulates nucleosome dynamics to promote DNA accessibility," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    5. Robert H. Lampe & Tyler H. Coale & Kiefer O. Forsch & Loay J. Jabre & Samuel Kekuewa & Erin M. Bertrand & Aleš Horák & Miroslav Oborník & Ariel J. Rabines & Elden Rowland & Hong Zheng & Andreas J. And, 2023. "Short-term acidification promotes diverse iron acquisition and conservation mechanisms in upwelling-associated phytoplankton," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    6. Isabelle Rose Leo & Luay Aswad & Matthias Stahl & Elena Kunold & Frederik Post & Tom Erkers & Nona Struyf & Georgios Mermelekas & Rubin Narayan Joshi & Eva Gracia-Villacampa & Päivi Östling & Olli P. , 2022. "Integrative multi-omics and drug response profiling of childhood acute lymphoblastic leukemia cell lines," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    7. Heather Schiller & Yirui Hong & Joshua Kouassi & Theopi Rados & Jasmin Kwak & Anthony DiLucido & Daniel Safer & Anita Marchfelder & Friedhelm Pfeiffer & Alexandre Bisson & Stefan Schulze & Mechthild P, 2024. "Identification of structural and regulatory cell-shape determinants in Haloferax volcanii," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    8. Guanlan Xu & Tiffany D. Grimes & Truman B. Grayson & Junqin Chen & Lance A. Thielen & Hubert M. Tse & Peng Li & Matt Kanke & Tai-Tu Lin & Athena A. Schepmoes & Adam C. Swensen & Vladislav A. Petyuk & , 2022. "Exploratory study reveals far reaching systemic and cellular effects of verapamil treatment in subjects with type 1 diabetes," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    9. Aviv Meir & Vivek B. Raina & Carly E. Rivera & Léa Marie & Lorraine S. Symington & Eric C. Greene, 2023. "The separation pin distinguishes the pro– and anti–recombinogenic functions of Saccharomyces cerevisiae Srs2," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    10. Haris Babačić & Wanda Christ & José Eduardo Araújo & Georgios Mermelekas & Nidhi Sharma & Janne Tynell & Marina García & Renata Varnaite & Hilmir Asgeirsson & Hedvig Glans & Janne Lehtiö & Sara Gredma, 2023. "Comprehensive proteomics and meta-analysis of COVID-19 host response," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    11. Bo Wen & Bing Zhang, 2023. "PepQuery2 democratizes public MS proteomics data for rapid peptide searching," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    12. Wonseok Hwang & Il-Buem Lee & Seok-Cheol Hong & Changbong Hyeon, 2016. "Decoding Single Molecule Time Traces with Dynamic Disorder," PLOS Computational Biology, Public Library of Science, vol. 12(12), pages 1-29, December.
    13. Jong Woo Bae & Sangtae Kim & V. Narry Kim & Jong-Seo Kim, 2021. "Photoactivatable ribonucleosides mark base-specific RNA-binding sites," Nature Communications, Nature, vol. 12(1), pages 1-10, December.

    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:13:y:2022:i:1:d:10.1038_s41467-022-29387-1. 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.