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Dynamic transitions of initiator binding coordinate the replication of the two chromosomes in Vibrio cholerae

Author

Listed:
  • Théophile Niault

    (Département Génomes et Génétique
    Collège Doctoral)

  • Ariel Talavera

    (Boulevard du Triomphe)

  • Eric Le Cam

    (Gustave Roussy)

  • Sonia Baconnais

    (Gustave Roussy)

  • Ole Skovgaard

    (Roskilde University)

  • Florian Fournes

    (Département Génomes et Génétique)

  • Léa Wagner

    (Département Génomes et Génétique)

  • Hedvig Tamman

    (Boulevard du Triomphe)

  • Andrew Thompson

    (Saint-Aubin - BP48)

  • Dannele Echemendia-Blanco

    (Boulevard du Triomphe)

  • Noa Guzzi

    (Département Génomes et Génétique
    Collège Doctoral)

  • Abel Garcia-Pino

    (Boulevard du Triomphe
    WEL Research Institute)

  • Didier Mazel

    (Département Génomes et Génétique)

  • Marie-Eve Val

    (Département Génomes et Génétique)

Abstract

The replication of the two chromosomes in the pathogenic bacterium Vibrio cholerae is coordinated by the binding of initiator protein RctB to a checkpoint sequence, crtS. Replication of crtS on the primary chromosome (Chr1) triggers replication of the secondary chromosome (Chr2), but the details are poorly understood. Here, we analyze RctB binding patterns in the V. cholerae genome across various cell cycle stages. We find that RctB primarily binds to sites inhibiting replication initiation at the Chr2 origin (ori2). This inhibitory effect is counteracted when crtS is replicated on Chr1, causing a shift in RctB binding to sites that activate replication at ori2. Structural analyzes indicate the formation of diverse oligomeric states of RctB, coupled to the allosteric effect of DNA, which determine ori2 accessibility. We propose a synchronization model where, upon replication, crtS locally destabilizes the RctB inhibition complex, releasing the Chr2 replication origin.

Suggested Citation

  • Théophile Niault & Ariel Talavera & Eric Le Cam & Sonia Baconnais & Ole Skovgaard & Florian Fournes & Léa Wagner & Hedvig Tamman & Andrew Thompson & Dannele Echemendia-Blanco & Noa Guzzi & Abel Garcia, 2025. "Dynamic transitions of initiator binding coordinate the replication of the two chromosomes in Vibrio cholerae," Nature Communications, Nature, vol. 16(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-024-55598-9
    DOI: 10.1038/s41467-024-55598-9
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    References listed on IDEAS

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    1. Josh Abramson & Jonas Adler & Jack Dunger & Richard Evans & Tim Green & Alexander Pritzel & Olaf Ronneberger & Lindsay Willmore & Andrew J. Ballard & Joshua Bambrick & Sebastian W. Bodenstein & David , 2024. "Accurate structure prediction of biomolecular interactions with AlphaFold 3," Nature, Nature, vol. 630(8016), pages 493-500, June.
    2. Michaël Deghelt & Caroline Mullier & Jean-François Sternon & Nayla Francis & Géraldine Laloux & Delphine Dotreppe & Charles Van der Henst & Christine Jacobs-Wagner & Jean-Jacques Letesson & Xavier De , 2014. "G1-arrested newborn cells are the predominant infectious form of the pathogen Brucella abortus," Nature Communications, Nature, vol. 5(1), pages 1-12, September.
    3. John F. Heidelberg & Jonathan A. Eisen & William C. Nelson & Rebecca A. Clayton & Michelle L. Gwinn & Robert J. Dodson & Daniel H. Haft & Erin K. Hickey & Jeremy D. Peterson & Lowell Umayam & Steven R, 2000. "DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae," Nature, Nature, vol. 406(6795), pages 477-483, August.
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    Cited by:

    1. Aline Cuénod & Denise Chac & Ashraful I. Khan & Fahima Chowdhury & Randy W. Hyppa & Susan M. Markiewicz & Amelia Rice & Akhil Kholwadwala & Stephen B. Calderwood & Edward T. Ryan & Jason B. Harris & R, 2025. "Prevalent chromosome fusion in Vibrio cholerae O1," Nature Communications, Nature, vol. 16(1), pages 1-10, December.

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