IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v16y2025i1d10.1038_s41467-024-55598-9.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-55598-9
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-55598-9?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. 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.
    2. 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.
    3. 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.
    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. Pantelis Livanos & Choy Kriechbaum & Sophia Remers & Arvid Herrmann & Sabine Müller, 2025. "Kinesin-12 POK2 polarization is a prerequisite for a fully functional division site and aids cell plate positioning," Nature Communications, Nature, vol. 16(1), pages 1-17, December.
    2. Xin Yong & Guowen Jia & Qin Yang & Chunzhuang Zhou & Sitao Zhang & Huaqing Deng & Daniel D. Billadeau & Zhaoming Su & Da Jia, 2025. "Cryo-EM structure of the BLOC-3 complex provides insights into the pathogenesis of Hermansky-Pudlak syndrome," Nature Communications, Nature, vol. 16(1), pages 1-15, December.
    3. Sisira Mambram Kunnath & Elad Arad & Ran Zalk & Itamar Kass & Anat Shahar & Albert Batushansky & Hanna Rapaport & Raz Jelinek, 2025. "Allosteric amyloid catalysis by coiled coil fibrils," Nature Communications, Nature, vol. 16(1), pages 1-14, December.
    4. Jinhao Que & Guangfu Xue & Tao Wang & Xiyun Jin & Zuxiang Wang & Yideng Cai & Wenyi Yang & Meng Luo & Qian Ding & Jinwei Zhang & Yilin Wang & Yuexin Yang & Fenglan Pang & Yi Hui & Zheng Wei & Jun Xion, 2025. "Identifying T cell antigen at the atomic level with graph convolutional network," Nature Communications, Nature, vol. 16(1), pages 1-19, December.
    5. Qianqian Ming & Daniel Antfolk & David A. Price & Anna Manturova & Elliot Medina & Srishti Singh & Charlotte Mason & Timothy H. Tran & Keiran S. M. Smalley & Daisy W. Leung & Vincent C. Luca, 2024. "Structural basis for mouse LAG3 interactions with the MHC class II molecule I-Ab," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    6. Itxaso Anso & Samira Zouhir & Thibault Géry Sana & Petya Violinova Krasteva, 2024. "Structural basis for synthase activation and cellulose modification in the E. coli Type II Bcs secretion system," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    7. Julian O. Streit & Sammy H. S. Chan & Saifu Daya & John Christodoulou, 2025. "Rational design of 19F NMR labelling sites to probe protein structure and interactions," Nature Communications, Nature, vol. 16(1), pages 1-15, December.
    8. Xuhang Lu & Dongmei Li & Yaojie Wang & Gaohua Zhang & Tianlei Wen & Yue Lu & Nan Jia & Xuedi Wang & Shenghai Chang & Xing Zhang & Jianping Lin & Yu-hang Chen & Xue Yang & Yuequan Shen, 2025. "Structural insights into the activation mechanism of the human zinc-activated channel," Nature Communications, Nature, vol. 16(1), pages 1-12, December.
    9. Michal Beffinger & Linda Schellhammer & Betül Taskoparan & Sereina Deplazes & Ulisse Salazar & Nazanin Tatari & Frauke Seehusen & Leopold Balthazar & Carl Philipp Zinner & Sabine Spath & Tala Shekaria, 2025. "FcRn-silencing of IL-12Fc prevents toxicity of local IL-12 therapy and prolongs survival in experimental glioblastoma," Nature Communications, Nature, vol. 16(1), pages 1-19, December.
    10. Paloma García Casas & Michela Rossini & Linnea Påvénius & Mezida Saeed & Nikita Arnst & Sonia Sonda & Tânia Fernandes & Irene D’Arsiè & Matteo Bruzzone & Valeria Berno & Andrea Raimondi & Maria Livia , 2024. "Simultaneous detection of membrane contact dynamics and associated Ca2+ signals by reversible chemogenetic reporters," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    11. Jidong Fei & Dongdong Zhao & Caiyi Pang & Ju Li & Siwei Li & Wentao Qiao & Juan Tan & Changhao Bi & Xueli Zhang, 2025. "Mismatch prime editing gRNA increased efficiency and reduced indels," Nature Communications, Nature, vol. 16(1), pages 1-10, December.
    12. William J. Nicolas & Anna Shiriaeva & Michael W. Martynowycz & Angus C. Grey & Yasmeen N. Ruma & Paul J. Donaldson & Tamir Gonen, 2025. "Structure of the lens MP20 mediated adhesive junction," Nature Communications, Nature, vol. 16(1), pages 1-10, December.
    13. Ai Tamura & Kazuyuki Yamagata & Takashi Kono & Masanori Fujimoto & Takahiro Fuchigami & Motoi Nishimura & Masataka Yokoyama & Akitoshi Nakayama & Naoko Hashimoto & Ikki Sakuma & Nobuyuki Mitsukawa & Y, 2025. "p53-inducible lncRNA LOC644656 causes genotoxic stress-induced stem cell maldifferentiation and cancer chemoresistance," Nature Communications, Nature, vol. 16(1), pages 1-22, December.
    14. Cornelia Sala & Martin Würtz & Enrico Salvatore Atorino & Annett Neuner & Patrick Partscht & Thomas Hoffmann & Sebastian Eustermann & Elmar Schiebel, 2024. "An interaction network of inner centriole proteins organised by POC1A-POC1B heterodimer crosslinks ensures centriolar integrity," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    15. Gašper Šolinc & Marija Srnko & Franci Merzel & Ana Crnković & Mirijam Kozorog & Marjetka Podobnik & Gregor Anderluh, 2025. "Cryo-EM structures of a protein pore reveal a cluster of cholesterol molecules and diverse roles of membrane lipids," Nature Communications, Nature, vol. 16(1), pages 1-11, December.
    16. Tae-Kyeong Jeong & R. Ciaran MacKenzie Frater & Jongha Yoon & Anja Groth & Ji-Joon Song, 2025. "CODANIN-1 sequesters ASF1 by using a histone H3 mimic helix to regulate the histone supply," Nature Communications, Nature, vol. 16(1), pages 1-17, December.
    17. Timothy Atkinson & Thomas D. Barrett & Scott Cameron & Bora Guloglu & Matthew Greenig & Charlie B. Tan & Louis Robinson & Alex Graves & Liviu Copoiu & Alexandre Laterre, 2025. "Protein sequence modelling with Bayesian flow networks," Nature Communications, Nature, vol. 16(1), pages 1-14, December.
    18. Yannick Weyer & Sinead I. Schwabl & Xuechen Tang & Astha Purwar & Konstantin Siegmann & Angela Ruepp & Theresia Dunzendorfer-Matt & Michael A. Widerin & Veronika Niedrist & Noa J. M. Mutsters & Maria , 2024. "The Dsc ubiquitin ligase complex identifies transmembrane degrons to degrade orphaned proteins at the Golgi," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    19. Juan G. Carvajal-Patiño & Vincent Mallet & David Becerra & Luis Fernando Niño Vasquez & Carlos Oliver & Jérôme Waldispühl, 2025. "RNAmigos2: accelerated structure-based RNA virtual screening with deep graph learning," Nature Communications, Nature, vol. 16(1), pages 1-12, December.
    20. Jianan Zhang & Yuko Tsutsui & Hengyi Li & Tongqing Li & Yueyue Wang & Salma Laraki & Sofia Alarcon-Frias & Steven E. Stayrook & Daryl E. Klein, 2025. "Structural basis for the interaction between the Drosophila RTK Sevenless (dROS1) and the GPCR BOSS," Nature Communications, Nature, vol. 16(1), pages 1-12, 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:16:y:2025:i:1:d:10.1038_s41467-024-55598-9. 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.