IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-47849-6.html
   My bibliography  Save this article

Chromosome organization shapes replisome dynamics in Caulobacter crescentus

Author

Listed:
  • Chen Zhang

    (Ecole Polytechnique Fédérale de Lausanne (EPFL))

  • Asha Mary Joseph

    (Tata Institute of Fundamental Research)

  • Laurent Casini

    (University of Lausanne)

  • Justine Collier

    (University of Lausanne)

  • Anjana Badrinarayanan

    (Tata Institute of Fundamental Research)

  • Suliana Manley

    (Ecole Polytechnique Fédérale de Lausanne (EPFL))

Abstract

DNA replication in bacteria takes place on highly compacted chromosomes, where segregation, transcription, and repair must occur simultaneously. Within this dynamic environment, colocalization of sister replisomes has been observed in many bacterial species, driving the hypothesis that a physical linker may tether them together. However, replisome splitting has also been reported in many of the same species, leaving the principles behind replisome organization a long-standing puzzle. Here, by tracking the replisome β-clamp subunit in live Caulobacter crescentus, we find that rapid DNA segregation can give rise to a second focus which resembles a replisome, but does not replicate DNA. Sister replisomes can remain colocalized, or split apart to travel along DNA separately upon disruption of chromosome inter-arm alignment. Furthermore, chromosome arm-specific replication-transcription conflicts differentially modify replication speed on the two arms, facilitate the decoupling of the two replisomes. With these observations, we conclude that the dynamic chromosome organization flexibly shapes the organization of sister replisomes, and we outline principles which can help to reconcile previously conflicting models of replisome architecture.

Suggested Citation

  • Chen Zhang & Asha Mary Joseph & Laurent Casini & Justine Collier & Anjana Badrinarayanan & Suliana Manley, 2024. "Chromosome organization shapes replisome dynamics in Caulobacter crescentus," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47849-6
    DOI: 10.1038/s41467-024-47849-6
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-47849-6
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-47849-6?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. Sarah M Mangiameli & Brian T Veit & Houra Merrikh & Paul A Wiggins, 2017. "The Replisomes Remain Spatially Proximal throughout the Cell Cycle in Bacteria," PLOS Genetics, Public Library of Science, vol. 13(1), pages 1-17, January.
    2. M. Charl Moolman & Sriram Tiruvadi Krishnan & Jacob W. J. Kerssemakers & Aafke van den Berg & Pawel Tulinski & Martin Depken & Rodrigo Reyes-Lamothe & David J. Sherratt & Nynke H. Dekker, 2014. "Slow unloading leads to DNA-bound β2-sliding clamp accumulation in live Escherichia coli cells," Nature Communications, Nature, vol. 5(1), pages 1-11, December.
    3. Dean Huang & Anna E. Johnson & Brandon S. Sim & Teresa W. Lo & Houra Merrikh & Paul A. Wiggins, 2023. "The in vivo measurement of replication fork velocity and pausing by lag-time analysis," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    4. Aleksandre Japaridze & Christos Gogou & Jacob W. J. Kerssemakers & Huyen My Nguyen & Cees Dekker, 2020. "Direct observation of independently moving replisomes in Escherichia coli," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    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. Konrad Gras & David Fange & Johan Elf, 2024. "The Escherichia coli chromosome moves to the replisome," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    2. Janni Harju & Muriel C. F. Teeseling & Chase P. Broedersz, 2024. "Loop-extruders alter bacterial chromosome topology to direct entropic forces for segregation," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    3. Mareike Berger & Pieter Rein ten Wolde, 2022. "Robust replication initiation from coupled homeostatic mechanisms," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    4. David Geisel & Peter Lenz, 2022. "Machine learning classification of trajectories from molecular dynamics simulations of chromosome segregation," PLOS ONE, Public Library of Science, vol. 17(1), pages 1-33, January.
    5. Miloš Tišma & Florian Patrick Bock & Jacob Kerssemakers & Hammam Antar & Aleksandre Japaridze & Stephan Gruber & Cees Dekker, 2024. "Direct observation of a crescent-shape chromosome in expanded Bacillus subtilis cells," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    6. Agathe Couturier & Chloé Virolle & Kelly Goldlust & Annick Berne-Dedieu & Audrey Reuter & Sophie Nolivos & Yoshiharu Yamaichi & Sarah Bigot & Christian Lesterlin, 2023. "Real-time visualisation of the intracellular dynamics of conjugative plasmid transfer," Nature Communications, Nature, vol. 14(1), pages 1-15, 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:15:y:2024:i:1:d:10.1038_s41467-024-47849-6. 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.