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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
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    References listed on IDEAS

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    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.
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