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Loop-extruders alter bacterial chromosome topology to direct entropic forces for segregation

Author

Listed:
  • Janni Harju

    (Vrije Universiteit Amsterdam)

  • Muriel C. F. Teeseling

    (Friedrich-Schiller-Universität)

  • Chase P. Broedersz

    (Vrije Universiteit Amsterdam
    Ludwig-Maximilian-University Munich)

Abstract

Entropic forces have been argued to drive bacterial chromosome segregation during replication. In many bacterial species, however, specifically evolved mechanisms, such as loop-extruding SMC complexes and the ParABS origin segregation system, contribute to or are even required for chromosome segregation, suggesting that entropic forces alone may be insufficient. The interplay between and the relative contributions of these segregation mechanisms remain unclear. Here, we develop a biophysical model showing that purely entropic forces actually inhibit bacterial chromosome segregation until late replication stages. By contrast, our model reveals that loop-extruders loaded at the origins of replication, as observed in many bacterial species, alter the effective topology of the chromosome, thereby redirecting and enhancing entropic forces to enable accurate chromosome segregation during replication. We confirm our model predictions with polymer simulations: purely entropic forces do not allow for concurrent replication and segregation, whereas entropic forces steered by specifically loaded loop-extruders lead to robust, global chromosome segregation during replication. Finally, we show how loop-extruders can complement locally acting origin separation mechanisms, such as the ParABS system. Together, our results illustrate how changes in the geometry and topology of the polymer, induced by DNA-replication and loop-extrusion, impact the organization and segregation of bacterial chromosomes.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49039-w
    DOI: 10.1038/s41467-024-49039-w
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    References listed on IDEAS

    as
    1. Fabai Wu & Aleksandre Japaridze & Xuan Zheng & Jakub Wiktor & Jacob W. J. Kerssemakers & Cees Dekker, 2019. "Direct imaging of the circular chromosome in a live bacterium," Nature Communications, Nature, vol. 10(1), pages 1-9, December.
    2. Eugene Kim & Jacob Kerssemakers & Indra A. Shaltiel & Christian H. Haering & Cees Dekker, 2020. "DNA-loop extruding condensin complexes can traverse one another," Nature, Nature, vol. 579(7799), pages 438-442, March.
    3. Peter Eastman & Jason Swails & John D Chodera & Robert T McGibbon & Yutong Zhao & Kyle A Beauchamp & Lee-Ping Wang & Andrew C Simmonett & Matthew P Harrigan & Chaya D Stern & Rafal P Wiewiora & Bernar, 2017. "OpenMM 7: Rapid development of high performance algorithms for molecular dynamics," PLOS Computational Biology, Public Library of Science, vol. 13(7), pages 1-17, July.
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    5. Joris J. B. Messelink & Muriel C. F. Teeseling & Jacqueline Janssen & Martin Thanbichler & Chase P. Broedersz, 2021. "Learning the distribution of single-cell chromosome conformations in bacteria reveals emergent order across genomic scales," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
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