Interdependent progression of bidirectional sister replisomes in E. coli

  1. Po Jui Chen
  2. Anna B McMullin
  3. Bryan J Visser
  4. Qian Mei
  5. Susan M Rosenberg
  6. David Bates  Is a corresponding author
  1. Baylor College of Medicine, United States
  2. Rice University, United States

Abstract

Bidirectional DNA replication complexes initiated from the same origin remain colocalized in a factory configuration for part or all their lifetimes. However, there is little evidence that sister replisomes are functionally interdependent, and the consequence of factory replication is unknown. Here, we investigated the functional relationship between sister replisomes in E. coli, which naturally exhibits both factory and solitary configurations in the same replication cycle. Using an inducible transcription factor roadblocking system, we found that blocking one replisome caused a significant decrease in overall progression and velocity of the sister replisome. Remarkably, progression was impaired only if the block occurred while sister replisomes were still in a factory configuration - blocking one fork had no significant effect on the other replisome when sister replisomes were physically separate. Disruption of factory replication also led to increased fork stalling and requirement of fork restart mechanisms. These results suggest that physical association between sister replisomes is important for establishing an efficient and uninterrupted replication program. We discuss the implications of our findings on mechanisms of replication factory structure and function, and cellular strategies of replicating problematic DNA such as highly transcribed segments.

Data availability

Sequencing data generated in this study have been deposited in the National Center for Biotechnology (NCBI) Sequence Read Archive (SRA), BioProject PRJNA860928.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Po Jui Chen

    Molecular Virology and Microbiology, Baylor College of Medicine, Houston, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Anna B McMullin

    Molecular Virology and Microbiology, Baylor College of Medicine, Houston, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Bryan J Visser

    Graduate Program in Integrative Molecular and Biomedical Sciences, Baylor College of Medicine, Houston, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Qian Mei

    Systems, Synthetic, and Physical Biology Program, Rice University, Houston, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Susan M Rosenberg

    Graduate Program in Integrative Molecular and Biomedical Sciences, Baylor College of Medicine, Houston, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. David Bates

    Molecular Virology and Microbiology, Baylor College of Medicine, Houston, United States
    For correspondence
    bates@bcm.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0870-055X

Funding

National Institutes of Health (R01 GM102679)

  • David Bates

National Institutes of Health (R01 GM135368)

  • David Bates

National Institutes of Health (R35 GM122598)

  • Susan M Rosenberg

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2023, Chen et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Po Jui Chen
  2. Anna B McMullin
  3. Bryan J Visser
  4. Qian Mei
  5. Susan M Rosenberg
  6. David Bates
(2023)
Interdependent progression of bidirectional sister replisomes in E. coli
eLife 12:e82241.
https://doi.org/10.7554/eLife.82241

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https://doi.org/10.7554/eLife.82241