A low Smc flux avoids collisions and facilitates chromosome organization in B. subtilis

  1. Anna Anchimiuk
  2. Virginia S Lioy
  3. Florian Patrick Bock
  4. Anita Minnen
  5. Frederic Boccard
  6. Stephan Gruber  Is a corresponding author
  1. University of Lausanne, Switzerland
  2. Université Paris-Saclay, France
  3. Max Planck Institute of Biochemistry, Germany

Abstract

SMC complexes are widely conserved ATP-powered DNA-loop-extrusion motors indispensable for organizing and faithfully segregating chromosomes. How SMC complexes translocate along DNA for loop extrusion and what happens when two complexes meet on the same DNA molecule is largely unknown. Revealing the origins and the consequences of SMC encounters is crucial for understanding the folding process not only of bacterial, but also of eukaryotic chromosomes. Here, we uncover several factors that influence bacterial chromosome organization by modulating the probability of such clashes. These factors include the number, the strength, and the distribution of Smc loading sites, the residency time on the chromosome, the translocation rate, and the cellular abundance of Smc complexes. By studying various mutants, we show that these parameters are fine-tuned to reduce the frequency of encounters between Smc complexes, presumably as a risk mitigation strategy. Mild perturbations hamper chromosome organization by causing Smc collisions, implying that the cellular capacity to resolve them is limited. Altogether, we identify mechanisms that help to avoid Smc collisions and their resolution by Smc traversal or other potentially risky molecular transactions.

Data availability

All deep sequencing data has been deposited to the NCBI GEO database and will be available at GEO Accession number: GSE163573All other raw data will be made available via Mendeley Data DOI:10.17632/kvjd6nj2bh.2

The following data sets were generated
    1. Anchimiuk A
    2. Gruber S
    (2021) Smc_collisions
    Mendeley Data, V2, doi: 10.17632/kvjd6nj2bh.2.

Article and author information

Author details

  1. Anna Anchimiuk

    Department of Fundamental Microbiology, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  2. Virginia S Lioy

    Institute for Integrative Biology of the Cell (I2BC), Université Paris-Saclay, Gif-sur-Yvette, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Florian Patrick Bock

    Department of Fundamental Microbiology, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  4. Anita Minnen

    Chromosome Organisation and Dynamics, Max Planck Institute of Biochemistry, Martinsried, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Frederic Boccard

    Institute for Integrative Biology of the Cell (I2BC), Université Paris-Saclay, Gif-sur-Yvette, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Stephan Gruber

    Department of Fundamental Microbiology, University of Lausanne, Lausanne, Switzerland
    For correspondence
    stephan.gruber@unil.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0150-0395

Funding

European Reserach Council Horizon 2020 (724482)

  • Stephan Gruber

Agence Nationale de la Recherche (ANR-CE12-0013-01)

  • Frederic Boccard

Assocation pour la Recherche contre le Cancer

  • Frederic Boccard

Max Planck Institute for Dynamics of Complex Technical Systems Magdeburg

  • Anita Minnen

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

Reviewing Editor

  1. Michael T Laub, Massachusetts Institute of Technology, United States

Publication history

  1. Preprint posted: December 4, 2020 (view preprint)
  2. Received: December 4, 2020
  3. Accepted: July 28, 2021
  4. Accepted Manuscript published: August 4, 2021 (version 1)
  5. Version of Record published: August 11, 2021 (version 2)

Copyright

© 2021, Anchimiuk 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. Anna Anchimiuk
  2. Virginia S Lioy
  3. Florian Patrick Bock
  4. Anita Minnen
  5. Frederic Boccard
  6. Stephan Gruber
(2021)
A low Smc flux avoids collisions and facilitates chromosome organization in B. subtilis
eLife 10:e65467.
https://doi.org/10.7554/eLife.65467

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