Self-organised segregation of bacterial chromosomal origins

  1. Andreas Hofmann
  2. Jarno Mäkelä
  3. David J Sherratt
  4. Dieter Heermann
  5. Sean M Murray  Is a corresponding author
  1. Heidelberg University, Germany
  2. University of Oxford, United Kingdom
  3. Max Planck Institute for Terrestrial Microbiology, Germany

Abstract

The chromosomal replication origin region (ori) of characterized bacteria is dynamically positioned throughout the cell cycle. In slowly growing Escherichia coli, ori is maintained at mid-cell from birth until its replication, after which newly replicated sister oris move to opposite quarter positions. Here, we provide an explanation for ori positioning based on the self-organisation of the Structural Maintenance of Chromosomes complex, MukBEF, which forms dynamically positioned clusters on the chromosome. We propose that a non-trivial feedback between the self-organising gradient of MukBEF complexes and the oris leads to accurate ori positioning. We find excellent agreement with quantitative experimental measurements and confirm key predictions. Specifically, we show that oris exhibit biased motion towards MukBEF clusters, rather than mid-cell. Our findings suggest that MukBEF and oris act together as a self-organising system in chromosome organisation-segregation and introduces protein self-organisation as an important consideration for future studies of chromosome dynamics.

Data availability

Experimental source data files have been provided for Figure 1. We also used the ori localisation tracks provided as supplementary data to Kuwada et al., 2014 and the co-localisation curves from Figure 1c of Nolivos et al., 2016.

Article and author information

Author details

  1. Andreas Hofmann

    Institute for Theoretical Physics, Heidelberg University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Jarno Mäkelä

    Department of Biochemistry, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. David J Sherratt

    Department of Biochemistry, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2104-5430
  4. Dieter Heermann

    Institute for Theoretical Physics, Heidelberg University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Sean M Murray

    Systems and Synthetic Microbiology, Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
    For correspondence
    sean.murray@synmikro.mpi-marburg.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2260-0774

Funding

Wellcome (DSJ: 200782/Z/16/Z)

  • Jarno Mäkelä
  • David J Sherratt

Deutsche Forschungsgemeinschaft (GSC 220)

  • Andreas Hofmann

Max-Planck-Gesellschaft (Open-access funding)

  • Sean M Murray

Human Frontier Science Program (RGP0014/2014)

  • Andreas Hofmann

Deutsche Forschungsgemeinschaft (INST 35/1134-1 FUGG)

  • Andreas Hofmann
  • Dieter Heermann

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

Reviewing Editor

  1. Raymond E Goldstein, University of Cambridge, United Kingdom

Version history

  1. Received: March 5, 2019
  2. Accepted: August 9, 2019
  3. Accepted Manuscript published: August 9, 2019 (version 1)
  4. Version of Record published: August 20, 2019 (version 2)

Copyright

© 2019, Hofmann 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. Andreas Hofmann
  2. Jarno Mäkelä
  3. David J Sherratt
  4. Dieter Heermann
  5. Sean M Murray
(2019)
Self-organised segregation of bacterial chromosomal origins
eLife 8:e46564.
https://doi.org/10.7554/eLife.46564

Share this article

https://doi.org/10.7554/eLife.46564

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