Evidence for a DNA-relay mechanism in ParABS-mediated chromosome segregation

  1. Hoong Chuin Lim
  2. Ivan V Surovtsev
  3. Bruno G Beltran
  4. Fang Huang
  5. Jörg Bewersdorf
  6. Christine Jacobs-Wagner  Is a corresponding author
  1. Yale University, United States
  2. Microbial Diversity Institute, Yale University, United States
  3. Louisiana State University, United States
  4. Yale School of Medicine, United States

Abstract

The widely conserved ParABS system plays a major role in bacterial chromosome segregation. How the components of this system work together to generate translocation force and directional motion remains uncertain. Here, we combine biochemical approaches, quantitative imaging and mathematical modeling to examine the mechanism by which ParA drives the translocation of the ParB/parS partition complex in Caulobacter crescentus. Our experiments, together with simulations grounded on experimentally-determined biochemical and cellular parameters, suggest a novel 'DNA-relay' mechanism in which the chromosome plays a mechanical function. In this model, DNA-bound ParA-ATP dimers serve as transient tethers that harness the elastic dynamics of the chromosome to relay the partition complex from one DNA region to another across a ParA-ATP dimer gradient. Since ParA-like proteins are implicated in the partitioning of various cytoplasmic cargos, the conservation of their DNA-binding activity suggests that the DNA-relay mechanism may be a general form of intracellular transport in bacteria.

Article and author information

Author details

  1. Hoong Chuin Lim

    Yale University, New Haven, United States
    Competing interests
    No competing interests declared.
  2. Ivan V Surovtsev

    Microbial Diversity Institute, Yale University, West Haven, United States
    Competing interests
    No competing interests declared.
  3. Bruno G Beltran

    Louisiana State University, Baton Rouge, United States
    Competing interests
    No competing interests declared.
  4. Fang Huang

    Yale School of Medicine, New Haven, United States
    Competing interests
    No competing interests declared.
  5. Jörg Bewersdorf

    Yale School of Medicine, New Haven, United States
    Competing interests
    Jörg Bewersdorf, J.B. discloses significant financial interest in Vutara, Inc (Salt Lake City, UT)..
  6. Christine Jacobs-Wagner

    Microbial Diversity Institute, Yale University, West Haven, United States
    For correspondence
    christine.jacobs-wagner@yale.edu
    Competing interests
    No competing interests declared.

Reviewing Editor

  1. Mohan Balasubramanian, University of Warwick, United Kingdom

Version history

  1. Received: March 11, 2014
  2. Accepted: May 16, 2014
  3. Accepted Manuscript published: May 23, 2014 (version 1)
  4. Version of Record published: June 24, 2014 (version 2)

Copyright

© 2014, Lim 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.

Metrics

  • 5,203
    views
  • 800
    downloads
  • 199
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Hoong Chuin Lim
  2. Ivan V Surovtsev
  3. Bruno G Beltran
  4. Fang Huang
  5. Jörg Bewersdorf
  6. Christine Jacobs-Wagner
(2014)
Evidence for a DNA-relay mechanism in ParABS-mediated chromosome segregation
eLife 3:e02758.
https://doi.org/10.7554/eLife.02758

Share this article

https://doi.org/10.7554/eLife.02758