Cell wall remodeling drives engulfment during Bacillus subtilis sporulation

  1. Nikola Ojkic
  2. Javier López-Garrido
  3. Kit Pogliano  Is a corresponding author
  4. Robert G Endres  Is a corresponding author
  1. Imperial College London, United Kingdom
  2. University of California, San Diego, United States

Abstract

When starved, the Gram-positive bacterium Bacillus subtilis forms durable spores for survival. Sporulation initiates with an asymmetric cell division, creating a large mother cell and a small forespore. Subsequently, the mother cell membrane engulfs the forespore in a phagocytosis-like process. However, the force generation mechanism for forward membrane movement remains unknown. Here, we show that membrane migration is driven by cell wall remodeling at the leading edge of the engulfing membrane, with peptidoglycan synthesis and degradation mediated by penicillin binding proteins in the forespore and a cell wall degradation protein complex in the mother cell. We propose a simple model for engulfment in which the junction between the septum and the lateral cell wall moves around the forespore by a mechanism resembling the 'template model'. Hence, we establish a biophysical mechanism for the creation of a force for engulfment based on the coordination between cell wall synthesis and degradation.

Article and author information

Author details

  1. Nikola Ojkic

    Department of Life Sciences, Imperial College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Javier López-Garrido

    Division of Biological Sciences, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Kit Pogliano

    Division of Biological Sciences, University of California, San Diego, La Jolla, United States
    For correspondence
    kpogliano@ucsd.edu
    Competing interests
    The authors declare that no competing interests exist.
  4. Robert G Endres

    Department of Life Sciences, Imperial College London, London, United Kingdom
    For correspondence
    r.endres@imperial.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1379-659X

Funding

European Research Council (280492-PPHPI)

  • Nikola Ojkic
  • Robert G Endres

European Molecular Biology Organization (ATLF1274-2011)

  • Javier López-Garrido

National Institutes of Health (R01-GM57045)

  • Kit Pogliano

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

Reviewing Editor

  1. Avigdor Eldar, Tel Aviv University, Israel

Publication history

  1. Received: June 10, 2016
  2. Accepted: November 14, 2016
  3. Accepted Manuscript published: November 17, 2016 (version 1)
  4. Version of Record published: December 8, 2016 (version 2)

Copyright

© 2016, Ojkic 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. Nikola Ojkic
  2. Javier López-Garrido
  3. Kit Pogliano
  4. Robert G Endres
(2016)
Cell wall remodeling drives engulfment during Bacillus subtilis sporulation
eLife 5:e18657.
https://doi.org/10.7554/eLife.18657

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