MreB filaments align along greatest principal membrane curvature to orient cell wall synthesis
- Harvard University, United States
- MRC Laboratory of Molecular Biology, United Kingdom
- Harvard John A. Paulson School of Engineering and Applied Sciences, United States
- Leibniz Institute of Polymer Research, Germany
Abstract
MreB is essential for rod shape in many bacteria. Membrane-associated MreB filaments move around the rod circumference, helping to insert cell wall in the radial direction to reinforce rod shape. To understand how oriented MreB motion arises, we altered the shape of Bacillus subtilis. MreB motion is isotropic in round cells, and orientation is restored when rod shape is externally imposed. Stationary filaments orient within protoplasts, and purified MreB tubulates liposomes in vitro, orienting within tubes. Together, this demonstrates MreB orients along the greatest principal membrane curvature, a conclusion supported with biophysical modeling. We observed that spherical cells regenerate into rods in a local, self-reinforcing manner: rapidly propagating rods emerge from small bulges, exhibiting oriented MreB motion. We propose that the coupling of MreB filament alignment to shape-reinforcing peptidoglycan synthesis creates a locally-acting, self-organizing mechanism allowing the rapid establishment and stable maintenance of emergent rod shape.
Article and author information
Author details
Funding
National Institutes of Health (DP2AI117923-01)
- Ethan C Garner
Volkswagen Foundation
- Lars D Renner
- Ariel Amir
- Ethan C Garner
Wellcome (095514/Z/11/Z)
- Jan Löwe
National Science Foundation (GFRP)
- Felix Wong
Medical Research Council (U105184326)
- Jan Löwe
Howard Hughes Medical Institute (International Student Research Fellow)
- Saman Hussain
National Institutes of Health (R01 GM076710)
- Suzanne Walker
Searle Scholar Fellowship
- Ethan C Garner
Alfred P. Sloan Foundation
- Ariel Amir
Smith Family Award
- Ethan C Garner
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2018, Hussain 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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MreB filaments align along greatest principal membrane curvature to orient cell wall synthesis
eLife 7:e32471.
https://doi.org/10.7554/eLife.32471
Further reading
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Teichoic acids (TA) are linear phospho-saccharidic polymers and important constituents of the cell envelope of Gram-positive bacteria, either bound to the peptidoglycan as wall teichoic acids (WTA) or to the membrane as lipoteichoic acids (LTA). The composition of TA varies greatly but the presence of both WTA and LTA is highly conserved, hinting at an underlying fundamental function that is distinct from their specific roles in diverse organisms. We report the observation of a periplasmic space in Streptococcus pneumoniae by cryo-electron microscopy of vitreous sections. The thickness and appearance of this region change upon deletion of genes involved in the attachment of TA, supporting their role in the maintenance of a periplasmic space in Gram-positive bacteria as a possible universal function. Consequences of these mutations were further examined by super-resolved microscopy, following metabolic labeling and fluorophore coupling by click chemistry. This novel labeling method also enabled in-gel analysis of cell fractions. With this approach, we were able to titrate the actual amount of TA per cell and to determine the ratio of WTA to LTA. In addition, we followed the change of TA length during growth phases, and discovered that a mutant devoid of LTA accumulates the membrane-bound polymerized TA precursor.
