Letter

Mechanical strain sensing implicated in cell shape recovery in Escherichia coli

  • Nature Microbiology 2, Article number: 17115 (2017)
  • doi:10.1038/nmicrobiol.2017.115
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Abstract

The shapes of most bacteria are imparted by the structures of their peptidoglycan cell walls, which are determined by many dynamic processes that can be described on various length scales ranging from short-range glycan insertions to cellular-scale elasticity1,​2,​3,​4,​5,​6,​7,​8,​9,​10,​11. Understanding the mechanisms that maintain stable, rod-like morphologies in certain bacteria has proved to be challenging due to an incomplete understanding of the feedback between growth and the elastic and geometric properties of the cell wall3,4,12,​13,​14. Here, we probe the effects of mechanical strain on cell shape by modelling the mechanical strains caused by bending and differential growth of the cell wall. We show that the spatial coupling of growth to regions of high mechanical strain can explain the plastic response of cells to bending4 and quantitatively predict the rate at which bent cells straighten. By growing filamentous Escherichia coli cells in doughnut-shaped microchambers, we find that the cells recovered their straight, native rod-shaped morphologies when released from captivity at a rate consistent with the theoretical prediction. We then measure the localization of MreB, an actin homologue crucial to cell wall synthesis, inside confinement and during the straightening process, and find that it cannot explain the plastic response to bending or the observed straightening rate. Our results implicate mechanical strain sensing, implemented by components of the elongasome yet to be fully characterized, as an important component of robust shape regulation in E. coli.

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Acknowledgements

F.W. was supported by the National Science Foundation Graduate Research Fellowship under grant no. DGE1144152. L.D.R., S.v.T. and A.A. were supported by the Volkswagen Foundation. G.O. and S.v.T. were supported by funds from the European Research Council (ERC-2015-STG RCSB 679980), the LabEx IBEID (Integrative Biology of Emerging Infectious Diseases) programme, the Mairie de Paris ‘Emergence(s)’ programme, and the ANR ‘Investissement d'Avenir Programme’ (10-LABX-62-IBEID) to S.v.T. J.P. acknowledges funding by a Delta ITP Zwaartekracht grant. A.A. was supported by the Alfred P. Sloan Foundation. The authors thank J. Hutchinson for discussions on shell theory, J. Hutchinson, E.C. Garner and C. Wivagg for comments on the manuscript, L. Mahadevan and C. Wivagg for discussions on the model, K. Bertoldi and J. Liu for help with simulation software, E. Oldewurtel and E. Brambilla for help with microscopy and N. Ouzounov for providing the MreB-msfGFP strain.

Author information

Author notes

    • Felix Wong
    •  & Lars D. Renner

    These authors contributed equally to this work.

Affiliations

  1. School of Engineering and Applied Sciences, Harvard University, Cambridge, Massachusetts 02138, USA

    • Felix Wong
    •  & Ariel Amir
  2. Leibniz Institute of Polymer Research and the Max Bergmann Center of Biomaterials, 01069 Dresden, Germany

    • Lars D. Renner
  3. Department of Biochemistry, University of Wisconsin-Madison, Madison, Wisconsin 53706, USA

    • Lars D. Renner
    •  & Douglas B. Weibel
  4. Department of Microbiology, Institut Pasteur, 75724 Paris, France

    • Gizem Özbaykal
    •  & Sven van Teeffelen
  5. Departments of Physics and Integrative Biology, University of California, Berkeley, California 94720, USA

    • Jayson Paulose
  6. Department of Biomedical Engineering, University of Wisconsin-Madison, Madison, Wisconsin 53706, USA

    • Douglas B. Weibel

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Contributions

F.W. and A.A. developed the model of straightening. F.W. and J.P. performed simulations. L.D.R., G.Ö., D.B.W., S.v.T. and A.A. designed the experiments. L.D.R. and G.Ö. performed the experiments. F.W., L.D.R. and G.Ö. analysed the data. F.W. and G.Ö. wrote cell-tracking software. F.W., L.D.R., G.Ö., S.v.T. and A.A. wrote the paper.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Lars D. Renner or Ariel Amir.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    Supplementary Notes 1 and 2, Supplementary Discussion, Supplementary Methods, Supplementary References, Supplementary Tables 1 and 2, Supplementary Figures 1–11.

Videos

  1. 1.

    Supplementary Video 1

    Straightening dynamics of single E. coli cells. Supplementary Videos 1–10 show individual, filamentous E. coli cells recovering their native rod shapes as they grow after release from toroidal microchambers. The time between frames is 2 minutes, the time lapses cover a period of around 40 minutes, and the field of view is approximately 40 μm wide.

  2. 2.

    Supplementary Video 2

    Straightening dynamics of single E. coli cells.

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    Supplementary Video 3

    Straightening dynamics of single E. coli cells.

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    Supplementary Video 4

    Straightening dynamics of single E. coli cells.

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    Supplementary Video 5

    Straightening dynamics of single E. coli cells.

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    Supplementary Video 6

    Straightening dynamics of single E. coli cells.

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    Supplementary Video 7

    Straightening dynamics of single E. coli cells.

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    Supplementary Video 8

    Straightening dynamics of single E. coli cells.

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    Supplementary Video 9

    Straightening dynamics of single E. coli cells.

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    Supplementary Video 10

    Straightening dynamics of single E. coli cells.

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    Supplementary Video 11

    Numerical simulation of the growth process. Numerical simulations in (1) the case of zero processivity; (2) the case of infinite processivity; and (3) the case of a self-consistent areal strain coupling that results in a constant differential growth in phase 1 and straightening in phase 2. The simulation methodology is detailed in the Supplementary Methods.