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Mechanical strain sensing implicated in cell shape recovery in Escherichia coli

Nature Microbiology volume 2, Article number: 17115 (2017) Cite this article

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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 elasticity1–11. 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 wall3,4,12–14. 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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Figure 1: Three theories for cellular shape regulation.
Figure 2: Areal strain-dependent PG elongation quantitatively predicts shape recovery dynamics.
Figure 3: Quantitative analysis of cellular straightening dynamics.
Figure 4: MreB–msfGFP fusion cells exhibit MreB enrichment at negative Gaussian curvature, but MreB enrichment alone cannot explain straightening.

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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

  1. Felix Wong and Lars D. Renner: These authors contributed equally to this work.

Authors and Affiliations

  1. School of Engineering and Applied Sciences, Harvard University, Cambridge, 02138, Massachusetts, 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, 53706, Wisconsin, 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, 94720, California, USA

    Jayson Paulose

  6. Department of Biomedical Engineering, University of Wisconsin-Madison, Madison, 53706, Wisconsin, 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.

Corresponding authors

Correspondence to Lars D. Renner or Ariel Amir.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Notes 1 and 2, Supplementary Discussion, Supplementary Methods, Supplementary References, Supplementary Tables 1 and 2, Supplementary Figures 1–11. (PDF 14721 kb)

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. (MOV 73 kb)

Supplementary Video 2

Straightening dynamics of single E. coli cells. (MOV 58 kb)

Supplementary Video 3

Straightening dynamics of single E. coli cells. (MOV 63 kb)

Supplementary Video 4

Straightening dynamics of single E. coli cells. (MOV 34 kb)

Supplementary Video 5

Straightening dynamics of single E. coli cells. (MOV 123 kb)

Supplementary Video 6

Straightening dynamics of single E. coli cells. (MOV 92 kb)

Supplementary Video 7

Straightening dynamics of single E. coli cells. (MOV 52 kb)

Supplementary Video 8

Straightening dynamics of single E. coli cells. (MOV 94 kb)

Supplementary Video 9

Straightening dynamics of single E. coli cells. (MOV 72 kb)

Supplementary Video 10

Straightening dynamics of single E. coli cells. (MOV 20 kb)

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. (MP4 5860 kb)

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Wong, F., Renner, L., Özbaykal, G. et al. Mechanical strain sensing implicated in cell shape recovery in Escherichia coli. Nat Microbiol 2, 17115 (2017). https://doi.org/10.1038/nmicrobiol.2017.115

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