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Symmetry and scale orient Min protein patterns in shaped bacterial sculptures

Nature Nanotechnology volume 10, pages 719–726 (2015)Cite this article

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Abstract

The boundary of a cell defines the shape and scale of its subcellular organization. However, the effects of the cell's spatial boundaries as well as the geometry sensing and scale adaptation of intracellular molecular networks remain largely unexplored. Here, we show that living bacterial cells can be ‘sculpted’ into defined shapes, such as squares and rectangles, which are used to explore the spatial adaptation of Min proteins that oscillate pole-to-pole in rod-shaped Escherichia coli to assist cell division. In a wide geometric parameter space, ranging from 2 × 1 × 1 to 11 × 6 × 1 μm3, Min proteins exhibit versatile oscillation patterns, sustaining rotational, longitudinal, diagonal, stripe and even transversal modes. These patterns are found to directly capture the symmetry and scale of the cell boundary, and the Min concentration gradients scale with the cell size within a characteristic length range of 3–6 μm. Numerical simulations reveal that local microscopic Turing kinetics of Min proteins can yield global symmetry selection, gradient scaling and an adaptive range, when and only when facilitated by the three-dimensional confinement of the cell boundary. These findings cannot be explained by previous geometry-sensing models based on the longest distance, membrane area or curvature, and reveal that spatial boundaries can facilitate simple molecular interactions to result in far more versatile functions than previously understood.

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Figure 1: Min proteins oscillate along the symmetry axes of E. coli shaped by the ‘cell-sculpting’ technique.
Figure 2: A characteristic range dictates the Min oscillation axis choice.
Figure 3: Robustness and variation of Min patterns in a wide geometric parameter space.
Figure 4: Symmetry selection, gradient scaling and adaptive range in Min patterns.
Figure 5: Numerical simulations of a three-dimensional reaction–diffusion model explain the sensing of symmetry and scale by Min proteins.

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  • 25 June 2015

    In the version of this Article previously published online the Methods section was inadvertently omitted. This has been corrected for all versions of the Article.

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Acknowledgements

The authors thank E. van Rijn, D. de Graaff, W. Postek, J. van der Does, J. Kerssenmakers and Z. Huang for technical assistance, Y. Caspi, Y-L. Shih, A. Lindert, L. Rothfield, A. Meyer and C. Plesa for materials, E. Frey and J. Halatek for discussions on their model, C. Danelon and F. Hol for discussions, and the CSHL Computational Cell Biology Summer School and VirtualCell (NIH grant P41-GM103313). This work was partly supported by the Netherlands Organisation for Scientific Research (NWO/OCW) as part of the Frontiers of Nanoscience programme, NanoNextNL programme 3B (F.W.) and European Research Council NanoforBio no. 247072 (C.D.).

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Author notes

  1. Juan E. Keymer

    Present address: Present address: IEB & Department of Ecology, School of Biological Sciences, P. Catholic University, Casilla 114-D, Santiago, Chile,

Authors and Affiliations

  1. Department of Bionanoscience, Kavli Institute of Nanoscience, Delft University of Technology, Lorentzweg 1, Delft, 2628 CJ, The Netherlands

    Fabai Wu, Bas G. C. van Schie, Juan E. Keymer & Cees Dekker

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Contributions

F.W., J.E.K. and C.D. conceived the experiments, discussed the work and wrote the paper. F.W. and B.v.S performed the experiments. F.W. analysed the data, derived the mechanisms and carried out computer simulations.

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Correspondence to Cees Dekker.

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The authors declare no competing financial interests.

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Wu, F., van Schie, B., Keymer, J. et al. Symmetry and scale orient Min protein patterns in shaped bacterial sculptures. Nature Nanotech 10, 719–726 (2015). https://doi.org/10.1038/nnano.2015.126

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