Rod-like bacterial shape is maintained by feedback between cell curvature and cytoskeletal localization

Proc Natl Acad Sci U S A. 2014 Mar 18;111(11):E1025-34. doi: 10.1073/pnas.1317174111. Epub 2014 Feb 18.

Abstract

Cells typically maintain characteristic shapes, but the mechanisms of self-organization for robust morphological maintenance remain unclear in most systems. Precise regulation of rod-like shape in Escherichia coli cells requires the MreB actin-like cytoskeleton, but the mechanism by which MreB maintains rod-like shape is unknown. Here, we use time-lapse and 3D imaging coupled with computational analysis to map the growth, geometry, and cytoskeletal organization of single bacterial cells at subcellular resolution. Our results demonstrate that feedback between cell geometry and MreB localization maintains rod-like cell shape by targeting cell wall growth to regions of negative cell wall curvature. Pulse-chase labeling indicates that growth is heterogeneous and correlates spatially and temporally with MreB localization, whereas MreB inhibition results in more homogeneous growth, including growth in polar regions previously thought to be inert. Biophysical simulations establish that curvature feedback on the localization of cell wall growth is an effective mechanism for cell straightening and suggest that surface deformations caused by cell wall insertion could direct circumferential motion of MreB. Our work shows that MreB orchestrates persistent, heterogeneous growth at the subcellular scale, enabling robust, uniform growth at the cellular scale without requiring global organization.

Keywords: bacterial cytoskeleton; biophysical modeling; morphogenesis.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Biophysics
  • Cell Wall / physiology*
  • Computer Simulation
  • Cytoskeleton / physiology
  • Cytoskeleton / ultrastructure*
  • Escherichia coli / cytology*
  • Escherichia coli / growth & development*
  • Escherichia coli Proteins / metabolism*
  • Fluorescence
  • Imaging, Three-Dimensional
  • Models, Biological
  • Morphogenesis / physiology*
  • Time-Lapse Imaging

Substances

  • Escherichia coli Proteins
  • MreB protein, E coli