Processivity of peptidoglycan synthesis provides a built-in mechanism for the robustness of straight-rod cell morphology

Oleksii Sliusarenko, Matthew T. Cabeen, Charles William Wolgemuth, Christine Jacobs-Wagner, Thierry Emonet

Research output: Contribution to journalArticle

29 Citations (Scopus)

Abstract

The propagation of cell shape across generations is remarkably robust in most bacteria. Even when deformations are acquired, growing cells progressively recover their original shape once the deforming factors are eliminated. For instance, straight-rod-shaped bacteria grow curved when confined to circular microchambers, but straighten in a growth-dependent fashion when released. Bacterial cell shape is maintained by the peptidoglycan (PG) cell wall, a giant macromolecule of glycan strands that are synthesized by processive enzymes and cross-linked by peptide chains. Changes in cell geometry require modifying the PG and therefore depend directly on the molecular-scale properties of PG structure and synthesis. Using a mathematical model we quantify the straightening of curved Caulobacter crescentus cells after disruption of the cell-curving crescentin structure. We observe that cells straighten at a rate that is about half (57%) the cell growth rate. Next we show that in the absence of other effects there exists a mathematical relationship between the rate of cell straightening and the processivity of PG synthesis - the number of subunits incorporated before termination of synthesis. From the measured rate of cell straightening this relationship predicts processivity values that are in good agreement with our estimates from published data. Finally, we consider the possible role of three other mechanisms in cell straightening. We conclude that regardless of the involvement of other factors, intrinsic properties of PG processivity provide a robust mechanism for cell straightening that is hardwired to the cell wall synthesis machinery.

Original languageEnglish (US)
Pages (from-to)10086-10091
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume107
Issue number22
DOIs
StatePublished - Jun 1 2010
Externally publishedYes

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Peptidoglycan
Cell Shape
Cell Wall
Caulobacter crescentus
Bacteria
Intrinsic Factor
Growth
Polysaccharides
Theoretical Models
Peptides

Keywords

  • Cell curvature
  • Cell shape
  • Cell wall
  • Modeling

ASJC Scopus subject areas

  • General

Cite this

Processivity of peptidoglycan synthesis provides a built-in mechanism for the robustness of straight-rod cell morphology. / Sliusarenko, Oleksii; Cabeen, Matthew T.; Wolgemuth, Charles William; Jacobs-Wagner, Christine; Emonet, Thierry.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 107, No. 22, 01.06.2010, p. 10086-10091.

Research output: Contribution to journalArticle

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