Literature DB >> 20479277

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

Oleksii Sliusarenko1, Matthew T Cabeen, Charles W Wolgemuth, Christine Jacobs-Wagner, Thierry Emonet.   

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.

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Year:  2010        PMID: 20479277      PMCID: PMC2890421          DOI: 10.1073/pnas.1000737107

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  41 in total

1.  The bacterial cytoskeleton: an intermediate filament-like function in cell shape.

Authors:  Nora Ausmees; Jeffrey R Kuhn; Christine Jacobs-Wagner
Journal:  Cell       Date:  2003-12-12       Impact factor: 41.582

2.  The polysaccharide chain of chitin.

Authors:  D CARLSTROM
Journal:  Biochim Biophys Acta       Date:  1962-05-21

3.  Controlling the shape of filamentous cells of Escherichia coli.

Authors:  Shoji Takeuchi; Willow R DiLuzio; Douglas B Weibel; George M Whitesides
Journal:  Nano Lett       Date:  2005-09       Impact factor: 11.189

4.  Crystal structure of a peptidoglycan glycosyltransferase suggests a model for processive glycan chain synthesis.

Authors:  Yanqiu Yuan; Dianah Barrett; Yi Zhang; Daniel Kahne; Piotr Sliz; Suzanne Walker
Journal:  Proc Natl Acad Sci U S A       Date:  2007-03-08       Impact factor: 11.205

5.  Bacterial cell curvature through mechanical control of cell growth.

Authors:  Matthew T Cabeen; Godefroid Charbon; Waldemar Vollmer; Petra Born; Nora Ausmees; Douglas B Weibel; Christine Jacobs-Wagner
Journal:  EMBO J       Date:  2009-03-12       Impact factor: 11.598

6.  Envelope-associated nucleoid from Caulobacter crescentus stalked and swarmer cells.

Authors:  M Evinger; N Agabian
Journal:  J Bacteriol       Date:  1977-10       Impact factor: 3.490

7.  Oriented fragmentation of Escherichia coli sacculi by sonication.

Authors:  R W Verwer; E H Beachey; W Keck; A M Stoub; J E Poldermans
Journal:  J Bacteriol       Date:  1980-01       Impact factor: 3.490

8.  Actin homolog MreBH governs cell morphogenesis by localization of the cell wall hydrolase LytE.

Authors:  Rut Carballido-López; Alex Formstone; Ying Li; S Dusko Ehrlich; Philippe Noirot; Jeff Errington
Journal:  Dev Cell       Date:  2006-09       Impact factor: 12.270

9.  The direction of glycan synthesis in a bacterial peptidoglycan.

Authors:  J B Ward; H R Perkins
Journal:  Biochem J       Date:  1973-12       Impact factor: 3.857

Review 10.  Murein (peptidoglycan) structure, architecture and biosynthesis in Escherichia coli.

Authors:  Waldemar Vollmer; Ute Bertsche
Journal:  Biochim Biophys Acta       Date:  2007-06-16
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  23 in total

Review 1.  Physics of bacterial morphogenesis.

Authors:  Sean X Sun; Hongyuan Jiang
Journal:  Microbiol Mol Biol Rev       Date:  2011-12       Impact factor: 11.056

2.  Dislocation-mediated growth of bacterial cell walls.

Authors:  Ariel Amir; David R Nelson
Journal:  Proc Natl Acad Sci U S A       Date:  2012-06-01       Impact factor: 11.205

3.  Elasticity and biochemistry of growth relate replication rate to cell length and cross-link density in rod-shaped bacteria.

Authors:  Akeisha M T Belgrave; Charles W Wolgemuth
Journal:  Biophys J       Date:  2013-06-18       Impact factor: 4.033

Review 4.  Getting into shape: How do rod-like bacteria control their geometry?

Authors:  Ariel Amir; Sven van Teeffelen
Journal:  Syst Synth Biol       Date:  2014-04-22

Review 5.  From the regulation of peptidoglycan synthesis to bacterial growth and morphology.

Authors:  Athanasios Typas; Manuel Banzhaf; Carol A Gross; Waldemar Vollmer
Journal:  Nat Rev Microbiol       Date:  2011-12-28       Impact factor: 60.633

6.  An essential tyrosine phosphatase homolog regulates cell separation, outer membrane integrity, and morphology in Caulobacter crescentus.

Authors:  Elaine B Shapland; Sarah J Reisinger; Amrita K Bajwa; Kathleen R Ryan
Journal:  J Bacteriol       Date:  2011-06-24       Impact factor: 3.490

7.  Mechanics and dynamics of translocating MreB filaments on curved membranes.

Authors:  Felix Wong; Ethan C Garner; Ariel Amir
Journal:  Elife       Date:  2019-02-18       Impact factor: 8.140

Review 8.  How to Build a Bacterial Cell: MreB as the Foreman of E. coli Construction.

Authors:  Handuo Shi; Benjamin P Bratton; Zemer Gitai; Kerwyn Casey Huang
Journal:  Cell       Date:  2018-03-08       Impact factor: 41.582

9.  Growth of curved and helical bacterial cells.

Authors:  Hongyuan Jiang; Sean X Sun
Journal:  Soft Matter       Date:  2012-07-28       Impact factor: 3.679

10.  Form equals function? Bacterial shape and its consequences for pathogenesis.

Authors:  Jonathan Dworkin
Journal:  Mol Microbiol       Date:  2010-11       Impact factor: 3.501

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