Bacterial cell curvature through mechanical control of cell growth.
Journal: 2009/May - EMBO Journal
ISSN: 1460-2075
Abstract:
The cytoskeleton is a key regulator of cell morphogenesis. Crescentin, a bacterial intermediate filament-like protein, is required for the curved shape of Caulobacter crescentus and localizes to the inner cell curvature. Here, we show that crescentin forms a single filamentous structure that collapses into a helix when detached from the cell membrane, suggesting that it is normally maintained in a stretched configuration. Crescentin causes an elongation rate gradient around the circumference of the sidewall, creating a longitudinal cell length differential and hence curvature. Such curvature can be produced by physical force alone when cells are grown in circular microchambers. Production of crescentin in Escherichia coli is sufficient to generate cell curvature. Our data argue for a model in which physical strain borne by the crescentin structure anisotropically alters the kinetics of cell wall insertion to produce curved growth. Our study suggests that bacteria may use the cytoskeleton for mechanical control of growth to alter morphology.
Relations:
Content
Citations
(72)
References
(67)
Chemicals
(2)
Organisms
(2)
Processes
(2)
Anatomy
(1)
Affiliates
(1)
Similar articles
Articles by the same authors
Discussion board
EMBO J 28(9): 1208-1219

Bacterial cell curvature through mechanical control of cell growth

Supplementary Material

Supplementary Movie 1

Supplementary Movie 2

Supplementary Movie 3

Supplementary Information

Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT, USA
Institute for Cell and Molecular Biosciences, Medical School, Newcastle University, Newcastle upon Tyne, UK
Department of Cell and Molecular Biology, Uppsala University, Uppsala, Sweden
Department of Biochemistry, University of Wisconsin-Madison, Madison, WI, USA
Section of Microbial Pathogenesis, Yale School of Medicine, New Haven, CT, USA
Howard Hughes Medical Institute, Yale University, New Haven, CT, USA
Department of Molecular, Cellular, and Developmental Biology, Yale University, KBT 1032, PO Box 208103, New Haven, CT 06520, USA. Tel.: +203 432 5170; Fax: +203 432 9960; E-mail: ude.elay@rengaw-sbocaj.enitsirhc
Received 2008 Oct 25; Accepted 2009 Feb 13.

Abstract

The cytoskeleton is a key regulator of cell morphogenesis. Crescentin, a bacterial intermediate filament-like protein, is required for the curved shape of Caulobacter crescentus and localizes to the inner cell curvature. Here, we show that crescentin forms a single filamentous structure that collapses into a helix when detached from the cell membrane, suggesting that it is normally maintained in a stretched configuration. Crescentin causes an elongation rate gradient around the circumference of the sidewall, creating a longitudinal cell length differential and hence curvature. Such curvature can be produced by physical force alone when cells are grown in circular microchambers. Production of crescentin in Escherichia coli is sufficient to generate cell curvature. Our data argue for a model in which physical strain borne by the crescentin structure anisotropically alters the kinetics of cell wall insertion to produce curved growth. Our study suggests that bacteria may use the cytoskeleton for mechanical control of growth to alter morphology.

Keywords: bacterial cell morphogenesis, cell curvature, crescentin, cytoskeleton, peptidoglycan
Abstract
Click here to view.(878K, mov)Click here to view.(6.9M, mov)Click here to view.(885K, mov)Click here to view.(304K, pdf)

Acknowledgments

We thank O Sliusarenko and T Emonet for help with the automated cell shape analysis and for helpful discussions; Z Jiang for help with the SEM; G Ebersbach for advice about E. coli experiments; J Beckwith for the pBAD vectors; H Schwarz for help with transmission EM; E Dufresne for helpful discussions; and the Jacobs-Wagner laboratory for critical reading of the manuscript. MTC was supported by the NSF GRFP and the Mustard Seed Foundation. This work was supported by the European Commission (LSHM-CT-2004-512138 to WV), the German Research Council DFG (FOR449 to WV), the Searle Scholars Program (to DW), 3M Corporation National (DW), the National Institutes of Health ({"type":"entrez-nucleotide","attrs":{"text":"GM076698","term_id":"221361742","term_text":"GM076698"}}GM076698 to CJ-W) and the Pew Charitable Trusts (to CJ-W). Author contributions: MTC, GC, NA, CJ-W designed research; MTC, WV, PB, DBW performed experiments; MTC, WV, CJ-W analysed the data; MTC and CJ-W wrote the paper.

Acknowledgments
Collaboration tool especially designed for Life Science professionals.Drag-and-drop any entity to your messages.