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Mutations in the Lipopolysaccharide Biosynthesis Pathway Interfere with Crescentin-Mediated Cell Curvature in Caulobacter crescentus

Cabeen, Matthew T. and Murolo, Michelle A. and Briegel, Ariane and Bui, N. Khai and Vollmer, Waldemar and Ausmees, Nora and Jensen, Grant J. and Jacobs-Wagner, Christine (2010) Mutations in the Lipopolysaccharide Biosynthesis Pathway Interfere with Crescentin-Mediated Cell Curvature in Caulobacter crescentus. Journal of Bacteriology, 192 (13). pp. 3368-3378. ISSN 0021-9193. PMCID PMC2897673. https://resolver.caltech.edu/CaltechAUTHORS:20110804-135325381

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Abstract

Bacterial cell morphogenesis requires coordination among multiple cellular systems, including the bacterial cytoskeleton and the cell wall. In the vibrioid bacterium Caulobacter crescentus, the intermediate filament-like protein crescentin forms a cell envelope-associated cytoskeletal structure that controls cell wall growth to generate cell curvature. We undertook a genetic screen to find other cellular components important for cell curvature. Here we report that deletion of a gene (wbqL) involved in the lipopolysaccharide (LPS) biosynthesis pathway abolishes cell curvature. Loss of WbqL function leads to the accumulation of an aberrant Opolysaccharide species and to the release of the S layer in the culture medium. Epistasis and microscopy experiments show that neither S-layer nor O-polysaccharide production is required for curved cell morphology per se but that production of the altered O-polysaccharide species abolishes cell curvature by apparently interfering with the ability of the crescentin structure to associate with the cell envelope. Our data suggest that perturbations in a cellular pathway that is itself fully dispensable for cell curvature can cause a disruption of cell morphogenesis, highlighting the delicate harmony among unrelated cellular systems. Using the wbqL mutant, we also show that the normal assembly and growth properties of the crescentin structure are independent of its association with the cell envelope. However, this envelope association is important for facilitating the local disruption of the stable crescentin structure at the division site during cytokinesis.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1128/JB.01371-09 DOIArticle
http://jb.asm.org/cgi/content/abstract/192/13/3368PublisherArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2897673/PubMed CentralArticle
ORCID:
AuthorORCID
Briegel, Ariane0000-0003-3733-3725
Jensen, Grant J.0000-0003-1556-4864
Additional Information:© 2010 American Society for Microbiology. Received 19 October 2009; Accepted 20 April 2010. Published ahead of print on 30 April 2010. We thank J. Smit for gifts of strains, anti-O-polysaccharide, and anti-RsaA antibodies, O. Sliusarenko and T. Emonet for assistance with cell curvature analysis, H. Lam for plasmids, J. Wertz for technical help, and the members of the Jacobs-Wagner laboratory for critical reading of the manuscript. This work was supported by the National Science Foundation GRFP (to M.T.C.), the Mustard Seed Foundation (to M.T.C.), a Howard Hughes Medical Institute predoctoral fellowship (to M.A.M.), NIH grants AI067548 (to G.J.J.) and GM076698 (to C.J.-W.), gifts to Caltech from the Gordon and Betty Moore Foundation and Agouron Institute, the Pew Scholars Program in the Biological Sciences, sponsored by the Pew Charitable Trust (to C.J.-W.), and the HEALTHF3-2009-223431 DIVINOCELL collaborative project grant from the Commission of the European Communities (to W.V.). C.J.-W. and G.J.J. are Howard Hughes Medical Institute investigators.
Funders:
Funding AgencyGrant Number
NSFUNSPECIFIED
Mustard Seed FoundationUNSPECIFIED
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
NIHAI067548
NIHGM076698
Pew Charitable TrustUNSPECIFIED
European CommissionHEALTH-F3-2009-223431
Gordon and Betty Moore FoundationUNSPECIFIED
Agouron InstituteUNSPECIFIED
Issue or Number:13
PubMed Central ID:PMC2897673
Record Number:CaltechAUTHORS:20110804-135325381
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20110804-135325381
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:24692
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:04 Aug 2011 21:34
Last Modified:03 Oct 2019 02:59

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