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Peptidoglycan transformations during Bacillus subtilis sporulation

Tocheva, Elitza I. and López-Garrido, Javier and Hughes, H. Velocity and Fredlund, Jennifer and Kuru, Erkin and VanNieuwenhze, Michael S. and Brun, Yves V. and Pogliano, Kit and Jensen, Grant J. (2013) Peptidoglycan transformations during Bacillus subtilis sporulation. Molecular Microbiology, 88 (4). pp. 673-686. ISSN 0950-382X. PMCID PMC3893088. https://resolver.caltech.edu/CaltechAUTHORS:20130624-140301008

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Abstract

While vegetative Bacillus subtilis cells and mature spores are both surrounded by a thick layer of peptidoglycan (PG, a polymer of glycan strands crosslinked by peptide bridges), it has remained unclear whether PG surrounds prespores during engulfment. To clarify this issue, we generated a slender DponA mutant that enabled high-resolution electron cryotomographic imaging. Three-dimensional reconstructions of whole cells in near-native states revealed a thin PG-like layer extending from the lateral cell wall around the prespore throughout engulfment. Cryotomography of purified sacculi and fluorescent labelling of PG in live cells confirmed that PG surrounds the prespore. The presence of PG throughout engulfment suggests new roles for PG in sporulation, including a new model for how PG synthesis might drive engulfment, and obviates the need to synthesize a PG layer de novo during cortex formation. In addition, it reveals that B. subtilis can synthesize thin, Gram-negativelike PG layers as well as its thick, archetypal Grampositive cell wall. The continuous transformations from thick to thin and back to thick during sporulation suggest that both forms of PG have the same basic architecture (circumferential). Endopeptidase activity may be the main switch that governs whether a thin or a thick PG layer is assembled.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1111/mmi.12201PublisherArticle
http://onlinelibrary.wiley.com/doi/10.1111/mmi.12201/abstractDOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3893088PubMed CentralArticle
ORCID:
AuthorORCID
Tocheva, Elitza I.0000-0002-4869-8319
Jensen, Grant J.0000-0003-1556-4864
Additional Information:© 2013 John Wiley & Sons Ltd. First published online 27 March 2013. We thank Poochit Nonejuie for the construction of DponA B. subtilis mutant, and Dr Tim Baker and Norm Olsen for training J.F. in microscopy. This work was supported by the Howard Hughes Medical Foundation, gifts to Caltech from the Gordon and Betty Moore Foundation (to G.J.J.), GM57045 (to K.P.), AI059327 (to M.S.V.) and GM051986 (to Y.V.B.).
Funders:
Funding AgencyGrant Number
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Gordon and Betty Moore FoundationUNSPECIFIED
NIHGM57045
NIHAI059327
NIHGM051986
Issue or Number:4
PubMed Central ID:PMC3893088
Record Number:CaltechAUTHORS:20130624-140301008
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20130624-140301008
Official Citation:Tocheva, E. I., López-Garrido, J., Hughes, H. V., Fredlund, J., Kuru, E., VanNieuwenhze, M. S., Brun, Y. V., Pogliano, K. and Jensen, G. J. (2013), Peptidoglycan transformations during Bacillus subtilis sporulation. Molecular Microbiology, 88: 673–686. doi: 10.1111/mmi.12201
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:39055
Collection:CaltechAUTHORS
Deposited By: John Wade
Deposited On:24 Jun 2013 21:54
Last Modified:03 Oct 2019 05:03

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