FtsEX-mediated regulation of the final stages of cell division reveals morphogenetic plasticity in Caulobacter crescentus

Meier, Elizabeth L. and Daitch, Allison K. and Yao, Qing and Bhargava, Anant and Jensen, Grant J. and Goley, Erin D. (2017) FtsEX-mediated regulation of the final stages of cell division reveals morphogenetic plasticity in Caulobacter crescentus. PLOS Genetics, 13 (9). Art. No. e1006999. ISSN 1553-7404. PMCID PMC5607218. https://resolver.caltech.edu/CaltechAUTHORS:20170918-095203888

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	Image (TIFF) (S1 Fig. In vivo LdpF-mCherry has a diffuse, patchy localization in WT and ΔftsE cells) - Supplemental Material Creative Commons Attribution. 1608Kb
	Image (TIFF) (S2 Fig. LdpF binds the extracellular loop (ECL) of FtsX but does not activate AmiC in vitro) - Supplemental Material Creative Commons Attribution. 508Kb
	Image (TIFF) (S3 Fig. Electron cryotomography (ECT) of cells lacking FtsE and AmiC reveal stalk-like connections of heterogeneous widths) - Supplemental Material Creative Commons Attribution. 2905Kb
	Image (TIFF) (S4 Fig. ftsE mutants incorporate new cell wall material throughout skinny connections between cell bodies) - Supplemental Material Creative Commons Attribution. 2867Kb
	Image (TIFF) (S5 Fig. Overproducing LdpF, the LytM domain (LytM) of LdpF or AmiC is not lytic in vivo) - Supplemental Material Creative Commons Attribution. 680Kb
	Image (TIFF) (S6 Fig. Treatment of WT or ΔftsE cells with 5 or 250 μM MP265 partially or completely arrests growth and delocalizes Venus-MreB) - Supplemental Material Creative Commons Attribution. 4Mb
	Image (TIFF) (S7 Fig. New PG synthesis localizes at the skinny connections in ΔftsE mutants and at cell poles in WT and ΔftsE mutants when MreB is inhibited) - Supplemental Material Creative Commons Attribution. 2646Kb
	Image (TIFF) (S8 Fig. Whole mount transmission electron microscopy (TEM) of MP265-treated WT or ΔftsE cells depleted for AmiC) - Supplemental Material Creative Commons Attribution. 4Mb
	MS Word (S1 Text. Supporting results and discussion describing biochemical investigation of cell wall hydrolase activities of LytM proteins and AmiC) - Supplemental Material Creative Commons Attribution. 23Kb
	MS Excel (S1 Table. Strains and plasmids used in this study with their methods of construction) - Supplemental Material Creative Commons Attribution. 43Kb

Use this Persistent URL to link to this item: https://resolver.caltech.edu/CaltechAUTHORS:20170918-095203888

Abstract

During its life cycle, Caulobacter crescentus undergoes a series of coordinated shape changes, including generation of a polar stalk and reshaping of the cell envelope to produce new daughter cells through the process of cytokinesis. The mechanisms by which these morphogenetic processes are coordinated in time and space remain largely unknown. Here we demonstrate that the conserved division complex FtsEX controls both the early and late stages of cytokinesis in C. crescentus, namely initiation of constriction and final cell separation. ΔftsE cells display a striking phenotype: cells are chained, with skinny connections between cell bodies resulting from defects in inner membrane fusion and cell separation. Surprisingly, the thin connections in ΔftsE cells share morphological and molecular features with C. crescentus stalks. Our data uncover unanticipated morphogenetic plasticity in C. crescentus, with loss of FtsE causing a stalk-like program to take over at failed division sites.

Item Type:

Article

Related URLs:

URL	URL Type	Description
https://doi.org/10.1371/journal.pgen.1006999	DOI	Article
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5607218/	PubMed Central	Article
https://doi.org/10.1371/journal.pgen.1006999.s001	DOI	S1 Fig.
https://doi.org/10.1371/journal.pgen.1006999.s002	DOI	S2 Fig.
https://doi.org/10.1371/journal.pgen.1006999.s003	DOI	S3 Fig.
https://doi.org/10.1371/journal.pgen.1006999.s004	DOI	S4 Fig.
https://doi.org/10.1371/journal.pgen.1006999.s005	DOI	S5 Fig.
https://doi.org/10.1371/journal.pgen.1006999.s006	DOI	S6 Fig.
https://doi.org/10.1371/journal.pgen.1006999.s007	DOI	S7 Fig.
https://doi.org/10.1371/journal.pgen.1006999.s008	DOI	S8 Fig.
https://doi.org/10.1371/journal.pgen.1006999.s009	DOI	S1 Text
https://doi.org/10.1371/journal.pgen.1006999.s010	DOI	S1 Table
https://doi.org/10.1101/124214	DOI	Discussion Paper

ORCID:

Author	ORCID
Yao, Qing	0000-0003-3575-9909
Jensen, Grant J.	0000-0003-1556-4864

Alternate Title:

FtsEX-Mediated Regulation Of Inner Membrane Fusion And Cell Separation Reveals Morphogenetic Plasticity In Caulobacter crescentus

Additional Information:

© 2017 Meier et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Received: April 5, 2017; Accepted: August 25, 2017; Published: September 8, 2017. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. This work was supported in part by the National Institute of General Medical Sciences through grant numbers R35 GM122588 (GJJ) and R01 GM108640 (EDG). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The authors have declared that no competing interests exist. We thank Jasmine Burrell for her work characterizing stalk protein localization in ΔftsE; Martin Thanbichler for sharing plasmids, strains and preliminary LdpF data; Yves Brun, Erkin Kuru, and Michael van Nieuwehnze for HADA; Kousik Sundararajan for assistance with TEM; Yves Brun and Ellen Quardokus for assistance with TEM and for sharing the StpX-CFP plasmid; and Zhuo Li for providing the wild-type stalks images in S3 Fig. Author Contributions: Conceptualization: Elizabeth L. Meier, Erin D. Goley. Formal analysis: Elizabeth L. Meier, Allison K. Daitch, Qing Yao, Anant Bhargava, Erin D. Goley. Funding acquisition: Grant J. Jensen, Erin D. Goley. Investigation: Elizabeth L. Meier, Allison K. Daitch, Qing Yao, Erin D. Goley. Methodology: Elizabeth L. Meier, Allison K. Daitch, Qing Yao, Anant Bhargava. Supervision: Grant J. Jensen, Erin D. Goley. Writing ± original draft: Elizabeth L. Meier. Writing ± review & editing: Elizabeth L. Meier, Allison K. Daitch, Qing Yao, Anant Bhargava, Grant J. Jensen, Erin D. Goley.

Funders:

Funding Agency	Grant Number
NIH	R35 GM122588
NIH	R01 GM108640

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PubMed Central ID:

PMC5607218

Record Number:

CaltechAUTHORS:20170918-095203888

Persistent URL:

https://resolver.caltech.edu/CaltechAUTHORS:20170918-095203888

Official Citation:

Meier EL, Daitch AK, Yao Q, Bhargava A, Jensen GJ, Goley ED (2017) FtsEX-mediated regulation of the final stages of cell division reveals morphogenetic plasticity in Caulobacter crescentus. PLoS Genet 13(9): e1006999. https://doi.org/10.1371/journal.pgen.1006999

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No commercial reproduction, distribution, display or performance rights in this work are provided.

ID Code:

81518

Collection:

CaltechAUTHORS

Deposited By:

Tony Diaz

Deposited On:

18 Sep 2017 17:33

Last Modified:

08 Oct 2019 20:54

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