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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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[img] Image (TIFF) (S1 Fig. In vivo LdpF-mCherry has a diffuse, patchy localization in WT and ΔftsE cells) - Supplemental Material
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[img] Image (TIFF) (S2 Fig. LdpF binds the extracellular loop (ECL) of FtsX but does not activate AmiC in vitro) - Supplemental Material
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[img] Image (TIFF) (S3 Fig. Electron cryotomography (ECT) of cells lacking FtsE and AmiC reveal stalk-like connections of heterogeneous widths) - Supplemental Material
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[img] Image (TIFF) (S4 Fig. ftsE mutants incorporate new cell wall material throughout skinny connections between cell bodies) - Supplemental Material
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[img] Image (TIFF) (S5 Fig. Overproducing LdpF, the LytM domain (LytM) of LdpF or AmiC is not lytic in vivo) - Supplemental Material
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[img] 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
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[img] 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
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[img] Image (TIFF) (S8 Fig. Whole mount transmission electron microscopy (TEM) of MP265-treated WT or ΔftsE cells depleted for AmiC) - Supplemental Material
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[img] MS Word (S1 Text. Supporting results and discussion describing biochemical investigation of cell wall hydrolase activities of LytM proteins and AmiC) - Supplemental Material
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[img] MS Excel (S1 Table. Strains and plasmids used in this study with their methods of construction) - Supplemental Material
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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:
URLURL TypeDescription
https://doi.org/10.1371/journal.pgen.1006999DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5607218/PubMed CentralArticle
https://doi.org/10.1371/journal.pgen.1006999.s001DOIS1 Fig.
https://doi.org/10.1371/journal.pgen.1006999.s002DOIS2 Fig.
https://doi.org/10.1371/journal.pgen.1006999.s003DOIS3 Fig.
https://doi.org/10.1371/journal.pgen.1006999.s004DOIS4 Fig.
https://doi.org/10.1371/journal.pgen.1006999.s005DOIS5 Fig.
https://doi.org/10.1371/journal.pgen.1006999.s006DOIS6 Fig.
https://doi.org/10.1371/journal.pgen.1006999.s007DOIS7 Fig.
https://doi.org/10.1371/journal.pgen.1006999.s008DOIS8 Fig.
https://doi.org/10.1371/journal.pgen.1006999.s009DOIS1 Text
https://doi.org/10.1371/journal.pgen.1006999.s010DOIS1 Table
https://doi.org/10.1101/124214DOIDiscussion Paper
ORCID:
AuthorORCID
Yao, Qing0000-0003-3575-9909
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 AgencyGrant Number
NIHR35 GM122588
NIHR01 GM108640
Issue or Number:9
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
Usage Policy: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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