Literature DB >> 29425492

Chromosome Translocation Inflates Bacillus Forespores and Impacts Cellular Morphology.

Javier Lopez-Garrido1, Nikola Ojkic2, Kanika Khanna1, Felix R Wagner1, Elizabeth Villa1, Robert G Endres3, Kit Pogliano4.   

Abstract

The means by which the physicochemical properties of different cellular components together determine bacterial cell shape remain poorly understood. Here, we investigate a programmed cell-shape change during Bacillus subtilis sporulation, when a rod-shaped vegetative cell is transformed to an ovoid spore. Asymmetric cell division generates a bigger mother cell and a smaller, hemispherical forespore. The septum traps the forespore chromosome, which is translocated to the forespore by SpoIIIE. Simultaneously, forespore size increases as it is reshaped into an ovoid. Using genetics, timelapse microscopy, cryo-electron tomography, and mathematical modeling, we demonstrate that forespore growth relies on membrane synthesis and SpoIIIE-mediated chromosome translocation, but not on peptidoglycan or protein synthesis. Our data suggest that the hydrated nucleoid swells and inflates the forespore, displacing ribosomes to the cell periphery, stretching septal peptidoglycan, and reshaping the forespore. Our results illustrate how simple biophysical interactions between core cellular components contribute to cellular morphology.
Copyright © 2018 Elsevier Inc. All rights reserved.

Entities:  

Keywords:  Bacillus subtilis; Gibbs/Donnan effect; Langevin simulations; SpoIIIE; cell shape; cell size; chromosome translocation; cryo-electron tomography; sporulation; turgor pressure

Mesh:

Substances:

Year:  2018        PMID: 29425492      PMCID: PMC6370482          DOI: 10.1016/j.cell.2018.01.027

Source DB:  PubMed          Journal:  Cell        ISSN: 0092-8674            Impact factor:   41.582


  64 in total

1.  A vital stain for studying membrane dynamics in bacteria: a novel mechanism controlling septation during Bacillus subtilis sporulation.

Authors:  J Pogliano; N Osborne; M D Sharp; A Abanes-De Mello; A Perez; Y L Sun; K Pogliano
Journal:  Mol Microbiol       Date:  1999-02       Impact factor: 3.501

2.  Dynamic SpoIIIE assembly mediates septal membrane fission during Bacillus subtilis sporulation.

Authors:  Tinya C Fleming; Jae Yen Shin; Sang-Hyuk Lee; Eric Becker; Kerwyn Casey Huang; Carlos Bustamante; Kit Pogliano
Journal:  Genes Dev       Date:  2010-06-01       Impact factor: 11.361

3.  Cell-specific SpoIIIE assembly and DNA translocation polarity are dictated by chromosome orientation.

Authors:  Eric C Becker; Kit Pogliano
Journal:  Mol Microbiol       Date:  2007-12       Impact factor: 3.501

4.  Dual-axis tomography: an approach with alignment methods that preserve resolution.

Authors:  D N Mastronarde
Journal:  J Struct Biol       Date:  1997-12       Impact factor: 2.867

5.  The persistence length of DNA is reached from the persistence length of its null isomer through an internal electrostatic stretching force.

Authors:  Gerald S Manning
Journal:  Biophys J       Date:  2006-08-25       Impact factor: 4.033

6.  Physical and functional characterization of the Bacillus subtilis spoIIM gene.

Authors:  K Smith; M E Bayer; P Youngman
Journal:  J Bacteriol       Date:  1993-06       Impact factor: 3.490

Review 7.  Recent progress in Bacillus subtilis sporulation.

Authors:  Douglas Higgins; Jonathan Dworkin
Journal:  FEMS Microbiol Rev       Date:  2011-10-25       Impact factor: 16.408

8.  Response of Escherichia coli growth rate to osmotic shock.

Authors:  Enrique Rojas; Julie A Theriot; Kerwyn Casey Huang
Journal:  Proc Natl Acad Sci U S A       Date:  2014-05-12       Impact factor: 11.205

9.  Visualization and functional dissection of coaxial paired SpoIIIE channels across the sporulation septum.

Authors:  Jae Yen Shin; Javier Lopez-Garrido; Sang-Hyuk Lee; Cesar Diaz-Celis; Tinya Fleming; Carlos Bustamante; Kit Pogliano
Journal:  Elife       Date:  2015-05-07       Impact factor: 8.140

10.  Two-subunit DNA escort mechanism and inactive subunit bypass in an ultra-fast ring ATPase.

Authors:  Ninning Liu; Gheorghe Chistol; Carlos Bustamante
Journal:  Elife       Date:  2015-10-09       Impact factor: 8.140

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  18 in total

1.  A Roadblock-and-Kill Mechanism of Action Model for the DNA-Targeting Antibiotic Ciprofloxacin.

Authors:  Nikola Ojkic; Elin Lilja; Susana Direito; Angela Dawson; Rosalind J Allen; Bartlomiej Waclaw
Journal:  Antimicrob Agents Chemother       Date:  2020-08-20       Impact factor: 5.191

2.  Shaping an Endospore: Architectural Transformations During Bacillus subtilis Sporulation.

Authors:  Kanika Khanna; Javier Lopez-Garrido; Kit Pogliano
Journal:  Annu Rev Microbiol       Date:  2020-07-13       Impact factor: 15.500

3.  Differential requirements for conserved peptidoglycan remodeling enzymes during Clostridioides difficile spore formation.

Authors:  John W Ribis; Kelly A Fimlaid; Aimee Shen
Journal:  Mol Microbiol       Date:  2018-11       Impact factor: 3.501

4.  Spatiotemporally regulated proteolysis to dissect the role of vegetative proteins during Bacillus subtilis sporulation: cell-specific requirement of σH and σA.

Authors:  Eammon P Riley; Aude Trinquier; Madeline L Reilly; Marine Durchon; Varahenage R Perera; Kit Pogliano; Javier Lopez-Garrido
Journal:  Mol Microbiol       Date:  2018-02-12       Impact factor: 3.501

Review 5.  Bacterial Vivisection: How Fluorescence-Based Imaging Techniques Shed a Light on the Inner Workings of Bacteria.

Authors:  Alexander Cambré; Abram Aertsen
Journal:  Microbiol Mol Biol Rev       Date:  2020-10-28       Impact factor: 11.056

6.  Preparing samples from whole cells using focused-ion-beam milling for cryo-electron tomography.

Authors:  Felix R Wagner; Reika Watanabe; Ruud Schampers; Digvijay Singh; Hans Persoon; Miroslava Schaffer; Peter Fruhstorfer; Jürgen Plitzko; Elizabeth Villa
Journal:  Nat Protoc       Date:  2020-05-13       Impact factor: 13.491

Review 7.  To Feed or to Stick? Genomic Analysis Offers Clues for the Role of a Molecular Machine in Endospore Formers.

Authors:  Patrick Stragier
Journal:  J Bacteriol       Date:  2022-08-01       Impact factor: 3.476

8.  Antibiotic Resistance via Bacterial Cell Shape-Shifting.

Authors:  Nikola Ojkic; Diana Serbanescu; Shiladitya Banerjee
Journal:  mBio       Date:  2022-05-26       Impact factor: 7.786

9.  Chromosome Segregation and Peptidoglycan Remodeling Are Coordinated at a Highly Stabilized Septal Pore to Maintain Bacterial Spore Development.

Authors:  Ahmed M T Mohamed; Helena Chan; Johana Luhur; Elda Bauda; Benoit Gallet; Cécile Morlot; Louise Cole; Milena Awad; Simon Crawford; Dena Lyras; David Z Rudner; Christopher D A Rodrigues
Journal:  Dev Cell       Date:  2020-12-30       Impact factor: 12.270

10.  Practical Approaches for Cryo-FIB Milling and Applications for Cellular Cryo-Electron Tomography.

Authors:  Vinson Lam; Elizabeth Villa
Journal:  Methods Mol Biol       Date:  2021
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