Literature DB >> 20444098

Cell wall synthesis is necessary for membrane dynamics during sporulation of Bacillus subtilis.

Pablo Meyer1, Jennifer Gutierrez, Kit Pogliano, Jonathan Dworkin.   

Abstract

During Bacillus subtilis sporulation, an endocytic-like process called engulfment results in one cell being entirely encased in the cytoplasm of another cell. The driving force underlying this process of membrane movement has remained unclear, although components of the machinery have been characterized. Here we provide evidence that synthesis of peptidoglycan, the rigid, strength bearing extracellular polymer of bacteria, is a key part of the missing force-generating mechanism for engulfment. We observed that sites of peptidoglycan synthesis initially coincide with the engulfing membrane and later with the site of engulfment membrane fission. Furthermore, compounds that block muropeptide synthesis or polymerization prevented membrane migration in cells lacking a component of the engulfment machinery (SpoIIQ), and blocked the membrane fission event at the completion of engulfment in all cells. In addition, these compounds inhibited bulge and vesicle formation that occur in spoIID mutant cells unable to initiate engulfment, as did genetic ablation of a protein that polymerizes muropeptides. This is the first report to our knowledge that peptidoglycan synthesis is necessary for membrane movements in bacterial cells and has implications for the mechanism of force generation during cytokinesis.

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Year:  2010        PMID: 20444098      PMCID: PMC2893020          DOI: 10.1111/j.1365-2958.2010.07155.x

Source DB:  PubMed          Journal:  Mol Microbiol        ISSN: 0950-382X            Impact factor:   3.501


  58 in total

1.  Buckling microtubules in vesicles.

Authors: 
Journal:  Phys Rev Lett       Date:  1996-05-20       Impact factor: 9.161

2.  A cytoskeleton-like role for the bacterial cell wall during engulfment of the Bacillus subtilis forespore.

Authors:  Angelica Abanes-De Mello; Ya-Lin Sun; Stefan Aung; Kit Pogliano
Journal:  Genes Dev       Date:  2002-12-15       Impact factor: 11.361

3.  Magnetosomes are cell membrane invaginations organized by the actin-like protein MamK.

Authors:  Arash Komeili; Zhuo Li; Dianne K Newman; Grant J Jensen
Journal:  Science       Date:  2005-12-22       Impact factor: 47.728

4.  Condensation of FtsZ filaments can drive bacterial cell division.

Authors:  Ganhui Lan; Brian R Daniels; Terrence M Dobrowsky; Denis Wirtz; Sean X Sun
Journal:  Proc Natl Acad Sci U S A       Date:  2008-12-30       Impact factor: 11.205

5.  Force generation by a dynamic Z-ring in Escherichia coli cell division.

Authors:  Jun F Allard; Eric N Cytrynbaum
Journal:  Proc Natl Acad Sci U S A       Date:  2008-12-29       Impact factor: 11.205

6.  Cell wall peptidoglycan architecture in Bacillus subtilis.

Authors:  Emma J Hayhurst; Lekshmi Kailas; Jamie K Hobbs; Simon J Foster
Journal:  Proc Natl Acad Sci U S A       Date:  2008-09-10       Impact factor: 11.205

7.  SpoIIB localizes to active sites of septal biogenesis and spatially regulates septal thinning during engulfment in bacillus subtilis.

Authors:  A R Perez; A Abanes-De Mello; K Pogliano
Journal:  J Bacteriol       Date:  2000-02       Impact factor: 3.490

8.  Analysis by fluorescence microscopy of the development of compartment-specific gene expression during sporulation of Bacillus subtilis.

Authors:  J E Bylund; L Zhang; M A Haines; M L Higgins; P J Piggot
Journal:  J Bacteriol       Date:  1994-05       Impact factor: 3.490

Review 9.  Force generation by microtubule assembly/disassembly in mitosis and related movements.

Authors:  S Inoué; E D Salmon
Journal:  Mol Biol Cell       Date:  1995-12       Impact factor: 4.138

10.  Thickness and elasticity of gram-negative murein sacculi measured by atomic force microscopy.

Authors:  X Yao; M Jericho; D Pink; T Beveridge
Journal:  J Bacteriol       Date:  1999-11       Impact factor: 3.490

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  38 in total

1.  Daptomycin-mediated reorganization of membrane architecture causes mislocalization of essential cell division proteins.

Authors:  Joe Pogliano; Nicolas Pogliano; Jared A Silverman
Journal:  J Bacteriol       Date:  2012-06-01       Impact factor: 3.490

2.  Bacterial outer membrane evolution via sporulation?

Authors:  Waldemar Vollmer
Journal:  Nat Chem Biol       Date:  2011-12-15       Impact factor: 15.040

3.  A LytM domain dictates the localization of proteins to the mother cell-forespore interface during bacterial endospore formation.

Authors:  Jeffrey Meisner; Charles P Moran
Journal:  J Bacteriol       Date:  2010-11-19       Impact factor: 3.490

4.  Mechanical consequences of cell-wall turnover in the elongation of a Gram-positive bacterium.

Authors:  Gaurav Misra; Enrique R Rojas; Ajay Gopinathan; Kerwyn Casey Huang
Journal:  Biophys J       Date:  2013-06-04       Impact factor: 4.033

5.  Peptidoglycan remodeling and conversion of an inner membrane into an outer membrane during sporulation.

Authors:  Elitza I Tocheva; Eric G Matson; Dylan M Morris; Farshid Moussavi; Jared R Leadbetter; Grant J Jensen
Journal:  Cell       Date:  2011-09-02       Impact factor: 41.582

Review 6.  Spore formation in Bacillus subtilis.

Authors:  Irene S Tan; Kumaran S Ramamurthi
Journal:  Environ Microbiol Rep       Date:  2013-12-17       Impact factor: 3.541

Review 7.  Illumination of growth, division and secretion by metabolic labeling of the bacterial cell surface.

Authors:  M Sloan Siegrist; Benjamin M Swarts; Douglas M Fox; Shion An Lim; Carolyn R Bertozzi
Journal:  FEMS Microbiol Rev       Date:  2015-01-23       Impact factor: 16.408

8.  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

9.  Contributions of turgor pressure, the contractile ring, and septum assembly to forces in cytokinesis in fission yeast.

Authors:  Stephen A Proctor; Nicolas Minc; Arezki Boudaoud; Fred Chang
Journal:  Curr Biol       Date:  2012-07-26       Impact factor: 10.834

10.  Peptidoglycan transformations during Bacillus subtilis sporulation.

Authors:  Elitza I Tocheva; Javier López-Garrido; H Velocity Hughes; Jennifer Fredlund; Erkin Kuru; Michael S Vannieuwenhze; Yves V Brun; Kit Pogliano; Grant J Jensen
Journal:  Mol Microbiol       Date:  2013-03-27       Impact factor: 3.501

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