Literature DB >> 21501250

Mechanisms for maintaining cell shape in rod-shaped Gram-negative bacteria.

Leon Furchtgott1, Ned S Wingreen, Kerwyn Casey Huang.   

Abstract

For the rod-shaped Gram-negative bacterium Escherichia coli, changes in cell shape have critical consequences for motility, immune system evasion, proliferation and adhesion. For most bacteria, the peptidoglycan cell wall is both necessary and sufficient to determine cell shape. However, how the synthesis machinery assembles a peptidoglycan network with a robustly maintained micron-scale shape has remained elusive. To explore shape maintenance, we have quantified the robustness of cell shape in three Gram-negative bacteria in different genetic backgrounds and in the presence of an antibiotic that inhibits division. Building on previous modelling suggesting a prominent role for mechanical forces in shape regulation, we introduce a biophysical model for the growth dynamics of rod-shaped cells to investigate the roles of spatial regulation of peptidoglycan synthesis, glycan-strand biochemistry and mechanical stretching during insertion. Our studies reveal that rod-shape maintenance requires insertion to be insensitive to fluctuations in cell-wall density and stress, and even a simple helical pattern of insertion is sufficient for over sixfold elongation without significant loss in shape. In addition, we demonstrate that both the length and pre-stretching of newly inserted strands regulate cell width. In sum, we show that simple physical rules can allow bacteria to achieve robust, shape-preserving cell-wall growth.
© 2011 Blackwell Publishing Ltd.

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Year:  2011        PMID: 21501250      PMCID: PMC3134142          DOI: 10.1111/j.1365-2958.2011.07616.x

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


  42 in total

1.  Peptidoglycan crosslinking relaxation promotes Helicobacter pylori's helical shape and stomach colonization.

Authors:  Laura K Sycuro; Zachary Pincus; Kimberley D Gutierrez; Jacob Biboy; Chelsea A Stern; Waldemar Vollmer; Nina R Salama
Journal:  Cell       Date:  2010-05-28       Impact factor: 41.582

2.  The MreB and Min cytoskeletal-like systems play independent roles in prokaryotic polar differentiation.

Authors:  Yu-Ling Shih; Ikuro Kawagishi; Lawrence Rothfield
Journal:  Mol Microbiol       Date:  2005-11       Impact factor: 3.501

3.  Mechanical properties of Bacillus subtilis cell walls: effects of removing residual culture medium.

Authors:  J J Thwaites; U C Surana
Journal:  J Bacteriol       Date:  1991-01       Impact factor: 3.490

4.  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

5.  Biophysical characterization of changes in amounts and activity of Escherichia coli cell and compartment water and turgor pressure in response to osmotic stress.

Authors:  D S Cayley; H J Guttman; M T Record
Journal:  Biophys J       Date:  2000-04       Impact factor: 4.033

Review 6.  Bacterial shape: two-dimensional questions and possibilities.

Authors:  Kevin D Young
Journal:  Annu Rev Microbiol       Date:  2010       Impact factor: 15.500

7.  Alterations of murein structure and of penicillin-binding proteins in minicells from Escherichia coli.

Authors:  W Obermann; J V Höltje
Journal:  Microbiology       Date:  1994-01       Impact factor: 2.777

8.  Isolation and separation of the glycan strands from murein of Escherichia coli by reversed-phase high-performance liquid chromatography.

Authors:  H Harz; K Burgdorf; J V Höltje
Journal:  Anal Biochem       Date:  1990-10       Impact factor: 3.365

9.  FtsZ directs a second mode of peptidoglycan synthesis in Escherichia coli.

Authors:  Archana Varma; Miguel A de Pedro; Kevin D Young
Journal:  J Bacteriol       Date:  2007-05-18       Impact factor: 3.490

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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  54 in total

1.  Rotate into shape: MreB and bacterial morphogenesis.

Authors:  Sven van Teeffelen; Zemer Gitai
Journal:  EMBO J       Date:  2011-12-14       Impact factor: 11.598

2.  Helical insertion of peptidoglycan produces chiral ordering of the bacterial cell wall.

Authors:  Siyuan Wang; Leon Furchtgott; Kerwyn Casey Huang; Joshua W Shaevitz
Journal:  Proc Natl Acad Sci U S A       Date:  2012-02-17       Impact factor: 11.205

3.  Dislocation-mediated growth of bacterial cell walls.

Authors:  Ariel Amir; David R Nelson
Journal:  Proc Natl Acad Sci U S A       Date:  2012-06-01       Impact factor: 11.205

4.  RodZ links MreB to cell wall synthesis to mediate MreB rotation and robust morphogenesis.

Authors:  Randy M Morgenstein; Benjamin P Bratton; Jeffrey P Nguyen; Nikolay Ouzounov; Joshua W Shaevitz; Zemer Gitai
Journal:  Proc Natl Acad Sci U S A       Date:  2015-09-22       Impact factor: 11.205

5.  The fission yeast cytokinetic contractile ring regulates septum shape and closure.

Authors:  Sathish Thiyagarajan; Emilia Laura Munteanu; Rajesh Arasada; Thomas D Pollard; Ben O'Shaughnessy
Journal:  J Cell Sci       Date:  2015-08-03       Impact factor: 5.285

6.  Mechanisms of bacterial morphogenesis: evolutionary cell biology approaches provide new insights.

Authors:  Chao Jiang; Paul D Caccamo; Yves V Brun
Journal:  Bioessays       Date:  2015-02-09       Impact factor: 4.345

7.  Elasticity and biochemistry of growth relate replication rate to cell length and cross-link density in rod-shaped bacteria.

Authors:  Akeisha M T Belgrave; Charles W Wolgemuth
Journal:  Biophys J       Date:  2013-06-18       Impact factor: 4.033

8.  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

9.  A microfluidic platform for profiling biomechanical properties of bacteria.

Authors:  Xuanhao Sun; William D Weinlandt; Harsh Patel; Mingming Wu; Christopher J Hernandez
Journal:  Lab Chip       Date:  2014-07-21       Impact factor: 6.799

10.  Distribution of mechanical stress in the Escherichia coli cell envelope.

Authors:  Hyea Hwang; Nicolò Paracini; Jerry M Parks; Jeremy H Lakey; James C Gumbart
Journal:  Biochim Biophys Acta Biomembr       Date:  2018-09-29       Impact factor: 3.747

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