Literature DB >> 24550515

Rod-like bacterial shape is maintained by feedback between cell curvature and cytoskeletal localization.

Tristan S Ursell1, Jeffrey Nguyen, Russell D Monds, Alexandre Colavin, Gabriel Billings, Nikolay Ouzounov, Zemer Gitai, Joshua W Shaevitz, Kerwyn Casey Huang.   

Abstract

Cells typically maintain characteristic shapes, but the mechanisms of self-organization for robust morphological maintenance remain unclear in most systems. Precise regulation of rod-like shape in Escherichia coli cells requires the MreB actin-like cytoskeleton, but the mechanism by which MreB maintains rod-like shape is unknown. Here, we use time-lapse and 3D imaging coupled with computational analysis to map the growth, geometry, and cytoskeletal organization of single bacterial cells at subcellular resolution. Our results demonstrate that feedback between cell geometry and MreB localization maintains rod-like cell shape by targeting cell wall growth to regions of negative cell wall curvature. Pulse-chase labeling indicates that growth is heterogeneous and correlates spatially and temporally with MreB localization, whereas MreB inhibition results in more homogeneous growth, including growth in polar regions previously thought to be inert. Biophysical simulations establish that curvature feedback on the localization of cell wall growth is an effective mechanism for cell straightening and suggest that surface deformations caused by cell wall insertion could direct circumferential motion of MreB. Our work shows that MreB orchestrates persistent, heterogeneous growth at the subcellular scale, enabling robust, uniform growth at the cellular scale without requiring global organization.

Entities:  

Keywords:  bacterial cytoskeleton; biophysical modeling; morphogenesis

Mesh:

Substances:

Year:  2014        PMID: 24550515      PMCID: PMC3964057          DOI: 10.1073/pnas.1317174111

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  40 in total

1.  Dynamic movement of actin-like proteins within bacterial cells.

Authors:  Hervé Joël Defeu Soufo; Peter L Graumann
Journal:  EMBO Rep       Date:  2004-07-23       Impact factor: 8.807

2.  Controlling the shape of filamentous cells of Escherichia coli.

Authors:  Shoji Takeuchi; Willow R DiLuzio; Douglas B Weibel; George M Whitesides
Journal:  Nano Lett       Date:  2005-09       Impact factor: 11.189

Review 3.  Microtubule cortical array organization and plant cell morphogenesis.

Authors:  Alex Paradez; Amanda Wright; David W Ehrhardt
Journal:  Curr Opin Plant Biol       Date:  2006-09-28       Impact factor: 7.834

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.  The bacterial actin MreB rotates, and rotation depends on cell-wall assembly.

Authors:  Sven van Teeffelen; Siyuan Wang; Leon Furchtgott; Kerwyn Casey Huang; Ned S Wingreen; Joshua W Shaevitz; Zemer Gitai
Journal:  Proc Natl Acad Sci U S A       Date:  2011-09-08       Impact factor: 11.205

Review 6.  The cytoskeleton in plant and fungal cell tip growth.

Authors:  A Geitmann; A M Emons
Journal:  J Microsc       Date:  2000-06       Impact factor: 1.758

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

Authors:  Leon Furchtgott; Ned S Wingreen; Kerwyn Casey Huang
Journal:  Mol Microbiol       Date:  2011-04-18       Impact factor: 3.501

8.  Resistance to beta-lactam antibiotics by re-modelling the active site of an E. coli penicillin-binding protein.

Authors:  P J Hedge; B G Spratt
Journal:  Nature       Date:  1985 Dec 5-11       Impact factor: 49.962

9.  A22 disrupts the bacterial actin cytoskeleton by directly binding and inducing a low-affinity state in MreB.

Authors:  G J Bean; S T Flickinger; W M Westler; M E McCully; D Sept; D B Weibel; K J Amann
Journal:  Biochemistry       Date:  2009-06-09       Impact factor: 3.162

10.  A curvature-mediated mechanism for localization of lipids to bacterial poles.

Authors:  Kerwyn Casey Huang; Ranjan Mukhopadhyay; Ned S Wingreen
Journal:  PLoS Comput Biol       Date:  2006-10-04       Impact factor: 4.475

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  113 in total

1.  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

2.  High-throughput, Highly Sensitive Analyses of Bacterial Morphogenesis Using Ultra Performance Liquid Chromatography.

Authors:  Samantha M Desmarais; Carolina Tropini; Amanda Miguel; Felipe Cava; Russell D Monds; Miguel A de Pedro; Kerwyn Casey Huang
Journal:  J Biol Chem       Date:  2015-10-14       Impact factor: 5.157

3.  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

Review 4.  Bacterial protein networks: properties and functions.

Authors:  Athanasios Typas; Victor Sourjik
Journal:  Nat Rev Microbiol       Date:  2015-08-10       Impact factor: 60.633

5.  Defining the rate-limiting processes of bacterial cytokinesis.

Authors:  Carla Coltharp; Jackson Buss; Trevor M Plumer; Jie Xiao
Journal:  Proc Natl Acad Sci U S A       Date:  2016-02-01       Impact factor: 11.205

Review 6.  Bacterial Filament Systems: Toward Understanding Their Emergent Behavior and Cellular Functions.

Authors:  Ye-Jin Eun; Mrinal Kapoor; Saman Hussain; Ethan C Garner
Journal:  J Biol Chem       Date:  2015-05-08       Impact factor: 5.157

7.  A Periplasmic Polymer Curves Vibrio cholerae and Promotes Pathogenesis.

Authors:  Thomas M Bartlett; Benjamin P Bratton; Amit Duvshani; Amanda Miguel; Ying Sheng; Nicholas R Martin; Jeffrey P Nguyen; Alexandre Persat; Samantha M Desmarais; Michael S VanNieuwenhze; Kerwyn Casey Huang; Jun Zhu; Joshua W Shaevitz; Zemer Gitai
Journal:  Cell       Date:  2017-01-12       Impact factor: 41.582

8.  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

Review 9.  The Unsolved Problem of How Cells Sense Micron-Scale Curvature.

Authors:  Kevin S Cannon; Benjamin L Woods; Amy S Gladfelter
Journal:  Trends Biochem Sci       Date:  2017-10-28       Impact factor: 13.807

10.  Depletion of Undecaprenyl Pyrophosphate Phosphatases Disrupts Cell Envelope Biogenesis in Bacillus subtilis.

Authors:  Heng Zhao; Yingjie Sun; Jason M Peters; Carol A Gross; Ethan C Garner; John D Helmann
Journal:  J Bacteriol       Date:  2016-10-07       Impact factor: 3.490

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