Actin-like cytoskeleton filaments contribute to cell mechanics in bacteria

Wang, Siyuan; Arellano-Santoyo, Hugo; Combs, Peter A.; Shaevitz, Joshua W.

doi:10.1073/pnas.0911517107

Cited by 134 publications

(153 citation statements)

References 24 publications

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“…The material is characterized by several material constants, such as Young's modulus and Poisson's ratio. Indeed, this type of modeling of the cell wall was used previously, and the material constants have been measured for several bacterial cells (153,166,176). However, to fully explain the morphology of bacterial cells, these models have to be modified to include cell wall material growth and the dynamic turnover of PG material.…”

Section: Models Of Cell Growth and Cell Shapementioning

confidence: 99%

Physics of Bacterial Morphogenesis

Sun

Jiang

2011

Microbiol Mol Biol Rev

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SUMMARY Bacterial cells utilize three-dimensional (3D) protein assemblies to perform important cellular functions such as growth, division, chemoreception, and motility. These assemblies are composed of mechanoproteins that can mechanically deform and exert force. Sometimes, small-nucleotide hydrolysis is coupled to mechanical deformations. In this review, we describe the general principle for an understanding of the coupling of mechanics with chemistry in mechanochemical systems. We apply this principle to understand bacterial cell shape and morphogenesis and how mechanical forces can influence peptidoglycan cell wall growth. We review a model that can potentially reconcile the growth dynamics of the cell wall with the role of cytoskeletal proteins such as MreB and crescentin. We also review the application of mechanochemical principles to understand the assembly and constriction of the FtsZ ring. A number of potential mechanisms are proposed, and important questions are discussed.

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Section: Models Of Cell Growth and Cell Shapementioning

confidence: 99%

Physics of Bacterial Morphogenesis

Sun

Jiang

2011

Microbiol Mol Biol Rev

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“…How might MreB sense curvature? Given that MreB affects cellular stiffness (37), the mechanics of MreB polymers may enable robust curvature sensing, with the ATP hydrolysis state, length of the polymer, bundling of the polymer, and/or other binding partners such as RodZ (21), possibly imposing geometric preferences. Additionally, it is possible that MreB localization indirectly depends on curvature through its association with other cell wall-associated proteins.…”

Section: Discussionmentioning

confidence: 99%

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

Ursell

Nguyen

Monds

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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238

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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. Pulsechase 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.bacterial cytoskeleton | biophysical modeling | morphogenesis H ow cells maintain stable and defined morphologies is a fundamental question in all branches of life. Building cellularscale structures with the correct spatial architecture and mechanical properties requires that nanometer-scale proteins have the ability to detect and alter cell shape across multiple length scales. In walled organisms such as plants (1-5), fungi (6), and bacteria (7-10), morphogenesis is often achieved through an interplay between the cytoskeleton and cell wall synthesis. A central challenge in bacterial physiology is to understand the feedback between cell shape and the coordination of wall growth by the cytoskeleton.The cell wall plays a critical mechanical role in balancing turgor stress in virtually all bacteria and is both necessary and sufficient to define cell shape (11). The bacterial cell wall is a mesh-like network of sugar strands cross-linked by peptides (11,12). In rod-shaped Escherichia coli cells, cell wall growth occurs along the cylindrical body. Biophysical modeling has suggested that a random pattern of insertion cannot preserve cell shape (13), indicating that spatial coordination of the growth machinery is necessary for cell shape maintenance. Several lines of evidence demonstrate that the actin homolog MreB (14, 15) plays a major role in this coordination in most rod-shaped bacteria. The small molecule A22 depolymerizes MreB and causes a gradual transition from a rod-like to a spherical shape (15)(16)(17). This observation suggests that the disruption of MreB changes the patterning of new material insertion, although the nature of this...

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“…Strikingly, many rod-like bacteria elongate by expanding their cell envelope all along the cell envelope, as compared to growing from the tip only. These cells maintain their diameter even if cell division is inhibited and cell length reaches dozens of microns (Wang et al 2010).…”

Section: Introductionmentioning

confidence: 99%

Getting into shape: How do rod-like bacteria control their geometry?

Amir¹,

Teeffelen²

2014

Syst Synth Biol

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Rod-like bacteria maintain their cylindrical shapes with remarkable precision during growth. However, they are also capable to adapt their shapes to external forces and constraints, for example by growing into narrow or curved confinements. Despite being one of the simplest morphologies, we are still far from a full understanding of how shape is robustly regulated, and how bacteria obtain their near-perfect cylindrical shapes with excellent precision. However, recent experimental and theoretical findings suggest that cell-wall geometry and mechanical stress play important roles in regulating cell shape in rod-like bacteria. We review our current understanding of the cell wall architecture and the growth dynamics, and discuss possible candidates for regulatory cues of shape regulation in the absence or presence of external constraints. Finally, we suggest further future experimental and theoretical directions which may help to shed light on this fundamental problem.

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Actin-like cytoskeleton filaments contribute to cell mechanics in bacteria

Cited by 134 publications

References 24 publications

Physics of Bacterial Morphogenesis

Physics of Bacterial Morphogenesis

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

Getting into shape: How do rod-like bacteria control their geometry?

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