MreB filaments align along greatest principal membrane curvature to orient cell wall synthesis

Hussain, Saman; Wivagg, Carl N.; Szwedziak, Piotr; Wong, Felix; Schaefer, Kaitlin; Izoré, Thierry; Renner, Lars D.; Holmes, Matthew J; Sun, Yingjie; Bisson‐Filho, Alexandre W.; Walker, Suzanne; Amir, Ariel; Löwe, Jan; Garner, Ethan C.

doi:10.7554/elife.32471

Cited by 181 publications

(267 citation statements)

References 68 publications

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“…Organisms whose shape is maintained by MreB have been shown to achieve de novo rod morphogenesis by different strategies. Gradual cell thinning and elongation, discrete polar protrusion, and division prior to rod regeneration have all been observed in sphere-to-rod transition of such bacteria (Billings et al, 2014;Hussain et al, 2018;Ranjit et al, 2017;Takacs et al, 2010). Figure S5).…”

Section: Resultsmentioning

confidence: 93%

“…Despite our efforts to obtain a homogenous starting population of spheres, we noted that 5-20% of cells retain rod shape following enzymatic cell wall digestion or DivIVA depletion. Gradual cell thinning and elongation, discrete polar protrusion, and division prior to rod regeneration have all been observed in sphere-to-rod transition of such bacteria (Billings et al, 2014;Hussain et al, 2018;Ranjit et al, 2017;Takacs et al, 2010). In this scenario, the spherical state is irreversible, either because such cells are not viable or because they are unable to regain rod morphology.…”

Section: Resultsmentioning

confidence: 99%

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DivIVA concentrates mycobacterial cell envelope assembly for initiation and stabilization of polar growth

et al. 2018

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In many model organisms, diffuse patterning of cell wall peptidoglycan synthesis by the actin homolog MreB enables the bacteria to maintain their characteristic rod shape. In Caulobacter crescentus and Escherichia coli, MreB is also required to sculpt this morphology de novo. Mycobacteria are rod-shaped but expand their cell wall from discrete polar or subpolar zones. In this genus, the tropomyosin-like protein DivIVA is required for the maintenance of cell morphology. DivIVA has also been proposed to direct peptidoglycan synthesis to the tips of the mycobacterial cell. The precise nature of this regulation is unclear, as is its role in creating rod shape from scratch. We find that DivIVA localizes nascent cell wall and covalently associated mycomembrane but is dispensable for the assembly process itself. Mycobacterium smegmatis rendered spherical by peptidoglycan digestion or by DivIVA depletion are able to regain rod shape at the population level in the presence of DivIVA. At the single cell level, there is a close spatiotemporal correlation between DivIVA foci, rod extrusion and concentrated cell wall synthesis. Thus, although the precise mechanistic details differ from other organisms, M. smegmatis also establish and propagate rod shape by cytoskeleton-controlled patterning of peptidoglycan. Our data further support the emerging notion that morphology is a hardwired trait of bacterial cells.

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Section: Resultsmentioning

confidence: 93%

Section: Resultsmentioning

confidence: 99%

DivIVA concentrates mycobacterial cell envelope assembly for initiation and stabilization of polar growth

et al. 2018

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“…In many unicellular rodshaped bacteria, such as in the model organisms Escherichia coli and Bacillus subtilis, the cell wall expands by the incorporation of new PG along the length of the cell 12,13 . This lateral elongation is guided by highly curved MreB filaments along the cell circumference [14][15][16][17] . In contrast, other bacteria, including actinobacteria and Agrobacterium species, grow by polar cell wall elongation, which is independent of MreB 18,19 .…”

Section: Introductionmentioning

confidence: 99%

Teichoic acids anchor distinct cell wall lamellae in an apically growing bacterium

Ultee

Aart

Dissel

et al. 2019

Preprint

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The bacterial cell wall is a dynamic, multicomponent structure that provides structural support for cell shape and physical protection from the environment. In monoderm species, the thick cell wall is made up predominantly of peptidoglycan, teichoic acids and a variety of capsular glycans. Filamentous monoderm Actinobacteria, such as Streptomyces coelicolor, incorporate new cell wall material at the apex of their hyphal cells during growth. In this study we use cryo-electron tomography to reveal the structural architecture of the cell wall of this bacterium. Our data shows a density difference between the apex and subapical regions of chemically isolated sacculi. Removal of the teichoic acids with hydrofluoric acid reveals a rough and patchy cell wall and distinct lamellae in a number of sacculi. Absence of the extracellular glycans poly-β-1,6-N-acetylglucosamine and a cellulose-like polymer, produced by the MatAB and CslA proteins respectively, results in a thinner sacculus and absence of lamellae and patches. Extracellular glycans might thus form or lead to the formation of the outer cell wall lamella. Based on these findings we propose a revisited model for the complex cell wall architecture of an apically growing bacterium, in which the network of peptidoglycan together with extracellular polymers is structurally supported by teichoic acids. " 1 " 2 " 13

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“…Proteins such as α -synuclein (Pranke et al, 2011), Opi1 (Hofbauer et al, 2018), and ArfGAP1 (Drin et al, 2007) employ this mechanism to sense curvature. Interestingly, known micrometer-scale curvature sensors including SpoVM (Ramamurthi et al, 2009), MreB (Ursell et al, 2014;Hussain et al, 2018) contain AHs.…”

Section: Introductionmentioning

confidence: 99%

An amphipathic helix enables septins to sense micron-scale membrane curvature

Cannon

Woods

Crutchley

et al. 2018

Preprint

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The geometry of cells is well described by membrane curvature. Septins are filament forming, GTP-binding proteins that assemble on positive, micrometer-scale curvatures. Here, we examine the molecular basis of curvature sensing by septins. We show that differences in affinity and the number of binding sites drive curvature-specific adsorption of septins. Moreover, we find septin assembly onto curved membranes is cooperative and show that geometry influences higher-order arrangement of septin filaments. Although septins must form polymers to stay associated with membranes, septin filaments do not have to span micrometers in length to sense curvature, as we find that single septin complexes have curvature-dependent association rates.We trace this ability to an amphipathic helix (AH) located on the C-terminus of Cdc12. The AH domain is necessary and sufficient for curvature sensing both in vitro and in vivo. These data show that curvature sensing by septins operates at much smaller length scales than the micrometer curvatures being detected. We thank the Gladfelter lab and Danny Lew for useful discussions, Matthias Garten for ideas in setting up the rod assay, the UNC EM facility (Victoria Madden and Kristen White) for support with SEM and HHMI Faculty Scholars award to ASG. Author contributionsKSC, BLW conducted experiments, BLW and JMC constructed strains for experiments, BLW and JMC constructed plasmids for experiments, KSC, BLW, and ASG designed experiments.

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MreB filaments align along greatest principal membrane curvature to orient cell wall synthesis

Cited by 181 publications

References 68 publications

DivIVA concentrates mycobacterial cell envelope assembly for initiation and stabilization of polar growth

DivIVA concentrates mycobacterial cell envelope assembly for initiation and stabilization of polar growth

Teichoic acids anchor distinct cell wall lamellae in an apically growing bacterium

An amphipathic helix enables septins to sense micron-scale membrane curvature

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