Chiral twisting in a bacterial cytoskeletal polymer affects filament size and orientation

Shi, Handuo; Quint, David; Grason, Gregory M.; Gopinathan, Ajay; Huang, Kerwyn Casey

doi:10.1038/s41467-020-14752-9

Cited by 33 publications

(25 citation statements)

References 59 publications

(80 reference statements)

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“…Molecular dynamics simulations have shown that the twist of MreB double protofilaments can be reduced by membrane binding. The moderated dynamics of MreB filaments resulted in shorter filaments, and possibly provides tuning to their flexibilty and length 44 . The untwisted antiparallel structure of pairs of protofilaments can allow bending of the MreB filaments, which may stabilize the curvature of a membrane 44 .…”

Section: Discussionmentioning

confidence: 99%

“…The moderated dynamics of MreB filaments resulted in shorter filaments, and possibly provides tuning to their flexibilty and length 44 . The untwisted antiparallel structure of pairs of protofilaments can allow bending of the MreB filaments, which may stabilize the curvature of a membrane 44 . High calcium concentrations 45 , near a membrane, may induce longer persistence lengths in MreB polymers.…”

Section: Discussionmentioning

confidence: 99%

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Intracellular ion concentrations and cation-dependent remodelling of bacterial MreB assemblies

Szatmári

Sárkány

Kocsis

et al. 2020

Sci Rep

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Here, we measured the concentrations of several ions in cultivated Gram-negative and Gram-positive bacteria, and analyzed their effects on polymer formation by the actin homologue MreB. We measured potassium, sodium, chloride, calcium and magnesium ion concentrations in Leptospira interrogans, Bacillus subtilis and Escherichia coli. Intracellular ionic strength contributed from these ions varied within the 130–273 mM range. The intracellular sodium ion concentration range was between 122 and 296 mM and the potassium ion concentration range was 5 and 38 mM. However, the levels were significantly influenced by extracellular ion levels. L. interrogans, Rickettsia rickettsii and E. coli MreBs were heterologously expressed and purified from E. coli using a novel filtration method to prepare MreB polymers. The structures and stability of Alexa-488 labeled MreB polymers, under varying ionic strength conditions, were investigated by confocal microscopy and MreB polymerization rates were assessed by measuring light scattering. MreB polymerization was fastest in the presence of monovalent cations in the 200–300 mM range. MreB filaments showed high stability in this concentration range and formed large assemblies of tape-like bundles that transformed to extensive sheets at higher ionic strengths. Changing the calcium concentration from 0.2 to 0 mM and then to 2 mM initialized rapid remodelling of MreB polymers.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Intracellular ion concentrations and cation-dependent remodelling of bacterial MreB assemblies

Szatmári

Sárkány

Kocsis

et al. 2020

Sci Rep

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“…In the rod-shaped bacterium Escherichia coli, left-handed chirality of the MreB cytoskeleton (a bacterial F-actin-like polymer) guides local insertion of wall material into the peptidoglycan network, and causes cells to twist in a left-handed helix during elongation growth [69]. Molecular dynamics simulations for MreB in Caulobacter crescentus, another rod-shaped bacterium, suggest MreB double protofilaments can exhibit left-handed twisting and induce a stable membrane curvature when bound to the membrane [70]. Chiral arrangements of polar cytoskeletons underneath the cell-enclosing membrane may provide a common paradigm for helical growth in cylindrical plant cells and rod-shaped bacteria.…”

Section: Discussionmentioning

confidence: 99%

Mechanistic Insights into Plant Chiral Growth

Nakamura

Hashimoto

2020

Symmetry

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The latent left–right asymmetry (chirality) of vascular plants is best witnessed as a helical elongation of cylindrical organs in climbing plants. Interestingly, helical handedness is usually fixed in given species, suggesting genetic control of chirality. Arabidopsis thaliana, a small mustard plant, normally does not twist but can be mutated to exhibit helical growth in elongating organs. Genetic, molecular and cell biological analyses of these twisting mutants are providing mechanistic insights into the left–right handedness as well as how potential organ skewing is suppressed in most plants. Growth direction of elongating plant cells is determined by alignment of cellulose microfibrils in cell walls, which is guided by cortical microtubules localized just beneath the plasma membrane. Mutations in tubulins and regulators of microtubule assembly or organization give rise to helical arrangements of cortical microtubule arrays in Arabidopsis cells and cause helical growth of fixed handedness in axial organs such as roots and stems. Whether tubulins are assembled into a microtubule composed of straight or tilted protofilaments might determine straight or twisting growth. Mechanistic understanding of helical plant growth will provide a paradigm for connecting protein filament structure to cellular organization.

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“…On the other hand, as in most rod-shaped bacteria, M. xanthus MreB plays conserved roles in PG assembly. As MreB filaments are intrinsically curved, and bind to the cytoplasmic membranes, the balance between filament bending and membrane deformation can lead MreB filaments to localize at inwardly curved regions [ 31 , 74 , 75 , 76 , 77 , 78 ]. This localization preference, in turn, affects the localization and dynamics of Rod complexes, which could be sufficient for the maintenance of rod shape [ 31 , 32 , 33 , 71 , 76 , 79 , 80 ].…”

Section: Perspectivesmentioning

confidence: 99%

Myxococcus xanthus as a Model Organism for Peptidoglycan Assembly and Bacterial Morphogenesis

2021

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A fundamental question in biology is how cell shapes are genetically encoded and enzymatically generated. Prevalent shapes among walled bacteria include spheres and rods. These shapes are chiefly determined by the peptidoglycan (PG) cell wall. Bacterial division results in two daughter cells, whose shapes are predetermined by the mother. This makes it difficult to explore the origin of cell shapes in healthy bacteria. In this review, we argue that the Gram-negative bacterium Myxococcus xanthus is an ideal model for understanding PG assembly and bacterial morphogenesis, because it forms rods and spheres at different life stages. Rod-shaped vegetative cells of M. xanthus can thoroughly degrade their PG and form spherical spores. As these spores germinate, cells rebuild their PG and reestablish rod shape without preexisting templates. Such a unique sphere-to-rod transition provides a rare opportunity to visualize de novo PG assembly and rod-like morphogenesis in a well-established model organism.

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Chiral twisting in a bacterial cytoskeletal polymer affects filament size and orientation

Cited by 33 publications

References 59 publications

Intracellular ion concentrations and cation-dependent remodelling of bacterial MreB assemblies

Intracellular ion concentrations and cation-dependent remodelling of bacterial MreB assemblies

Mechanistic Insights into Plant Chiral Growth

Myxococcus xanthus as a Model Organism for Peptidoglycan Assembly and Bacterial Morphogenesis

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