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Simulations of Proposed Mechanisms of FtsZ-Driven Cell Constriction

To divide, bacteria must constrict their membranes against significant force from turgor pressure. A tubulin homolog, FtsZ, is thought to drive constriction, but how FtsZ filaments might generate constrictive force in the absence of motor proteins is not well understood. There are two predominant mo...

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Detalles Bibliográficos
Autores principales: Nguyen, Lam T., Oikonomou, Catherine M., Jensen, Grant J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7811198/
https://www.ncbi.nlm.nih.gov/pubmed/33199285
http://dx.doi.org/10.1128/JB.00576-20
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author Nguyen, Lam T.
Oikonomou, Catherine M.
Jensen, Grant J.
author_facet Nguyen, Lam T.
Oikonomou, Catherine M.
Jensen, Grant J.
author_sort Nguyen, Lam T.
collection PubMed
description To divide, bacteria must constrict their membranes against significant force from turgor pressure. A tubulin homolog, FtsZ, is thought to drive constriction, but how FtsZ filaments might generate constrictive force in the absence of motor proteins is not well understood. There are two predominant models in the field. In one, FtsZ filaments overlap to form complete rings around the circumference of the cell, and attractive forces cause filaments to slide past each other to maximize lateral contact. In the other, filaments exert force on the membrane by a GTP-hydrolysis-induced switch in conformation from straight to bent. Here, we developed software, ZCONSTRICT, for quantitative three-dimensional (3D) simulations of Gram-negative bacterial cell division to test these two models and identify critical conditions required for them to work. We find that the avidity of any kind of lateral interactions quickly halts the sliding of filaments, so a mechanism such as depolymerization or treadmilling is required to sustain constriction by filament sliding. For filament bending, we find that a mechanism such as the presence of a rigid linker is required to constrain bending to within the division plane and maintain the distance observed in vivo between the filaments and the membrane. Of these two models, only the filament bending model is consistent with our lab’s recent observation of constriction associated with a single, short FtsZ filament. IMPORTANCE FtsZ is thought to generate constrictive force to divide the cell, possibly via one of two predominant models in the field. In one, FtsZ filaments overlap to form complete rings which constrict as filaments slide past each other to maximize lateral contact. In the other, filaments exert force on the membrane by switching conformation from straight to bent. Here, we developed software, ZCONSTRICT, for three-dimensional (3D) simulations to test these two models. We find that a mechanism such as depolymerization or treadmilling are required to sustain constriction by filament sliding. For filament bending, we find that a mechanism that constrains bending to within the division plane is required to maintain the distance observed in vivo between the filaments and the membrane.
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spelling pubmed-78111982021-02-05 Simulations of Proposed Mechanisms of FtsZ-Driven Cell Constriction Nguyen, Lam T. Oikonomou, Catherine M. Jensen, Grant J. J Bacteriol Research Article To divide, bacteria must constrict their membranes against significant force from turgor pressure. A tubulin homolog, FtsZ, is thought to drive constriction, but how FtsZ filaments might generate constrictive force in the absence of motor proteins is not well understood. There are two predominant models in the field. In one, FtsZ filaments overlap to form complete rings around the circumference of the cell, and attractive forces cause filaments to slide past each other to maximize lateral contact. In the other, filaments exert force on the membrane by a GTP-hydrolysis-induced switch in conformation from straight to bent. Here, we developed software, ZCONSTRICT, for quantitative three-dimensional (3D) simulations of Gram-negative bacterial cell division to test these two models and identify critical conditions required for them to work. We find that the avidity of any kind of lateral interactions quickly halts the sliding of filaments, so a mechanism such as depolymerization or treadmilling is required to sustain constriction by filament sliding. For filament bending, we find that a mechanism such as the presence of a rigid linker is required to constrain bending to within the division plane and maintain the distance observed in vivo between the filaments and the membrane. Of these two models, only the filament bending model is consistent with our lab’s recent observation of constriction associated with a single, short FtsZ filament. IMPORTANCE FtsZ is thought to generate constrictive force to divide the cell, possibly via one of two predominant models in the field. In one, FtsZ filaments overlap to form complete rings which constrict as filaments slide past each other to maximize lateral contact. In the other, filaments exert force on the membrane by switching conformation from straight to bent. Here, we developed software, ZCONSTRICT, for three-dimensional (3D) simulations to test these two models. We find that a mechanism such as depolymerization or treadmilling are required to sustain constriction by filament sliding. For filament bending, we find that a mechanism that constrains bending to within the division plane is required to maintain the distance observed in vivo between the filaments and the membrane. American Society for Microbiology 2021-01-11 /pmc/articles/PMC7811198/ /pubmed/33199285 http://dx.doi.org/10.1128/JB.00576-20 Text en Copyright © 2021 Nguyen et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Nguyen, Lam T.
Oikonomou, Catherine M.
Jensen, Grant J.
Simulations of Proposed Mechanisms of FtsZ-Driven Cell Constriction
title Simulations of Proposed Mechanisms of FtsZ-Driven Cell Constriction
title_full Simulations of Proposed Mechanisms of FtsZ-Driven Cell Constriction
title_fullStr Simulations of Proposed Mechanisms of FtsZ-Driven Cell Constriction
title_full_unstemmed Simulations of Proposed Mechanisms of FtsZ-Driven Cell Constriction
title_short Simulations of Proposed Mechanisms of FtsZ-Driven Cell Constriction
title_sort simulations of proposed mechanisms of ftsz-driven cell constriction
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7811198/
https://www.ncbi.nlm.nih.gov/pubmed/33199285
http://dx.doi.org/10.1128/JB.00576-20
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