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Biomolecular condensate drives polymerization and bundling of the bacterial tubulin FtsZ to regulate cell division

Cell division is spatiotemporally precisely regulated, but the underlying mechanisms are incompletely understood. In the social bacterium Myxococcus xanthus, the PomX/PomY/PomZ proteins form a single megadalton-sized complex that directly positions and stimulates cytokinetic ring formation by the tu...

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Autores principales: Ramm, Beatrice, Schumacher, Dominik, Harms, Andrea, Heermann, Tamara, Klos, Philipp, Müller, Franziska, Schwille, Petra, Søgaard-Andersen, Lotte
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10307791/
https://www.ncbi.nlm.nih.gov/pubmed/37380708
http://dx.doi.org/10.1038/s41467-023-39513-2
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author Ramm, Beatrice
Schumacher, Dominik
Harms, Andrea
Heermann, Tamara
Klos, Philipp
Müller, Franziska
Schwille, Petra
Søgaard-Andersen, Lotte
author_facet Ramm, Beatrice
Schumacher, Dominik
Harms, Andrea
Heermann, Tamara
Klos, Philipp
Müller, Franziska
Schwille, Petra
Søgaard-Andersen, Lotte
author_sort Ramm, Beatrice
collection PubMed
description Cell division is spatiotemporally precisely regulated, but the underlying mechanisms are incompletely understood. In the social bacterium Myxococcus xanthus, the PomX/PomY/PomZ proteins form a single megadalton-sized complex that directly positions and stimulates cytokinetic ring formation by the tubulin homolog FtsZ. Here, we study the structure and mechanism of this complex in vitro and in vivo. We demonstrate that PomY forms liquid-like biomolecular condensates by phase separation, while PomX self-assembles into filaments generating a single large cellular structure. The PomX structure enriches PomY, thereby guaranteeing the formation of precisely one PomY condensate per cell through surface-assisted condensation. In vitro, PomY condensates selectively enrich FtsZ and nucleate GTP-dependent FtsZ polymerization and bundle FtsZ filaments, suggesting a cell division site positioning mechanism in which the single PomY condensate enriches FtsZ to guide FtsZ-ring formation and division. This mechanism shares features with microtubule nucleation by biomolecular condensates in eukaryotes, supporting this mechanism’s ancient origin.
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spelling pubmed-103077912023-06-30 Biomolecular condensate drives polymerization and bundling of the bacterial tubulin FtsZ to regulate cell division Ramm, Beatrice Schumacher, Dominik Harms, Andrea Heermann, Tamara Klos, Philipp Müller, Franziska Schwille, Petra Søgaard-Andersen, Lotte Nat Commun Article Cell division is spatiotemporally precisely regulated, but the underlying mechanisms are incompletely understood. In the social bacterium Myxococcus xanthus, the PomX/PomY/PomZ proteins form a single megadalton-sized complex that directly positions and stimulates cytokinetic ring formation by the tubulin homolog FtsZ. Here, we study the structure and mechanism of this complex in vitro and in vivo. We demonstrate that PomY forms liquid-like biomolecular condensates by phase separation, while PomX self-assembles into filaments generating a single large cellular structure. The PomX structure enriches PomY, thereby guaranteeing the formation of precisely one PomY condensate per cell through surface-assisted condensation. In vitro, PomY condensates selectively enrich FtsZ and nucleate GTP-dependent FtsZ polymerization and bundle FtsZ filaments, suggesting a cell division site positioning mechanism in which the single PomY condensate enriches FtsZ to guide FtsZ-ring formation and division. This mechanism shares features with microtubule nucleation by biomolecular condensates in eukaryotes, supporting this mechanism’s ancient origin. Nature Publishing Group UK 2023-06-28 /pmc/articles/PMC10307791/ /pubmed/37380708 http://dx.doi.org/10.1038/s41467-023-39513-2 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Ramm, Beatrice
Schumacher, Dominik
Harms, Andrea
Heermann, Tamara
Klos, Philipp
Müller, Franziska
Schwille, Petra
Søgaard-Andersen, Lotte
Biomolecular condensate drives polymerization and bundling of the bacterial tubulin FtsZ to regulate cell division
title Biomolecular condensate drives polymerization and bundling of the bacterial tubulin FtsZ to regulate cell division
title_full Biomolecular condensate drives polymerization and bundling of the bacterial tubulin FtsZ to regulate cell division
title_fullStr Biomolecular condensate drives polymerization and bundling of the bacterial tubulin FtsZ to regulate cell division
title_full_unstemmed Biomolecular condensate drives polymerization and bundling of the bacterial tubulin FtsZ to regulate cell division
title_short Biomolecular condensate drives polymerization and bundling of the bacterial tubulin FtsZ to regulate cell division
title_sort biomolecular condensate drives polymerization and bundling of the bacterial tubulin ftsz to regulate cell division
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10307791/
https://www.ncbi.nlm.nih.gov/pubmed/37380708
http://dx.doi.org/10.1038/s41467-023-39513-2
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