Novel Divisome-Associated Protein Spatially Coupling the Z-Ring with the Chromosomal Replication Terminus in <named-content content-type="genus-species">Caulobacter crescentus</named-content>

ABSTRACT Cell division requires proper spatial coordination with the chromosome, which undergoes dynamic changes during chromosome replication and segregation. FtsZ is a bacterial cytoskeletal protein that assembles into the Z-ring, providing a platform to build the cell division apparatus. In the m...

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Autores principales:	Shogo Ozaki, Urs Jenal, Tsutomu Katayama
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Caulobacter crescentus cell division chromosome organization chromosome segregation subcellular localization Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d08156d931294c3287febc6b17138ae0
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spelling	oai:doaj.org-article:d08156d931294c3287febc6b17138ae02021-11-15T15:57:02ZNovel Divisome-Associated Protein Spatially Coupling the Z-Ring with the Chromosomal Replication Terminus in <named-content content-type="genus-species">Caulobacter crescentus</named-content>10.1128/mBio.00487-202150-7511https://doaj.org/article/d08156d931294c3287febc6b17138ae02020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00487-20https://doaj.org/toc/2150-7511ABSTRACT Cell division requires proper spatial coordination with the chromosome, which undergoes dynamic changes during chromosome replication and segregation. FtsZ is a bacterial cytoskeletal protein that assembles into the Z-ring, providing a platform to build the cell division apparatus. In the model bacterium Caulobacter crescentus, the cellular localization of the Z-ring is controlled during the cell cycle in a chromosome replication-coupled manner. Although dynamic localization of the Z-ring at midcell is driven primarily by the replication origin-associated FtsZ inhibitor MipZ, the mechanism ensuring accurate positioning of the Z-ring remains unclear. In this study, we showed that the Z-ring colocalizes with the replication terminus region, located opposite the origin, throughout most of the C. crescentus cell cycle. Spatial organization of the two is mediated by ZapT, a previously uncharacterized protein that interacts with the terminus region and associates with ZapA and ZauP, both of which are part of the incipient division apparatus. While the Z-ring and the terminus region coincided with the presence of ZapT, colocalization of the two was perturbed in cells lacking zapT, which is accompanied by delayed midcellular positioning of the Z-ring. Moreover, cells overexpressing ZapT showed compromised positioning of the Z-ring and MipZ. These findings underscore the important role of ZapT in controlling cell division processes. We propose that ZapT acts as a molecular bridge that physically links the terminus region to the Z-ring, thereby ensuring accurate site selection for the Z-ring. Because ZapT is conserved in proteobacteria, these findings may define a general mechanism coordinating cell division with chromosome organization. IMPORTANCE Growing bacteria require careful tuning of cell division processes with dynamic organization of replicating chromosomes. In enteric bacteria, ZapA associates with the cytoskeletal Z-ring and establishes a physical linkage to the chromosomal replication terminus through its interaction with ZapB-MatP-DNA complexes. However, because ZapB and MatP are found only in enteric bacteria, it remains unclear how the Z-ring and the terminus are coordinated in the vast majority of bacteria. Here, we provide evidence that a novel conserved protein, termed ZapT, mediates colocalization of the Z-ring with the terminus in Caulobacter crescentus, a model organism that is phylogenetically distant from enteric bacteria. Given that ZapT facilitates cell division processes in C. crescentus, this study highlights the universal importance of the physical linkage between the Z-ring and the terminus in maintaining cell integrity.Shogo OzakiUrs JenalTsutomu KatayamaAmerican Society for MicrobiologyarticleCaulobacter crescentuscell divisionchromosome organizationchromosome segregationsubcellular localizationMicrobiologyQR1-502ENmBio, Vol 11, Iss 2 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Caulobacter crescentus cell division chromosome organization chromosome segregation subcellular localization Microbiology QR1-502
spellingShingle	Caulobacter crescentus cell division chromosome organization chromosome segregation subcellular localization Microbiology QR1-502 Shogo Ozaki Urs Jenal Tsutomu Katayama Novel Divisome-Associated Protein Spatially Coupling the Z-Ring with the Chromosomal Replication Terminus in <named-content content-type="genus-species">Caulobacter crescentus</named-content>
description	ABSTRACT Cell division requires proper spatial coordination with the chromosome, which undergoes dynamic changes during chromosome replication and segregation. FtsZ is a bacterial cytoskeletal protein that assembles into the Z-ring, providing a platform to build the cell division apparatus. In the model bacterium Caulobacter crescentus, the cellular localization of the Z-ring is controlled during the cell cycle in a chromosome replication-coupled manner. Although dynamic localization of the Z-ring at midcell is driven primarily by the replication origin-associated FtsZ inhibitor MipZ, the mechanism ensuring accurate positioning of the Z-ring remains unclear. In this study, we showed that the Z-ring colocalizes with the replication terminus region, located opposite the origin, throughout most of the C. crescentus cell cycle. Spatial organization of the two is mediated by ZapT, a previously uncharacterized protein that interacts with the terminus region and associates with ZapA and ZauP, both of which are part of the incipient division apparatus. While the Z-ring and the terminus region coincided with the presence of ZapT, colocalization of the two was perturbed in cells lacking zapT, which is accompanied by delayed midcellular positioning of the Z-ring. Moreover, cells overexpressing ZapT showed compromised positioning of the Z-ring and MipZ. These findings underscore the important role of ZapT in controlling cell division processes. We propose that ZapT acts as a molecular bridge that physically links the terminus region to the Z-ring, thereby ensuring accurate site selection for the Z-ring. Because ZapT is conserved in proteobacteria, these findings may define a general mechanism coordinating cell division with chromosome organization. IMPORTANCE Growing bacteria require careful tuning of cell division processes with dynamic organization of replicating chromosomes. In enteric bacteria, ZapA associates with the cytoskeletal Z-ring and establishes a physical linkage to the chromosomal replication terminus through its interaction with ZapB-MatP-DNA complexes. However, because ZapB and MatP are found only in enteric bacteria, it remains unclear how the Z-ring and the terminus are coordinated in the vast majority of bacteria. Here, we provide evidence that a novel conserved protein, termed ZapT, mediates colocalization of the Z-ring with the terminus in Caulobacter crescentus, a model organism that is phylogenetically distant from enteric bacteria. Given that ZapT facilitates cell division processes in C. crescentus, this study highlights the universal importance of the physical linkage between the Z-ring and the terminus in maintaining cell integrity.
format	article
author	Shogo Ozaki Urs Jenal Tsutomu Katayama
author_facet	Shogo Ozaki Urs Jenal Tsutomu Katayama
author_sort	Shogo Ozaki
title	Novel Divisome-Associated Protein Spatially Coupling the Z-Ring with the Chromosomal Replication Terminus in <named-content content-type="genus-species">Caulobacter crescentus</named-content>
title_short	Novel Divisome-Associated Protein Spatially Coupling the Z-Ring with the Chromosomal Replication Terminus in <named-content content-type="genus-species">Caulobacter crescentus</named-content>
title_full	Novel Divisome-Associated Protein Spatially Coupling the Z-Ring with the Chromosomal Replication Terminus in <named-content content-type="genus-species">Caulobacter crescentus</named-content>
title_fullStr	Novel Divisome-Associated Protein Spatially Coupling the Z-Ring with the Chromosomal Replication Terminus in <named-content content-type="genus-species">Caulobacter crescentus</named-content>
title_full_unstemmed	Novel Divisome-Associated Protein Spatially Coupling the Z-Ring with the Chromosomal Replication Terminus in <named-content content-type="genus-species">Caulobacter crescentus</named-content>
title_sort	novel divisome-associated protein spatially coupling the z-ring with the chromosomal replication terminus in <named-content content-type="genus-species">caulobacter crescentus</named-content>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/d08156d931294c3287febc6b17138ae0
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Novel Divisome-Associated Protein Spatially Coupling the Z-Ring with the Chromosomal Replication Terminus in <named-content content-type="genus-species">Caulobacter crescentus</named-content>

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