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Mid-cell migration of the chromosomal terminus is coupled to origin segregation in Escherichia coli

Bacterial chromosomes are dynamically and spatially organised within cells. In slow-growing Escherichia coli, the chromosomal terminus is initially located at the new pole and must therefore migrate to midcell during replication to reproduce the same pattern in the daughter cells. Here, we use high-...

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Autores principales: Sadhir, Ismath, Murray, Seán M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10657355/
https://www.ncbi.nlm.nih.gov/pubmed/37980336
http://dx.doi.org/10.1038/s41467-023-43351-7
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author Sadhir, Ismath
Murray, Seán M.
author_facet Sadhir, Ismath
Murray, Seán M.
author_sort Sadhir, Ismath
collection PubMed
description Bacterial chromosomes are dynamically and spatially organised within cells. In slow-growing Escherichia coli, the chromosomal terminus is initially located at the new pole and must therefore migrate to midcell during replication to reproduce the same pattern in the daughter cells. Here, we use high-throughput time-lapse microscopy to quantify this transition, its timing and its relationship to chromosome segregation. We find that terminus centralisation is a rapid discrete event that occurs ~25 min after initial separation of duplicated origins and ~50 min before the onset of bulk nucleoid segregation but with substantial variation between cells. Despite this variation, its movement is tightly coincident with the completion of origin segregation, even in the absence of its linkage to the divisome, suggesting a coupling between these two events. Indeed, we find that terminus centralisation does not occur if origin segregation away from mid-cell is disrupted, which results in daughter cells having an inverted chromosome organisation. Overall, our study quantifies the choreography of origin-terminus positioning and identifies an unexplored connection between these loci, furthering our understanding of chromosome segregation in this bacterium.
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spelling pubmed-106573552023-11-18 Mid-cell migration of the chromosomal terminus is coupled to origin segregation in Escherichia coli Sadhir, Ismath Murray, Seán M. Nat Commun Article Bacterial chromosomes are dynamically and spatially organised within cells. In slow-growing Escherichia coli, the chromosomal terminus is initially located at the new pole and must therefore migrate to midcell during replication to reproduce the same pattern in the daughter cells. Here, we use high-throughput time-lapse microscopy to quantify this transition, its timing and its relationship to chromosome segregation. We find that terminus centralisation is a rapid discrete event that occurs ~25 min after initial separation of duplicated origins and ~50 min before the onset of bulk nucleoid segregation but with substantial variation between cells. Despite this variation, its movement is tightly coincident with the completion of origin segregation, even in the absence of its linkage to the divisome, suggesting a coupling between these two events. Indeed, we find that terminus centralisation does not occur if origin segregation away from mid-cell is disrupted, which results in daughter cells having an inverted chromosome organisation. Overall, our study quantifies the choreography of origin-terminus positioning and identifies an unexplored connection between these loci, furthering our understanding of chromosome segregation in this bacterium. Nature Publishing Group UK 2023-11-18 /pmc/articles/PMC10657355/ /pubmed/37980336 http://dx.doi.org/10.1038/s41467-023-43351-7 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Sadhir, Ismath
Murray, Seán M.
Mid-cell migration of the chromosomal terminus is coupled to origin segregation in Escherichia coli
title Mid-cell migration of the chromosomal terminus is coupled to origin segregation in Escherichia coli
title_full Mid-cell migration of the chromosomal terminus is coupled to origin segregation in Escherichia coli
title_fullStr Mid-cell migration of the chromosomal terminus is coupled to origin segregation in Escherichia coli
title_full_unstemmed Mid-cell migration of the chromosomal terminus is coupled to origin segregation in Escherichia coli
title_short Mid-cell migration of the chromosomal terminus is coupled to origin segregation in Escherichia coli
title_sort mid-cell migration of the chromosomal terminus is coupled to origin segregation in escherichia coli
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10657355/
https://www.ncbi.nlm.nih.gov/pubmed/37980336
http://dx.doi.org/10.1038/s41467-023-43351-7
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