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Chromosome choreography during the non-binary cell cycle of a predatory bacterium

In bacteria, the dynamics of chromosome replication and segregation are tightly coordinated with cell-cycle progression and largely rely on specific spatiotemporal arrangement of the chromosome. Whereas these key processes are mostly investigated in species that divide by binary fission, they remain...

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Autores principales: Kaljević, Jovana, Saaki, Terrens N.V., Govers, Sander K., Remy, Ophélie, van Raaphorst, Renske, Lamot, Thomas, Laloux, Géraldine
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cell Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8445325/
https://www.ncbi.nlm.nih.gov/pubmed/34256020
http://dx.doi.org/10.1016/j.cub.2021.06.024
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author Kaljević, Jovana
Saaki, Terrens N.V.
Govers, Sander K.
Remy, Ophélie
van Raaphorst, Renske
Lamot, Thomas
Laloux, Géraldine
author_facet Kaljević, Jovana
Saaki, Terrens N.V.
Govers, Sander K.
Remy, Ophélie
van Raaphorst, Renske
Lamot, Thomas
Laloux, Géraldine
author_sort Kaljević, Jovana
collection PubMed
description In bacteria, the dynamics of chromosome replication and segregation are tightly coordinated with cell-cycle progression and largely rely on specific spatiotemporal arrangement of the chromosome. Whereas these key processes are mostly investigated in species that divide by binary fission, they remain mysterious in bacteria producing larger number of descendants. Here, we establish the predatory bacterium Bdellovibrio bacteriovorus as a model to investigate the non-binary processing of a circular chromosome. We found that its single chromosome is highly compacted in a polarized nucleoid that excludes freely diffusing proteins during the non-proliferative stage of the cell cycle. A binary-like cycle of DNA replication and asymmetric segregation is followed by multiple asynchronous rounds of replication and progressive ParABS-dependent partitioning, uncoupled from cell division. Finally, we provide the first evidence for an on-off behavior of the ParB protein, which localizes at the centromere in a cell-cycle-regulated manner. Altogether, our findings support a model of complex chromosome choreography leading to the generation of variable, odd, or even numbers of offspring and highlight the adaptation of conserved mechanisms to achieve non-binary reproduction.
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spelling pubmed-84453252021-09-22 Chromosome choreography during the non-binary cell cycle of a predatory bacterium Kaljević, Jovana Saaki, Terrens N.V. Govers, Sander K. Remy, Ophélie van Raaphorst, Renske Lamot, Thomas Laloux, Géraldine Curr Biol Article In bacteria, the dynamics of chromosome replication and segregation are tightly coordinated with cell-cycle progression and largely rely on specific spatiotemporal arrangement of the chromosome. Whereas these key processes are mostly investigated in species that divide by binary fission, they remain mysterious in bacteria producing larger number of descendants. Here, we establish the predatory bacterium Bdellovibrio bacteriovorus as a model to investigate the non-binary processing of a circular chromosome. We found that its single chromosome is highly compacted in a polarized nucleoid that excludes freely diffusing proteins during the non-proliferative stage of the cell cycle. A binary-like cycle of DNA replication and asymmetric segregation is followed by multiple asynchronous rounds of replication and progressive ParABS-dependent partitioning, uncoupled from cell division. Finally, we provide the first evidence for an on-off behavior of the ParB protein, which localizes at the centromere in a cell-cycle-regulated manner. Altogether, our findings support a model of complex chromosome choreography leading to the generation of variable, odd, or even numbers of offspring and highlight the adaptation of conserved mechanisms to achieve non-binary reproduction. Cell Press 2021-09-13 /pmc/articles/PMC8445325/ /pubmed/34256020 http://dx.doi.org/10.1016/j.cub.2021.06.024 Text en © 2021 The Author(s) https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Article
Kaljević, Jovana
Saaki, Terrens N.V.
Govers, Sander K.
Remy, Ophélie
van Raaphorst, Renske
Lamot, Thomas
Laloux, Géraldine
Chromosome choreography during the non-binary cell cycle of a predatory bacterium
title Chromosome choreography during the non-binary cell cycle of a predatory bacterium
title_full Chromosome choreography during the non-binary cell cycle of a predatory bacterium
title_fullStr Chromosome choreography during the non-binary cell cycle of a predatory bacterium
title_full_unstemmed Chromosome choreography during the non-binary cell cycle of a predatory bacterium
title_short Chromosome choreography during the non-binary cell cycle of a predatory bacterium
title_sort chromosome choreography during the non-binary cell cycle of a predatory bacterium
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8445325/
https://www.ncbi.nlm.nih.gov/pubmed/34256020
http://dx.doi.org/10.1016/j.cub.2021.06.024
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