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Chromosome organization by a conserved condensin-ParB system in the actinobacterium Corynebacterium glutamicum

Higher-order chromosome folding and segregation are tightly regulated in all domains of life. In bacteria, details on nucleoid organization regulatory mechanisms and function remain poorly characterized, especially in non-model species. Here, we investigate the role of DNA-partitioning protein ParB...

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Autores principales: Böhm, Kati, Giacomelli, Giacomo, Schmidt, Andreas, Imhof, Axel, Koszul, Romain, Marbouty, Martial, Bramkamp, Marc
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7083940/
https://www.ncbi.nlm.nih.gov/pubmed/32198399
http://dx.doi.org/10.1038/s41467-020-15238-4
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author Böhm, Kati
Giacomelli, Giacomo
Schmidt, Andreas
Imhof, Axel
Koszul, Romain
Marbouty, Martial
Bramkamp, Marc
author_facet Böhm, Kati
Giacomelli, Giacomo
Schmidt, Andreas
Imhof, Axel
Koszul, Romain
Marbouty, Martial
Bramkamp, Marc
author_sort Böhm, Kati
collection PubMed
description Higher-order chromosome folding and segregation are tightly regulated in all domains of life. In bacteria, details on nucleoid organization regulatory mechanisms and function remain poorly characterized, especially in non-model species. Here, we investigate the role of DNA-partitioning protein ParB and SMC condensin complexes in the actinobacterium Corynebacterium glutamicum. Chromosome conformation capture reveals SMC-mediated long-range interactions around ten centromere-like parS sites clustered at the replication origin (oriC). At least one oriC-proximal parS site is necessary for reliable chromosome segregation. We use chromatin immunoprecipitation and photoactivated single-molecule localization microscopy to show the formation of distinct, parS-dependent ParB-nucleoprotein subclusters. We further show that SMC/ScpAB complexes, loaded via ParB at parS sites, mediate chromosomal inter-arm contacts (as previously shown in Bacillus subtilis). However, the MukBEF-like SMC complex MksBEFG does not contribute to chromosomal DNA-folding; instead, this complex is involved in plasmid maintenance and interacts with the polar oriC-tethering factor DivIVA. Our results complement current models of ParB-SMC/ScpAB crosstalk and show that some condensin complexes evolved functions that are apparently uncoupled from chromosome folding.
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spelling pubmed-70839402020-03-23 Chromosome organization by a conserved condensin-ParB system in the actinobacterium Corynebacterium glutamicum Böhm, Kati Giacomelli, Giacomo Schmidt, Andreas Imhof, Axel Koszul, Romain Marbouty, Martial Bramkamp, Marc Nat Commun Article Higher-order chromosome folding and segregation are tightly regulated in all domains of life. In bacteria, details on nucleoid organization regulatory mechanisms and function remain poorly characterized, especially in non-model species. Here, we investigate the role of DNA-partitioning protein ParB and SMC condensin complexes in the actinobacterium Corynebacterium glutamicum. Chromosome conformation capture reveals SMC-mediated long-range interactions around ten centromere-like parS sites clustered at the replication origin (oriC). At least one oriC-proximal parS site is necessary for reliable chromosome segregation. We use chromatin immunoprecipitation and photoactivated single-molecule localization microscopy to show the formation of distinct, parS-dependent ParB-nucleoprotein subclusters. We further show that SMC/ScpAB complexes, loaded via ParB at parS sites, mediate chromosomal inter-arm contacts (as previously shown in Bacillus subtilis). However, the MukBEF-like SMC complex MksBEFG does not contribute to chromosomal DNA-folding; instead, this complex is involved in plasmid maintenance and interacts with the polar oriC-tethering factor DivIVA. Our results complement current models of ParB-SMC/ScpAB crosstalk and show that some condensin complexes evolved functions that are apparently uncoupled from chromosome folding. Nature Publishing Group UK 2020-03-20 /pmc/articles/PMC7083940/ /pubmed/32198399 http://dx.doi.org/10.1038/s41467-020-15238-4 Text en © The Author(s) 2020 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/.
spellingShingle Article
Böhm, Kati
Giacomelli, Giacomo
Schmidt, Andreas
Imhof, Axel
Koszul, Romain
Marbouty, Martial
Bramkamp, Marc
Chromosome organization by a conserved condensin-ParB system in the actinobacterium Corynebacterium glutamicum
title Chromosome organization by a conserved condensin-ParB system in the actinobacterium Corynebacterium glutamicum
title_full Chromosome organization by a conserved condensin-ParB system in the actinobacterium Corynebacterium glutamicum
title_fullStr Chromosome organization by a conserved condensin-ParB system in the actinobacterium Corynebacterium glutamicum
title_full_unstemmed Chromosome organization by a conserved condensin-ParB system in the actinobacterium Corynebacterium glutamicum
title_short Chromosome organization by a conserved condensin-ParB system in the actinobacterium Corynebacterium glutamicum
title_sort chromosome organization by a conserved condensin-parb system in the actinobacterium corynebacterium glutamicum
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7083940/
https://www.ncbi.nlm.nih.gov/pubmed/32198399
http://dx.doi.org/10.1038/s41467-020-15238-4
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