Coordination of cell division and chromosome segregation by iron and a sRNA in Escherichia coli

Iron is a vital metal ion frequently present as a cofactor in metabolic enzymes involved in central carbon metabolism, respiratory chain, and DNA synthesis. Notably, iron starvation was previously shown to inhibit cell division, although the mechanism underlying this observation remained obscure. In...

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Main Authors: Evelyne Ng Kwan Lim, Marc Grüll, Nadia Larabi, David Lalaouna, Eric Massé
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-10-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2024.1493811/full
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author Evelyne Ng Kwan Lim
Marc Grüll
Nadia Larabi
David Lalaouna
Eric Massé
author_facet Evelyne Ng Kwan Lim
Marc Grüll
Nadia Larabi
David Lalaouna
Eric Massé
author_sort Evelyne Ng Kwan Lim
collection DOAJ
description Iron is a vital metal ion frequently present as a cofactor in metabolic enzymes involved in central carbon metabolism, respiratory chain, and DNA synthesis. Notably, iron starvation was previously shown to inhibit cell division, although the mechanism underlying this observation remained obscure. In bacteria, the sRNA RyhB has been intensively characterized to regulate genes involved in iron metabolism during iron starvation. While using the screening tool MAPS for new RyhB targets, we found that the mRNA zapB, a factor coordinating chromosome segregation and cell division (cytokinesis), was significantly enriched in association with RyhB. To confirm the interaction between RyhB and zapB mRNA, we conducted both in vitro and in vivo experiments, which showed that RyhB represses zapB translation by binding at two distinct sites. Microscopy and flow cytometry assays revealed that, in the absence of RyhB, cells become shorter and display impaired chromosome segregation during iron starvation. We hypothesized that RyhB might suppress ZapB expression and reduce cell division during iron starvation. Moreover, we observed that deleting zapB gene completely rescued the slow growth phenotype observed in ryhB mutant during strict iron starvation. Altogether, these results suggest that during growth in the absence of iron, RyhB sRNA downregulates zapB mRNA, which leads to longer cells containing extra chromosomes, potentially to optimize survival. Thus, the RyhB-zapB interaction demonstrates intricate regulatory mechanisms between cell division and chromosome segregation depending on iron availability in E. coli.
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spelling doaj-art-6dafcc57188c4b0b871a007d783d78d02024-11-08T18:20:28ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2024-10-011510.3389/fmicb.2024.14938111493811Coordination of cell division and chromosome segregation by iron and a sRNA in Escherichia coliEvelyne Ng Kwan LimMarc GrüllNadia LarabiDavid LalaounaEric MasséIron is a vital metal ion frequently present as a cofactor in metabolic enzymes involved in central carbon metabolism, respiratory chain, and DNA synthesis. Notably, iron starvation was previously shown to inhibit cell division, although the mechanism underlying this observation remained obscure. In bacteria, the sRNA RyhB has been intensively characterized to regulate genes involved in iron metabolism during iron starvation. While using the screening tool MAPS for new RyhB targets, we found that the mRNA zapB, a factor coordinating chromosome segregation and cell division (cytokinesis), was significantly enriched in association with RyhB. To confirm the interaction between RyhB and zapB mRNA, we conducted both in vitro and in vivo experiments, which showed that RyhB represses zapB translation by binding at two distinct sites. Microscopy and flow cytometry assays revealed that, in the absence of RyhB, cells become shorter and display impaired chromosome segregation during iron starvation. We hypothesized that RyhB might suppress ZapB expression and reduce cell division during iron starvation. Moreover, we observed that deleting zapB gene completely rescued the slow growth phenotype observed in ryhB mutant during strict iron starvation. Altogether, these results suggest that during growth in the absence of iron, RyhB sRNA downregulates zapB mRNA, which leads to longer cells containing extra chromosomes, potentially to optimize survival. Thus, the RyhB-zapB interaction demonstrates intricate regulatory mechanisms between cell division and chromosome segregation depending on iron availability in E. coli.https://www.frontiersin.org/articles/10.3389/fmicb.2024.1493811/fullcell divisionsmall RNAschromosome segregationiron starvationRyhBZapB
spellingShingle Evelyne Ng Kwan Lim
Marc Grüll
Nadia Larabi
David Lalaouna
Eric Massé
Coordination of cell division and chromosome segregation by iron and a sRNA in Escherichia coli
Frontiers in Microbiology
cell division
small RNAs
chromosome segregation
iron starvation
RyhB
ZapB
title Coordination of cell division and chromosome segregation by iron and a sRNA in Escherichia coli
title_full Coordination of cell division and chromosome segregation by iron and a sRNA in Escherichia coli
title_fullStr Coordination of cell division and chromosome segregation by iron and a sRNA in Escherichia coli
title_full_unstemmed Coordination of cell division and chromosome segregation by iron and a sRNA in Escherichia coli
title_short Coordination of cell division and chromosome segregation by iron and a sRNA in Escherichia coli
title_sort coordination of cell division and chromosome segregation by iron and a srna in escherichia coli
topic cell division
small RNAs
chromosome segregation
iron starvation
RyhB
ZapB
url https://www.frontiersin.org/articles/10.3389/fmicb.2024.1493811/full
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