Cell Cycle Control by the Master Regulator CtrA in Sinorhizobium meliloti.
In all domains of life, proper regulation of the cell cycle is critical to coordinate genome replication, segregation and cell division. In some groups of bacteria, e.g. Alphaproteobacteria, tight regulation of the cell cycle is also necessary for the morphological and functional differentiation of...
| Main Authors: | , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2015-05-01
|
| Series: | PLoS Genetics |
| Online Access: | http://europepmc.org/articles/PMC4433202?pdf=render |
| _version_ | 1819132063562858496 |
|---|---|
| author | Francesco Pini Nicole J De Nisco Lorenzo Ferri Jon Penterman Antonella Fioravanti Matteo Brilli Alessio Mengoni Marco Bazzicalupo Patrick H Viollier Graham C Walker Emanuele G Biondi |
| author_facet | Francesco Pini Nicole J De Nisco Lorenzo Ferri Jon Penterman Antonella Fioravanti Matteo Brilli Alessio Mengoni Marco Bazzicalupo Patrick H Viollier Graham C Walker Emanuele G Biondi |
| author_sort | Francesco Pini |
| collection | DOAJ |
| description | In all domains of life, proper regulation of the cell cycle is critical to coordinate genome replication, segregation and cell division. In some groups of bacteria, e.g. Alphaproteobacteria, tight regulation of the cell cycle is also necessary for the morphological and functional differentiation of cells. Sinorhizobium meliloti is an alphaproteobacterium that forms an economically and ecologically important nitrogen-fixing symbiosis with specific legume hosts. During this symbiosis S. meliloti undergoes an elaborate cellular differentiation within host root cells. The differentiation of S. meliloti results in massive amplification of the genome, cell branching and/or elongation, and loss of reproductive capacity. In Caulobacter crescentus, cellular differentiation is tightly linked to the cell cycle via the activity of the master regulator CtrA, and recent research in S. meliloti suggests that CtrA might also be key to cellular differentiation during symbiosis. However, the regulatory circuit driving cell cycle progression in S. meliloti is not well characterized in both the free-living and symbiotic state. Here, we investigated the regulation and function of CtrA in S. meliloti. We demonstrated that depletion of CtrA cause cell elongation, branching and genome amplification, similar to that observed in nitrogen-fixing bacteroids. We also showed that the cell cycle regulated proteolytic degradation of CtrA is essential in S. meliloti, suggesting a possible mechanism of CtrA depletion in differentiated bacteroids. Using a combination of ChIP-Seq and gene expression microarray analysis we found that although S. meliloti CtrA regulates similar processes as C. crescentus CtrA, it does so through different target genes. For example, our data suggest that CtrA does not control the expression of the Fts complex to control the timing of cell division during the cell cycle, but instead it negatively regulates the septum-inhibiting Min system. Our findings provide valuable insight into how highly conserved genetic networks can evolve, possibly to fit the diverse lifestyles of different bacteria. |
| first_indexed | 2024-12-22T09:25:27Z |
| format | Article |
| id | doaj.art-864287eec880431a94366b4d14030e8e |
| institution | Directory Open Access Journal |
| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2024-12-22T09:25:27Z |
| publishDate | 2015-05-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj.art-864287eec880431a94366b4d14030e8e2022-12-21T18:31:06ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042015-05-01115e100523210.1371/journal.pgen.1005232Cell Cycle Control by the Master Regulator CtrA in Sinorhizobium meliloti.Francesco PiniNicole J De NiscoLorenzo FerriJon PentermanAntonella FioravantiMatteo BrilliAlessio MengoniMarco BazzicalupoPatrick H ViollierGraham C WalkerEmanuele G BiondiIn all domains of life, proper regulation of the cell cycle is critical to coordinate genome replication, segregation and cell division. In some groups of bacteria, e.g. Alphaproteobacteria, tight regulation of the cell cycle is also necessary for the morphological and functional differentiation of cells. Sinorhizobium meliloti is an alphaproteobacterium that forms an economically and ecologically important nitrogen-fixing symbiosis with specific legume hosts. During this symbiosis S. meliloti undergoes an elaborate cellular differentiation within host root cells. The differentiation of S. meliloti results in massive amplification of the genome, cell branching and/or elongation, and loss of reproductive capacity. In Caulobacter crescentus, cellular differentiation is tightly linked to the cell cycle via the activity of the master regulator CtrA, and recent research in S. meliloti suggests that CtrA might also be key to cellular differentiation during symbiosis. However, the regulatory circuit driving cell cycle progression in S. meliloti is not well characterized in both the free-living and symbiotic state. Here, we investigated the regulation and function of CtrA in S. meliloti. We demonstrated that depletion of CtrA cause cell elongation, branching and genome amplification, similar to that observed in nitrogen-fixing bacteroids. We also showed that the cell cycle regulated proteolytic degradation of CtrA is essential in S. meliloti, suggesting a possible mechanism of CtrA depletion in differentiated bacteroids. Using a combination of ChIP-Seq and gene expression microarray analysis we found that although S. meliloti CtrA regulates similar processes as C. crescentus CtrA, it does so through different target genes. For example, our data suggest that CtrA does not control the expression of the Fts complex to control the timing of cell division during the cell cycle, but instead it negatively regulates the septum-inhibiting Min system. Our findings provide valuable insight into how highly conserved genetic networks can evolve, possibly to fit the diverse lifestyles of different bacteria.http://europepmc.org/articles/PMC4433202?pdf=render |
| spellingShingle | Francesco Pini Nicole J De Nisco Lorenzo Ferri Jon Penterman Antonella Fioravanti Matteo Brilli Alessio Mengoni Marco Bazzicalupo Patrick H Viollier Graham C Walker Emanuele G Biondi Cell Cycle Control by the Master Regulator CtrA in Sinorhizobium meliloti. PLoS Genetics |
| title | Cell Cycle Control by the Master Regulator CtrA in Sinorhizobium meliloti. |
| title_full | Cell Cycle Control by the Master Regulator CtrA in Sinorhizobium meliloti. |
| title_fullStr | Cell Cycle Control by the Master Regulator CtrA in Sinorhizobium meliloti. |
| title_full_unstemmed | Cell Cycle Control by the Master Regulator CtrA in Sinorhizobium meliloti. |
| title_short | Cell Cycle Control by the Master Regulator CtrA in Sinorhizobium meliloti. |
| title_sort | cell cycle control by the master regulator ctra in sinorhizobium meliloti |
| url | http://europepmc.org/articles/PMC4433202?pdf=render |
| work_keys_str_mv | AT francescopini cellcyclecontrolbythemasterregulatorctrainsinorhizobiummeliloti AT nicolejdenisco cellcyclecontrolbythemasterregulatorctrainsinorhizobiummeliloti AT lorenzoferri cellcyclecontrolbythemasterregulatorctrainsinorhizobiummeliloti AT jonpenterman cellcyclecontrolbythemasterregulatorctrainsinorhizobiummeliloti AT antonellafioravanti cellcyclecontrolbythemasterregulatorctrainsinorhizobiummeliloti AT matteobrilli cellcyclecontrolbythemasterregulatorctrainsinorhizobiummeliloti AT alessiomengoni cellcyclecontrolbythemasterregulatorctrainsinorhizobiummeliloti AT marcobazzicalupo cellcyclecontrolbythemasterregulatorctrainsinorhizobiummeliloti AT patrickhviollier cellcyclecontrolbythemasterregulatorctrainsinorhizobiummeliloti AT grahamcwalker cellcyclecontrolbythemasterregulatorctrainsinorhizobiummeliloti AT emanuelegbiondi cellcyclecontrolbythemasterregulatorctrainsinorhizobiummeliloti |