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: | , , , , , , , , , , |
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| Format: | Article |
| Language: | en_US |
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Public Library of Science
2015
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| Online Access: | http://hdl.handle.net/1721.1/97105 https://orcid.org/0000-0001-7243-8261 https://orcid.org/0000-0002-7670-5301 |
| _version_ | 1811090618721501184 |
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| author | Pini, Francesco De Nisco, Nicole J. Ferri, Lorenzo Penterman, Jon Fioravanti, Antonella Brilli, Matteo Mengoni, Alessio Bazzicalupo, Marco Viollier, Patrick H. Walker, Graham C. Biondi, Emanuele G. |
| author2 | Massachusetts Institute of Technology. Department of Biology |
| author_facet | Massachusetts Institute of Technology. Department of Biology Pini, Francesco De Nisco, Nicole J. Ferri, Lorenzo Penterman, Jon Fioravanti, Antonella Brilli, Matteo Mengoni, Alessio Bazzicalupo, Marco Viollier, Patrick H. Walker, Graham C. Biondi, Emanuele G. |
| author_sort | Pini, Francesco |
| collection | MIT |
| 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 | 2024-09-23T14:49:04Z |
| format | Article |
| id | mit-1721.1/97105 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T14:49:04Z |
| publishDate | 2015 |
| publisher | Public Library of Science |
| record_format | dspace |
| spelling | mit-1721.1/971052022-10-01T22:40:17Z Cell Cycle Control by the Master Regulator CtrA in Sinorhizobium meliloti Pini, Francesco De Nisco, Nicole J. Ferri, Lorenzo Penterman, Jon Fioravanti, Antonella Brilli, Matteo Mengoni, Alessio Bazzicalupo, Marco Viollier, Patrick H. Walker, Graham C. Biondi, Emanuele G. Massachusetts Institute of Technology. Department of Biology De Nisco, Nicole J. Penterman, Jon Walker, Graham C. 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. France. Agence nationale de la recherche (ANR-JCJC-2011-Castacc) National Institutes of Health (U.S.) (Grant GM31010) National Institutes of Health (U.S.) (Grant P30 ES002109) National Institutes of Health (U.S.) (Pre-doctoral Training Grant T32GM007287) 2015-05-29T12:56:36Z 2015-05-29T12:56:36Z 2015-05 2014-12 Article http://purl.org/eprint/type/JournalArticle 1553-7404 1553-7390 http://hdl.handle.net/1721.1/97105 Pini, Francesco, Nicole J. De Nisco, Lorenzo Ferri, Jon Penterman, Antonella Fioravanti, Matteo Brilli, Alessio Mengoni, et al. “Cell Cycle Control by the Master Regulator CtrA in Sinorhizobium Meliloti.” Edited by Josep Casadesús. PLoS Genet 11, no. 5 (May 15, 2015): e1005232. https://orcid.org/0000-0001-7243-8261 https://orcid.org/0000-0002-7670-5301 en_US http://dx.doi.org/10.1371/journal.pgen.1005232 PLOS Genetics Creative Commons Attribution http://creativecommons.org/licenses/by/4.0/ application/pdf Public Library of Science Public Library of Science |
| spellingShingle | Pini, Francesco De Nisco, Nicole J. Ferri, Lorenzo Penterman, Jon Fioravanti, Antonella Brilli, Matteo Mengoni, Alessio Bazzicalupo, Marco Viollier, Patrick H. Walker, Graham C. Biondi, Emanuele G. Cell Cycle Control by the Master Regulator CtrA in Sinorhizobium meliloti |
| 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://hdl.handle.net/1721.1/97105 https://orcid.org/0000-0001-7243-8261 https://orcid.org/0000-0002-7670-5301 |
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