Modularity of the Bacterial Cell Cycle Enables Independent Spatial and Temporal Control of DNA Replication
Background: Complex regulatory circuits in biology are often built of simpler subcircuits or modules. In most cases, the functional consequences and evolutionary origins of modularity remain poorly defined. Results: Here, by combining single-cell microscopy with genetic approaches, we demonstrate...
| Main Authors: | , , , , |
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| Other Authors: | |
| Format: | Article |
| Language: | en_US |
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Elsevier
2014
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| Online Access: | http://hdl.handle.net/1721.1/84668 https://orcid.org/0000-0002-8288-7607 |
| _version_ | 1811080714646454272 |
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| author | Jonas, Kristina Chen, Y. Erin Chen, Y. Erin Laub, Michael T. Laub, Michael T |
| author2 | Massachusetts Institute of Technology. Department of Biology |
| author_facet | Massachusetts Institute of Technology. Department of Biology Jonas, Kristina Chen, Y. Erin Chen, Y. Erin Laub, Michael T. Laub, Michael T |
| author_sort | Jonas, Kristina |
| collection | MIT |
| description | Background:
Complex regulatory circuits in biology are often built of simpler subcircuits or modules. In most cases, the functional consequences and evolutionary origins of modularity remain poorly defined.
Results:
Here, by combining single-cell microscopy with genetic approaches, we demonstrate that two separable modules independently govern the temporal and spatial control of DNA replication in the asymmetrically dividing bacterium Caulobacter crescentus. DNA replication control involves DnaA, which promotes initiation, and CtrA, which silences initiation. We show that oscillations in DnaA activity dictate the periodicity of replication while CtrA governs the asymmetric replicative fates of daughter cells. Importantly, we demonstrate that DnaA activity oscillates independently of CtrA.
Conclusions:
The genetic separability of spatial and temporal control modules in Caulobacter reflects their evolutionary history. DnaA is the central component of an ancient and phylogenetically widespread circuit that governs replication periodicity in Caulobacter and most other bacteria. By contrast, CtrA, which is found only in the asymmetrically dividing α-proteobacteria, was integrated later in evolution to enforce replicative asymmetry on daughter cells. |
| first_indexed | 2024-09-23T11:35:36Z |
| format | Article |
| id | mit-1721.1/84668 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T11:35:36Z |
| publishDate | 2014 |
| publisher | Elsevier |
| record_format | dspace |
| spelling | mit-1721.1/846682022-10-01T04:37:45Z Modularity of the Bacterial Cell Cycle Enables Independent Spatial and Temporal Control of DNA Replication Jonas, Kristina Chen, Y. Erin Chen, Y. Erin Laub, Michael T. Laub, Michael T Massachusetts Institute of Technology. Department of Biology Jonas, Kristina Chen, Y. Erin Laub, Michael T. Background: Complex regulatory circuits in biology are often built of simpler subcircuits or modules. In most cases, the functional consequences and evolutionary origins of modularity remain poorly defined. Results: Here, by combining single-cell microscopy with genetic approaches, we demonstrate that two separable modules independently govern the temporal and spatial control of DNA replication in the asymmetrically dividing bacterium Caulobacter crescentus. DNA replication control involves DnaA, which promotes initiation, and CtrA, which silences initiation. We show that oscillations in DnaA activity dictate the periodicity of replication while CtrA governs the asymmetric replicative fates of daughter cells. Importantly, we demonstrate that DnaA activity oscillates independently of CtrA. Conclusions: The genetic separability of spatial and temporal control modules in Caulobacter reflects their evolutionary history. DnaA is the central component of an ancient and phylogenetically widespread circuit that governs replication periodicity in Caulobacter and most other bacteria. By contrast, CtrA, which is found only in the asymmetrically dividing α-proteobacteria, was integrated later in evolution to enforce replicative asymmetry on daughter cells. National Institutes of Health (U.S.) (Grant 5R01GM082899) 2014-02-07T14:40:45Z 2014-02-07T14:40:45Z 2011-06 2011-04 Article http://purl.org/eprint/type/JournalArticle 09609822 1879-0445 http://hdl.handle.net/1721.1/84668 Jonas, Kristina, Y. Erin Chen, and Michael T. Laub. “Modularity of the Bacterial Cell Cycle Enables Independent Spatial and Temporal Control of DNA Replication.” Current Biology 21, no. 13 (July 2011): 1092-1101. Copyright © 2011 Elsevier Ltd. https://orcid.org/0000-0002-8288-7607 en_US http://dx.doi.org/10.1016/j.cub.2011.05.040 Current Biology Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf Elsevier Elsevier Open Archive |
| spellingShingle | Jonas, Kristina Chen, Y. Erin Chen, Y. Erin Laub, Michael T. Laub, Michael T Modularity of the Bacterial Cell Cycle Enables Independent Spatial and Temporal Control of DNA Replication |
| title | Modularity of the Bacterial Cell Cycle Enables Independent Spatial and Temporal Control of DNA Replication |
| title_full | Modularity of the Bacterial Cell Cycle Enables Independent Spatial and Temporal Control of DNA Replication |
| title_fullStr | Modularity of the Bacterial Cell Cycle Enables Independent Spatial and Temporal Control of DNA Replication |
| title_full_unstemmed | Modularity of the Bacterial Cell Cycle Enables Independent Spatial and Temporal Control of DNA Replication |
| title_short | Modularity of the Bacterial Cell Cycle Enables Independent Spatial and Temporal Control of DNA Replication |
| title_sort | modularity of the bacterial cell cycle enables independent spatial and temporal control of dna replication |
| url | http://hdl.handle.net/1721.1/84668 https://orcid.org/0000-0002-8288-7607 |
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