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The diversity and evolution of cell cycle regulation in alpha-proteobacteria: a comparative genomic analysis.

Brilli M, Fondi M, Fani R, Mengoni A, Ferri L, Bazzicalupo M, Biondi EG - BMC Syst Biol (2010)

Bottom Line: The regulatory cell cycle architecture was identified in all representative alpha-proteobacteria, revealing a high diversification of circuits but also a conservation of logical features.An evolutionary model was proposed where ancient alphas already possessed all modules found in Caulobacter arranged in a variety of connections.Two schemes appeared to evolve: a complex circuit in Caulobacterales and Rhizobiales and a simpler one found in Rhodobacterales.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Evolutionary Biology, University of Florence, via Romana, 17, Florence, Italy.

ABSTRACT

Background: In the bacterium Caulobacter crescentus, CtrA coordinates DNA replication, cell division, and polar morphogenesis and is considered the cell cycle master regulator. CtrA activity varies during cell cycle progression and is modulated by phosphorylation, proteolysis and transcriptional control. In a phosphorylated state, CtrA binds specific DNA sequences, regulates the expression of genes involved in cell cycle progression and silences the origin of replication. Although the circuitry regulating CtrA is known in molecular detail in Caulobacter, its conservation and functionality in the other alpha-proteobacteria are still poorly understood.

Results: Orthologs of Caulobacter factors involved in the regulation of CtrA were systematically scanned in genomes of alpha-proteobacteria. In particular, orthologous genes of the divL-cckA-chpT-ctrA phosphorelay, the divJ-pleC-divK two-component system, the cpdR-rcdA-clpPX proteolysis system, the methyltransferase ccrM and transcriptional regulators dnaA and gcrA were identified in representative genomes of alpha-proteobacteria. CtrA, DnaA and GcrA binding sites and CcrM putative methylation sites were predicted in promoter regions of all these factors and functions controlled by CtrA in all alphas were predicted.

Conclusions: The regulatory cell cycle architecture was identified in all representative alpha-proteobacteria, revealing a high diversification of circuits but also a conservation of logical features. An evolutionary model was proposed where ancient alphas already possessed all modules found in Caulobacter arranged in a variety of connections. Two schemes appeared to evolve: a complex circuit in Caulobacterales and Rhizobiales and a simpler one found in Rhodobacterales.

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Regulatory circuits of clusters A, B, C, E. See the "Results" and "Discussion" sections for more details. Interactions via phosphorylation, as well as proteolysis, were suggested only considering the interaction demonstrated in Caulobacter. Moreover, DivK inhibition on CckA was considered, as in Biondi (2006), only in Caulobacter [20]. The presence of binding sites of transcription factors CtrA, DnaA and GcrA is shown as a continuous line if predicted binding sites were present in at least 90% of the gene promoters of a cluster. In contrast, the connection is shown as a dotted line for binding sites present in ca. 70%. The Caulobacter-like group corresponds to B. japonicum, P. lavamentivorans and M. maris.
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Figure 7: Regulatory circuits of clusters A, B, C, E. See the "Results" and "Discussion" sections for more details. Interactions via phosphorylation, as well as proteolysis, were suggested only considering the interaction demonstrated in Caulobacter. Moreover, DivK inhibition on CckA was considered, as in Biondi (2006), only in Caulobacter [20]. The presence of binding sites of transcription factors CtrA, DnaA and GcrA is shown as a continuous line if predicted binding sites were present in at least 90% of the gene promoters of a cluster. In contrast, the connection is shown as a dotted line for binding sites present in ca. 70%. The Caulobacter-like group corresponds to B. japonicum, P. lavamentivorans and M. maris.

Mentions: Based on data of Figures 2, 3, and 5, we reconstructed the architecture of the seven clusters (A to G) found in the BBH analysis; as discussed below, only four clusters revealed a defined architecture as illustrated in Figure 7. Models of CtrA regulation are shown in the clusters (clusters A, B, C and E) where interactions between factors were found. This modeling is essential in order to underline differences and conservation of several features of cell cycle regulation in alpha proteobacteria.


The diversity and evolution of cell cycle regulation in alpha-proteobacteria: a comparative genomic analysis.

Brilli M, Fondi M, Fani R, Mengoni A, Ferri L, Bazzicalupo M, Biondi EG - BMC Syst Biol (2010)

Regulatory circuits of clusters A, B, C, E. See the "Results" and "Discussion" sections for more details. Interactions via phosphorylation, as well as proteolysis, were suggested only considering the interaction demonstrated in Caulobacter. Moreover, DivK inhibition on CckA was considered, as in Biondi (2006), only in Caulobacter [20]. The presence of binding sites of transcription factors CtrA, DnaA and GcrA is shown as a continuous line if predicted binding sites were present in at least 90% of the gene promoters of a cluster. In contrast, the connection is shown as a dotted line for binding sites present in ca. 70%. The Caulobacter-like group corresponds to B. japonicum, P. lavamentivorans and M. maris.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2877005&req=5

Figure 7: Regulatory circuits of clusters A, B, C, E. See the "Results" and "Discussion" sections for more details. Interactions via phosphorylation, as well as proteolysis, were suggested only considering the interaction demonstrated in Caulobacter. Moreover, DivK inhibition on CckA was considered, as in Biondi (2006), only in Caulobacter [20]. The presence of binding sites of transcription factors CtrA, DnaA and GcrA is shown as a continuous line if predicted binding sites were present in at least 90% of the gene promoters of a cluster. In contrast, the connection is shown as a dotted line for binding sites present in ca. 70%. The Caulobacter-like group corresponds to B. japonicum, P. lavamentivorans and M. maris.
Mentions: Based on data of Figures 2, 3, and 5, we reconstructed the architecture of the seven clusters (A to G) found in the BBH analysis; as discussed below, only four clusters revealed a defined architecture as illustrated in Figure 7. Models of CtrA regulation are shown in the clusters (clusters A, B, C and E) where interactions between factors were found. This modeling is essential in order to underline differences and conservation of several features of cell cycle regulation in alpha proteobacteria.

Bottom Line: The regulatory cell cycle architecture was identified in all representative alpha-proteobacteria, revealing a high diversification of circuits but also a conservation of logical features.An evolutionary model was proposed where ancient alphas already possessed all modules found in Caulobacter arranged in a variety of connections.Two schemes appeared to evolve: a complex circuit in Caulobacterales and Rhizobiales and a simpler one found in Rhodobacterales.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Evolutionary Biology, University of Florence, via Romana, 17, Florence, Italy.

ABSTRACT

Background: In the bacterium Caulobacter crescentus, CtrA coordinates DNA replication, cell division, and polar morphogenesis and is considered the cell cycle master regulator. CtrA activity varies during cell cycle progression and is modulated by phosphorylation, proteolysis and transcriptional control. In a phosphorylated state, CtrA binds specific DNA sequences, regulates the expression of genes involved in cell cycle progression and silences the origin of replication. Although the circuitry regulating CtrA is known in molecular detail in Caulobacter, its conservation and functionality in the other alpha-proteobacteria are still poorly understood.

Results: Orthologs of Caulobacter factors involved in the regulation of CtrA were systematically scanned in genomes of alpha-proteobacteria. In particular, orthologous genes of the divL-cckA-chpT-ctrA phosphorelay, the divJ-pleC-divK two-component system, the cpdR-rcdA-clpPX proteolysis system, the methyltransferase ccrM and transcriptional regulators dnaA and gcrA were identified in representative genomes of alpha-proteobacteria. CtrA, DnaA and GcrA binding sites and CcrM putative methylation sites were predicted in promoter regions of all these factors and functions controlled by CtrA in all alphas were predicted.

Conclusions: The regulatory cell cycle architecture was identified in all representative alpha-proteobacteria, revealing a high diversification of circuits but also a conservation of logical features. An evolutionary model was proposed where ancient alphas already possessed all modules found in Caulobacter arranged in a variety of connections. Two schemes appeared to evolve: a complex circuit in Caulobacterales and Rhizobiales and a simpler one found in Rhodobacterales.

Show MeSH
Related in: MedlinePlus