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Lessons from the modular organization of the transcriptional regulatory network of Bacillus subtilis.

Freyre-González JA, Manjarrez-Casas AM, Merino E, Martinez-Nuñez M, Perez-Rueda E, Gutiérrez-Ríos RM - BMC Syst Biol (2013)

Bottom Line: Among the different kind of mechanisms modulating gene transcription, the one based on DNA binding transcription factors, is the most extensively studied and the results, for a great number of model organisms, have been compiled making it possible the in silico construction of their corresponding transcriptional regulatory networks and the analysis of the biological relationships of the components of these intricate networks, that allows to elucidate the significant aspects of their organization and evolution.We discussed that some particular functions were distributed in more than one module and that some modules contained more than one related function.The intricate organization is the product of a non-random network evolution that primarily follows a hierarchical organization based on the presence of transcription and σ factor, which is reflected in the connections that exist within and between modules.

View Article: PubMed Central - HTML - PubMed

Affiliation: Departamentos de Microbiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Apdo, Postal 510-3, Cuernavaca, Morelos 62250, México. rmaria@ibt.unam.mx.

ABSTRACT

Background: The regulation of gene expression at the transcriptional level is a fundamental process in prokaryotes. Among the different kind of mechanisms modulating gene transcription, the one based on DNA binding transcription factors, is the most extensively studied and the results, for a great number of model organisms, have been compiled making it possible the in silico construction of their corresponding transcriptional regulatory networks and the analysis of the biological relationships of the components of these intricate networks, that allows to elucidate the significant aspects of their organization and evolution.

Results: We present a thorough review of each regulatory element that constitutes the transcriptional regulatory network of Bacillus subtilis. For facilitating the discussion, we organized the network in topological modules. Our study highlight the importance of σ factors, some of them acting as master regulators which characterize modules by inter- or intra-connecting them and play a key role in the cascades that define relevant cellular processes in this organism. We discussed that some particular functions were distributed in more than one module and that some modules contained more than one related function. We confirm that the presence of paralogous proteins confers advantages to B. subtilis to adapt and select strategies to successfully face the extreme and changing environmental conditions in which it lives.

Conclusions: The intricate organization is the product of a non-random network evolution that primarily follows a hierarchical organization based on the presence of transcription and σ factor, which is reflected in the connections that exist within and between modules.

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Paralogous transcription factors not belonging to a module. In red are the paralogous TFs belonging to the carbon metabolism module. Paralogous TFs associated with the general stress response module are indicated in light green. TFs involved in nucleotide biosynthesis are shown in dark green. TFs devoted to the respiration module are shown in pink. TFs related to the secretion stress module are shown in orange. Paralogous regulatory proteins clustered in the cell differentiation module are shown in purple. TFs regulating nitrogen metabolism are shown in yellow. Paralogous TFs clustered in the mother cell module are shown in brown. TFs representing degradative enzymes are shown in blue. A group of regulatory genes that were not clustered in a module (grey) but are paralogous to a TF belonging to a module is also shown. A group of structural genes that are related to paralogous TFs are shown in light yellow. The line represents the paralogous relationship between structural and/or regulatory genes.
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Figure 5: Paralogous transcription factors not belonging to a module. In red are the paralogous TFs belonging to the carbon metabolism module. Paralogous TFs associated with the general stress response module are indicated in light green. TFs involved in nucleotide biosynthesis are shown in dark green. TFs devoted to the respiration module are shown in pink. TFs related to the secretion stress module are shown in orange. Paralogous regulatory proteins clustered in the cell differentiation module are shown in purple. TFs regulating nitrogen metabolism are shown in yellow. Paralogous TFs clustered in the mother cell module are shown in brown. TFs representing degradative enzymes are shown in blue. A group of regulatory genes that were not clustered in a module (grey) but are paralogous to a TF belonging to a module is also shown. A group of structural genes that are related to paralogous TFs are shown in light yellow. The line represents the paralogous relationship between structural and/or regulatory genes.

Mentions: In our previous study, we found that TnrA and GlpR located in M1, are paralogous proteins (Figure 5) [31] that belong to the MerR family [32], and interestingly, their DNA-binding sites have the same consensus sequence [33]. A large fraction of neighboring TF binding sites have been formed by local duplications of a common sequence and might diverge as a consequence of point mutations [34]; further, these sites may have been selected for specific environmental conditions, as suggested by Singh and Hannenhalli [35]. Additional examples of interchangeable DNA-binding sites have been observed in other families of E. coli regulatory proteins, such as CRP and FNR [36].


Lessons from the modular organization of the transcriptional regulatory network of Bacillus subtilis.

Freyre-González JA, Manjarrez-Casas AM, Merino E, Martinez-Nuñez M, Perez-Rueda E, Gutiérrez-Ríos RM - BMC Syst Biol (2013)

Paralogous transcription factors not belonging to a module. In red are the paralogous TFs belonging to the carbon metabolism module. Paralogous TFs associated with the general stress response module are indicated in light green. TFs involved in nucleotide biosynthesis are shown in dark green. TFs devoted to the respiration module are shown in pink. TFs related to the secretion stress module are shown in orange. Paralogous regulatory proteins clustered in the cell differentiation module are shown in purple. TFs regulating nitrogen metabolism are shown in yellow. Paralogous TFs clustered in the mother cell module are shown in brown. TFs representing degradative enzymes are shown in blue. A group of regulatory genes that were not clustered in a module (grey) but are paralogous to a TF belonging to a module is also shown. A group of structural genes that are related to paralogous TFs are shown in light yellow. The line represents the paralogous relationship between structural and/or regulatory genes.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4225672&req=5

Figure 5: Paralogous transcription factors not belonging to a module. In red are the paralogous TFs belonging to the carbon metabolism module. Paralogous TFs associated with the general stress response module are indicated in light green. TFs involved in nucleotide biosynthesis are shown in dark green. TFs devoted to the respiration module are shown in pink. TFs related to the secretion stress module are shown in orange. Paralogous regulatory proteins clustered in the cell differentiation module are shown in purple. TFs regulating nitrogen metabolism are shown in yellow. Paralogous TFs clustered in the mother cell module are shown in brown. TFs representing degradative enzymes are shown in blue. A group of regulatory genes that were not clustered in a module (grey) but are paralogous to a TF belonging to a module is also shown. A group of structural genes that are related to paralogous TFs are shown in light yellow. The line represents the paralogous relationship between structural and/or regulatory genes.
Mentions: In our previous study, we found that TnrA and GlpR located in M1, are paralogous proteins (Figure 5) [31] that belong to the MerR family [32], and interestingly, their DNA-binding sites have the same consensus sequence [33]. A large fraction of neighboring TF binding sites have been formed by local duplications of a common sequence and might diverge as a consequence of point mutations [34]; further, these sites may have been selected for specific environmental conditions, as suggested by Singh and Hannenhalli [35]. Additional examples of interchangeable DNA-binding sites have been observed in other families of E. coli regulatory proteins, such as CRP and FNR [36].

Bottom Line: Among the different kind of mechanisms modulating gene transcription, the one based on DNA binding transcription factors, is the most extensively studied and the results, for a great number of model organisms, have been compiled making it possible the in silico construction of their corresponding transcriptional regulatory networks and the analysis of the biological relationships of the components of these intricate networks, that allows to elucidate the significant aspects of their organization and evolution.We discussed that some particular functions were distributed in more than one module and that some modules contained more than one related function.The intricate organization is the product of a non-random network evolution that primarily follows a hierarchical organization based on the presence of transcription and σ factor, which is reflected in the connections that exist within and between modules.

View Article: PubMed Central - HTML - PubMed

Affiliation: Departamentos de Microbiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Apdo, Postal 510-3, Cuernavaca, Morelos 62250, México. rmaria@ibt.unam.mx.

ABSTRACT

Background: The regulation of gene expression at the transcriptional level is a fundamental process in prokaryotes. Among the different kind of mechanisms modulating gene transcription, the one based on DNA binding transcription factors, is the most extensively studied and the results, for a great number of model organisms, have been compiled making it possible the in silico construction of their corresponding transcriptional regulatory networks and the analysis of the biological relationships of the components of these intricate networks, that allows to elucidate the significant aspects of their organization and evolution.

Results: We present a thorough review of each regulatory element that constitutes the transcriptional regulatory network of Bacillus subtilis. For facilitating the discussion, we organized the network in topological modules. Our study highlight the importance of σ factors, some of them acting as master regulators which characterize modules by inter- or intra-connecting them and play a key role in the cascades that define relevant cellular processes in this organism. We discussed that some particular functions were distributed in more than one module and that some modules contained more than one related function. We confirm that the presence of paralogous proteins confers advantages to B. subtilis to adapt and select strategies to successfully face the extreme and changing environmental conditions in which it lives.

Conclusions: The intricate organization is the product of a non-random network evolution that primarily follows a hierarchical organization based on the presence of transcription and σ factor, which is reflected in the connections that exist within and between modules.

Show MeSH
Related in: MedlinePlus