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Identification of network topological units coordinating the global expression response to glucose in Bacillus subtilis and its comparison to Escherichia coli.

Vázquez CD, Freyre-González JA, Gosset G, Loza JA, Gutiérrez-Ríos RM - BMC Microbiol. (2009)

Bottom Line: In terms of topological functional units in both these bacteria, we found interconnected modules that cluster together genes relating to heat shock, respiratory functions, carbon and peroxide metabolism.Interestingly, B. subtilis functions not found in E. coli, such as sporulation and competence were shown to be interconnected, forming modules subject to catabolic repression at the level of transcription.Our results demonstrate that the response to glucose is partially conserved in model organisms E. coli and B. subtilis, including genes encoding basic functions such as transcription, translation, replication and genes involved in the central carbon metabolism.

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. cvazquez@ibt.unam.mx

ABSTRACT

Background: Glucose is the preferred carbon and energy source for Bacillus subtilis and Escherichia coli. A complex regulatory network coordinates gene expression, transport and enzymatic activities, in response to the presence of this sugar. We present a comparison of the cellular response to glucose in these two model organisms, using an approach combining global transcriptome and regulatory network analyses.

Results: Transcriptome data from strains grown in Luria-Bertani medium (LB) or LB+glucose (LB+G) were analyzed, in order to identify differentially transcribed genes in B. subtilis. We detected 503 genes in B. subtilis that change their relative transcript levels in the presence of glucose. A similar previous study identified 380 genes in E. coli, which respond to glucose. Catabolic repression was detected in the case of transport and metabolic interconversion activities for both bacteria in LB+G. We detected an increased capacity for de novo synthesis of nucleotides, amino acids and proteins. A comparison between orthologous genes revealed that global regulatory functions such as transcription, translation, replication and genes relating to the central carbon metabolism, presented similar changes in their levels of expression. An analysis of the regulatory network of a subset of genes in both organisms revealed that the set of regulatory proteins responsible for similar physiological responses observed in the transcriptome analysis are not orthologous. An example of this observation is that of transcription factors mediating catabolic repression for most of the genes that displayed reduced transcript levels in the case of both organisms. In terms of topological functional units in both these bacteria, we found interconnected modules that cluster together genes relating to heat shock, respiratory functions, carbon and peroxide metabolism. Interestingly, B. subtilis functions not found in E. coli, such as sporulation and competence were shown to be interconnected, forming modules subject to catabolic repression at the level of transcription.

Conclusion: Our results demonstrate that the response to glucose is partially conserved in model organisms E. coli and B. subtilis, including genes encoding basic functions such as transcription, translation, replication and genes involved in the central carbon metabolism.

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Conserved glucose responding modules between B. subtilis and E. coli. Whereas there is extensive rewiring in the regulatory network, some modules have conserved their physiological functions and expression profile, showing the high plasticity of regulatory networks in terms of evolution. Dashed thin lines show orthology relations, whereas blue dash-dot lines bound modules. Green ellipses indicate repressed genes; red ones show activated genes and grey ones indicate genes, which are not significantly expressed. E. coli modules IDs are taken from Gutierrez-Rios et al. [13]. Regarding the aspartate catabolism module, it has been suggested that L-aspartase encoded by ansB is an strictly catabolic enzime (catalyzing the reaction aspartate → fumarate + NH4+), thus providing carbon skeletons to Krebs cycle.
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Figure 4: Conserved glucose responding modules between B. subtilis and E. coli. Whereas there is extensive rewiring in the regulatory network, some modules have conserved their physiological functions and expression profile, showing the high plasticity of regulatory networks in terms of evolution. Dashed thin lines show orthology relations, whereas blue dash-dot lines bound modules. Green ellipses indicate repressed genes; red ones show activated genes and grey ones indicate genes, which are not significantly expressed. E. coli modules IDs are taken from Gutierrez-Rios et al. [13]. Regarding the aspartate catabolism module, it has been suggested that L-aspartase encoded by ansB is an strictly catabolic enzime (catalyzing the reaction aspartate → fumarate + NH4+), thus providing carbon skeletons to Krebs cycle.

Mentions: A comparison was carried out, considering the modular structure of the sub-network of E. coli in the presence of glucose [13] and the modular structure for B. subtilis, generated during this study. Figure 4 presents orthologous genes that were organized into modular structures. At this level, we could see that most of the genes clustering in modules in both sub-networks, related to carbon metabolism. Those genes encoding for proteins of the PTS system were outstanding (levDE, ptsG), the degradative enzyme galK and the gene rbsB encoding as a transporter. All of the genes previously described except ptsG belong to the modules classified as Carbon Modules in both sub-networks. In the case of E. coli, genes in this module were clustered because they were regulated by CRP and in the case of B. subtilis by the relationship of the genes to the regulatory protein CcpA. The disconnection of ptsG from the carbon module in B. subtilis can be explained by the absence of regulation by CcpA (Figure 4, Table 1).


Identification of network topological units coordinating the global expression response to glucose in Bacillus subtilis and its comparison to Escherichia coli.

Vázquez CD, Freyre-González JA, Gosset G, Loza JA, Gutiérrez-Ríos RM - BMC Microbiol. (2009)

Conserved glucose responding modules between B. subtilis and E. coli. Whereas there is extensive rewiring in the regulatory network, some modules have conserved their physiological functions and expression profile, showing the high plasticity of regulatory networks in terms of evolution. Dashed thin lines show orthology relations, whereas blue dash-dot lines bound modules. Green ellipses indicate repressed genes; red ones show activated genes and grey ones indicate genes, which are not significantly expressed. E. coli modules IDs are taken from Gutierrez-Rios et al. [13]. Regarding the aspartate catabolism module, it has been suggested that L-aspartase encoded by ansB is an strictly catabolic enzime (catalyzing the reaction aspartate → fumarate + NH4+), thus providing carbon skeletons to Krebs cycle.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2749860&req=5

Figure 4: Conserved glucose responding modules between B. subtilis and E. coli. Whereas there is extensive rewiring in the regulatory network, some modules have conserved their physiological functions and expression profile, showing the high plasticity of regulatory networks in terms of evolution. Dashed thin lines show orthology relations, whereas blue dash-dot lines bound modules. Green ellipses indicate repressed genes; red ones show activated genes and grey ones indicate genes, which are not significantly expressed. E. coli modules IDs are taken from Gutierrez-Rios et al. [13]. Regarding the aspartate catabolism module, it has been suggested that L-aspartase encoded by ansB is an strictly catabolic enzime (catalyzing the reaction aspartate → fumarate + NH4+), thus providing carbon skeletons to Krebs cycle.
Mentions: A comparison was carried out, considering the modular structure of the sub-network of E. coli in the presence of glucose [13] and the modular structure for B. subtilis, generated during this study. Figure 4 presents orthologous genes that were organized into modular structures. At this level, we could see that most of the genes clustering in modules in both sub-networks, related to carbon metabolism. Those genes encoding for proteins of the PTS system were outstanding (levDE, ptsG), the degradative enzyme galK and the gene rbsB encoding as a transporter. All of the genes previously described except ptsG belong to the modules classified as Carbon Modules in both sub-networks. In the case of E. coli, genes in this module were clustered because they were regulated by CRP and in the case of B. subtilis by the relationship of the genes to the regulatory protein CcpA. The disconnection of ptsG from the carbon module in B. subtilis can be explained by the absence of regulation by CcpA (Figure 4, Table 1).

Bottom Line: In terms of topological functional units in both these bacteria, we found interconnected modules that cluster together genes relating to heat shock, respiratory functions, carbon and peroxide metabolism.Interestingly, B. subtilis functions not found in E. coli, such as sporulation and competence were shown to be interconnected, forming modules subject to catabolic repression at the level of transcription.Our results demonstrate that the response to glucose is partially conserved in model organisms E. coli and B. subtilis, including genes encoding basic functions such as transcription, translation, replication and genes involved in the central carbon metabolism.

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. cvazquez@ibt.unam.mx

ABSTRACT

Background: Glucose is the preferred carbon and energy source for Bacillus subtilis and Escherichia coli. A complex regulatory network coordinates gene expression, transport and enzymatic activities, in response to the presence of this sugar. We present a comparison of the cellular response to glucose in these two model organisms, using an approach combining global transcriptome and regulatory network analyses.

Results: Transcriptome data from strains grown in Luria-Bertani medium (LB) or LB+glucose (LB+G) were analyzed, in order to identify differentially transcribed genes in B. subtilis. We detected 503 genes in B. subtilis that change their relative transcript levels in the presence of glucose. A similar previous study identified 380 genes in E. coli, which respond to glucose. Catabolic repression was detected in the case of transport and metabolic interconversion activities for both bacteria in LB+G. We detected an increased capacity for de novo synthesis of nucleotides, amino acids and proteins. A comparison between orthologous genes revealed that global regulatory functions such as transcription, translation, replication and genes relating to the central carbon metabolism, presented similar changes in their levels of expression. An analysis of the regulatory network of a subset of genes in both organisms revealed that the set of regulatory proteins responsible for similar physiological responses observed in the transcriptome analysis are not orthologous. An example of this observation is that of transcription factors mediating catabolic repression for most of the genes that displayed reduced transcript levels in the case of both organisms. In terms of topological functional units in both these bacteria, we found interconnected modules that cluster together genes relating to heat shock, respiratory functions, carbon and peroxide metabolism. Interestingly, B. subtilis functions not found in E. coli, such as sporulation and competence were shown to be interconnected, forming modules subject to catabolic repression at the level of transcription.

Conclusion: Our results demonstrate that the response to glucose is partially conserved in model organisms E. coli and B. subtilis, including genes encoding basic functions such as transcription, translation, replication and genes involved in the central carbon metabolism.

Show MeSH
Related in: MedlinePlus