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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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Comparison of the significantly induced orrepressed orthologous genes in E. coli and B. subtilis. The figure illustrates a cluster of orthologous genes, comparing B subtilis (column 1) and E. coli (column 2) transcribed levels, as they respond to glucose. Induced genes are represented in red and repressed genes are represented in green. Gene names and functional class are indicated on the right hand side.
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Figure 3: Comparison of the significantly induced orrepressed orthologous genes in E. coli and B. subtilis. The figure illustrates a cluster of orthologous genes, comparing B subtilis (column 1) and E. coli (column 2) transcribed levels, as they respond to glucose. Induced genes are represented in red and repressed genes are represented in green. Gene names and functional class are indicated on the right hand side.

Mentions: We performed a computational search for the bidirectional best hits (BBHs) found in all open reading frames for the genomes of E. coli and B. subtilis, as described in the methods section. As a result, 1199 orthologous genes were shown to be present in these two organisms. From this set, 134 genes manifested significant differences in terms of repression/activation when B. subtilis was grown in the presence or absence of glucose. Out of these, 52 genes were orthologous and responsive to the presence of glucose in the case of both organisms. Figure 3, shows that 47 genes exhibited the same expression pattern in the case of both organisms and five differed. These five genes are pta (phosphoacetyltransferase), gapA (glyceraldehide-3-phosphate dehydrogenase), prsA (peptidyl-prolyl-cis-trans-isomerase), sdhA (succinate deshydrogenase and mutS (methyl-directed mismatch repair). The pta gene was found to be repressed in the B. subtilis microarray data, a result which was inconsistent with a previous report by Presecan-Siedel et al [32], which demonstrated that pta, as is the case with other genes involved in acetate production are induced in the presence of glucose. An induction was also observed for the pta gene of E. coli [33]. The gapA gene was induced in B. subtilis and repressed in E. coli. The observation was consistent with other reports where the gapA of B. subtilis and other bacillus was described as being induced in the presence of glucose, as a result of its participation in the glycolitic pathway [33]. The opposite response for gapA in E. coli may be a consequence of its participation in gluconegenesis [13]. Very little is known about the regulation of mutS in E. coli and B. subtilis. This gene has been described as a DNA repair protein in the context of both bacteria [34]. Something similar happens to psrA in B subtilis, also known as ppiC in E. coli; where both enzymes function as molecular chaperones. It has been reported that prsA is essential for the stability of secreted proteins at certain stages, following translocation across the membrane [35]. Finally, the results observed for the genes sdhA (succinate deshydrogenase en B. subtilis) and frdA (fumarate reductase in E. coli) are quite interesting. Apparently, the functions of these two enzymes seem to be different; the succinate dehydrogenases of aerobic bacteria catalyze the oxidation of succinate by respiratory quinones (succinate:quinone reductase), and the quinols are reoxidized by O2 (succinate oxidase) [36]. In the case of B. subtilis; for some time it was thought that this enzyme has only this function, but in a recent report, the authors demonstrated that resting cells are able to catalyze fumarate reduction, with glucose or glycerol. The enzymatic system for fumarate reduction in B. subtilis was shown to be an electron transport chain, comprising a NADH dehydrogenase, menaquinone and succinate dehydrogenase [36]. Therefore, this enzyme is able to modify its function depending on the growth condition and energetic state of the cell.


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)

Comparison of the significantly induced orrepressed orthologous genes in E. coli and B. subtilis. The figure illustrates a cluster of orthologous genes, comparing B subtilis (column 1) and E. coli (column 2) transcribed levels, as they respond to glucose. Induced genes are represented in red and repressed genes are represented in green. Gene names and functional class are indicated on the right hand side.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: Comparison of the significantly induced orrepressed orthologous genes in E. coli and B. subtilis. The figure illustrates a cluster of orthologous genes, comparing B subtilis (column 1) and E. coli (column 2) transcribed levels, as they respond to glucose. Induced genes are represented in red and repressed genes are represented in green. Gene names and functional class are indicated on the right hand side.
Mentions: We performed a computational search for the bidirectional best hits (BBHs) found in all open reading frames for the genomes of E. coli and B. subtilis, as described in the methods section. As a result, 1199 orthologous genes were shown to be present in these two organisms. From this set, 134 genes manifested significant differences in terms of repression/activation when B. subtilis was grown in the presence or absence of glucose. Out of these, 52 genes were orthologous and responsive to the presence of glucose in the case of both organisms. Figure 3, shows that 47 genes exhibited the same expression pattern in the case of both organisms and five differed. These five genes are pta (phosphoacetyltransferase), gapA (glyceraldehide-3-phosphate dehydrogenase), prsA (peptidyl-prolyl-cis-trans-isomerase), sdhA (succinate deshydrogenase and mutS (methyl-directed mismatch repair). The pta gene was found to be repressed in the B. subtilis microarray data, a result which was inconsistent with a previous report by Presecan-Siedel et al [32], which demonstrated that pta, as is the case with other genes involved in acetate production are induced in the presence of glucose. An induction was also observed for the pta gene of E. coli [33]. The gapA gene was induced in B. subtilis and repressed in E. coli. The observation was consistent with other reports where the gapA of B. subtilis and other bacillus was described as being induced in the presence of glucose, as a result of its participation in the glycolitic pathway [33]. The opposite response for gapA in E. coli may be a consequence of its participation in gluconegenesis [13]. Very little is known about the regulation of mutS in E. coli and B. subtilis. This gene has been described as a DNA repair protein in the context of both bacteria [34]. Something similar happens to psrA in B subtilis, also known as ppiC in E. coli; where both enzymes function as molecular chaperones. It has been reported that prsA is essential for the stability of secreted proteins at certain stages, following translocation across the membrane [35]. Finally, the results observed for the genes sdhA (succinate deshydrogenase en B. subtilis) and frdA (fumarate reductase in E. coli) are quite interesting. Apparently, the functions of these two enzymes seem to be different; the succinate dehydrogenases of aerobic bacteria catalyze the oxidation of succinate by respiratory quinones (succinate:quinone reductase), and the quinols are reoxidized by O2 (succinate oxidase) [36]. In the case of B. subtilis; for some time it was thought that this enzyme has only this function, but in a recent report, the authors demonstrated that resting cells are able to catalyze fumarate reduction, with glucose or glycerol. The enzymatic system for fumarate reduction in B. subtilis was shown to be an electron transport chain, comprising a NADH dehydrogenase, menaquinone and succinate dehydrogenase [36]. Therefore, this enzyme is able to modify its function depending on the growth condition and energetic state of the cell.

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