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Transcriptional regulation of the carbohydrate utilization network in Thermotoga maritima.

Rodionov DA, Rodionova IA, Li X, Ravcheev DA, Tarasova Y, Portnoy VA, Zengler K, Osterman AL - Front Microbiol (2013)

Bottom Line: The observed upregulation of genes involved in catabolism of pectin, trehalose, cellobiose, arabinose, rhamnose, xylose, glucose, galactose, and ribose showed a strong correlation with the UxaR, TreR, BglR, CelR, AraR, RhaR, XylR, GluR, GalR, and RbsR regulons.Ultimately, this study elucidated the transcriptional regulatory network and mechanisms controlling expression of carbohydrate utilization genes in T. maritima.In addition to improving the functional annotations of associated transporters and catabolic enzymes, this research provides novel insights into the evolution of regulatory networks in Thermotogales.

View Article: PubMed Central - PubMed

Affiliation: Sanford-Burnham Medical Research Institute La Jolla, CA, USA ; A. A. Kharkevich Institute for Information Transmission Problems, Russian Academy of Sciences Moscow, Russia.

ABSTRACT
Hyperthermophilic bacteria from the Thermotogales lineage can produce hydrogen by fermenting a wide range of carbohydrates. Previous experimental studies identified a large fraction of genes committed to carbohydrate degradation and utilization in the model bacterium Thermotoga maritima. Knowledge of these genes enabled comprehensive reconstruction of biochemical pathways comprising the carbohydrate utilization network. However, transcriptional factors (TFs) and regulatory mechanisms driving this network remained largely unknown. Here, we used an integrated approach based on comparative analysis of genomic and transcriptomic data for the reconstruction of the carbohydrate utilization regulatory networks in 11 Thermotogales genomes. We identified DNA-binding motifs and regulons for 19 orthologous TFs in the Thermotogales. The inferred regulatory network in T. maritima contains 181 genes encoding TFs, sugar catabolic enzymes and ABC-family transporters. In contrast to many previously described bacteria, a transcriptional regulation strategy of Thermotoga does not employ global regulatory factors. The reconstructed regulatory network in T. maritima was validated by gene expression profiling on a panel of mono- and disaccharides and by in vitro DNA-binding assays. The observed upregulation of genes involved in catabolism of pectin, trehalose, cellobiose, arabinose, rhamnose, xylose, glucose, galactose, and ribose showed a strong correlation with the UxaR, TreR, BglR, CelR, AraR, RhaR, XylR, GluR, GalR, and RbsR regulons. Ultimately, this study elucidated the transcriptional regulatory network and mechanisms controlling expression of carbohydrate utilization genes in T. maritima. In addition to improving the functional annotations of associated transporters and catabolic enzymes, this research provides novel insights into the evolution of regulatory networks in Thermotogales.

No MeSH data available.


Genomic context of 15 sugar catabolic regulons in T. maritima. Validated and predicted effectors of TFs are listed in red and black, respectively. TF binding sites and downstream regulated genes are shown by circles and arrows, respectively. Validated sites are labeled with red check marks. Sequence logos representing the consensus binding site motifs were built using all candidate sites in the Thermotogales genomes. Genes encoding transcriptional regulators and components of sugar transporters are shown in black and red, respectively, whereas the genes encoding the secreted and intracellular sugar catabolic enzymes are in green and yellow, respectively. Hypothetical genes are in gray. Genes that were upregulated on specific sugars (listed in the last column) have their names highlighted in magenta.
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Figure 2: Genomic context of 15 sugar catabolic regulons in T. maritima. Validated and predicted effectors of TFs are listed in red and black, respectively. TF binding sites and downstream regulated genes are shown by circles and arrows, respectively. Validated sites are labeled with red check marks. Sequence logos representing the consensus binding site motifs were built using all candidate sites in the Thermotogales genomes. Genes encoding transcriptional regulators and components of sugar transporters are shown in black and red, respectively, whereas the genes encoding the secreted and intracellular sugar catabolic enzymes are in green and yellow, respectively. Hypothetical genes are in gray. Genes that were upregulated on specific sugars (listed in the last column) have their names highlighted in magenta.

Mentions: The obtained TF-binding motifs and respective sets of co-regulated operons in T. maritima are illustrated in Figure 2. Regulon content for orthologous TFs in other Thermotogales genomes is available in the RegPrecise database (Novichkov et al., 2010a) and in Table S2 in Supplementary Material. Metabolic content of 15 functionally annotated regulons is visualized on the integrative T. maritima sugar catabolic network (Figure 3). Below, we describe the reconstructed transcriptional regulatory network for sugar catabolism in the Thermotogales in more detail.


Transcriptional regulation of the carbohydrate utilization network in Thermotoga maritima.

Rodionov DA, Rodionova IA, Li X, Ravcheev DA, Tarasova Y, Portnoy VA, Zengler K, Osterman AL - Front Microbiol (2013)

Genomic context of 15 sugar catabolic regulons in T. maritima. Validated and predicted effectors of TFs are listed in red and black, respectively. TF binding sites and downstream regulated genes are shown by circles and arrows, respectively. Validated sites are labeled with red check marks. Sequence logos representing the consensus binding site motifs were built using all candidate sites in the Thermotogales genomes. Genes encoding transcriptional regulators and components of sugar transporters are shown in black and red, respectively, whereas the genes encoding the secreted and intracellular sugar catabolic enzymes are in green and yellow, respectively. Hypothetical genes are in gray. Genes that were upregulated on specific sugars (listed in the last column) have their names highlighted in magenta.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3750489&req=5

Figure 2: Genomic context of 15 sugar catabolic regulons in T. maritima. Validated and predicted effectors of TFs are listed in red and black, respectively. TF binding sites and downstream regulated genes are shown by circles and arrows, respectively. Validated sites are labeled with red check marks. Sequence logos representing the consensus binding site motifs were built using all candidate sites in the Thermotogales genomes. Genes encoding transcriptional regulators and components of sugar transporters are shown in black and red, respectively, whereas the genes encoding the secreted and intracellular sugar catabolic enzymes are in green and yellow, respectively. Hypothetical genes are in gray. Genes that were upregulated on specific sugars (listed in the last column) have their names highlighted in magenta.
Mentions: The obtained TF-binding motifs and respective sets of co-regulated operons in T. maritima are illustrated in Figure 2. Regulon content for orthologous TFs in other Thermotogales genomes is available in the RegPrecise database (Novichkov et al., 2010a) and in Table S2 in Supplementary Material. Metabolic content of 15 functionally annotated regulons is visualized on the integrative T. maritima sugar catabolic network (Figure 3). Below, we describe the reconstructed transcriptional regulatory network for sugar catabolism in the Thermotogales in more detail.

Bottom Line: The observed upregulation of genes involved in catabolism of pectin, trehalose, cellobiose, arabinose, rhamnose, xylose, glucose, galactose, and ribose showed a strong correlation with the UxaR, TreR, BglR, CelR, AraR, RhaR, XylR, GluR, GalR, and RbsR regulons.Ultimately, this study elucidated the transcriptional regulatory network and mechanisms controlling expression of carbohydrate utilization genes in T. maritima.In addition to improving the functional annotations of associated transporters and catabolic enzymes, this research provides novel insights into the evolution of regulatory networks in Thermotogales.

View Article: PubMed Central - PubMed

Affiliation: Sanford-Burnham Medical Research Institute La Jolla, CA, USA ; A. A. Kharkevich Institute for Information Transmission Problems, Russian Academy of Sciences Moscow, Russia.

ABSTRACT
Hyperthermophilic bacteria from the Thermotogales lineage can produce hydrogen by fermenting a wide range of carbohydrates. Previous experimental studies identified a large fraction of genes committed to carbohydrate degradation and utilization in the model bacterium Thermotoga maritima. Knowledge of these genes enabled comprehensive reconstruction of biochemical pathways comprising the carbohydrate utilization network. However, transcriptional factors (TFs) and regulatory mechanisms driving this network remained largely unknown. Here, we used an integrated approach based on comparative analysis of genomic and transcriptomic data for the reconstruction of the carbohydrate utilization regulatory networks in 11 Thermotogales genomes. We identified DNA-binding motifs and regulons for 19 orthologous TFs in the Thermotogales. The inferred regulatory network in T. maritima contains 181 genes encoding TFs, sugar catabolic enzymes and ABC-family transporters. In contrast to many previously described bacteria, a transcriptional regulation strategy of Thermotoga does not employ global regulatory factors. The reconstructed regulatory network in T. maritima was validated by gene expression profiling on a panel of mono- and disaccharides and by in vitro DNA-binding assays. The observed upregulation of genes involved in catabolism of pectin, trehalose, cellobiose, arabinose, rhamnose, xylose, glucose, galactose, and ribose showed a strong correlation with the UxaR, TreR, BglR, CelR, AraR, RhaR, XylR, GluR, GalR, and RbsR regulons. Ultimately, this study elucidated the transcriptional regulatory network and mechanisms controlling expression of carbohydrate utilization genes in T. maritima. In addition to improving the functional annotations of associated transporters and catabolic enzymes, this research provides novel insights into the evolution of regulatory networks in Thermotogales.

No MeSH data available.