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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.


Integrative reconstruction of sugar utilization pathways and regulons in T. maritima. Diagram includes 190 carbohydrate utilization genes encoding catabolic enzymes (solid arrows), transporters (dotted arrows), and transcriptional factors (in ovals of different colors). Genes involved in the reconstructed regulatory network (161 genes regulated by 15 TFs) are highlighted by a matching background color. Three hypothetical sugar utilization pathways and the respective regulons (UgtR, UctR, UgpR) are not shown.
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Figure 3: Integrative reconstruction of sugar utilization pathways and regulons in T. maritima. Diagram includes 190 carbohydrate utilization genes encoding catabolic enzymes (solid arrows), transporters (dotted arrows), and transcriptional factors (in ovals of different colors). Genes involved in the reconstructed regulatory network (161 genes regulated by 15 TFs) are highlighted by a matching background color. Three hypothetical sugar utilization pathways and the respective regulons (UgtR, UctR, UgpR) are not shown.

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)

Integrative reconstruction of sugar utilization pathways and regulons in T. maritima. Diagram includes 190 carbohydrate utilization genes encoding catabolic enzymes (solid arrows), transporters (dotted arrows), and transcriptional factors (in ovals of different colors). Genes involved in the reconstructed regulatory network (161 genes regulated by 15 TFs) are highlighted by a matching background color. Three hypothetical sugar utilization pathways and the respective regulons (UgtR, UctR, UgpR) are not shown.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: Integrative reconstruction of sugar utilization pathways and regulons in T. maritima. Diagram includes 190 carbohydrate utilization genes encoding catabolic enzymes (solid arrows), transporters (dotted arrows), and transcriptional factors (in ovals of different colors). Genes involved in the reconstructed regulatory network (161 genes regulated by 15 TFs) are highlighted by a matching background color. Three hypothetical sugar utilization pathways and the respective regulons (UgtR, UctR, UgpR) are not shown.
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.