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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 and conservation of trehalose and glucose utilization genes and regulons in Thermotogales.
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Figure 4: Genomic context and conservation of trehalose and glucose utilization genes and regulons in Thermotogales.

Mentions: The ROK-family transcription factors GluR and TreR in T. maritima control the glucose and trehalose utilization pathways (Kazanov et al., 2013). The trehalose-responsive regulator TreR co-regulates the trehalose ABC transporter treEFG and the trehalose synthase-like gene treT, whereas GluR controls the glucose ABC transporter gluEFK in response to glucose. The glucose regulator has an additional binding site upstream of the treEFG operon, which is conserved in five closely related Thermotoga genomes (Figure 4). These results suggest that the trehalose transporter is under dual control of both regulators. The TreR regulon is conserved in all studied Thermotogales genomes except for Petrotoga mobilis.


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 and conservation of trehalose and glucose utilization genes and regulons in Thermotogales.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 4: Genomic context and conservation of trehalose and glucose utilization genes and regulons in Thermotogales.
Mentions: The ROK-family transcription factors GluR and TreR in T. maritima control the glucose and trehalose utilization pathways (Kazanov et al., 2013). The trehalose-responsive regulator TreR co-regulates the trehalose ABC transporter treEFG and the trehalose synthase-like gene treT, whereas GluR controls the glucose ABC transporter gluEFK in response to glucose. The glucose regulator has an additional binding site upstream of the treEFG operon, which is conserved in five closely related Thermotoga genomes (Figure 4). These results suggest that the trehalose transporter is under dual control of both regulators. The TreR regulon is conserved in all studied Thermotogales genomes except for Petrotoga mobilis.

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.