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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 .

Transcriptional regulation of the carbohydrate utilization network in Thermotoga maritima