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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.


Properties of 11 Thermotogales species analyzed in this study. (A) The geographic isolation sites for the Thermotogales strains. (B) Distribution of sugar utilization pathways and cognate transcriptional regulators. The presence of orthologous genes encoding regulators and associated sugar catabolic pathways is shown by “+” and colored circles, respectively. The phylogenetic species tree was constructed using the concatenated alignment of 78 universal bacterial proteins in the MicrobesOnline database (http://www.microbesonline.org/cgi-bin/speciesTree.cgi).
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Figure 1: Properties of 11 Thermotogales species analyzed in this study. (A) The geographic isolation sites for the Thermotogales strains. (B) Distribution of sugar utilization pathways and cognate transcriptional regulators. The presence of orthologous genes encoding regulators and associated sugar catabolic pathways is shown by “+” and colored circles, respectively. The phylogenetic species tree was constructed using the concatenated alignment of 78 universal bacterial proteins in the MicrobesOnline database (http://www.microbesonline.org/cgi-bin/speciesTree.cgi).

Mentions: Thermotoga spp. are anaerobic fermentative bacteria that are able to grow on various simple and complex carbohydrates including glucose, starch, cellobiose, xylan, and pectin while producing hydrogen, carbon dioxide, and acetate (Chhabra et al., 2002; Kluskens et al., 2003; Conners et al., 2006). T. maritima MSB8, a model bacterium in the Thermotoga group, was isolated from geothermally heated marine sediments of Volcano Island in Italy (Huber et al., 1986). A closely related bacterium, T. neapolitana, was isolated from a submarine thermal vent near Lucrino, Bay of Naples, Italy (Jannasch et al., 1988). Other Thermotogales have a broad geographic distribution (see Figure 1) including hydrothermal vents in the Azores [Themotoga sp. RQ-2, (Swithers et al., 2011)], a sulfate-reducing bioreactor in Europe [T. lettingae, (Balk et al., 2002)], a hot spring in New Zealand [Fervidobacterium nodosum, (Patel et al., 1985)], and an offshore oil reservoir in Japan [T. naphthophila, T. petrophila, (Takahata et al., 2000)].


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)

Properties of 11 Thermotogales species analyzed in this study. (A) The geographic isolation sites for the Thermotogales strains. (B) Distribution of sugar utilization pathways and cognate transcriptional regulators. The presence of orthologous genes encoding regulators and associated sugar catabolic pathways is shown by “+” and colored circles, respectively. The phylogenetic species tree was constructed using the concatenated alignment of 78 universal bacterial proteins in the MicrobesOnline database (http://www.microbesonline.org/cgi-bin/speciesTree.cgi).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Properties of 11 Thermotogales species analyzed in this study. (A) The geographic isolation sites for the Thermotogales strains. (B) Distribution of sugar utilization pathways and cognate transcriptional regulators. The presence of orthologous genes encoding regulators and associated sugar catabolic pathways is shown by “+” and colored circles, respectively. The phylogenetic species tree was constructed using the concatenated alignment of 78 universal bacterial proteins in the MicrobesOnline database (http://www.microbesonline.org/cgi-bin/speciesTree.cgi).
Mentions: Thermotoga spp. are anaerobic fermentative bacteria that are able to grow on various simple and complex carbohydrates including glucose, starch, cellobiose, xylan, and pectin while producing hydrogen, carbon dioxide, and acetate (Chhabra et al., 2002; Kluskens et al., 2003; Conners et al., 2006). T. maritima MSB8, a model bacterium in the Thermotoga group, was isolated from geothermally heated marine sediments of Volcano Island in Italy (Huber et al., 1986). A closely related bacterium, T. neapolitana, was isolated from a submarine thermal vent near Lucrino, Bay of Naples, Italy (Jannasch et al., 1988). Other Thermotogales have a broad geographic distribution (see Figure 1) including hydrothermal vents in the Azores [Themotoga sp. RQ-2, (Swithers et al., 2011)], a sulfate-reducing bioreactor in Europe [T. lettingae, (Balk et al., 2002)], a hot spring in New Zealand [Fervidobacterium nodosum, (Patel et al., 1985)], and an offshore oil reservoir in Japan [T. naphthophila, T. petrophila, (Takahata et al., 2000)].

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.