Transcriptional regulation of the carbohydrate utilization network in Thermotoga maritima

Rodionov, Dmitry A.; Rodionova, Irina A.; Li, Xiaoqing; Ravcheev, Dmitry A.; Tarasova, Yekaterina; Portnoy, Vasiliy A.; Zengler, Karsten; Osterman, Andrei L.

doi:10.3389/fmicb.2013.00244

Transcriptional regulation of the carbohydrate utilization network in Thermotoga maritima

Journal Article · Mon Dec 31 23:00:00 EST 2012 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2013.00244· OSTI ID:1628093

Rodionov, Dmitry A. ^[1]; Rodionova, Irina A. ^[2]; Li, Xiaoqing ^[2]; Ravcheev, Dmitry A. ^[3]; Tarasova, Yekaterina ^[4]; Portnoy, Vasiliy A. ^[4]; Zengler, Karsten ^[4]; Osterman, Andrei L. ^[2]

Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA (United States); Russian Academy of Sciences (RAS), Moscow (Russian Federation). A.A. Kharkevich Inst. for Informaiton Transmission Problems; DOE/OSTI
Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA (United States)
Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA (United States); Russian Academy of Sciences (RAS), Moscow (Russian Federation). A.A. Kharkevich Inst. for Informaiton Transmission Problems
Univ. of California, San Diego, CA (United States). Dept. of Bioengineering

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.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of California, San Diego, CA (United States); Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: FG02-08ER64686; SC0004999

OSTI ID:: 1628093

Journal Information:: Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 4; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

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Transcriptional regulation of the carbohydrate utilization network in Thermotoga maritima

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