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Original Research ARTICLE

Front. Microbiol., 23 August 2013 | http://dx.doi.org/10.3389/fmicb.2013.00244

Transcriptional regulation of the carbohydrate utilization network in Thermotoga maritima

Dmitry A. Rodionov1,2*, Irina A. Rodionova1, Xiaoqing Li1, Dmitry A. Ravcheev1,2, Yekaterina Tarasova3, Vasiliy A. Portnoy3, Karsten Zengler3 and Andrei L. Osterman1
  • 1Sanford-Burnham Medical Research Institute, La Jolla, CA, USA
  • 2A. A. Kharkevich Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow, Russia
  • 3Department of Bioengineering, University of California San Diego, La Jolla, CA, USA

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.

Keywords: carbohydrate metabolism, transcriptional regulation, regulon, comparative genomics, Thermotoga

Citation: Rodionov DA, Rodionova IA, Li X, Ravcheev DA, Tarasova Y, Portnoy VA, Zengler K and Osterman AL (2013) Transcriptional regulation of the carbohydrate utilization network in Thermotoga maritima. Front. Microbiol. 4:244. doi: 10.3389/fmicb.2013.00244

Received: 13 June 2013; Accepted: 31 July 2013;
Published online: 23 August 2013.

Edited by:

Aindrila Mukhopadhyay, Lawrence Berkeley National Laboratory, USA

Reviewed by:

Dong-Woo Lee, Kyungpook National University, South Korea
Aindrila Mukhopadhyay, Lawrence Berkeley National Laboratory, USA

Copyright © 2013 Rodionov, Rodionova, Li, Ravcheev, Tarasova, Portnoy, Zengler and Osterman. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Dmitry A. Rodionov, Sanford-Burnham Medical Research Institute, 10901 North Torrey Pines Road, La Jolla, CA 92037, USA e-mail: rodionov@burnham.org