This article is part of the supplement: Validation methods for functional genome annotation

Open Access Research

Comparative genomic reconstruction of transcriptional networks controlling central metabolism in the Shewanella genus

Dmitry A Rodionov12*, Pavel S Novichkov3, Elena D Stavrovskaya24, Irina A Rodionova1, Xiaoqing Li1, Marat D Kazanov12, Dmitry A Ravcheev12, Anna V Gerasimova3, Alexey E Kazakov23, Galina Yu Kovaleva2, Elizabeth A Permina5, Olga N Laikova5, Ross Overbeek6, Margaret F Romine7, James K Fredrickson7, Adam P Arkin3, Inna Dubchak38, Andrei L Osterman16 and Mikhail S Gelfand24

Author Affiliations

1 Sanford-Burnham Medical Research Institute, La Jolla, California, USA

2 Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow, Russia

3 Lawrence Berkeley National Laboratory, Berkeley, California, USA

4 Faculty of Bioengineering and Bioinformatics, Moscow State University, Moscow, Russia

5 State Scientific Center GosNIIGenetika, Moscow, Russia

6 Fellowship for Interpretation of Genomes, Burr Ridge, Illinois, USA

7 Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA

8 Department of Energy Joint Genome Institute, Walnut Creek, California, USA

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BMC Genomics 2011, 12(Suppl 1):S3  doi:10.1186/1471-2164-12-S1-S3

Published: 15 June 2011

Abstract

Background

Genome-scale prediction of gene regulation and reconstruction of transcriptional regulatory networks in bacteria is one of the critical tasks of modern genomics. The Shewanella genus is comprised of metabolically versatile gamma-proteobacteria, whose lifestyles and natural environments are substantially different from Escherichia coli and other model bacterial species. The comparative genomics approaches and computational identification of regulatory sites are useful for the in silico reconstruction of transcriptional regulatory networks in bacteria.

Results

To explore conservation and variations in the Shewanella transcriptional networks we analyzed the repertoire of transcription factors and performed genomics-based reconstruction and comparative analysis of regulons in 16 Shewanella genomes. The inferred regulatory network includes 82 transcription factors and their DNA binding sites, 8 riboswitches and 6 translational attenuators. Forty five regulons were newly inferred from the genome context analysis, whereas others were propagated from previously characterized regulons in the Enterobacteria and Pseudomonas spp.. Multiple variations in regulatory strategies between the Shewanella spp. and E. coli include regulon contraction and expansion (as in the case of PdhR, HexR, FadR), numerous cases of recruiting non-orthologous regulators to control equivalent pathways (e.g. PsrA for fatty acid degradation) and, conversely, orthologous regulators to control distinct pathways (e.g. TyrR, ArgR, Crp).

Conclusions

We tentatively defined the first reference collection of ~100 transcriptional regulons in 16 Shewanella genomes. The resulting regulatory network contains ~600 regulated genes per genome that are mostly involved in metabolism of carbohydrates, amino acids, fatty acids, vitamins, metals, and stress responses. Several reconstructed regulons including NagR for N-acetylglucosamine catabolism were experimentally validated in S. oneidensis MR-1. Analysis of correlations in gene expression patterns helps to interpret the reconstructed regulatory network. The inferred regulatory interactions will provide an additional regulatory constrains for an integrated model of metabolism and regulation in S. oneidensis MR-1.