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Open Access Research article

Genomic encyclopedia of sugar utilization pathways in the Shewanella genus

Dmitry A Rodionov12, Chen Yang13, Xiaoqing Li1, Irina A Rodionova1, Yanbing Wang4, Anna Y Obraztsova47, Olga P Zagnitko5, Ross Overbeek5, Margaret F Romine6, Samantha Reed6, James K Fredrickson6, Kenneth H Nealson47 and Andrei L Osterman15*

Author affiliations

1 Burnham Institute for Medical Research, La Jolla, California 92037, USA

2 Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow 127994, Russia

3 Key Laboratory of Synthetic Biology, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China

4 Department of Earth Sciences, University of Southern California, Los Angeles, California 90089, USA

5 Fellowship for Interpretation of Genomes, Burr Ridge, Illinois 60527, USA

6 Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington 99352, USA

7 J. Craig Venter Institute, San Diego, California 92121, USA

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Citation and License

BMC Genomics 2010, 11:494  doi:10.1186/1471-2164-11-494

Published: 13 September 2010

Abstract

Background

Carbohydrates are a primary source of carbon and energy for many bacteria. Accurate projection of known carbohydrate catabolic pathways across diverse bacteria with complete genomes constitutes a substantial challenge due to frequent variations in components of these pathways. To address a practically and fundamentally important challenge of reconstruction of carbohydrate utilization machinery in any microorganism directly from its genomic sequence, we combined a subsystems-based comparative genomic approach with experimental validation of selected bioinformatic predictions by a combination of biochemical, genetic and physiological experiments.

Results

We applied this integrated approach to systematically map carbohydrate utilization pathways in 19 genomes from the Shewanella genus. The obtained genomic encyclopedia of sugar utilization includes ~170 protein families (mostly metabolic enzymes, transporters and transcriptional regulators) spanning 17 distinct pathways with a mosaic distribution across Shewanella species providing insights into their ecophysiology and adaptive evolution. Phenotypic assays revealed a remarkable consistency between predicted and observed phenotype, an ability to utilize an individual sugar as a sole source of carbon and energy, over the entire matrix of tested strains and sugars.

Comparison of the reconstructed catabolic pathways with E. coli identified multiple differences that are manifested at various levels, from the presence or absence of certain sugar catabolic pathways, nonorthologous gene replacements and alternative biochemical routes to a different organization of transcription regulatory networks.

Conclusions

The reconstructed sugar catabolome in Shewanella spp includes 62 novel isofunctional families of enzymes, transporters, and regulators. In addition to improving our knowledge of genomics and functional organization of carbohydrate utilization in Shewanella, this study led to a substantial expansion of our current version of the Genomic Encyclopedia of Carbohydrate Utilization. A systematic and iterative application of this approach to multiple taxonomic groups of bacteria will further enhance it, creating a knowledge base adequate for the efficient analysis of any newly sequenced genome as well as of the emerging metagenomic data.