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Genomic Encyclopedia of Sugar Utilization Pathways in The Rodionov et al. BMC Genomics 2010, 11:494 http://www.biomedcentral.com/1471-2164/11/494 RESEARCH ARTICLE Open Access Genomic encyclopedia of sugar utilization pathways in the Shewanella genus Dmitry A Rodionov1,2, Chen Yang1,3, Xiaoqing Li1, Irina A Rodionova1, Yanbing Wang4, Anna Y Obraztsova4,7, Olga P Zagnitko5, Ross Overbeek5, Margaret F Romine6, Samantha Reed6, James K Fredrickson6, Kenneth H Nealson4,7, Andrei L Osterman1,5* 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 replace- ments 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. Background phylogenetically closely-related microorganisms. An abil- Carbohydrates comprise a key natural source of carbon ity to confidently reconstruct this machinery directly and energy for a variety of heterotrophic microbes. The from genomic sequence is crucial to an understanding diversity of carbohydrates (polymers, oligo- and mono- of microbial ecophysiology, evolution, adaptation, and saccharides)invariousecosystemsaswellasthediver- even interactions between microorganisms and their sity of microbial lifestyles is reflected in substantial var- animal, insect, or plant hosts. However, despite many iations of sugar catabolic machinery even between studies, the bulk of our knowledge about sugar utiliza- tion pathways is limited to a handful of model bacteria such as E. coli. An accurate projection of this knowledge * Correspondence: [email protected] across the growing variety of divergent bacteria with 1Burnham Institute for Medical Research, La Jolla, California 92037, USA Full list of author information is available at the end of the article completely sequenced genomes constitutes a substantial © 2010 Rodionov et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Rodionov et al. BMC Genomics 2010, 11:494 Page 2 of 19 http://www.biomedcentral.com/1471-2164/11/494 challenge. This is largely due to the aforementioned var- them are performed by a rather narrow spectrum of iations including numerous cases of non-orthologous enzymatic activities such as kinases, isomerases, oxidore- gene replacements, families of paralogous proteins with ductases, hydrolases, and aldolases. Sugar kinases or varying substrate specificity as well as alternative and phosphoenolpyruvate:sugar phosphotransferase systems presently unknown biochemical routes. Due to this (PTS) catalyze an essential phosphorylation step (as all complexity, genomic annotations of carbohydrate utili- intermediates of central carbon pathways to the point of zation genes derived solely from sequence similarity pyruvate are anchored by one or two phosphates). We analysis are often imprecise and incomplete, especially also included in this analysis associated transcriptional for relatively distant and poorly studied bacteria. regulators of sugar utilization pathways that mediate Shewanellaceae are a versatile family of Gram-negative specific induction of a catabolic pathway. For utilization g-proteobacteria that have adapted for survival in highly of various natural polysaccharides, many pathways are varied aquatic and sedimentary environments that exhibit equipped by upstream hydrolytic enzymes producing extremes in salinity, temperature, redox chemistry, and oligo-, di- or mono-saccharides that are then trans- hydrostatic pressure [1]. Although Shewanella can ported into the cell and further metabolized. These and respire with a diverse array of electron acceptors that other upstream and auxiliary (e.g. involved in sensing include organic compounds and metal oxides [2], they and chemotaxis) components of the carbohydrate utiliza- were thought to possess a relatively narrow capacity for tion machinery were typically excluded from our analy- utilizing electron donors, preferring simple carbon com- sis, except for those that share genomic context with pounds such as formate, lactate, and acetate. The recent other sugar utilization components. results from comparative and functional genomic analysis Ubiquitousprotein families [3], physiological experiments [4] and microarray analysis Despite their functional diversity, many characterized [5] demonstrated that S. oneidensis MR-1 can use a wide components of sugar utilization pathways occur in a array of complex carbon compounds including nucleo- limited number of protein families containing multiple tides, amino acids, mono- and polysaccharides. paralogs with varying substrate specificities. Representa- A subsystems-based approach to genome analysis tives of these families can be recognized by homology- allows us to substantially improve the accuracy of based genomic searches, thus providing a source of gene genomic annotations and to predict functions of pre- candidates for pathway reconstruction. On the other viously unknown gene families [6,7]. This approach hand, homology-based methods, taken alone, often fail includes a combination of comparative genomic tech- to reliably identify the exact substrate specificity. This niques such as the analysis of conserved operons and can be accomplished by additional reasoning based on regulons, with pathway reconstruction across a large the analysis of functional and genomic context (func- variety of genomes. Recently, we used a subsystems- tional coupling) [10]. based approach to predict and experimentally verify Strong functional coupling novel pathways of N-acetylglucosamine and lactate Bacterial genes involved in sugar catabolism are often utilization in Shewanella [8,9]. In the current study we organized in compact operons and/or regulated by com- have expanded this analysis towards genomic recon- mitted transcription factors. Therefore, genome context struction of the entire repertoire of carbohydrate utili- analysis techniques [6] based on the identification of zation pathways in a group of 19 species from the conserved chromosomal clusters (operons) and shared genus Shewanella with completely sequenced regulatory sites (regulons) are particularly efficient for genomes. accurate functional assignment of previously uncharac- terized genes of sugar utilization pathways. Results Based on the above considerations we developed the Reconstruction of carbohydrate utilization machinery in bioinformatic workflow that was applied for the analysis Shewanella spp of 19 complete Shewanella genomes (Fig. 1). The key To address the challenge of genomic reconstruction of starting point of this workflow was a collection of the carbohydrate utilization machinery we took advan- manually curated subsystems in the SEED genomic tage of several features characteristic of many sugar uti- database [7] capturing a substantial fraction of known lization pathways, such as: sugar utilization pathways projected across many bacter- Uniform functional organization ial species. A compilation of ~480 groups of isofunc- A typical sugar utilization pathway includes a transport tional homologs from this collection (see additional data system for sugar uptake and a set of intracellular file 1) was used as a source of queries for homology- enzymes that perform biochemical transformations. based scanning of 19 Shewanella genomes
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