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Article: Comparative Genomic Analysis of the Human Gut Microbiome Reveals a Broad Distribution of Metabolic Pathways for the Degradation of Host-Synthetized Mucin Glycans and Utilization of Mucin-Derived Monosaccharides.

Ravcheev, Dmitry A / Thiele, Ines

2017 Volume 8, Page(s) 111

Abstract: The colonic mucus layer is a dynamic and complex structure formed by secreted and transmembrane mucins, which are high-molecular-weight and heavily glycosylated proteins. Colonic mucus consists of a loose outer layer and a dense epithelium-attached layer. ...

Abstract	The colonic mucus layer is a dynamic and complex structure formed by secreted and transmembrane mucins, which are high-molecular-weight and heavily glycosylated proteins. Colonic mucus consists of a loose outer layer and a dense epithelium-attached layer. The outer layer is inhabited by various representatives of the human gut microbiota (HGM). Glycans of the colonic mucus can be used by the HGM as a source of carbon and energy when dietary fibers are not sufficiently available. Both commensals and pathogens can utilize mucin glycans. Commensals are mostly involved in the cleavage of glycans, while pathogens mostly utilize monosaccharides released by commensals. This HGM-derived degradation of the mucus layer increases pathogen susceptibility and causes many other health disorders. Here, we analyzed 397 individual HGM genomes to identify pathways for the cleavage of host-synthetized mucin glycans to monosaccharides as well as for the catabolism of the derived monosaccharides. Our key results are as follows: (i) Genes for the cleavage of mucin glycans were found in 86% of the analyzed genomes, which significantly higher than a previous estimation. (ii) Genes for the catabolism of derived monosaccharides were found in 89% of the analyzed genomes. (iii) Comparative genomic analysis identified four alternative forms of the monosaccharide-catabolizing enzymes and four alternative forms of monosaccharide transporters. (iv) Eighty-five percent of the analyzed genomes may be involved in potential feeding pathways for the monosaccharides derived from cleaved mucin glycans. (v) The analyzed genomes demonstrated different abilities to degrade known mucin glycans. Generally, the ability to degrade at least one type of mucin glycan was predicted for 81% of the analyzed genomes. (vi) Eighty-two percent of the analyzed genomes can form mutualistic pairs that are able to degrade mucin glycans and are not degradable by any of the paired organisms alone. Taken together, these findings provide further insight into the inter-microbial communications of the HGM as well as into host-HGM interactions.
Language	English
Publishing date	2017-08-29
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2606823-0
ISSN	1664-8021
ISSN	1664-8021
DOI	10.3389/fgene.2017.00111
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Article: Genomic Analysis of the Human Gut Microbiome Suggests Novel Enzymes Involved in Quinone Biosynthesis.

Ravcheev, Dmitry A / Thiele, Ines

Frontiers in microbiology

2016 Volume 7, Page(s) 128

Abstract: Ubiquinone and menaquinone are membrane lipid-soluble carriers of electrons that are essential for cellular respiration. Eukaryotic cells can synthesize ubiquinone but not menaquinone, whereas prokaryotes can synthesize both quinones. So far, most of the ...

Abstract	Ubiquinone and menaquinone are membrane lipid-soluble carriers of electrons that are essential for cellular respiration. Eukaryotic cells can synthesize ubiquinone but not menaquinone, whereas prokaryotes can synthesize both quinones. So far, most of the human gut microbiome (HGM) studies have been based on metagenomic analysis. Here, we applied an analysis of individual HGM genomes to the identification of ubiquinone and menaquinone biosynthetic pathways. In our opinion, the shift from metagenomics to analysis of individual genomes is a pivotal milestone in investigation of bacterial communities, including the HGM. The key results of this study are as follows. (i) The distribution of the canonical pathways in the HGM genomes was consistent with previous reports and with the distribution of the quinone-dependent reductases for electron acceptors. (ii) The comparative genomics analysis identified four alternative forms of the previously known enzymes for quinone biosynthesis. (iii) Genes for the previously unknown part of the futalosine pathway were identified, and the corresponding biochemical reactions were proposed. We discuss the remaining gaps in the menaquinone and ubiquinone pathways in some of the microbes, which indicate the existence of further alternate genes or routes. Together, these findings provide further insight into the biosynthesis of quinones in bacteria and the physiology of the HGM.
Language	English
Publishing date	2016-02-09
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2587354-4
ISSN	1664-302X
ISSN	1664-302X
DOI	10.3389/fmicb.2016.00128
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Article: Comparative Genomic Analysis Reveals Novel Microcompartment-Associated Metabolic Pathways in the Human Gut Microbiome.

Ravcheev, Dmitry A / Moussu, Lubin / Smajic, Semra / Thiele, Ines

Frontiers in genetics

2019 Volume 10, Page(s) 636

Abstract: Bacterial microcompartments are self-assembling subcellular structures surrounded by a semipermeable protein shell and found only in bacteria, but not archaea or eukaryotes. The general functions of the bacterial microcompartments are to concentrate ... ...

Abstract	Bacterial microcompartments are self-assembling subcellular structures surrounded by a semipermeable protein shell and found only in bacteria, but not archaea or eukaryotes. The general functions of the bacterial microcompartments are to concentrate enzymes, metabolites, and cofactors for multistep pathways; maintain the cofactor ratio; protect the cell from toxic metabolic intermediates; and protect the encapsulated pathway from unwanted side reactions. The bacterial microcompartments were suggested to play a significant role in organisms of the human gut microbiome, especially for various pathogens. Here, we used a comparative genomics approach to analyze the bacterial microcompartments in 646 individual genomes of organisms commonly found in the human gut microbiome. The bacterial microcompartments were found in 150 (23.2%) analyzed genomes. These microcompartments include previously known ones for the utilization of ethanolamine, 1,2-propanediol, choline, and fucose/rhamnose. Moreover, we reconstructed two novel pathways associated with the bacterial microcompartments. These pathways are catabolic pathways for the utilization of 1-amino-2-propanol/1-amino-2-propanone and xanthine. Remarkably, the xanthine utilization pathway does not demonstrate similarity to previously known microcompartment-associated pathways. Thus, we describe a novel type of bacterial microcompartment.
Language	English
Publishing date	2019-07-04
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2606823-0
ISSN	1664-8021
ISSN	1664-8021
DOI	10.3389/fgene.2019.00636
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Article: Systematic genomic analysis reveals the complementary aerobic and anaerobic respiration capacities of the human gut microbiota.

Ravcheev, Dmitry A / Thiele, Ines

Frontiers in microbiology

2014 Volume 5, Page(s) 674

Abstract: Because of the specific anatomical and physiological properties of the human intestine, a specific oxygen gradient builds up within this organ that influences the intestinal microbiota. The intestinal microbiome has been intensively studied in recent ... ...

Abstract	Because of the specific anatomical and physiological properties of the human intestine, a specific oxygen gradient builds up within this organ that influences the intestinal microbiota. The intestinal microbiome has been intensively studied in recent years, and certain respiratory substrates used by gut inhabiting microbes have been shown to play a crucial role in human health. Unfortunately, a systematic analysis has not been previously performed to determine the respiratory capabilities of human gut microbes (HGM). Here, we analyzed the distribution of aerobic and anaerobic respiratory reductases in 254 HGM genomes. In addition to the annotation of known enzymes, we also predicted a novel microaerobic reductase and novel thiosulfate reductase. Based on this comprehensive assessment of respiratory reductases in the HGM, we proposed a number of exchange pathways among different bacteria involved in the reduction of various nitrogen oxides. The results significantly expanded our knowledge of HGM metabolism and interactions in bacterial communities.
Language	English
Publishing date	2014-12-05
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2587354-4
ISSN	1664-302X
ISSN	1664-302X
DOI	10.3389/fmicb.2014.00674
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Article ; Online: Systematic assessment of secondary bile acid metabolism in gut microbes reveals distinct metabolic capabilities in inflammatory bowel disease.

Heinken, Almut / Ravcheev, Dmitry A / Baldini, Federico / Heirendt, Laurent / Fleming, Ronan M T / Thiele, Ines

Microbiome

2019 Volume 7, Issue 1, Page(s) 75

Abstract: Background: The human gut microbiome performs important functions in human health and disease. A classic example for host-gut microbial co-metabolism is host biosynthesis of primary bile acids and their subsequent deconjugation and transformation by the ...

Abstract	Background: The human gut microbiome performs important functions in human health and disease. A classic example for host-gut microbial co-metabolism is host biosynthesis of primary bile acids and their subsequent deconjugation and transformation by the gut microbiome. To understand these system-level host-microbe interactions, a mechanistic, multi-scale computational systems biology approach that integrates the different types of omic data is needed. Here, we use a systematic workflow to computationally model bile acid metabolism in gut microbes and microbial communities. Results: Therefore, we first performed a comparative genomic analysis of bile acid deconjugation and biotransformation pathways in 693 human gut microbial genomes and expanded 232 curated genome-scale microbial metabolic reconstructions with the corresponding reactions (available at https://vmh.life ). We then predicted the bile acid biotransformation potential of each microbe and in combination with other microbes. We found that each microbe could produce maximally six of the 13 secondary bile acids in silico, while microbial pairs could produce up to 12 bile acids, suggesting bile acid biotransformation being a microbial community task. To investigate the metabolic potential of a given microbiome, publicly available metagenomics data from healthy Western individuals, as well as inflammatory bowel disease patients and healthy controls, were mapped onto the genomes of the reconstructed strains. We constructed for each individual a large-scale personalized microbial community model that takes into account strain-level abundances. Using flux balance analysis, we found considerable variation in the potential to deconjugate and transform primary bile acids between the gut microbiomes of healthy individuals. Moreover, the microbiomes of pediatric inflammatory bowel disease patients were significantly depleted in their bile acid production potential compared with that of controls. The contributions of each strain to overall bile acid production potential across individuals were found to be distinct between inflammatory bowel disease patients and controls. Finally, bottlenecks limiting secondary bile acid production potential were identified in each microbiome model. Conclusions: This large-scale modeling approach provides a novel way of analyzing metagenomics data to accelerate our understanding of the metabolic interactions between the host and gut microbiomes in health and diseases states. Our models and tools are freely available to the scientific community.
MeSH term(s)	Bile Acids and Salts/metabolism ; Gastrointestinal Microbiome ; Genomics ; Host-Pathogen Interactions ; Humans ; Inflammatory Bowel Diseases/metabolism ; Inflammatory Bowel Diseases/microbiology ; Lipid Metabolism ; Metagenomics ; Systems Biology
Chemical Substances	Bile Acids and Salts
Language	English
Publishing date	2019-05-15
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2697425-3
ISSN	2049-2618 ; 2049-2618
ISSN (online)	2049-2618
ISSN	2049-2618
DOI	10.1186/s40168-019-0689-3
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Article ; Online: Genome-scale metabolic reconstruction of 7,302 human microorganisms for personalized medicine.

Heinken, Almut / Hertel, Johannes / Acharya, Geeta / Ravcheev, Dmitry A / Nyga, Malgorzata / Okpala, Onyedika Emmanuel / Hogan, Marcus / Magnúsdóttir, Stefanía / Martinelli, Filippo / Nap, Bram / Preciat, German / Edirisinghe, Janaka N / Henry, Christopher S / Fleming, Ronan M T / Thiele, Ines

Nature biotechnology

2023 Volume 41, Issue 9, Page(s) 1320–1331

Abstract: The human microbiome influences the efficacy and safety of a wide variety of commonly prescribed drugs. Designing precision medicine approaches that incorporate microbial metabolism would require strain- and molecule-resolved, scalable computational ... ...

Abstract	The human microbiome influences the efficacy and safety of a wide variety of commonly prescribed drugs. Designing precision medicine approaches that incorporate microbial metabolism would require strain- and molecule-resolved, scalable computational modeling. Here, we extend our previous resource of genome-scale metabolic reconstructions of human gut microorganisms with a greatly expanded version. AGORA2 (assembly of gut organisms through reconstruction and analysis, version 2) accounts for 7,302 strains, includes strain-resolved drug degradation and biotransformation capabilities for 98 drugs, and was extensively curated based on comparative genomics and literature searches. The microbial reconstructions performed very well against three independently assembled experimental datasets with an accuracy of 0.72 to 0.84, surpassing other reconstruction resources and predicted known microbial drug transformations with an accuracy of 0.81. We demonstrate that AGORA2 enables personalized, strain-resolved modeling by predicting the drug conversion potential of the gut microbiomes from 616 patients with colorectal cancer and controls, which greatly varied between individuals and correlated with age, sex, body mass index and disease stages. AGORA2 serves as a knowledge base for the human microbiome and paves the way to personalized, predictive analysis of host-microbiome metabolic interactions.
MeSH term(s)	Humans ; Precision Medicine ; Genome ; Genomics ; Gastrointestinal Microbiome/genetics ; Microbiota
Language	English
Publishing date	2023-01-19
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1311932-1
ISSN	1546-1696 ; 1087-0156
ISSN (online)	1546-1696
ISSN	1087-0156
DOI	10.1038/s41587-022-01628-0
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Article: Nitrogen Fixation and Molecular Oxygen: Comparative Genomic Reconstruction of Transcription Regulation in Alphaproteobacteria.

Tsoy, Olga V / Ravcheev, Dmitry A / Čuklina, Jelena / Gelfand, Mikhail S

Frontiers in microbiology

2016 Volume 7, Page(s) 1343

Abstract: Biological nitrogen fixation plays a crucial role in the nitrogen cycle. An ability to fix atmospheric nitrogen, reducing it to ammonium, was described for multiple species of Bacteria and Archaea. The transcriptional regulatory network for nitrogen ... ...

Abstract	Biological nitrogen fixation plays a crucial role in the nitrogen cycle. An ability to fix atmospheric nitrogen, reducing it to ammonium, was described for multiple species of Bacteria and Archaea. The transcriptional regulatory network for nitrogen fixation was extensively studied in several representatives of the class Alphaproteobacteria. This regulatory network includes the activator of nitrogen fixation NifA, working in tandem with the alternative sigma-factor RpoN as well as oxygen-responsive regulatory systems, one-component regulators FnrN/FixK and two-component system FixLJ. Here we used a comparative genomics approach for in silico study of the transcriptional regulatory network in 50 genomes of Alphaproteobacteria. We extended the known regulons and proposed the scenario for the evolution of the nitrogen fixation transcriptional network. The reconstructed network substantially expands the existing knowledge of transcriptional regulation in nitrogen-fixing microorganisms and can be used for genetic experiments, metabolic reconstruction, and evolutionary analysis.
Language	English
Publishing date	2016-08-26
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2587354-4
ISSN	1664-302X
ISSN	1664-302X
DOI	10.3389/fmicb.2016.01343
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Article ; Online: Paracoccus denitrificans possesses two BioR homologs having a role in regulation of biotin metabolism.

Feng, Youjun / Kumar, Ritesh / Ravcheev, Dmitry A / Zhang, Huimin

MicrobiologyOpen

2015 Volume 4, Issue 4, Page(s) 644–659

Abstract: Recently, we determined that BioR, the GntR family of transcription factor, acts as a repressor for biotin metabolism exclusively distributed in certain species of α-proteobacteria, including the zoonotic agent Brucella melitensis and the plant pathogen ... ...

Abstract	Recently, we determined that BioR, the GntR family of transcription factor, acts as a repressor for biotin metabolism exclusively distributed in certain species of α-proteobacteria, including the zoonotic agent Brucella melitensis and the plant pathogen Agrobacterium tumefaciens. However, the scenario is unusual in Paracoccus denitrificans, another closely related member of the same phylum α-proteobacteria featuring with denitrification. Not only does it encode two BioR homologs Pden_1431 and Pden_2922 (designated as BioR1 and BioR2, respectively), but also has six predictive BioR-recognizable sites (the two bioR homolog each has one site, whereas the two bio operons (bioBFDAGC and bioYB) each contains two tandem BioR boxes). It raised the possibility that unexpected complexity is present in BioR-mediated biotin regulation. Here we report that this is the case. The identity of the purified BioR proteins (BioR1 and BioR2) was confirmed with LC-QToF-MS. Phylogenetic analyses combined with GC percentage raised a possibility that the bioR2 gene might be acquired by horizontal gene transfer. Gel shift assays revealed that the predicted BioR-binding sites are functional for the two BioR homologs, in much similarity to the scenario seen with the BioR site of A. tumefaciens bioBFDAZ. Using the A. tumefaciens reporter system carrying a plasmid-borne LacZ fusion, we revealed that the two homologs of P. denitrificans BioR are functional repressors for biotin metabolism. As anticipated, not only does the addition of exogenous biotin stimulate efficiently the expression of bioYB operon encoding biotin transport/uptake system BioY, but also inhibits the transcription of the bioBFDAGC operon resembling the de novo biotin synthetic pathway. EMSA-based screening failed to demonstrate that the biotin-related metabolite is involved in BioR-DNA interplay, which is consistent with our former observation with Brucella BioR. Our finding defined a complex regulatory network for biotin metabolism in P. denitrificans by two BioR proteins.
MeSH term(s)	Agrobacterium tumefaciens/genetics ; Agrobacterium tumefaciens/metabolism ; Artificial Gene Fusion ; Binding Sites ; Biotin/metabolism ; DNA, Bacterial/metabolism ; Electrophoretic Mobility Shift Assay ; Gene Expression Regulation, Bacterial ; Genes, Reporter ; Genetic Variation ; Paracoccus denitrificans/genetics ; Paracoccus denitrificans/metabolism ; Phylogeny ; Promoter Regions, Genetic ; Protein Binding ; Repressor Proteins/genetics ; Repressor Proteins/metabolism ; Sequence Homology ; beta-Galactosidase/analysis ; beta-Galactosidase/genetics
Chemical Substances	DNA, Bacterial ; Repressor Proteins ; Biotin (6SO6U10H04) ; beta-Galactosidase (EC 3.2.1.23)
Language	English
Publishing date	2015-08
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2661368-2
ISSN	2045-8827 ; 2045-8827
ISSN (online)	2045-8827
ISSN	2045-8827
DOI	10.1002/mbo3.270
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Article: 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

Frontiers in microbiology

2013 Volume 4, Page(s) 244

Abstract: 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 ... ...

Abstract	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.
Language	English
Publishing date	2013-08-23
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2587354-4
ISSN	1664-302X
ISSN	1664-302X
DOI	10.3389/fmicb.2013.00244
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Article ; Online: Polysaccharides utilization in human gut bacterium Bacteroides thetaiotaomicron: comparative genomics reconstruction of metabolic and regulatory networks.

Ravcheev, Dmitry A / Godzik, Adam / Osterman, Andrei L / Rodionov, Dmitry A

BMC genomics

2013 Volume 14, Page(s) 873

Abstract: Background: Bacteroides thetaiotaomicron, a predominant member of the human gut microbiota, is characterized by its ability to utilize a wide variety of polysaccharides using the extensive saccharolytic machinery that is controlled by an expanded ... ...

Abstract	Background: Bacteroides thetaiotaomicron, a predominant member of the human gut microbiota, is characterized by its ability to utilize a wide variety of polysaccharides using the extensive saccharolytic machinery that is controlled by an expanded repertoire of transcription factors (TFs). The availability of genomic sequences for multiple Bacteroides species opens an opportunity for their comparative analysis to enable characterization of their metabolic and regulatory networks. Results: A comparative genomics approach was applied for the reconstruction and functional annotation of the carbohydrate utilization regulatory networks in 11 Bacteroides genomes. Bioinformatics analysis of promoter regions revealed putative DNA-binding motifs and regulons for 31 orthologous TFs in the Bacteroides. Among the analyzed TFs there are 4 SusR-like regulators, 16 AraC-like hybrid two-component systems (HTCSs), and 11 regulators from other families. Novel DNA motifs of HTCSs and SusR-like regulators in the Bacteroides have the common structure of direct repeats with a long spacer between two conserved sites. Conclusions: The inferred regulatory network in B. thetaiotaomicron contains 308 genes encoding polysaccharide and sugar catabolic enzymes, carbohydrate-binding and transport systems, and TFs. The analyzed TFs control pathways for utilization of host and dietary glycans to monosaccharides and their further interconversions to intermediates of the central metabolism. The reconstructed regulatory network allowed us to suggest and refine specific functional assignments for sugar catabolic enzymes and transporters, providing a substantial improvement to the existing metabolic models for B. thetaiotaomicron. The obtained collection of reconstructed TF regulons is available in the RegPrecise database (http://regprecise.lbl.gov).
MeSH term(s)	Bacterial Proteins/genetics ; Bacterial Proteins/metabolism ; Bacteroides/classification ; Bacteroides/genetics ; Bacteroides/metabolism ; Base Sequence ; Binding Sites ; Gastrointestinal Tract/microbiology ; Gene Expression Regulation, Bacterial ; Gene Regulatory Networks ; Genomics ; Humans ; Metabolic Networks and Pathways ; Nucleotide Motifs ; Phylogeny ; Polysaccharides/metabolism ; Position-Specific Scoring Matrices ; Trans-Activators/genetics ; Trans-Activators/metabolism ; Transcription Factors/genetics ; Transcription Factors/metabolism
Chemical Substances	Bacterial Proteins ; Polysaccharides ; SusR protein, Bacteroides thetaiotaomicron ; Trans-Activators ; Transcription Factors
Language	English
Publishing date	2013-12-12
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ISSN	1471-2164
ISSN (online)	1471-2164
DOI	10.1186/1471-2164-14-873
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