Abstract
BackgroundBacteroides 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.ResultsA 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.ConclusionsThe 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).
Highlights
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)
We report the identification of novel DNA binding motifs for numerous Hybrid two-component system (HTCS) and SusR-like regulators, as well as for 11 other regulators from conventional TF families controlling the sugar metabolism
Repertoire of the SusR-like and HTCS regulatory systems in B. thetaiotaomicron To estimate the scale and diversity of the studied regulatory systems, we performed a genetic census of the putative HTCSs and SusR-like proteins in B. thetaiotaomicron and 10 related Bacteroides genomes
Summary
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). After digestion by extracellular enzymes, oligosaccharides are imported into the periplasm by utilizing the sugar-specific outer-membrane systems of SusC/D. These systems were named after the first described representative, starch utilization system (SUS), which is responsible for the transport of products of starch digestion [12]. Homologs of two of the sus operon members, susD and susC, are present in every PUL Proteins coded by these two genes, SusC-/SusD-like proteins, form a transport system consisting of an outer-membrane TonB-dependent porin (a SusC-like protein) and a glycan-binding SusD-like protein [13]. 101 individual pairs of genes coding for SusC-/D-like systems were detected in the B. thetaiotaomicron genome [14], forming 88 PUL systems (some PUL systems contain multiple SusC/D pairs)
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