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High-resolution view at the coding transcriptome and noncoding RNAs of major gut microbe Bacteroides thetaiotaomicron

ABSTRACT: Gram-negative, obligate anaerobic Bacteroides thetaiotaomicron is emerging as the model organism for gut microbiota research. Colonization of its host niche within the human colon depends to large parts on the extensive metabolic capacity encoded in the Bacteroides genome, but little is known about how its transcription is organized. Here, we transferred differential RNA-seq (dRNA-seq) to B. thetaiotaomicron type strain VPI-5482 to globally map transcription start sites (TSSs). Our screen identified ~4,500 TSSs and we globally determined untranslated regions (UTRs), operon structures, and promoter motifs. In addition, dRNA-seq led to the discovery of ~250 noncoding RNA elements, including 124 novel intergenic small RNAs (sRNAs), several of which we validated experimentally. One of them is the conserved, 145 nt-long sRNA BTnc035, that was highly expressed when B. thetaiotaomicron was grown in the presence of N-acetylglucosamine or glucuronic acid as the sole carbon source. Combining computational predictions with experimental data, we determined the secondary structure of BTnc035 and identified target genes of this sRNA. The emerging model places BTnc035 at the center of a metabolic feedback-loop, wherein sensing of N-acetyl-D-glucosamine and D-glucuronic acid induces BTnc035, which in turn may contribute to a metabolic switch from polysaccharide biosynthesis to break-down. Together, we compiled a single-nucleotide resolution transcriptome map of B. thetaiotaomicron and provide the first global analysis of noncoding RNAs in this important anaerobic model bacterium. To allow easy interrogation of our transcriptome data, we developed Theta-Base – an intuitive online browser that can be freely accessed at https://www.helmholtz-hiri.de/en/bacteroides.

ORGANISM(S): Bacteroides thetaiotaomicron

PROVIDER: GSE144492 | GEO | 2020/06/11

REPOSITORIES: GEO

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Project description:The large-scale application of genomic and metagenomic sequencing technologies has yielded a number of insights about the metabolic potential of symbiotic human gut microbes. Bacteria that colonize the mucosal layer that overlies the gut epithelium have access to highly-sulfated polysaccharides (i.e., mucin oligosaccharides and glycosaminoglycans), which they could potentially forage as nutrient sources. To be active, sulfatases must undergo a critical post-translational modification catalyzed in anaerobic bacteria by the AdoMet enzyme anSME (anaerobic Sulfatase-Maturating Enzyme). In the present study, we have tested the role of this pathway in the prominent gut symbiont Bacteroides thetaiotaomicron, which possesses more predicted sulfatases (28) than in the human genome and a single predicted anSME. In vitro studies revealed that deletion of its anSME (BT0238) results in loss of sulfatase activity and impaired ability to use sulfated polysaccharides as carbon sources. Co-colonization of germ-free animals with both isogenic strains, or invasion experiments involving the introduction of one then the other strain, established that anSME activity and the sulfatases that are activated via this pathway, are important fitness factors for B. thetaiotaomicron, especially when mice are fed a simple sugar diet that requires this saccharolytic bacterium to adaptively forage on host glycans as nutrients. Whole genome transcriptional profiling of wild-type and the anSME mutant in vivo revealed that loss of this enzyme alters expression of genes involved in mucin utilization and that this disrupted ability to access mucosal glycans likely underlies the observed dramatic colonization defect. Comparative genomic analysis reveals that 100% of 46 fully sequenced human gut Bacteroidetes contain homologs of BT0238 and genes encoding sulfatases, suggesting that this is an important and evolutionarily conserved feature. Three replicate samples from 4 different biological treatment groups: 1. Wild-type B. thetaiotaomicron from the cecum of gnotobiotic mice fed a simple-sugar diet; 2. chuR mutant B. thetaiotaomicron from the cecum of gnotobiotic mice fed a simple-sugar diet; 3. Wild-type B. thetaiotaomicron from the cecum of gnotobiotic mice fed a plant-rich diet; 4. chuR mutant B. thetaiotaomicron from the cecum of gnotobiotic mice fed a plant-rich diet.

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High-resolution view at the coding transcriptome and noncoding RNAs of major gut microbe Bacteroides thetaiotaomicron

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