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Extensive transfer of genes for edible seaweed digestion from marine to human gut bacteria

ABSTRACT: Humans harbor numerous species of colonic bacteria that digest the fiber polysaccharides in commonly consumed terrestrial plants. More recently in history, regional populations have consumed edible seaweeds (macroalgae) containing unique polysaccharides. However, it remains unclear how extensively gut bacteria have adapted to digest these novel nutrients. Here, we show that the ability of gut bacteria to digest seaweed polysaccharides is considerably more pervasive than previously appreciated. Using culture-based approaches, we show that known Bacteroides genes involved in seaweed degradation have mobilized into many members of this genus. We also identify new marine bacteria-derived genes, and their corresponding mobile DNA elements, that are involved in degrading several seaweed polysaccharides. Some of these new genes reside in gut-resident, Gram-positive Firmicutes, for which phylogenetic analysis suggests an origin in the Epulopiscium gut symbionts of marine fishes. Our results are important for understanding the metabolic plasticity of the human gut microbiome, the global exchange of genes in the context of dietary selective pressures and identifying new functions that can be introduced or engineered to design and fill orthogonal niches for a future generation of engineered probiotics.

INSTRUMENT(S): LTQ Orbitrap Classic

ORGANISM(S): Bacteroides Thetaiotaomicron

SUBMITTER: Stephanie Markert

LAB HEAD: Stephanie Markert

PROVIDER: PXD019149 | Pride | 2021-11-04

REPOSITORIES: Pride

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Utilization of alpha- and beta-mannan by marine Flavobacteriia

Project description:About one half of the global, biogenic carbon dioxide fixation into organic matter is driven by microscopic algae in the surface oceans. These microalgal activities generate, among other molecules, polysaccharides that are food for and recycled by bacteria with polysaccharide utilization loci (PULs). These genetic clusters of co-evolved genes, which work together in recognition, depolymerizing and uptake of one type of polysaccharide. However, we rarely know the substrates of PULs present in marine bacteria. Here we investigated the proteomic and physiological response of mannan PULs from marine Flavobacteriia isolated in the North Sea. The genomic clusters of these marine Bacteroidetes are related to PULs of human gut Bacteroides strains, which are known to digest α- and β-mannans from yeasts and plants respectively. Proteomics and defined growth experiments with these types of mannans as sole carbon source confirmed the functional prediction. Our data suggest that biochemical principles established for gut or terrestrial microbes apply to marine bacteria even though the PULs are evolutionary distant. Moreover, our data support discoveries from the 60th reporting mannans in microalgae suggesting that these polysaccharides play an important role in the marine carbon cycle.

2018-10-17 | PXD009066 | Pride

Utilization of alpha- and beta-mannan by marine Flavobacteriia

2018-10-17 | PXD009080 | Pride

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Project description:RNA-seq of human gut bacterial isolates grown on seaweed polysaccharides

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Project description:Symbiotic bacteria inhabiting the distal human gut have evolved under intense pressure to utilize complex carbohydrates, predominantly plant cell wall glycans abundant in our diets. These substrates are recalcitrant to depolymerization by digestive enzymes encoded in the human genome, but are efficiently targeted by some of the ~103-104 bacterial species that inhabit this niche. These species augment our comparatively narrow carbohydrate digestive capacity by unlocking otherwise unusable sugars and fermenting them into host-absorbable forms, such as short-chain fatty acids. We used phenotype profiling, whole-genome transcriptional analysis and molecular genetic approaches to investigate complex glycan utilization by two fully sequenced and closely related human gut symbionts: Bacteroides thetaiotaomicron and Bacteroides ovatus. Together these species target all of the common glycosidic linkages found in the plant cell wall, as well as host polysaccharides, but each species exhibits a unique ‘glycan niche’: in vitro B. thetaiotaomicron targets plant cell wall pectins in addition to linkages contained in host N- and O-glycans; B. ovatus uniquely targets hemicellulosic polysaccharides along with several pectins, but is deficient in host glycan utilization. Bacteroides ovatus bacteria were grown either in vitro on defined complex glycan sources, or in vivo in the intestinal tract of gnotobiotic mice fed variable diets. Increased in vitro gene expression was used to indicate the genes required for metabolism of complex glycans and compared to in vivo transcriptional activity to determine expression in the mouse gut.

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Development and validation of a microarray for the investigation of the CAZymes encoded by the human gut microbiome

Project description:Distal gut bacteria play a pivotal role in the digestion of dietary polysaccharides by producing a large number of carbohydrate-active enzymes (CAZymes) that the host otherwise does not produce. We report here the design of a high density custom microarray that we used to spot non-redundant DNA probes for more than 6,500 genes encoding glycoside hydrolases and lyases selected from 174 reference genomes from distal gut bacteria. The custom microarray was tested and validated by the hybridization of bacterial DNA extracted from the stool samples of lean, obese and anorexic individuals. Our results suggest that a microarray-based study can detect genes from low-abundance bacteria better than metagenomic-based studies. A striking example was the finding that a gene encoding a GH6-family cellulase was present in all subjects examined, whereas metagenomic studies have consistently failed to detect this gene in both human and animal gut microbiomes. In addition, an examination of eight stool samples allowed the identification of a corresponding CAZome core containing 46 families of glycoside hydrolases and polysaccharide lyases, which suggests the functional stability of the gut microbiota despite large taxonomical variations between individuals. Fecal samples were collected from eight female subjects. Three were obese subjects of BMI kg m-2: 35, 46.8 and 51.3, respectively; age: 42, 21 and 65 years old, respectively. Three were anorexic women of BMI kg m-2: 9.8, 10 and 13.7, respectively; age: 19, 23 and 49 years old, respectively. Finally, two fecal samples from lean women of BMI kg m-2: 18.6 and 23.42 were analyzed.

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Widespread consumption of the common food additive xanthan gum by the human gut microbiota

Project description:The diets of industrialized countries reflect the increasing use of processed foods, often with the inclusion of novel food additives. Xanthan gum is a complex polysaccharide with unique rheological properties that have established its use as a widespread stabilizer and thickening agent. Xanthan gum’s chemical structure is distinct from the host and dietary polysaccharides that are more commonly expected to transit the gastrointestinal tract, and little is known about its direct interaction with the gut microbiota, which plays a central role in digestion of other dietary fiber polysaccharides. Here, we show that the ability to digest xanthan gum is surprisingly common in industrialized human gut microbiomes and appears contingent on a single uncultured bacterium in the family Ruminococcaceae. Our data reveal that this primary degrader cleaves the xanthan gum backbone before processing the released oligosaccharides using additional enzymes. Surprisingly, some individuals harbor a Bacteroides intestinalis that is incapable of consuming polymeric xanthan gum but grows on oligosaccharide products generated by the Ruminococcaceae. Feeding xanthan gum to germfree mice colonized with a human microbiota containing the uncultured Ruminococcaceae supports the idea that this additive can drive expansion of this primary degrader along with exogenously introduced Bacteroides intestinalis. Our work demonstrates the existence of a potential xanthan gum food chain involving at least two members of different phyla of gut bacteria and provides an initial framework to understand how widespread consumption of a recently introduced food additive influences human microbiomes.

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2022-02-08 | PXD023756 | Pride

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