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The human gut Firmicute Roseburia intestinalis is a primary degrader of dietary ?-mannans.

ABSTRACT: ?-Mannans are plant cell wall polysaccharides that are commonly found in human diets. However, a mechanistic understanding into the key populations that degrade this glycan is absent, especially for the dominant Firmicutes phylum. Here, we show that the prominent butyrate-producing Firmicute Roseburia intestinalis expresses two loci conferring metabolism of ?-mannans. We combine multi-"omic" analyses and detailed biochemical studies to comprehensively characterize loci-encoded proteins that are involved in ?-mannan capturing, importation, de-branching and degradation into monosaccharides. In mixed cultures, R. intestinalis shares the available ?-mannan with Bacteroides ovatus, demonstrating that the apparatus allows coexistence in a competitive environment. In murine experiments, ?-mannan selectively promotes beneficial gut bacteria, exemplified by increased R. intestinalis, and reduction of mucus-degraders. Our findings highlight that R. intestinalis is a primary degrader of this dietary fiber and that this metabolic capacity could be exploited to selectively promote key members of the healthy microbiota using ?-mannan-based therapeutic interventions.

SUBMITTER: La Rosa SL

PROVIDER: S-EPMC6385246 | biostudies-literature | 2019 Feb

REPOSITORIES: biostudies-literature

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The human gut Firmicute Roseburia intestinalis is a primary degrader of dietary β-mannans.

La Rosa Sabina Leanti SL Leth Maria Louise ML Michalak Leszek L Hansen Morten Ejby ME Pudlo Nicholas A NA Glowacki Robert R Pereira Gabriel G Workman Christopher T CT Arntzen Magnus Ø MØ Pope Phillip B PB Martens Eric C EC Hachem Maher Abou MA Westereng Bjørge B

Nature communications 20190222 1

β-Mannans are plant cell wall polysaccharides that are commonly found in human diets. However, a mechanistic understanding into the key populations that degrade this glycan is absent, especially for the dominant Firmicutes phylum. Here, we show that the prominent butyrate-producing Firmicute Roseburia intestinalis expresses two loci conferring metabolism of β-mannans. We combine multi-"omic" analyses and detailed biochemical studies to comprehensively characterize loci-encoded proteins that are ...[more]

PMID: 30796211

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Project description:BackgroundThe community of gut microbes is a key factor controlling the intestinal barrier that communicates with the nervous system through the gut-brain axis. Based on our clinical data showing that populations of Roseburia intestinalis are dramatically decreased in the gut of patients with ulcerative colitis, we studied the efficacy of a strain belonging to this species in the context of colitis and stress using animal models.MethodsDextran sulfate sodium was used to induce colitis in rats, which then underwent an enema with R. intestinalis as a treatment. The disease activity index, fecal changes and body weight of rats were recorded to evaluate colitis, while histological and immunohistochemical analyses were carried out to examine colon function, and 16S rRNA sequencing was performed to evaluate the gut microbiota change. Behavioral assays and immunohistochemical staining of brain were performed to assess the effect of R. intestinalis on the gut-brain axis.ResultsColitis-related symptoms in rats were significantly relieved after R. intestinalis enema, and the stool traits and colon length of rats were significantly recovered after treatment. The gut epithelial integrity and intestinal barrier were restored in treated rats, as evidenced by the higher expression of Zo-1 in colon tissues, accompanied by the restoration of gut microbiota. Meanwhile, depressive-like behaviors of rats were reduced after treatment, and laboratory experiments on neuronal cells also showed that IL-6, IL-7 and 5-HT were downregulated by R. intestinalis treatment in both serum and brain tissue, while Iba-1 expression was reduced in treated rats.ConclusionsThe administration of R. intestinalis contributes to restoration of the gut microbiota, promoting colon repair and the recovery of gastrointestinal function. These alterations are accompanied by the relief of depressive-like behaviors through a process modulated by the neuronal network and the regulation of inflammation by the gut-brain axis.

Dataset Information

The human gut Firmicute Roseburia intestinalis is a primary degrader of dietary ?-mannans.

Publications

The human gut Firmicute Roseburia intestinalis is a primary degrader of dietary β-mannans.

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