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Dietary butyrate ameliorates metabolic health associated with selective proliferation of gut Lachnospiraceae bacterium 28-4.

ABSTRACT: Short-chain fatty acids, including butyrate, have multiple metabolic benefits in individuals who are lean but not in individuals with metabolic syndrome, with the underlying mechanisms still being unclear. We aimed to investigate the role of gut microbiota in the induction of metabolic benefits of dietary butyrate. We performed antibiotic-induced microbiota depletion of the gut and fecal microbiota transplantation (FMT) in APOE*3-Leiden.CETP mice, a well-established translational model for developing human-like metabolic syndrome, and revealed that dietary butyrate reduced appetite and ameliorated high-fat diet-induced (HFD-induced) weight gain dependent on the presence of gut microbiota. FMT from butyrate-treated lean donor mice, but not butyrate-treated obese donor mice, into gut microbiota-depleted recipient mice reduced food intake, attenuated HFD-induced weight gain, and improved insulin resistance. 16S rRNA and metagenomic sequencing on cecal bacterial DNA of recipient mice implied that these effects were accompanied by the selective proliferation of Lachnospiraceae bacterium 28-4 in the gut as induced by butyrate. Collectively, our findings reveal a crucial role of gut microbiota in the beneficial metabolic effects of dietary butyrate as strongly associated with the abundance of Lachnospiraceae bacterium 28-4.

SUBMITTER: Li Z

PROVIDER: S-EPMC9977501 | biostudies-literature | 2023 Feb

REPOSITORIES: biostudies-literature

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Dietary butyrate ameliorates metabolic health associated with selective proliferation of gut Lachnospiraceae bacterium 28-4.

Li Zhuang Z Zhou Enchen E Liu Cong C Wicks Hope H Yildiz Sena S Razack Farhana F Ying Zhixiong Z Kooijman Sander S Koonen Debby PY DPY Heijink Marieke M Kostidis Sarantos S Giera Martin M Sanders Ingrid MJG IMJG Kuijper Ed J EJ Smits Wiep Klaas WK van Dijk Ko Willems KW Rensen Patrick CN PCN Wang Yanan Y

JCI insight 20230222 4

Short-chain fatty acids, including butyrate, have multiple metabolic benefits in individuals who are lean but not in individuals with metabolic syndrome, with the underlying mechanisms still being unclear. We aimed to investigate the role of gut microbiota in the induction of metabolic benefits of dietary butyrate. We performed antibiotic-induced microbiota depletion of the gut and fecal microbiota transplantation (FMT) in APOE*3-Leiden.CETP mice, a well-established translational model for devel ...[more]

PMID: 36810253

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Project description:Sulfate-reducing bacteria (SRB) colonize the guts of ~50% of humans. We used genome-wide transposon mutagenesis and insertion-site sequencing (INSeq), RNA-Seq, plus mass spectrometry to characterize genetic and environmental factors that impact the niche of Desulfovibrio piger, the most common SRB in a surveyed cohort of healthy USA adults. Gnotobiotic mice were colonized with an assemblage of sequenced human gut bacterial species with or without D. piger and fed diets with different levels and types of carbohydrates and sulfur sources. Diet was a major determinant of functions expressed by this artificial 9-member community and of the genes that impact D. piger fitness; the latter includes high- and low-affinity systems for utilizing ammonia, a limiting resource for D. piger in mice consuming a polysaccharide-rich diet. While genes involved in hydrogen consumption and sulfate reduction are necessary for its colonization, varying dietary free sulfate levels did not significantly alter levels of D. piger, which can obtain sulfate from the host in part via cross-feeding mediated by Bacteroides-encoded sulfatases. Chondroitin sulfate, a common dietary supplement, increased D. piger and H2S levels without compromising gut barrier integrity. A chondroitin sulfate-supplemented diet together with D. piger impacted the assemblage’s substrate utilization preferences, allowing consumption of more reduced carbon sources, and increasing the abundance of the H2-producing Actinobacterium, Collinsella aerofaciens. Our findings provide genetic and metabolic details of how this H2-consuming SRB shapes the responses of a microbiota to diet ingredients, and a framework for examining how individuals lacking D. piger differ from those that harbor it. 8 samples total, 2 gropus of 4 mice: Proximal colon gene expression profiles of gnotobiotic mice colonized with an artificial gut community composed of 8 human gut species (group 1: NoDp) and from mice colonized with the same community plus D. piger (Dp). Mice were fed a HF/HS diet supplemented with 3% chondroitin sulfate. Animals were sacrificed 2 weeks after colonization

Dataset Information

Dietary butyrate ameliorates metabolic health associated with selective proliferation of gut Lachnospiraceae bacterium 28-4.

Publications

Dietary butyrate ameliorates metabolic health associated with selective proliferation of gut Lachnospiraceae bacterium 28-4.

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