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Single-cell genomics of uncultured bacteria reveals dietary fiber responders in the mouse gut microbiota.

ABSTRACT: BACKGROUND:The gut microbiota can have dramatic effects on host metabolism; however, current genomic strategies for uncultured bacteria have several limitations that hinder their ability to identify responders to metabolic changes in the microbiota. In this study, we describe a novel single-cell genomic sequencing technique that can identify metabolic responders at the species level without the need for reference genomes, and apply this method to identify bacterial responders to an inulin-based diet in the mouse gut microbiota. RESULTS:Inulin-feeding changed the mouse fecal microbiome composition to increase Bacteroides spp., resulting in the production of abundant succinate in the mouse intestine. Using our massively parallel single-cell genome sequencing technique, named SAG-gel platform, we obtained 346 single-amplified genomes (SAGs) from mouse gut microbes before and after dietary inulin supplementation. After quality control, the SAGs were classified as 267 bacteria, spanning 2 phyla, 4 classes, 7 orders, and 14 families, and 31 different strains of SAGs were graded as high- and medium-quality draft genomes. From these, we have successfully obtained the genomes of the dominant inulin-responders, Bacteroides spp., and identified their polysaccharide utilization loci and their specific metabolic pathways for succinate production. CONCLUSIONS:Our single-cell genomics approach generated a massive amount of SAGs, enabling a functional analysis of uncultured bacteria in the intestinal microbiome. This enabled us to estimate metabolic lineages involved in the bacterial fermentation of dietary fiber and metabolic outcomes such as short-chain fatty acid production in the intestinal environment based on the fibers ingested. The technique allows the in-depth isolation and characterization of uncultured bacteria with specific functions in the microbiota and could be exploited to improve human and animal health. Video abstract.

SUBMITTER: Chijiiwa R

PROVIDER: S-EPMC6977353 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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Single-cell genomics of uncultured bacteria reveals dietary fiber responders in the mouse gut microbiota.

Chijiiwa Rieka R Hosokawa Masahito M Kogawa Masato M Nishikawa Yohei Y Ide Keigo K Sakanashi Chikako C Takahashi Kai K Takeyama Haruko H

Microbiome 20200123 1

<h4>Background</h4>The gut microbiota can have dramatic effects on host metabolism; however, current genomic strategies for uncultured bacteria have several limitations that hinder their ability to identify responders to metabolic changes in the microbiota. In this study, we describe a novel single-cell genomic sequencing technique that can identify metabolic responders at the species level without the need for reference genomes, and apply this method to identify bacterial responders to an inuli ...[more]

PMID: 31969191

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Project description:Dietary fiber (DF) is increasingly thought to regulate diversity of piglet gut microbiota to alleviate weaning stress in piglets. This study was conducted to investigate the effects of DF on growth performance of piglets and composition of their gut microbiota, as well as the interaction between gut microbiota and short-chain fatty acids (SCFAs) in piglets. A total of 840 piglets were allocated to three dietary treatments consisting of a control group (CG), an alfalfa meal group (AG), and a commodity concentrated fiber group (OG) in a 30-day feeding trial. Gut mucosa and feces samples were used to determine bacterial community diversity by 16S rRNA gene amplicon sequencing. Fiber treatment had a positive effect on growth performance and metabolism of SCFAs in piglets, in particular, compared with CG, the diarrhea rate was significantly decreased, and the content of propionic acid (PA) in the cecum was markedly increased in AG. The Shannon indices of the jejunum microbiota in AG were higher than CG. At the genus level, compared to CG, in the duodenum, the relative abundance of Paenibacillus in AG and OG was higher; in the jejunum, the relative abundances of Bacillus, Oceanobacillus, Paenibacillus, Lactococcus, Enterococcus, and Exiguobacterium were higher, whereas the relative abundance of Mycoplasma was lower in AG; in the cecum, there was also lower relative abundance of Helicobacter in AG and OG, and furthermore, the relative abundance of Faecalibacterium in OG was higher than in CG and AG. Spearman correlation analysis showed that Pseudobutyrivibrio was positively correlated with acetic acid, PA, and butyric acid (BA), while Bacteroides and Anaerotruncus were negatively correlated with PA and BA. In addition, microbiota analyses among different intestine segments showed distinct differences in microbiota between the proximal and distal intestines. Bacteria in the proximal segments were mainly Firmicutes, while bacteria in the distal segments were mainly Bacteroidetes and Firmicutes. Overall, these findings suggested that DF treatment could reduce the diarrhea rate of piglets and had beneficial effects on gut health, which might be attributed to the alteration in gut microbiota induced by DF and the interaction of the gut microbiota with SCFAs.

Project description:BackgroundDietary fiber is an integral part of a healthy diet, but questions remain about the mechanisms that underlie effects and the causal contributions of the gut microbiota. Here, we performed a 6-week exploratory trial in adults with excess weight (BMI: 25-35 kg/m2) to compare the effects of a high-dose (females: 25 g/day; males: 35 g/day) supplement of fermentable corn bran arabinoxylan (AX; n = 15) with that of microbiota-non-accessible microcrystalline cellulose (MCC; n = 16). Obesity-related surrogate endpoints and biomarkers of host-microbiome interactions implicated in the pathophysiology of obesity (trimethylamine N-oxide, gut hormones, cytokines, and measures of intestinal barrier integrity) were assessed. We then determined whether clinical outcomes could be predicted by fecal microbiota features or mechanistic biomarkers.ResultsAX enhanced satiety after a meal and decreased homeostatic model assessment of insulin resistance (HOMA-IR), while MCC reduced tumor necrosis factor-α and fecal calprotectin. Machine learning models determined that effects on satiety could be predicted by fecal bacterial taxa that utilized AX, as identified by bioorthogonal non-canonical amino acid tagging. Reductions in HOMA-IR and calprotectin were associated with shifts in fecal bile acids, but correlations were negative, suggesting that the benefits of fiber may not be mediated by their effects on bile acid pools. Biomarkers of host-microbiome interactions often linked to bacterial metabolites derived from fiber fermentation (short-chain fatty acids) were not affected by AX supplementation when compared to non-accessible MCC.ConclusionThis study demonstrates the efficacy of purified dietary fibers when used as supplements and suggests that satietogenic effects of AX may be linked to bacterial taxa that ferment the fiber or utilize breakdown products. Other effects are likely microbiome independent. The findings provide a basis for fiber-type specific therapeutic applications and their personalization.Trial registrationClinicaltrials.gov, NCT02322112 , registered on July 3, 2015. Video Abstract.

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Single-cell genomics of uncultured bacteria reveals dietary fiber responders in the mouse gut microbiota.

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Single-cell genomics of uncultured bacteria reveals dietary fiber responders in the mouse gut microbiota.

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