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Murine Genetic Background Overcomes Gut Microbiota Changes to Explain Metabolic Response to High-Fat Diet.

ABSTRACT: Interactions of diet, gut microbiota, and host genetics play essential roles in the development of metabolic diseases. A/J and C57BL/6J (C57) are two mouse strains known to display different susceptibilities to metabolic disorders. In this context, we analyzed gut microbiota composition in A/J and C57 mice, and assessed its responses to high-fat diet (HFD) and antibiotic (AB) treatment. We also exchanged the gut microbiota between the two strains following AB treatment to evaluate its impact on the metabolism. We showed that A/J and C57 mice have different microbiome structure and composition at baseline. Moreover, A/J and C57 microbiomes responded differently to HFD and AB treatments. Exchange of the gut microbiota between the two strains was successful as recipients' microbiota resembled donor-strain microbiota. Seven weeks after inoculation, the differences between recipients persisted and were still closer from the donor-strain microbiota. Despite effective microbiota transplants, the response to HFD was not markedly modified in C57 and A/J mice. Particularly, body weight gain and glucose intolerance in response to HFD remained different in the two mouse strains whatever the changes in microbiome composition. This indicated that genetic background has a much stronger impact on metabolic responses to HFD than gut microbiome composition.

SUBMITTER: Safari Z

PROVIDER: S-EPMC7071469 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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Murine Genetic Background Overcomes Gut Microbiota Changes to Explain Metabolic Response to High-Fat Diet.

Safari Zahra Z Bruneau Aurélia A Monnoye Magali M Mariadassou Mahendra M Philippe Catherine C Zatloukal Kurt K Gérard Philippe P

Nutrients 20200121 2

Interactions of diet, gut microbiota, and host genetics play essential roles in the development of metabolic diseases. A/J and C57BL/6J (C57) are two mouse strains known to display different susceptibilities to metabolic disorders. In this context, we analyzed gut microbiota composition in A/J and C57 mice, and assessed its responses to high-fat diet (HFD) and antibiotic (AB) treatment. We also exchanged the gut microbiota between the two strains following AB treatment to evaluate its impact on ...[more]

PMID: 31973214

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Project description:Dietary fat intake and shifts in gut bacterial community composition are associated with the development of obesity. To date, characterization of microbiota in lean versus obese subjects has been dominated by studies of gut bacteria. Fungi, recently shown to affect gut inflammation, have received little study for their role in obesity. We sought to determine the effects of high-fat diet on fungal and bacterial community structures in a mouse model using the internal transcribed spacer region 2 (ITS2) of fungal ribosomal DNA (rDNA) and the 16S rRNA genes of bacteria. Mice fed a high-fat diet had significantly different abundances of 19 bacterial and 6 fungal taxa than did mice fed standard chow, with high-fat diet causing similar magnitudes of change in overall fungal and bacterial microbiome structures. We observed strong and complex diet-specific coabundance relationships between intra- and interkingdom microbial pairs and dramatic reductions in the number of coabundance correlations in mice fed a high-fat diet compared to those fed standard chow. Furthermore, predicted microbiome functional modules related to metabolism were significantly less abundant in high-fat-diet-fed than in standard-chow-fed mice. These results suggest a role for fungi and interkingdom interactions in the association between gut microbiomes and obesity. IMPORTANCE Recent research shows that gut microbes are involved in the development of obesity, a growing health problem in developed countries that is linked to increased risk for cardiovascular disease. However, studies showing links between microbes and metabolism have been limited to the analysis of bacteria and have ignored the potential contribution of fungi in metabolic health. This study provides evidence that ingestion of a high-fat diet is associated with changes to the fungal (and bacterial) microbiome in a mouse model. In addition, we find that interkingdom structural and functional relationships exist between fungi and bacteria within the gut and that these are perturbed by high-fat diet.

Project description:Fat is one of the most important nutrients which provides concentrated energy and essential fatty acids. High fat diet markedly changes the gut microbial composition in mammals, whereas little is known about the impact of fat type on gut microbiome. This study was to evaluate the effects of fat sources on intestinal microbiota of nursery pigs. Eighteen pigs (28 days of age, 8.13 ± 0.10 kg BW) were housed individually (n = 6 per treatment) and allotted to three treatments based on a randomized complete block design. Pigs were fed basal diets with three different fat sources: 6.0% soybean oil (SBO), 6.0% palm oil (PO), and 7.5% encapsulated palm oil (EPO, contains 80% palm oil) respectively. Pigs were euthanized after 28 days of ad libitum feeding, and the digesta in the distal duodenum, jejunum, ileum, cecum and colon of each pig were obtained for microbial composition analysis. Correlation analyses were also performed between microbial composition with nutrients digestibility or growth performance. The results showed that pigs fed PO had marked changes in the bacteria community composition with increasing the richness and diversity in duodenum and jejunum (P < 0.05). Increased abundances of Proteobacteria in duodenum, jejunum and cecum, and decreased abundance of Firmicutes in jejunum were observed in pigs fed PO compared to SBO and EPO. Pigs fed EPO decreased abundances of Proteobacteria in duodenum and jejunum, and increased abundance of Firmicutes compared to pigs fed PO, and was similar to pigs fed SBO. The microbial changes (genus) had significant negative correlation with the fat digestibility. These results indicate that palm oil supplementation in nursery pig diet alters the gut microbial composition, with the most significant changes observed in small intestine. Encapsulation of palm oil, which helps increase the digestibility of palm oil, have beneficial effect on the microbial disturbance caused by palm oil supplementation. Our findings provide a better understanding of how different fat types influence microbial composition in different parts of the intestinal tract and the correlation between bacteria composition and nutrients digestibility, which may provide a new perspective for the rational application of fat in diet.

Project description:Accumulating evidence suggests that high-fat diet (HFD) induced metabolic disorders are associated with dysbiosis of gut microbiota. However, no study has explored the effect of HFD on the gastric microbiota. This study established the HFD animal model to determine the impact of HFD on the gastric microbiota and its relationship with the alterations of gut microbiota. A total of 40 male C57BL/6 mice were randomly allocated to receive a standard chow diet (CD) or HFD for 12 weeks (12CD group and 12HFD group) and 24 weeks (24CD group and 24HFD group) (n = 10 mice per group). Body weight and length were measured and Lee's index was calculated at different time points. The insulin sensitivity and serum levels of metabolic parameters including blood glucose, insulin and lipid were also evaluated. The gastric mucosa and fecal microbiota of mice were characterized by 16S rRNA gene sequencing. The body weight was much heavier and the Lee's index was higher in 24HFD group than 12HFD. The insulin resistance and serum level of lipid were increased in 24HFD group compared to 12HFD, indicating the aggravation of metabolic disorders as HFD went on. 16S rRNA gene sequencing showed dysbiosis of gastric microbiota with decreased community diversity while no significant alteration in gut microbiota after 12 weeks of HFD. The phyla Firmicutes and Proteobacteria tended to increase whereas Bacteroidetes and Verrucomicrobia decrease in the gastric microbiota of 12HFD mice compared to 12CD. Moreover, a remarkable reduction of bacteria especially Akkermansia muciniphila, which has beneficial effects on host metabolism, was observed firstly in the stomach of 12HFD group and then in the gut of 24HFD group, indicating the earlier alterations of microbiota in stomach than gut after HFD. We also found structural segregation of microbiota in the stomach as well as gut between 12HFD and 24HFD group, which is accompanied by the aggregation of metabolic disorders. These data suggest that HFD affects not only gut microbiota but also gastric microbiota and the disruption of microbial ecosystem in the digestive tract may play a part in the development and progression of metabolic diseases although molecular mechanism requires further investigation.

Dataset Information

Murine Genetic Background Overcomes Gut Microbiota Changes to Explain Metabolic Response to High-Fat Diet.

Publications

Murine Genetic Background Overcomes Gut Microbiota Changes to Explain Metabolic Response to High-Fat Diet.

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