Differential effects of coconut versus soy oil on gut microbiota composition and predicted metabolic function in adult mice

Abstract

Background: Animal studies show that high fat (HF) diet-induced gut microbiota contributes to the development of obesity. Oil composition of high-fat diet affects metabolic inflammation differently with deleterious effects by saturated fat. The aim of the present study was to examine the diversity and metabolic capacity of the cecal bacterial community in C57BL/6 N mice administered two different diets, enriched respectively with coconut oil (HFC, high in saturated fat) or soy oil (HFS, high in polyunsaturated fat). The relative impact of each hypercaloric diet was evaluated after 2 and 8 weeks of feeding, and compared with that of a low-fat, control diet (LF).

Results: The HFC diet induced the same body weight gain and fat storage as the HFS diet, but produced higher plasma cholesterol levels after 8 weeks of treatment. At the same time point, the cecal microbiota of HFC diet-fed mice was characterized by an increased relative abundance of Allobaculum, Anaerofustis, F16, Lactobacillus reuteri and Deltaproteobacteria, and a decreased relative abundance of Akkermansia muciniphila compared to HFS mice. Comparison of cecal microbiota of high-fat fed mice versus control mice indicated major changes that were shared between the HFC and the HFS diet, including the increase in Lactobacillus plantarum, Lutispora, and Syntrophomonas, while some other shifts were specifically associated to either coconut or soy oil. Prediction of bacterial gene functions showed that the cecal microbiota of HFC mice was depleted of pathways involved in fatty acid metabolism, amino acid metabolism, xenobiotic degradation and metabolism of terpenoids and polyketides compared to mice on HFS diet. Correlation analysis revealed remarkable relationships between compositional changes in the cecal microbiota and alterations in the metabolic and transcriptomic phenotypes of high-fat fed mice.

Conclusions: The study highlights significant differences in cecal microbiota composition and predictive functions of mice consuming a diet enriched in coconut vs soy oil. The correlations established between specific bacterial taxa and various traits linked to host lipid metabolism and energy storage give insights into the role and functioning of the gut microbiota that may contribute to diet-induced metabolic disorders.

Keywords: 16S rDNA; Adipose tissue; High-fat diet; Illumina sequencing; Microbiota; Mouse; Obesity; Real-time PCR.

Fig. 1

Diversity of the cecal microbiota in mice fed the experimental diets. a PCoA plot based on Bray-Curtis dissimilarity between bacteria abundance profiles for each mouse at OTU level. b Box plots showing OTU richness and c Shannon diversity index for each experimental group (n = 6). No significant differences between group means were revealed by one-way ANOVA; differences were identified as statistically significant at P values < 0.05

Fig. 2

Phylum-level microbiota composition in cecal samples of mice fed the experimental diets. The heatmap plot describes the relative abundance (taxa accounting for > 0.5% are represented) of each bacterial phylum (columns) within each sample (rows). The color code (blue to dark red) displays the row z-score: red color indicates high abundance, blue color low abundance. The dendrogram shows hierarchical clustering of bacterial communities based on the Pearson correlation coefficient as the measure of similarity and Ward’s cluster agglomeration method

Fig. 3

Phylotypes showing a significant relative abundance change in response to high-fat diets. Barplots showing the average fold changes of cecal bacteria that varied significantly in (a) mice fed the HFC diet vs the HFS diet, (b) mice fed the HFC diet vs LF diet-fed controls, and (c) mice fed HFS diet vs LF diet-fed controls. Pairwise comparisons were performed between groups (n = 6) at week 2 and at week 8 of feeding treatment, respectively, and were evaluated through a generalized linear model likelihood ratio test. The Benjamini and Hochberg’s FDR-controlling procedure was used to correct for multiple comparisons (q-value < 0.05)

Fig. 4

Body weight and fat deposition in mice subjected to high-fat diet feeding. Body weight (a), daily gain (b), and ovarian fat (c) in mice fed the experimental diets for 2 and 8 weeks. Body weight (a) was measured weekly during the 8-week dietary intervention period. Bars show means and SD. Statistical significance was determined by one-way ANOVA with Bonferroni post-hoc test. Pairwise comparisons were performed between groups (n = 6) at week 2 and at week 8 of feeding treatment, respectively; differences were identified as statistically significant at P values < 0.05

Fig. 5

Metabolic phenotype of high-fat fed mice. a Plasma total cholesterol and (b) plasma triglycerides concentration in mice fed the experimental diets for 2 and 8 weeks. Data are expressed as mean ± SD and were analyzed by one-way ANOVA with Bonferroni post-hoc analysis. Pairwise comparisons were performed between all groups (n = 6) at week 2 and at week 8 of feeding treatment, respectively; differences were identified as statistically significant at P values < 0.05

Fig. 6

Histological sections of caecum from the three experimental groups of mice after 8 weeks of feeding. Black arrows indicate infiltrating leukocytes; red arrows put in evidence areas where the epithelial layer is damaged

Fig. 7

Associations between gut microbiota and host biological parameters after dietary intervention. Heat map of Spearman’s rank correlation coefficients rs (blue = negative rs, red = positive rs). All mice from the three experimental groups at 8 weeks (n = 18) were analyzed. The p-values of the associations were estimated via permutation testing (Monte Carlo procedure). The significant correlations (q < 0.05) are indicated by ‘ + ’; only host variables and bacteria with at least one significant correlation are shown

Fig. 8

Imputed metagenomic differences between HFC and HFS diet-fed mice. Extended error bar plot showing the relative abundances of predicted functions associated with bacterial metabolism in mice cecal samples at 8 weeks. HFS and HFC diet-fed mice were compared using the Kruskal–Wallis H-test with the Games–Howell post hoc test and the Benjamini–Hochberg FDR correction for multiple comparisons. Only KEGG pathways that were significantly different (IC: 95%, q-value < 0.05) were included in the figure