Functional Effects of EPS-Producing Bifidobacterium Administration on Energy Metabolic Alterations of Diet-Induced Obese Mice

Abstract

Obesity has been recognized by the World Health Organization as a global epidemic. The gut microbiota is considered as a factor involved in the regulation of numerous metabolic pathways by impacting several functions of the host. It has been suggested that probiotics can modulate host gene expression and metabolism, and thereby positively influence host adipose tissue development and obesity related-metabolic disorders. The aim of the present work was to evaluate the effect of an exopolysaccharide (EPS)-producing Bifidobacterium strain on host glucose and lipid metabolism and the gut microbial composition in a short-term diet-induced obesity (DIO) in mice. C57BL/6J male mice were randomly divided into three groups: a control group that received control standard diet, a group fed a high-fat diet (HF), and a group fed HF supplemented with Bifidobacterium animalis IPLA R1. Fasting serum insulin as well as triglycerides accumulation in the liver were significantly reduced in the group receiving B. animalis IPLA R1. The treatment with the EPS-producing B. animalis IPLA R1 tended to down-regulate the expression of host genes involved in the hepatic synthesis of fatty acids which was concomitant with an upregulation in the expression of genes related with fatty acid oxidation. B. animalis IPLA R1 not only promoted the increase of Bifidobacterium but also the levels of Bacteroides-Prevotella. Our data indicate that the EPS-producing Bifidobacterium IPLA R1 strain may have beneficial effects in metabolic disorders associated with obesity, by modulating the gut microbiota composition and promoting changes in lipids metabolism and glucose homeostasis.

Keywords: Bifidobacterium; bile acids; fatty acid oxidation; gut microbiota; liver fatty acid profile; obesity.

FIGURE 1

Impact of the EPS-producing B. animalis IPLA R1 strain after a short-term high fat diet (HFD) on lipid accumulation in the liver. Liver cholesterol (A) and triglycerides (TG) (B). Mice fed a control diet and delivery vehicle-skimmed milk in drinking water (CT), mice fed a HFD and delivery vehicle-skimmed milk in drinking water (HF), and mice fed a HFD supplemented with a suspension of 5 × 10⁸ cfu/mouse/day of B. animalis IPLA R1 strain in skimmed milk (HF-B) added to the drinking water. Data are expressed as the mean ± SEM. Data with different superscript letters are significantly different at p < 0.05 according to One-way analysis of variance statistical analysis followed by Tukey post hoc.

FIGURE 2

Statistically significant changes on liver fatty acid profile after a short-term high fat diet (HFD). Saturated fatty acids (SFA) profile. (A) Liver monounsaturated fatty acids (MUFA) profile (B). Liver polyunsaturated fatty acids (PUFA) profile (C). Desaturation ratio (D). Mice fed a control diet and delivery vehicle-skimmed milk in drinking water (CT), mice fed a HFD and delivery vehicle-skimmed milk in drinking water (HF), and mice fed a HFD supplemented with a suspension of 5 × 10⁸ cfu/mouse/day of B. animalis IPLA R1 strain in skimmed milk (HF-B) added to the drinking water. Data are expressed as the mean ± SEM. Data with different superscript letters are significantly different at p < 0.05 according to One-way analysis of variance statistical analysis followed by Tukey post hoc.

FIGURE 3

Liver gene expression of fatty acids metabolism (A) and gene expression of cholesterol and bile acid metabolism (B) after a short-term high fat diet (HFD). Mice fed a control diet and delivery vehicle-skimmed milk in drinking water (CT), mice fed a HFD and skimmed milk in drinking water (HF), and mice fed a HFD and supplemented with a suspension of 5 × 10⁸ cfu/mouse/day of B. animalis IPLA R1 strain in skimmed milk (HF-B) added to the drinking water. Each gene codes for the same name of the corresponding enzyme except Acaca that codes for ACC (Acetyl-CoA carboxylase) and Nr1h3 that codes for LXR (liver X receptor). Data are expressed as the mean ± SEM. Values are expressed as relative units with the mean of CT mice values set at 1. Data with different superscript letters are significantly different at p < 0.05 according to One-way analysis of variance statistical analysis followed by Tukey post hoc.

FIGURE 4

Impact of the EPS-producing B. animalis IPLA R1 strain after a short-term high fat diet (HFD) on cecal microbiota assessed by qPCR. Total bacteria (A), Bifidobacterium (B), B. animalis (C), Lactobacillus (D), Bacteroides-Prevotella (E), Roseburia (F), and A. muciniphila (G) in the cecal content of mice after 3 days of treatment. Mice fed a control diet and delivery vehicle-skimmed milk in drinking water (CT), mice fed a HFD and delivery vehicle-skimmed milk in drinking water (HF), and mice fed with HFD supplemented with a bacterial suspension in milk (5 × 10⁸ cfu/mouse/day) of B. animalis IPLA R1 strain (HF-B) added to the drinking water. Data are box and whiskers plots with minimum and maximum. Data with different superscript letters are significantly different at p < 0.05 according to One-way analysis of variance statistical analysis followed by Tukey post hoc.