Navy Bean Supplementation in Obesity Increases Akkermansia muciniphila Abundance and Attenuates Obesity Related Impairments in Gut Barrier Function

Fiber‐rich dietary pulses, such as common beans (Phaseolus vulgaris) have the potential to modify the colonic microenvironment (microbiota and host epithelial barrier) which can mitigate the severity of gut‐associated pathologies. Obesity is associated with impairments in the mucosal barrier (leaky gut) and specific changes in the abundance of bacteria communities within the gut microbiota. The objective was to assess the gut health promoting effects of 20% cooked navy bean flour supplementation in both the lean healthy and obese states. Two studies were conducted wherein male C57BL/6 mice were fed either a low fat control (LF, 10% fat as kcal) or an isocaloric bean supplemented diet (LF+B) for 3 weeks (Study 1: lean healthy), or a high fat diet (HF, 60% fat as kcal) or isocaloric bean supplemented (HF+B) diet for 12 weeks (Study 2: diet induced obesity). In lean mice, using fecal 16S rRNA sequencing, LF+B altered the abundance of critical gut microbial families including increased abundance of S24–7 (1.5‐fold) and Prevotellaceae (71‐fold) and decreased abundance of Peptococcaceae (3.7‐fold), Streptococcaceae (8.4‐fold), Clostridiaceae (12‐fold), Rikenellaceae (2.5‐fold) and Porphyromonadaceae (2.5‐fold) versus LF. These changes were associated with increased microbial activity (i.e, short chain fatty acid (SCFA) production) and colonic tissue expression of the SCFA receptors GPR41, 43 and 109a. LF+B improved gut barrier integrity and function by increasing i) mucus production, ii) anti‐microbial defenses, iii) tight junction protein expression, and iv) reducing serum lipopolysaccharide levels. These beneficial effects were sustained in obesity wherein HF+B fed mice exhibited improvements in both gut microbiota activity and community structure and aspects of the obese phenotype. Specifically, fecal abundance of Akkermansia muciniphila, whose abundance is inversely related to the severity of the obese phenotype, was increased in the HF+B group versus HF by 20‐fold, which was associated with a reduction in visceral adipose mRNA expression of the inflammatory mediators MCP‐1 and IL‐6 and increased expression of adiponectin. Colon epithelial barrier integrity was improved in the HF+B group versus HF, as evidenced by increased mRNA expression of tight junction components (ZO‐1, occludin, JAM‐A and claudin‐2) and functionally by reduced serum FITC‐dextran concentration in an in vivo gut permeability test. Additionally, evidence of an enhanced mucus barrier and anti‐microbial defence was apparent in the HF+B group versus HF based on increased goblet cell number and upregulated expression of Muc1‐3 and Reg3γ, respectively. In conclusion, bean supplementation enhanced gut barrier integrity and exerted a beneficial colon‐function priming effect that helps mitigate the severity of the obese phenotype.