Dynamics of structural and functional changes in gut microbiota during treatment with a microalgal β- glucan, paramylon and the impact on gut inflammation

Abstract

Background Previously, we have shown that oral administration of yeast derived β-1,3/1,6-D-glucan, a complex dietary polysaccharide, enhances immune regulation, reduces gut inflammation and alters the composition of the gut microbiota. However, it is not known if other structurally distinct β-glucans have similar properties. The aim of this study was, using B6 mice, to investigate the ability of a microalgae derived β-1,3-D-glucan, paramylon (PM), a widely used dietary supplement, in shaping the gut microbiota and modulating the susceptibility to gut inflammation. Results The community structure within the gut microbiota, based on 16S rRNA sequencing data, showed progressive changes including selective enrichment of specific communities and lowered community richness and diversity during prolonged oral treatment with PM. Compared to control mice, the gut microbiota of PM treated mice had significantly higher abundance of Verrucomicrobia (+ 16.46%; p = 0.002) and lower abundance of Firmicutes (-7.53%; p = 0.0147). Specific taxa that were significantly more abundant in PM treated mice include Akkermansia muciniphila (p = 0.037) and several Bacteroides members. Predictive functional analysis revealed overrepresentation of carbohydrate metabolism function in general (p = 0.0058) and glycosaminoglycan degradation (p = 0.015), fatty acid biosynthesis (p = 0.0082), and sugar (fructose, mannose) metabolism (p = 0.0065) in particular in the fecal microbiota of PM recipients compared to controls, and many of these functions were linked to Bacteroides spp. Pretreatment with PM not only diminished susceptibility to dextran sulfate sodium (DSS) to induced colitis severity (colon inflammation score; p = 0.029), but also caused enhanced immune regulation through increasing Foxp3 + T-cells (p = 0.0108) and IL10- producing cells (p = 0.0159), and decreasing IFNγ producing cells (p = 0.0224). Conclusions The use of PM as an oral dietary supplement effectively alters the composition of gut microbiota by enriching certain microbial communities such as Bacteroides spp. and carbohydrate metabolism function. These changes promote an anti-inflammatory/regulatory immune response which suppresses susceptibility to gut inflammation. Overall, this study demonstrates the prebiotic properties of PM and the potential benefits of its prolonged oral consumption to gut health.