Degradation of complex arabinoxylans by human colonic Bacteroidetes

Abstract

Some Bacteroidetes and other human colonic bacteria can degrade arabinoxylans, common polysaccharides found in dietary fiber. Previous work has identified gene clusters (polysaccharide-utilization loci, PULs) for degradation of simple arabinoxylans. However, the degradation of complex arabinoxylans (containing side chains such as ferulic acid, a phenolic compound) is poorly understood. Here, we identify a PUL that encodes multiple esterases for degradation of complex arabinoxylans in Bacteroides species. The PUL is specifically upregulated in the presence of complex arabinoxylans. We characterize some of the esterases biochemically and structurally, and show that they release ferulic acid from complex arabinoxylans. Growth of four different colonic Bacteroidetes members, including Bacteroides intestinalis, on complex arabinoxylans results in accumulation of ferulic acid, a compound known to have antioxidative and immunomodulatory properties.

Degradation Products of Complex Arabinoxylans by Bacteroides intestinalis Enhance the Host Immune Response

“…We attribute the congruent results of the treatment with ferulic acid and the culture supernatant from Bacteroides intestinalis grown in InWAX to the release of side-chain ferulic acid during the growth of this colonic bacterium on the complex polysaccharide, as we have previously reported high concentrations of ferulic acid in the culture supernatant from Bacteroides intestinalis cultured on insoluble arabinoxylans and also as shown in Figure 1 . Thus, the presence of ferulic acid in the bacterial culture supernatant may explain the anti-inflammatory activity of the degraded products of complex arabinoxylans by Bacteroides intestinalis [ 7 ].…”

“…Soluble wheat arabinoxylan with medium viscosity, insoluble wheat arabinoxylan, xylose, and arabinose were obtained from Megazyme (Bray, Ireland). Preparation of the de-starched wheat bran (DWB) was done as described in our earlier report [ 7 ]. Briefly, the DWB was prepared by milling 60 g of wheat bran (WB) to pass through a sieve of diameter < 0.5 mm, followed by suspension in 600 mL of phosphate buffer (80 mM, pH 6.2).…”

“…Arabinoxylans form the structure of cell walls of plants, including cereal grains [ 6 ]. The insoluble form of arabinoxylans contains large amounts of phenolic compounds, including ferulic acid [ 7 , 8 ].…”

“…The release of ferulic acid from dietary fiber requires the degradation of complex arabinoxylans [ 7 , 11 ]. However, as humans lack the enzymes capable of degrading arabinoxylans, the degradation of this complex polysaccharide depends on enzymes released by members of the gut microbiome [ 12 , 13 ].…”

“…In addition, we recently demonstrated that the degradation of complex arabinoxylans by Bacteroides spp. releases large amounts of ferulic acid [ 7 ]. Based on these observations, we hypothesized that the degradation products of complex arabinoxylans by Bacteroides intestinalis , a member of the human colonic Bacteriodetes , would enhance the host immune response.…”