Enzymatic Adaptation of Bifidobacterium bifidum to Host Glycans, Viewed from Glycoside Hydrolyases and Carbohydrate-Binding Modules

Abstract

Certain species of the genus Bifidobacterium represent human symbionts. Many studies have shown that the establishment of symbiosis with such bifidobacterial species confers various beneficial effects on human health. Among the more than ten (sub)species of human gut-associated Bifidobacterium that have significantly varied genetic characteristics at the species level, Bifidobacterium bifidum is unique in that it is found in the intestines of a wide age group, ranging from infants to adults. This species is likely to have adapted to efficiently degrade host-derived carbohydrate chains, such as human milk oligosaccharides (HMOs) and mucin O-glycans, which enabled the longitudinal colonization of intestines. The ability of this species to assimilate various host glycans can be attributed to the possession of an adequate set of extracellular glycoside hydrolases (GHs). Importantly, the polypeptides of those glycosidases frequently contain carbohydrate-binding modules (CBMs) with deduced affinities to the target glycans, which is also a distinct characteristic of this species among members of human gut-associated bifidobacteria. This review firstly describes the prevalence and distribution of B. bifidum in the human gut and then explains the enzymatic machinery that B. bifidum has developed for host glycan degradation by referring to the functions of GHs and CBMs. Finally, we show the data of co-culture experiments using host-derived glycans as carbon sources, which underpin the interesting altruistic behavior of this species as a cross-feeder.

Species- and Age/Generation-Dependent Adherence of Bifidobacterium bifidum to Human Intestinal Mucus In Vitro

“…Specific strains of B. bifidum, for example, B. bifidum TMC3115, may alter host immunity in a different manner from other bifidobacteria, and modify the allergic responses of host animals [ 14 , 25 , 26 ]. Furthermore, B. bifidum was found to possess many extracellular glycosidases specified for degrading host-derived glycans, including HMOs, by which mono- and disaccharides are liberated from host glycans and HMOs and released into living environmental niches or culture medium in vitro [ 27 , 28 ]. Therefore, B. bifidum could support the growth of other bifidobacteria by sharing products derived from glycan degradation within the community.…”

The genus Bifidobacterium: from genomics to functionality of an important component of the mammalian gut microbiota

“…The basic structure of these host-derived carbohydrates includes combinations of at least three of five distinct monosaccharides, including glucose, galactose, N -acetylglucosamine, fucose and sialic acid, the latter generally represented by N -acetyl-neuraminic acid [156] , [157] . All HMOs contain lactose at their reducing end and are extended in various ways with these HMO building blocks through various glycolytic linkages, resulting in an immense combinatorial potential, highlighted by the fact that more than 200 structurally different human milk oligosaccharides have been described [156] , [157] , [158] .…”

“…infantis is restricted to utilize HMOs with a relatively low degree of polymerization (DP ≤ 8), due to size limitations imposed by the ABC-type transporter [168] , [171] . In contrast, the production of extracellular fucosidases and sialidases, principally encoded by genes belonging to the GH20, GH29, GH33 and GH95 families, allows B. bifidum strains to activate an initial extracellular degradation of (larger) HMOs, thereby acquiring access to highly polymerized host-derived glycans and ensuring the ecological success of this bifidobacterial species in the (breast-fed) infant gut environment [68] , [158] , [171] , [172] , [173] , [174] , [175] . After the initial extracellular processing, the generated mono- or di-saccharides (galactose, glucose, lactose and lacto- N -biose) are subsequently imported to be further metabolized intracellularly through the central fermentative pathway [169] , [172] , [173] .…”

Analyzing the intestinal microbiome in inflammatory bowel disease: From RNA to multiomics

“…Of these differentially regulated taxa, 87 were common to both conditions. Some of the species that were unique to ulcerative colitis were the complex sugar‐metabolizing bacteria Bacteoides uniformis 6 and Bifidobacterium bifidum 7 . In contrast, patients with CD were found to have a decrease in bacteria such as Faecalibacterium prausnitzii , a butyrate‐producing bacteria with anti‐inflammatory properties, and Bifidobacterium longum , bacteria known to protect against infection by harmful bacteria.…”