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.
Highlights
Bifidobacteria are Gram-positive obligate anaerobes that represent common inhabitants of the gastrointestinal tract of animals [1]
In this review, when compared with other human gut-associated Bifidobacterium species, we reveal the unique characteristics of B. bifidum that have adaptively evolved for host glycan utilization
In the growth competition assays in the presence of B. bifidum, the colony-forming units of ∆gltA strain at 12 h culture were comparable with that of the wild-type in the media containing either human milk oligosaccharides (HMOs) or mucin (Figure 4E,F). These results indicate that the utilization of GNB/LNB was not prioritized by B. longum in the presence of many other sugars, such as Gal, GlcNAc, or lactose released from HMOs/mucin O-glycans under our experimental conditions
Summary
Bifidobacteria are Gram-positive obligate anaerobes that represent common inhabitants of the gastrointestinal tract of animals [1]. This observation is not paralleled with their in vitro growth ability in HMO-containing media, i.e., B. infantis and B. bifidum grow avidly with HMOs as a sole carbon source and obtain high cell density, but B. breve and B. longum show very limited growth in single culture experiments [87] This apparent inconsistency between the abundance in the intestinal tracts and abundance in vitro suggest that there is a more complicated mechanism underlying the bifidus-flora formation in infant guts. A correlation with the higher abundance of Bifidobacterium in the total microbiota was observed for B. bifidum in breast-fed infants, and for B. longum, B. adolescentis, and B. catenulatum group in human subjects with a wide age range [44]. A Cutibacterium avidum isolate from infant feces was shown to produce a higher amount of propionate when co-cultured with B. bifidum in yeast extract, casitone and fatty acid (YCFA) medium containing HMOs than when cultured alone in the same medium, suggesting inter-genus utilization of B. bifidum-released sugar metabolites [95]
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