Plant Glycan Metabolism by Bifidobacteria

Abstract

Members of the genus Bifidobacterium, of which the majority have been isolated as gut commensals, are Gram-positive, non-motile, saccharolytic, non-sporulating, anaerobic bacteria. Many bifidobacterial strains are considered probiotic and therefore are thought to bestow health benefits upon their host. Bifidobacteria are highly abundant among the gut microbiota of healthy, full term, breast-fed infants, yet the relative average abundance of bifidobacteria tends to decrease as the human host ages. Because of the inverse correlation between bifidobacterial abundance/prevalence and health, there has been an increasing interest in maintaining, increasing or restoring bifidobacterial populations in the infant, adult and elderly gut. In order to colonize and persist in the gastrointestinal environment, bifidobacteria must be able to metabolise complex dietary and/or host-derived carbohydrates, and be resistant to various environmental challenges of the gut. This is not only important for the autochthonous bifidobacterial species colonising the gut, but also for allochthonous bifidobacteria provided as probiotic supplements in functional foods. For example, Bifidobacterium longum subsp. longum is a taxon associated with the metabolism of plant-derived poly/oligosaccharides in the adult diet, being capable of metabolising hemicellulose and various pectin-associated glycans. Many of these plant glycans are believed to stimulate the metabolism and growth of specific bifidobacterial species and are for this reason classified as prebiotics. In this review, bifidobacterial carbohydrate metabolism, with a focus on plant poly-/oligosaccharide degradation and uptake, as well as its associated regulation, will be discussed.

Keywords: CAZy enzymes; bifidobacteria; carbohydrate metabolism; fiber; glycosyl hydrolase; plant glycans; plant oligosaccharides.

FIGURE 1

Plant cell wall composition and associated plant glycans/fibers. The primary cell wall is located outside of the plant plasma cell membrane. It is composed of cellulose microfibrils, hemicellulose and pectin. The secondary cell wall is located between the primary cell wall and the plasma cell wall. It consists of cellulose microfibrils, hemicellulose and lignin.

FIGURE 2

Structure of some of the hemicelluloses found in the plant cell wall. Hemicelluloses consist of a xylan backbone composed of β-1,4-linked D-xylose moieties, some of which may be substituted with an acetyl group. In glucoronoxylan (GX) the xylan backbone is substituted with D-glucuronic acid, while in the case of arabinoxylan (AX) the carbohydrate decorations consist of α-1,2-linked and/or α-1,3-linked arabinofuranose moieties. Finally, the glycan backbone of glucoronoarabinoxylan (GAX) possesses arabinose substitutions as in AX, in addition to D-glucuronic acid decorations that are α-1,2-linked to the xylan backbone, as well as D-xylose and L-galactose moieties that are β-1,2 linked and α-1,2-linked, respectively, to the arabinose substitutions.

FIGURE 3

Pectin polysaccharides associated with the plant cell wall. Pectin is made up of several polysaccharides including homogalacturonan, rhamnogalacturonan I and rhamnogalacturonan II, the structure of which is schematically depicted.

FIGURE 4

Summary of Inverting hydrolysis, retaining hydrolysis and transglycosylation. (A) Summary of inverting single displacement mechanism. (B) Summary of retaining double displacement mechanism. See text for details of the reactions.

FIGURE 5

Enzymatic degradation of xylan and xylo-oligosacharides (XOS). Degradation of the xylan backbone to XOS by endo-xylanases (A). Degradation of XOS by β-D-xylosidases (B). Degradation of XOS by a ‘Reducing end xylose releasing exo-oligoxylanase (C). DP = degree of polymerization. Enzyme names are indicated in bold. See text for details.

FIGURE 6

Enzymatic degradation of galactan. Degradation of galactan by exo-β1,3- or β1,4-galactanases (A). Degradation of galactan by exo-β1,6-galactanases (B). Degradation of galactan by endo-β1,3- or β1,4-galactanases (C). Degradation of a galactose-sugar moiety bond by β-galactosidases (D). Enzyme names are indicated in bold. See text for details.