Microbial degradation of complex carbohydrates in the gut

Abstract

Bacteria that colonize the mammalian intestine collectively possess a far larger repertoire of degradative enzymes and metabolic capabilities than their hosts. Microbial fermentation of complex non-digestible dietary carbohydrates and host-derived glycans in the human intestine has important consequences for health. Certain dominant species, notably among the Bacteroidetes, are known to possess very large numbers of genes that encode carbohydrate active enzymes and can switch readily between different energy sources in the gut depending on availability. Nevertheless, more nutritionally specialized bacteria appear to play critical roles in the community by initiating the degradation of complex substrates such as plant cell walls, starch particles and mucin. Examples are emerging from the Firmicutes, Actinobacteria and Verrucomicrobium phyla, but more information is needed on these little studied groups. The impact of dietary carbohydrates, including prebiotics, on human health requires understanding of the complex relationship between diet composition, the gut microbiota and metabolic outputs.

Figure 1. Major diet-derived polysaccharides and microbial carbohydrate-degrading enzyme activities. The enzyme families most associated with particular activities in gut bacteria are indicated as follows: GH, glycoside hydrolase; PL, polysaccharide lyase; CE, carbohydrate esterase; G, glucose; F, fructose; X, xylose; A, arabinose; GalU, galacturonic acid; GluU, glucuronic acid. [For details refer to the CAZY website (/www.cazy.org/)].

Figure 2. Plant cell wall structure. Diagrammatic representation of the major structural polysaccharide components of a "typical" primary plant cell wall.

Figure 3. Examples of cell surface organization of carbohydrate-degrading enzymes in anaerobic Gram-positive gut bacteria. A and C show the domain structures and organization of two major cell-surface anchored amylases from two human intestinal anaerobes (Numbering refers to the enzyme family (as in Figure 1) or carbohydrate binding module (CBM) family). B shows the domain structures of six examples of cellulosomal polysaccharidases from the rumen bacterium Ruminococcus flavefaciens FD1. D shows the likely organization of the cellulosome in R. flavefaciens FD1; scaE, scaB, scaA and scaC are structural proteins encoded by the sca gene cluster that interact with each-other and with the cellulosomal enzyme subunits via a series of specific, non-covalent dockerin:cohesin pairings (shown, in gray). The arrows in C and D indicate sortase-mediated anchoring to the bacterial cell wall (also indicated by cross-hatching in A).

Figure 4. Dominant bacterial species identified by analysis of 16S rRNA sequences in fecal samples from six individuals. Data are from Walker et al. (2011) and represent the mean of 26 fecal samples from six obese male volunteers (4, or in one case 6, samples per person) taken during a 12 week controlled dietary study. Phylotypes corresponding to the 25 most abundant cultured bacterial species, that accounted for almost 50% of all sequences, are shown in descending order of abundance on the right hand side. The gray area on the left represents the 295 additional phylotypes (both cultured and uncultured organisms) that were detected.

Figure 5.Bacteroides thetaiotaomicron sus system. A shows the order of genes in the sus cluster that is responsible for starch utilization in this species. B shows the inferred organization of gene products on or near the bacterial cell surface (OM outer membrane, CM cytoplasmic membrane). Starch molecules are shown as sugar chains, at various stages of hydrolysis.

Figure 6. Energy intake and expenditure. The diagram summarizes the potential of gut microorganisms to influence energy gain and expenditure in a mono-gastric animal such as man. The energy arising from microbial fermentation via the absorption of short chain fatty acids may be influenced by microbiota composition, but more especially by gut transit, affecting the efficiency of substrate breakdown, digestion and absorption. Other potentially important, but little understood, influences however include possible effects of microbial products on satiety and energy expenditure.