The development of human gut microbiota fermentation capacity during the first year of life

Abstract

Fermentation capacity of microbial ecosystems intrinsically depends on substrate supply and the ability of a microbial community to deliver monomers for fermentation. In established microbial ecosystems, the microbial community is adapted to efficiently degrade and ferment available biopolymers which is often concurrently reflected in the richness of the microbial community and its functional potential. During the first year of life, the human gut microbial environment is a rather dynamic system that is characterized by a change in physiological conditions (e.g. from aerobic to anaerobic conditions, physical growth of the gastrointestinal tract, development of the intestinal immune system) but also by a change in nutrient supply from a compositionally limited liquid to a diverse solid diet, which demands major compositional and functional changes of the intestinal microbiota. How these transitions link to intestinal microbial fermentation capacity has gained comparatively little interest so far. This mini-review aims to collect evidence that already after birth, there is seeding of a hidden population of various fermentation organisms which remain present at low abundance until the cessation of breastfeeding removes nutritional restrictions of a liquid milk-based diet. The introduction of solid food containing plant and animal material is accompanied by an altering microbiota. The concurrent increases in the abundance of degraders and fermenters lead to higher intestinal fermentation capacity indicated by increased faecal levels of the final fermentation metabolites propionate and butyrate. Recent reports indicate that the development of fermentation capacity is an important step during gut microbiota development, as chronic disorders such as allergy and atopic dermatitis have been linked to lower degradation and fermentation capacity indicated by reduced levels of final fermentation metabolites at 1 year of age.

FIGURE 1

Scheme indicating the succession of microbial degradation, fermentation and methanogenesis of dietary carbohydrates. Microbial communities in anaerobic ecosystems consisting of degraders, fermenters and methanogens interact (i) in releasing fermentable monosaccharides from complex carbohydrates, (ii) fermenting and cross‐feeding on fermentation metabolites and (iii) delivering substrates for methanogens. Overall fermentation capacity, that is, the potential to form C0₂ and CH₄ from carbohydrates, is determined by microbial community composition and functional diversity and fermentation potential. In infants, fermentation capacity increases during weaning.

FIGURE 2

Overview of major dietary carbohydrates before (A) and after (B) weaning. Undigested dietary carbohydrates of breastfed infants are mainly human milk oligosaccharides composed of five different monomers (A). For comparison, examples of structurally and compositionally diverse plant‐polysaccharides are shown which are introduced to the food plan during the weaning phase (B).

FIGURE 3

Scheme depicting the changes of microbial communities and faecal fermentation profiles that occur with the introduction of solid food. The intestinal microbiota changes from a Bifidobacterium dominated microbiota that produces mostly acetate and lactate to compositionally and functionally more diverse microbial communities with the introduction of solid food. This transformation leads to increasing faecal levels of propionate and butyrate. Figure was prepared using biorender. Ace, acetate; but, butyrate; lac, lactate; pro, propionate.