The impact of the milk glycobiome on the neonate gut microbiota

Abstract

Human milk is a complete source of nourishment for the infant. Exclusive breastfeeding not only sustains the infant's development but also guides the proliferation of a protective intestinal microbiota. Among the many components of milk that modulate the infant gut microbiota, the milk glycans, which comprise free oligosaccharides, glycoproteins, and glycolipids, are increasingly recognized as drivers of microbiota development and overall gut health. These glycans may display pleiotropic functions, conferring protection against infectious diseases and also acting as prebiotics, selecting for the growth of beneficial intestinal bacteria. The prebiotic effect of milk glycans has direct application to prevention of diseases such as necrotizing enterocolitis, a common and devastating disease of preterm infants. In this article, we review the impact of the human (and bovine) milk glycome on gut health through establishment of a milk-oriented microbiota in the neonate.

Keywords: bifidobacteria; glycobiome; milk bioactives; milk oligosaccharides; neonatal microbiota.

Figure 1

Structural diversity of the milk glycobiome. Abbreviations: BMO, bovine milk oligosaccharide; HMO, human milk oligosaccharide.

Figure 2

Consumption of milk glycans by bifidobacteria. This figure illustrates the transport and glycolytic degradation of human milk oligosaccharide (HMO) (as a representative milk glycan), highlighting the differences between the HMO degradation in Bifidobacterium infantis and Bifidobacterium bifidum. HMO consumption in B. infantis involves intracellular import by ABC transporters, then degradation by intracellular glycosyl hydrolases, releasing free monosaccharides that enter the central metabolism. In contrast, HMO is degraded extracellularly in B. bifidum by the action of membrane-anchored extracellular glycosyl hydrolases, followed by intracellular transport of mono- or disaccharides (GNB/LNB) via sugar permeases or ABC transporters that enter central metabolism. Modified with permission from Reference 188.

Figure 3

Milk bioactives protect against infectious diseases. Human milk oligosaccharides (HMOs) are ingested during consumption of breast milk and reach the intestine minimally digested. HMOs have local effects in the gastrointestinal tract, altering microbial composition (bifidogenic effect); promoting barrier function; and blocking adhesion sites of pathogenic viruses, bacteria, and bacterial toxins. HMO is also systemically absorbed, traveling through the bloodstream and reaching other organs, such as the bladder. Abbreviation: UPEC, uropathogenic Escherichia coli.