Consumption of human milk oligosaccharides by gut-related microbes

Abstract

Human milk contains large amounts of complex oligosaccharides that putatively modulate the intestinal microbiota of breast-fed infants by acting as decoy binding sites for pathogens and as prebiotics for enrichment of beneficial bacteria. Several bifidobacterial species have been shown to grow well on human milk oligosaccharides. However, few data exist on other bacterial species. This work examined 16 bacterial strains belonging to 10 different genera for growth on human milk oligosaccharides. For this propose, a chemically defined medium, ZMB1, was used, which allows vigorous growth of a number of gut-related microorganisms in a fashion similar to complex media. Interestingly, Bifidobacterium longum subsp. infantis, Bacteroides fragilis , and Bacteroides vulgatus strains were able to metabolize milk oligosaccharides with high efficiency, whereas Enterococcus , Streptococcus , Veillonella , Eubacterium , Clostridium , and Escherichia coli strains grew less well or not at all. Mass spectrometry-based glycoprofiling of the oligosaccharide consumption behavior revealed a specific preference for fucosylated oligosaccharides by Bi. longum subsp. infantis and Ba. vulgatus. This work expands the current knowledge of human milk oligosaccharide consumption by gut microbes, revealing bacteroides as avid consumers of this substrate. These results provide insight on how human milk oligosaccharides shape the infant intestinal microbiota.

Figures

Figure 1

Human milk oligosaccharide consumption profiles of Bifidobacterium infantis, Bacteroides fragilis and Bacteroides vulgatus in modified ZMB1 (2% HMO), as determined using MALDI-FTICR MS. Asterisks represents number of fucose residues on the specific oligosaccharide depicted by the mass/charge ratio (m/z).

Figure 2

Annotated genes coding for some carbohydrate active enzymes in the genomes of Bacteroides fragilis ATCC25285, Bacteroides vulgatus ATCC8483, Bifidobacterium infantis ATCC15697 and Bifidobacterium longum DJO10A, as it is described at the CAZy database (http://www.cazy.org) (27). The glycoside hydrolase families (GHF) shown are potentially related to the degradation of HMOs, and they include the following activities: GH2, α-galactosidase; GH3, β-N-Acetylgalactosaminidase; GH20, β-hexosaminidase; GH27, α-N-acetylgalactosaminidase; GH29, α-L-fucosidase; GH33, sialidase; GH42, β-galactosidase; GH95, α-1,2-L-fucosidase.