Journal Article

Breast milk-derived human milk oligosaccharides promote Bifidobacterium interactions within a single ecosystem

Hall, Lindsay J., O’Neill, Ian J., Flegg, Zak, Chalklen, Lisa, Gowrinadh Javvadi, Sree, Kujawska, Magdalena, Wijeyesekera, Anisha, Lawson, Melissa A. E.

2020

Overview

Diet-microbe interactions play an important role in modulating the early-life microbiota, with Bifidobacterium strains and species dominating the gut of breast-fed infants. Here, we sought to explore how infant diet drives distinct bifidobacterial community composition and dynamics within individual infant ecosystems. Genomic characterisation of 19 strains isolated from breast-fed infants revealed a diverse genomic architecture enriched in carbohydrate metabolism genes, which was distinct to each strain, but collectively formed a pangenome across infants. Presence of gene clusters implicated in digestion of human milk oligosaccharides (HMOs) varied between species, with growth studies indicating that within single infants there were differences in the ability to utilise 2′FL and LNnT HMOs between strains. Cross-feeding experiments were performed with HMO degraders and non-HMO users (using spent or ‘conditioned’ media and direct co-culture). Further 1 H-NMR analysis identified fucose, galactose, acetate, and N-acetylglucosamine as key by-products of HMO metabolism; as demonstrated by modest growth of non-HMO users on spend media from HMO metabolism. These experiments indicate how HMO metabolism permits the sharing of resources to maximise nutrient consumption from the diet and highlights the cooperative nature of bifidobacterial strains and their role as ‘foundation’ species in the infant ecosystem. The intra- and inter-infant bifidobacterial community behaviour may contribute to the diversity and dominance of Bifidobacterium in early life and suggests avenues for future development of new diet and microbiota-based therapies to promote infant health.

• Publisher: Nature Publishing Group UK,Oxford University Press
• Subject: 45/23 / 631/326/2565/2134 / 631/326/2565/855 / 631/326/41/1969 / Acetic acid / Babies / Bifidobacterium / Bifidobacterium - genetics / Bifidobacterium - isolation & purification / Bifidobacterium - physiology / Biomedical and Life Sciences / Breast / Breast Feeding / Breast milk / Breastfeeding & lactation / Carbohydrate metabolism / Carbohydrate Metabolism - genetics / Carbohydrates / Community composition / Community participation / Diet / Ecology / Ecosystem / Ecosystems / Evolutionary Biology / Female / Fucose / Galactose / Gene clusters / Genes, Bacterial / Genetic Variation / Genome, Bacterial / Humans / Infant / Infants / Life Sciences / Metabolism / Metagenome - genetics / Metagenome - physiology / Microbial Ecology / Microbial Genetics and Genomics / Microbial Interactions / Microbiology / Microbiota / Milk / Milk, Human - chemistry / N-Acetylglucosamine / NMR / Nuclear magnetic resonance / Oligosaccharides / Oligosaccharides - genetics / Oligosaccharides - metabolism / Species / Syntrophism