Microbial Glycoside Hydrolases in the First Year of Life: An Analysis Review on Their Presence and Importance in Infant Gut

Abstract

The first year of life is a crucial period during which the composition and functionality of the gut microbiota develop to stabilize and resemble that of adults. Throughout this process, the gut microbiota has been found to contribute to the maturation of the immune system, in gastrointestinal physiology, in cognitive advancement and in metabolic regulation. Breastfeeding, the “golden standard of infant nutrition,” is a cornerstone during this period, not only for its direct effect but also due to its indirect effect through the modulation of gut microbiota. Human milk is known to contain indigestible carbohydrates, termed human milk oligosaccharides (HMOs), that are utilized by intestinal microorganisms. Bacteria that degrade HMOs like Bifidobacterium longum subsp. infantis, Bifidobacterium bifidum, and Bifidobacterium breve dominate the infant gut microbiota during breastfeeding. A number of carbohydrate active enzymes have been found and identified in the infant gut, thus supporting the hypothesis that these bacteria are able to degrade HMOs. It is suggested that via resource-sharing and cross-feeding, the initial utilization of HMOs drives the interplay within the intestinal microbial communities. This is of pronounced importance since these communities promote healthy development and some of their species also persist in the adult microbiome. The emerging production and accessibility to metagenomic data make it increasingly possible to unravel the metabolic capacity of entire ecosystems. Such insights can increase understanding of how the gut microbiota in infants is assembled and makes it a possible target to support healthy growth. In this manuscript, we discuss the co-occurrence and function of carbohydrate active enzymes relevant to HMO utilization in the first year of life, based on publicly available metagenomic data. We compare the enzyme profiles of breastfed children throughout the first year of life to those of formula-fed infants.

Utilization Efficiency of Human Milk Oligosaccharides by Human-Associated Akkermansia Is Strain Dependent

“…Next, since we were interested in the ability of Akkermansia to degrade HMOs, we focused on HMO-associated GH families previously identified in other organisms ( 26 , 30 – 33 ). With this approach, we identified differences in the copy numbers of several GH families that are associated with the degradation of HMO glycans: α-fucosidases, α-sialidases, β-galactosidases, and N -acetyl β-hexosaminidases ( Table 2 ).…”

“…Thus, since HMO- Akkermansia interactions are strain specific, the corresponding pattern of early colonization with human-associated Akkermansia and the ensuing competitive advantage could also be strain specific in infants ingesting HMOs. Akkermansia bacteria are key contributors to the infants’ glycan-metabolizing capacity by as early as 4 months of age ( 33 ) and may therefore play a critical role in establishing a foundation of metabolic fitness in the naive microbiome. Taken together, these findings expand the known metabolic niche and interaction network of Akkermansia in the human gut early in life.…”

In Vitro Probiotic Modulation of the Intestinal Microbiota and 2′Fucosyllactose Consumption in Fecal Cultures from Infants at Two Months of Age

“…The most prevalent Bifidobacterium species in the infant gut are Bifidobacterium breve, Bifidobacterium bifidum, and Bifidobacterium longum [14]. Strains of B. bifidum, B. longum subsp infantis, and B. breve seem to be especially well adapted to metabolize HMOs [1,15,16].…”

Human Milk Oligosaccharide-Stimulated Bifidobacterium Species Contribute to Prevent Later Respiratory Tract Infections

“…Historically, HMOs were first described following the observation that breastfed and formula-fed infants are colonized with different microbes in early life [ 19 ]. In breastfed infants, specific HMOs such as 2′fucosyllactose (2′FL), lacto-N-tetraose (LNT) and lacto-N- neo tetraose (LNnT) are supposed to be fermented by the gut microbiota, leading to increased Bifidobacterium abundance and metabolic activity [ 20 , 21 , 22 , 23 , 24 ]. Breastfed infants having Bifidobacterium breve strains able to use FL showed the highest Bifidobacterium abundance and a gut environment with the highest acetate concentration.…”