Abstract
Relatively little is known about the ecological forces shaping the gut microbiota composition during infancy. Therefore, the objective of the present study was to identify the nutrient utilization- and short-chain fatty acid (SCFA) production potential of gut microbes in infants during the first year of life. Stool samples were obtained from mothers at 18 weeks of pregnancy and from infants at birth (first stool) at 3, 6, and 12-months of age from the general population-based PreventADALL cohort. We identified the taxonomic and SCFA composition in 100 mother-child pairs. The SCFA production and substrate utilization potential of gut microbes were observed by multiomics (shotgun sequencing and proteomics) on six infants. We found a four-fold increase in relative butyrate levels from 6 to 12 months of infant age. The increase was correlated to Eubacterium rectale and its bacterial network, and Faecalibacterium prausnitzii relative abundance, while low butyrate at 12 months was correlated to Ruminococcus gnavus and its associated network of bacteria. Both E. rectale and F. prausnitzii expressed enzymes needed for butyrate production and enzymes related to dietary fiber degradation, while R. gnavus expressed mucus-, fucose, and human milk oligosaccharides (HMO)-related degradation enzymes. Therefore, we believe that the presence of E. rectale, its network, and F. prausnitzii are key bacteria in the transition from an infant- to an adult-like gut microbiota with respect to butyrate production. Our results indicate that the transition from an infant- to an adult-like gut microbiota with respect to butyrate producing bacteria, occurs between 6 and 12 months of infant age. The bacteria associated with the increased butyrate ratio/levels were E. rectale and F. prausnitzii, which potentially utilize a variety of dietary fibers based on the glycoside hydrolases (GHs) expressed. R. gnavus with a negative association to butyrate potentially utilizes mucin, fucose, and HMO components. This knowledge could have future importance in understanding how microbial metabolites can impact infant health and development.
Highlights
The temporal development of the gut microbiota during infancy is essential for immunological and developmental programming [1]
The cut-off was set to 5000 sequences per sample, as the observed species rarefaction curve showed saturation at approximately 5000 sequences for all infant age groups (Supplementary Figure S1)
We believe that the E. rectale network co-occurring with F. prausnitzii could play a key role in the elevated relative abundance of butyrate
Summary
The temporal development of the gut microbiota during infancy is essential for immunological and developmental programming [1]. Regardless of when colonization occurs, the bacterial diversity in vaginally delivered newborns largely represent bacteria from the mother’s natural vaginal flora, such as Lactobacillus, Bifidobacterium, Prevotella, and Sneathia [5,7], as well as from the maternal gut flora [8]. The earliest colonization often consists of Proteobacteria, which is likely involved in facilitating a suitable environment for anaerobic bacteria by depleting the gut of oxygen [7]. The oxygen depletion increases the amount of Bacteroides, Clostridium, and Bifidobacterium. Bifidobacterium dominates from an early stage until weaning, due to their capacity to break down human milk oligosaccharides [7,9,10]. The infant’s gut microbiota composition starts to resemble the adult gut microbiota in terms of anaerobes, such as Clostridium and Bacteroides [11]
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