Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns

Abstract

Upon delivery, the neonate is exposed for the first time to a wide array of microbes from a variety of sources, including maternal bacteria. Although prior studies have suggested that delivery mode shapes the microbiota's establishment and, subsequently, its role in child health, most researchers have focused on specific bacterial taxa or on a single body habitat, the gut. Thus, the initiation stage of human microbiome development remains obscure. The goal of the present study was to obtain a community-wide perspective on the influence of delivery mode and body habitat on the neonate's first microbiota. We used multiplexed 16S rRNA gene pyrosequencing to characterize bacterial communities from mothers and their newborn babies, four born vaginally and six born via Cesarean section. Mothers' skin, oral mucosa, and vagina were sampled 1 h before delivery, and neonates' skin, oral mucosa, and nasopharyngeal aspirate were sampled <5 min, and meconium <24 h, after delivery. We found that in direct contrast to the highly differentiated communities of their mothers, neonates harbored bacterial communities that were undifferentiated across multiple body habitats, regardless of delivery mode. Our results also show that vaginally delivered infants acquired bacterial communities resembling their own mother's vaginal microbiota, dominated by Lactobacillus, Prevotella, or Sneathia spp., and C-section infants harbored bacterial communities similar to those found on the skin surface, dominated by Staphylococcus, Corynebacterium, and Propionibacterium spp. These findings establish an important baseline for studies tracking the human microbiome's successional development in different body habitats following different delivery modes, and their associated effects on infant health.

Fig. 1.

Bacterial 16S rRNA gene surveys reveal that the first microbiotas of human newborns are primarily structured by delivery mode. (A) Communities clustered using principal coordinates analysis of the unweighted UniFrac distance matrix. PC1 and PC2 are plotted on x- and y-axes. Each point corresponds to a community colored according to the mother's body habitat or the newborn's delivery mode. All newborn body habitats are shown. The percentage of variation explained by the plotted principal coordinates is indicated on the axes. The white arrow indicates a pair of superimposed points. Vaginal samples were not obtained from two of the mothers who delivered by C-section. (B) Average relative abundances of the dominant taxa found in this study in aggregated samples. (C) Relative abundances of the 20 most abundant taxa in mothers’ vaginal communities and in the babies they delivered vaginally. Sequences were classified to highest taxonomic level to which they could be confidently assigned.

Fig. 2.

The effect of delivery mode on the direct transmission of bacteria from mother to newborn. Average (±SEM) weighted UniFrac distance for pairwise comparisons between (A) vaginal microbiota of mothers who delivered vaginally, or (B) the skin microbiota of mothers who delivered via C-section and the microbiotas of the newborn babies. The maternal microbiota (vagina or skin) was compared with the microbiota of her own baby, or babies of the same or different delivery mode. Baby samples were from the skin (arms and forehead), oral mucosa, nasopharyngeal aspirate, and meconium. The mothers’ skin samples were from both arms.