Bacterial and Fungal Gut Community Dynamics Over the First 5 Years of Life in Predominantly Rural Communities in Ghana

Abstract

Background: Bacterial and fungal microbiotas are increasingly recognized as important in health and disease starting early in life. However, microbiota composition has not yet been investigated in most rural, low-resource settings, and in such settings, bacterial and fungal microbiotas have not been compared. Thus, we applied 16S and ITS2 amplicon sequencing, respectively, to investigate bacterial and fungal fecal microbiotas in rural Ghanaian children cross-sectionally from birth to 5 years of age. Corresponding maternal fecal and breast milk microbiotas were additionally investigated.

Results: While bacterial communities differed systematically across the age spectrum in composition and diversity, the same was not observed for the fungal microbiota. We also identified a novel and dramatic change in the maternal postpartum microbiota. This change included much higher abundance of Escherichia coli and much lower abundance of Prevotella in the first vs. fourth week postpartum. While infants shared more bacterial taxa with their mother's stool and breast milk than with those of unrelated mothers, there were far fewer shared fungal taxa.

Conclusion: Given the known ability of commensal fungi to influence host health, the distinct pattern of their acquisition likely has important health consequences. Similarly, the dynamics of mothers' bacterial microbiotas around the time of birth may have important consequences for their children's health. Both topics require further study.

Keywords: bacteria; breast milk; child; fungi; post partum microbiome.

FIGURE 1

Alpha diversity across the age spectrum for bacterial fecal communities (A) and fungal fecal communities (B). Coding indicates values significantly different from those of adult communities (Mothers of 26–35-day-old newborns): ****p < 0.0001, ***p < 0.001, **p < 0.01, *p < 0.05; Wilcoxon rank-sum test adjusted using the Bonferroni correction. Boxplots indicate medians with first and third quartiles (25–75%). Whiskers extend no farther than 1.5*IQR from the hinge.

FIGURE 2

Bacterial and fungal communities across the age spectrum. (A,B) Ordinations of community composition based on Bray–Curtis distance for bacterial (A) and fungal (B) fecal communities. (C) Bray–Curtis distance between each age bin and 5 years. ****p < 0.0001, ***p < 0.001, *p < 0.05, Wilcoxon rank-sum test, adjusted using the Bonferroni correction.

FIGURE 3

Relative abundance of the 25 most abundant genera. Bacterial (A) and fungal (B) community composition across the age spectrum.

FIGURE 4

Comparison of fecal bacterial microbiotas of mothers 1 and 4 weeks postpartum and children at 1 week. (A) Average pairwise similarity of the microbiotas of mothers vs. those of their children. (B) Operational taxonomic units (OTUs) identified by DESeq2 differentially abundant between mothers 1 week vs. 4 weeks postpartum. Negative fold-difference indicates greater abundance 1 week postpartum. (C–F) Relative abundance of selected taxa that were differentially abundant between mothers 1 week vs. 4 weeks postpartum. ****p < 0.0001, **p < 0.01, *p < 0.05, Wilcoxon rank-sum test, adjusted using the Bonferroni correction.

FIGURE 5

Breast milk bacterial and fungal community composition. (A,B) Top 25 most abundant bacterial (A) and fungal (B) genera across all samples reveal that both communities are dominated by common skin taxa but also contain a diverse repertoire of microbes at lower abundances. (C) Differentially abundant taxa between mothers in the first compared to the fourth postpartum week. (D,E) Number of shared bacterial (D) and fungal (E) operational taxonomic units (OTUs) between mother–infant pairs in the first and fourth postpartum weeks. Statistics: ***p < 0.001, *p < 0.05, Wilcoxon rank-sum test, adjusted using the Bonferroni correction.