Succession of microbial consortia in the developing infant gut microbiome

• Published in: Proceedings of the National Academy of Sciences - PNAS 2011-03, Vol.108 (Supplement 1), p.4578-4585
• Main Authors: Koenig, Jeremy E, Spor, AymÃ, Scalfone, Nicholas, Fricker, Ashwana D, Stombaugh, Jesse, Knight, Rob, Angenent, Largus T, Ley, Ruth E
• Format: Article
• Language: English
• Subjects: adults; Age Factors; Antibiotics; Bacteroidetes; Base Sequence; Biological Sciences; biosynthesis; case studies; Checkerboards; Cluster Analysis; Colloquium Papers; community structure; Diet; digestive system; DNA; DNA Barcoding, Taxonomic; DNA Primers - genetics; ecological succession; feces; Feces - microbiology; foods; Gastrointestinal Tract - microbiology; genes; health status; Humans; Infant; Infant, Newborn; infants; ingestion; intestinal microorganisms; Life events; Metagenome - genetics; Metagenomics; microbiome; Microbiota; Molecular Sequence Data; Phylogenetics; phylogeny; Polymerase chain reaction; polysaccharides; ribosomal RNA; RNA, Ribosomal, 16S - genetics; rRNA genes; Sequence Analysis, DNA; short chain fatty acids; Species Specificity
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1000081107

The colonization process of the infant gut microbiome has been called chaotic, but this view could reflect insufficient documentation of the factors affecting the microbiome. We performed a 2.5-y case study of the assembly of the human infant gut microbiome, to relate life events to microbiome composition and function. Sixty fecal samples were collected from a healthy infant along with a diary of diet and health status. Analysis of >300,000 16S rRNA genes indicated that the phylogenetic diversity of the microbiome increased gradually over time and that changes in community composition conformed to a smooth temporal gradient. In contrast, major taxonomic groups showed abrupt shifts in abundance corresponding to changes in diet or health. Community assembly was nonrandom: we observed discrete steps of bacterial succession punctuated by life events. Furthermore, analysis of [almost equal to]500,000 DNA metagenomic reads from 12 fecal samples revealed that the earliest microbiome was enriched in genes facilitating lactate utilization, and that functional genes involved in plant polysaccharide metabolism were present before the introduction of solid food, priming the infant gut for an adult diet. However, ingestion of table foods caused a sustained increase in the abundance of Bacteroidetes, elevated fecal short chain fatty acid levels, enrichment of genes associated with carbohydrate utilization, vitamin biosynthesis, and xenobiotic degradation, and a more stable community composition, all of which are characteristic of the adult microbiome. This study revealed that seemingly chaotic shifts in the microbiome are associated with life events; however, additional experiments ought to be conducted to assess how different infants respond to similar life events.