Comparative metagenomics and population dynamics of the gut microbiota in mother and infant - PubMed (original) (raw)

Comparative metagenomics and population dynamics of the gut microbiota in mother and infant

Parag A Vaishampayan et al. Genome Biol Evol. 2010.

Abstract

Colonization of the gastrointestinal tract (GIT) of human infants with a suitable microbial community is essential for numerous aspects of health, but the progression of events by which this microbiota becomes established is poorly understood. Here, we investigate two previously unexplored areas of microbiota development in infants: the deployment of functional capabilities at the community level and the population genetics of its most abundant genera. To assess the progression of the infant microbiota toward an adult-like state and to evaluate the contribution of maternal GIT bacteria to the infant gut, we compare the infant's microbiota with that of the mother at 1 and 11 months after delivery. These comparisons reveal that the infant's microbiota rapidly acquires and maintains the range of gene functions present in the mother, without replicating the phylogenetic composition of her microbiota. Microdiversity analyses for Bacteroides and Bifidobacterium, two of the main microbiota constituents, reveal that by 11 months, the phylotypes detected in the infant are distinct from those in the mother, although the maternal Bacteroides phylotypes were transiently present at 1 month of age. The configuration of genetic variants within these genera reveals populations far from equilibrium and likely to be undergoing rapid growth, consistent with recent population turnovers. Such compositional turnovers and the associated loss of maternal phylotypes should limit the potential for long-term coadaptation between specific bacterial and host genotypes.

Keywords: Bacteroides; Bifidobacterium; bacterial population genetics; community genomics; gut microbiota.

PubMed Disclaimer

Figures

F<sc>IG</sc>. 1.—

FIG. 1.—

Phylogenetic composition and general functional capabilities across GIT microbiota samples. (A) Distribution of COG functional categories in the GIT microbiota of mother and infant at 1 and 11 months after delivery. Distributions of COG functional classes are remarkably similar; observed differences across samples do not reach significance (D rank analysis; P > 0.05). (B) PCA of overall COG category profiles in the mother–infant GIT microbiota. Two additional samples (black and gray circles) from adult humans (Gill et al. 2006) are included for comparative purposes. Note the overlapping positions of the two maternal microbiota samples and the infant sample taken at 11 months. The large separation of I-1m from these three samples on the second PC axis stems from the fact that this is the only sample containing the COG category Extracellular Structures (W); the first PC axis separates the four samples in our study from those of Gill et al. (2006) due to the higher numbers of individual COGs represented within each category in these larger samples. (C) Bacterial diversity present in the gastrointestinal microbiota of mother and infant at 1 and 11 months after delivery. Taxonomic affiliation was assigned to the high-scoring (>90% identity) best BlastP matches of protein-coding genes in fosmid-end sequence reads against IMG/M reference isolate genomes. Most identified genera belong to only four phyla: Bacteroidetes (Bacteroides), Actinobacteria (Bifidobacterium, Collinsella, and_Eggerthella_), Proteobacteria (Escherichia, Klebsiella,Shigella, Salmonella,Citrobacter, and other enterics), and Firmicutes (Clostridium, Dorea, other clostridia, and Eubacterium).

F<sc>IG</sc>. 2.—

FIG. 2.—

Phylogeny of GIT haplotypes in relation to diversity within the corresponding genus. Phylogenies of the (A)Bifidobacterium and (B)Bacteroides 16S rRNA haplotypes with representative samples from each genus were derived by maximum likelihood with 1,000 bootstrap replicates under a general time-reversible model with invariant sites and gamma-distributed site rate variation. Scale bar represents 0.02 nucleotide substitutions per site. “Mixed” clades contain haplotypes recovered from both the mother and the infant.

F<sc>IG</sc>. 3.—

FIG. 3.—

Genealogy of Bacteroides haplotypes. (A) Haplotypes forming clade II in figure 2_B_, including haplotypes isolated from the mother at 1 month after delivery (M-1m; dark blue circles) as well as new haplotypes not present in the M-1m sample but detected in the infant at 1 month (I-1m; red) or the mother at 11 months after delivery (M-11m; light blue). (B) Haplotypes forming clade III in figure 2_B_, following the same color scheme described above. Haplotypes are numbered with the prefix “h.” Area of circles denotes haplotype frequency in the M-1m, M-11m, and I-1m samples combined; the smallest circles represent singletons and the large central circles the likely ancestors from which other haplotypes derive. Unmodified lines connecting haplotypes indicate single mutational steps, and tick marks on the lines indicate additional steps. Note that most derived haplotypes differ from the ancestor by a single mutational step.

Similar articles

Cited by

References

    1. Adlerberth I, et al. Reduced enterobacterial and increased staphylococcal colonization of the infantile bowel: an effect of hygienic lifestyle? Pediatr Res. 2006;59:96–101. - PubMed
    1. Bateman A, et al. The Pfam protein families database. Nucleic Acids Res. 2004;32:D138–D141. - PMC - PubMed
    1. Bernhard AE, Field KG. Identification of nonpoint sources of fecal pollution in coastal waters by using host-specific 16S ribosomal DNA genetic markers from fecal anaerobes. Appl Environ Microbiol. 2000;66:1587–1594. - PMC - PubMed
    1. Besemer J, Lomsadze A, Borodovsky M. GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Res. 2001;29:2607–2618. - PMC - PubMed
    1. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000;17:540–552. - PubMed

LinkOut - more resources