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PLoS Genet. 2014 Jun 5;10(6):e1004406. doi: 10.1371/journal.pgen.1004406. eCollection 2014 Jun.

Microbial succession in the gut: directional trends of taxonomic and functional change in a birth cohort of Spanish infants.

Author information

1
Unidad Mixta de Investigación en Genómica y Salud, Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunitat Valenciana (FISABIO)-Salud Pública/Institut Cavanilles de Biodiversitat i Biologia Evolutiva (Universitat de València), València, Spain.
2
Centro de Biología Molecular "Severo Ochoa" (CSIC-Universidad Autónoma de Madrid), Madrid, Spain.
3
Unidad Mixta de Investigación en Genómica y Salud, Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunitat Valenciana (FISABIO)-Salud Pública/Institut Cavanilles de Biodiversitat i Biologia Evolutiva (Universitat de València), València, Spain; CIBER en Epidemiología y Salud Pública (CIBERESP), Spain.
4
Unidad Mixta de Investigación en Genómica y Salud, Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunitat Valenciana (FISABIO)-Salud Pública/Institut Cavanilles de Biodiversitat i Biologia Evolutiva (Universitat de València), València, Spain; School of Natural Sciences, University of California Merced, Merced, California, United States of America.

Abstract

In spite of its major impact on life-long health, the process of microbial succession in the gut of infants remains poorly understood. Here, we analyze the patterns of taxonomic and functional change in the gut microbiota during the first year of life for a birth cohort of 13 infants. We detect that individual instances of gut colonization vary in the temporal dynamics of microbiota richness, diversity, and composition at both functional and taxonomic levels. Nevertheless, trends discernible in a majority of infants indicate that gut colonization occurs in two distinct phases of succession, separated by the introduction of solid foods to the diet. This change in resource availability causes a sharp decrease in the taxonomic richness of the microbiota due to the loss of rare taxa (p = 2.06e-9), although the number of core genera shared by all infants increases substantially. Moreover, although the gut microbial succession is not strictly deterministic, we detect an overarching directionality of change through time towards the taxonomic and functional composition of the maternal microbiota. Succession is however not complete by the one year mark, as significant differences remain between one-year-olds and their mothers in terms of taxonomic (p = 0.009) and functional (p = 0.004) microbiota composition, and in taxonomic richness (p = 2.76e-37) and diversity (p = 0.016). Our results also indicate that the taxonomic composition of the microbiota shapes its functional capacities. Therefore, the observed inter-individual variability in taxonomic composition during succession is not fully compensated by functional equivalence among bacterial genera and may have important physiological consequences. Finally, network analyses suggest that positive interactions among core genera during community assembly contribute to ensure their permanence within the gut, and highlight an expansion of complexity in the interactions network as the core of taxa shared by all infants grows following the introduction of solid foods.

PMID:
24901968
PMCID:
PMC4046925
DOI:
10.1371/journal.pgen.1004406
[Indexed for MEDLINE]
Free PMC Article

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