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

Yvonne Vallès,Alejandro Artacho,Juan José Abellán,Alberto Pascual-García,Maria Loreto Ferrús,M Pilar Francino,María José Gosalbes,David S Guttman

doi:10.1371/journal.pgen.1004406

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.

Highlights

The gastrointestinal tract (GIT) is a complex ecosystem where many factors, biotic and abiotic, play essential roles in reaching and maintaining a homeostatic equilibrium
Many studies have concentrated their efforts in the detection of a taxonomic core that would be shared by all individuals [6,7,8,9,10]
Arumugam et al [11] have stipulated that there are three universally distributed clusters of wellbalanced host-symbiont states named enterotypes, driven mainly by bacterial composition, and that every individual’s microbiota pertains to one of these enterotypes. The existence of such well-defined clusters of microbiota composition has been contested because their detection is highly dependent on the knowledge of the complex community of microbes that inhabits the human gut is constantly increasing, the successional process through which it develops during infancy remains poorly understood

Summary

Introduction

The gastrointestinal tract (GIT) is a complex ecosystem where many factors, biotic and abiotic, play essential roles in reaching and maintaining a homeostatic equilibrium. The gut is endowed with the most diverse and dense microbiota of the human body, which plays fundamental roles in gut maturation, angiogenesis, immune system modulation, digestion, and protection from pathogens [1,2] Given such important roles for health, the inter-individual variability of the human gut microbiota in adulthood and at any stage of development still defies our expectations. Many studies have concentrated their efforts in the detection of a taxonomic core that would be shared by all individuals [6,7,8,9,10] In that this search has been difficult, this view has recently evolved towards defining a few types of compositional profiles for the GIT microbiota. The existence of such well-defined clusters of microbiota composition has been contested because their detection is highly dependent on the

Author Summary

Findings

Materials and Methods