Cargando…

Microbial Succession in the Gut: Directional Trends of Taxonomic and Functional Change in a Birth Cohort of Spanish Infants

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Vallès, Yvonne, Artacho, Alejandro, Pascual-García, Alberto, Ferrús, Maria Loreto, Gosalbes, María José, Abellán, Juan José, Francino, M. Pilar
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4046925/
https://www.ncbi.nlm.nih.gov/pubmed/24901968
http://dx.doi.org/10.1371/journal.pgen.1004406
_version_ 1782480331090165760
author Vallès, Yvonne
Artacho, Alejandro
Pascual-García, Alberto
Ferrús, Maria Loreto
Gosalbes, María José
Abellán, Juan José
Francino, M. Pilar
author_facet Vallès, Yvonne
Artacho, Alejandro
Pascual-García, Alberto
Ferrús, Maria Loreto
Gosalbes, María José
Abellán, Juan José
Francino, M. Pilar
author_sort Vallès, Yvonne
collection PubMed
description 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.
format Online
Article
Text
id pubmed-4046925
institution National Center for Biotechnology Information
language English
publishDate 2014
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-40469252014-06-09 Microbial Succession in the Gut: Directional Trends of Taxonomic and Functional Change in a Birth Cohort of Spanish Infants Vallès, Yvonne Artacho, Alejandro Pascual-García, Alberto Ferrús, Maria Loreto Gosalbes, María José Abellán, Juan José Francino, M. Pilar PLoS Genet Research Article 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. Public Library of Science 2014-06-05 /pmc/articles/PMC4046925/ /pubmed/24901968 http://dx.doi.org/10.1371/journal.pgen.1004406 Text en © 2014 Vallès et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Vallès, Yvonne
Artacho, Alejandro
Pascual-García, Alberto
Ferrús, Maria Loreto
Gosalbes, María José
Abellán, Juan José
Francino, M. Pilar
Microbial Succession in the Gut: Directional Trends of Taxonomic and Functional Change in a Birth Cohort of Spanish Infants
title Microbial Succession in the Gut: Directional Trends of Taxonomic and Functional Change in a Birth Cohort of Spanish Infants
title_full Microbial Succession in the Gut: Directional Trends of Taxonomic and Functional Change in a Birth Cohort of Spanish Infants
title_fullStr Microbial Succession in the Gut: Directional Trends of Taxonomic and Functional Change in a Birth Cohort of Spanish Infants
title_full_unstemmed Microbial Succession in the Gut: Directional Trends of Taxonomic and Functional Change in a Birth Cohort of Spanish Infants
title_short Microbial Succession in the Gut: Directional Trends of Taxonomic and Functional Change in a Birth Cohort of Spanish Infants
title_sort microbial succession in the gut: directional trends of taxonomic and functional change in a birth cohort of spanish infants
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4046925/
https://www.ncbi.nlm.nih.gov/pubmed/24901968
http://dx.doi.org/10.1371/journal.pgen.1004406
work_keys_str_mv AT vallesyvonne microbialsuccessioninthegutdirectionaltrendsoftaxonomicandfunctionalchangeinabirthcohortofspanishinfants
AT artachoalejandro microbialsuccessioninthegutdirectionaltrendsoftaxonomicandfunctionalchangeinabirthcohortofspanishinfants
AT pascualgarciaalberto microbialsuccessioninthegutdirectionaltrendsoftaxonomicandfunctionalchangeinabirthcohortofspanishinfants
AT ferrusmarialoreto microbialsuccessioninthegutdirectionaltrendsoftaxonomicandfunctionalchangeinabirthcohortofspanishinfants
AT gosalbesmariajose microbialsuccessioninthegutdirectionaltrendsoftaxonomicandfunctionalchangeinabirthcohortofspanishinfants
AT abellanjuanjose microbialsuccessioninthegutdirectionaltrendsoftaxonomicandfunctionalchangeinabirthcohortofspanishinfants
AT francinompilar microbialsuccessioninthegutdirectionaltrendsoftaxonomicandfunctionalchangeinabirthcohortofspanishinfants