Developmental Stage, Solid Food Introduction, and Suckling Cessation Differentially Influence the Comaturation of the Gut Microbiota and Intestinal Epithelium in Rabbits.


Journal

The Journal of nutrition
ISSN: 1541-6100
Titre abrégé: J Nutr
Pays: United States
ID NLM: 0404243

Informations de publication

Date de publication:
03 03 2022
Historique:
received: 23 08 2021
revised: 16 09 2021
accepted: 01 12 2021
pubmed: 8 12 2021
medline: 27 4 2022
entrez: 7 12 2021
Statut: ppublish

Résumé

In mammals, the establishment around weaning of a symbiotic relationship between the gut microbiota and its host determines long-term health. The aim of this study was to identify the factors driving the comaturation of the gut microbiota and intestinal epithelium at the suckling-to-weaning transition. We hypothesized that the developmental stage, solid food ingestion, and suckling cessation contribute to this process. From birth to day 18, Hyplus rabbits were exclusively suckling. From day 18 to day 25, rabbits were 1) exclusively suckling; 2) suckling and ingesting solid food; or 3) exclusively ingesting solid food. The microbiota (16S amplicon sequencing), metabolome (nuclear magnetic resonance), and epithelial gene expression (high-throughput qPCR) were analyzed in the cecum at days 18 and 25. The microbiota structure and metabolic activity were modified with age when rabbits remained exclusively suckling. The epithelial gene expression of nutrient transporters, proliferation markers, and innate immune factors were also regulated with age (e.g., 1.5-fold decrease of TLR5). Solid food ingestion by suckling rabbits had a major effect on the gut microbiota by increasing its α diversity, remodeling its structure (e.g., 6.3-fold increase of Ruminococcaceae), and metabolic activity (e.g., 4.6-fold increase of butyrate). Solid food introduction also regulated the gene expression of nutrient transporters, differentiation markers, and innate immune factors in the epithelium (e.g., 3-fold increase of nitric oxide synthase). Suckling cessation had no effect on the microbiota, while it regulated the expression of genes involved in epithelial differentiation and immunoglobulin transport (e.g., 2.5-increase of the polymeric immunoglobulin receptor). In rabbits, the maturation of the microbiota at the suckling-to-weaning transition is driven by the introduction of solid food and, to a lesser extent, by the developmental stage. In contrast, the maturation of the intestinal epithelium at the suckling-to-weaning transition is under the influence of the developmental stage, solid food introduction, and suckling cessation.

Sections du résumé

BACKGROUND
In mammals, the establishment around weaning of a symbiotic relationship between the gut microbiota and its host determines long-term health.
OBJECTIVES
The aim of this study was to identify the factors driving the comaturation of the gut microbiota and intestinal epithelium at the suckling-to-weaning transition. We hypothesized that the developmental stage, solid food ingestion, and suckling cessation contribute to this process.
METHODS
From birth to day 18, Hyplus rabbits were exclusively suckling. From day 18 to day 25, rabbits were 1) exclusively suckling; 2) suckling and ingesting solid food; or 3) exclusively ingesting solid food. The microbiota (16S amplicon sequencing), metabolome (nuclear magnetic resonance), and epithelial gene expression (high-throughput qPCR) were analyzed in the cecum at days 18 and 25.
RESULTS
The microbiota structure and metabolic activity were modified with age when rabbits remained exclusively suckling. The epithelial gene expression of nutrient transporters, proliferation markers, and innate immune factors were also regulated with age (e.g., 1.5-fold decrease of TLR5). Solid food ingestion by suckling rabbits had a major effect on the gut microbiota by increasing its α diversity, remodeling its structure (e.g., 6.3-fold increase of Ruminococcaceae), and metabolic activity (e.g., 4.6-fold increase of butyrate). Solid food introduction also regulated the gene expression of nutrient transporters, differentiation markers, and innate immune factors in the epithelium (e.g., 3-fold increase of nitric oxide synthase). Suckling cessation had no effect on the microbiota, while it regulated the expression of genes involved in epithelial differentiation and immunoglobulin transport (e.g., 2.5-increase of the polymeric immunoglobulin receptor).
CONCLUSIONS
In rabbits, the maturation of the microbiota at the suckling-to-weaning transition is driven by the introduction of solid food and, to a lesser extent, by the developmental stage. In contrast, the maturation of the intestinal epithelium at the suckling-to-weaning transition is under the influence of the developmental stage, solid food introduction, and suckling cessation.

Identifiants

pubmed: 34875085
pii: S0022-3166(22)00578-8
doi: 10.1093/jn/nxab411
pmc: PMC8891179
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

723-736

Informations de copyright

© The Author(s) 2021. Published by Oxford University Press on behalf of the American Society for Nutrition.

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Auteurs

Martin Beaumont (M)

GenPhySE, Université de Toulouse, INRAE, ENVT, F-31326, Castanet-Tolosan, France.

Eloïse Mussard (E)

GenPhySE, Université de Toulouse, INRAE, ENVT, F-31326, Castanet-Tolosan, France.

Céline Barilly (C)

GenPhySE, Université de Toulouse, INRAE, ENVT, F-31326, Castanet-Tolosan, France.

Corinne Lencina (C)

GenPhySE, Université de Toulouse, INRAE, ENVT, F-31326, Castanet-Tolosan, France.

Laure Gress (L)

GenPhySE, Université de Toulouse, INRAE, ENVT, F-31326, Castanet-Tolosan, France.

Louise Painteaux (L)

GenPhySE, Université de Toulouse, INRAE, ENVT, F-31326, Castanet-Tolosan, France.

Béatrice Gabinaud (B)

GenPhySE, Université de Toulouse, INRAE, ENVT, F-31326, Castanet-Tolosan, France.

Laurent Cauquil (L)

GenPhySE, Université de Toulouse, INRAE, ENVT, F-31326, Castanet-Tolosan, France.

Patrick Aymard (P)

GenPhySE, Université de Toulouse, INRAE, ENVT, F-31326, Castanet-Tolosan, France.

Cécile Canlet (C)

Toxalim (Research Centre in Food Toxicology), Université de Toulouse, INRAE, ENVT, INP-Purpan, UPS, Toulouse, France.

Charlotte Paës (C)

GenPhySE, Université de Toulouse, INRAE, ENVT, F-31326, Castanet-Tolosan, France.

Christelle Knudsen (C)

GenPhySE, Université de Toulouse, INRAE, ENVT, F-31326, Castanet-Tolosan, France.

Sylvie Combes (S)

GenPhySE, Université de Toulouse, INRAE, ENVT, F-31326, Castanet-Tolosan, France.

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