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Early Introduction of Plant Polysaccharides Drives the Establishment of Rabbit Gut Bacterial Ecosystems and the Acquisition of Microbial Functions

In mammals, the introduction of solid food is pivotal for the establishment of the gut microbiota. However, the effects of the first food consumed on long-term microbiota trajectory and host response are still largely unknown. This study aimed to investigate the influences of (i) the timing of first...

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Autores principales: Paës, Charlotte, Gidenne, Thierry, Bébin, Karine, Duperray, Joël, Gohier, Charly, Guené-Grand, Emeline, Rebours, Gwénaël, Barilly, Céline, Gabinaud, Béatrice, Cauquil, Laurent, Castinel, Adrien, Pascal, Géraldine, Darbot, Vincent, Aymard, Patrick, Debrusse, Anne-Marie, Beaumont, Martin, Combes, Sylvie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9239267/
https://www.ncbi.nlm.nih.gov/pubmed/35674393
http://dx.doi.org/10.1128/msystems.00243-22
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author Paës, Charlotte
Gidenne, Thierry
Bébin, Karine
Duperray, Joël
Gohier, Charly
Guené-Grand, Emeline
Rebours, Gwénaël
Barilly, Céline
Gabinaud, Béatrice
Cauquil, Laurent
Castinel, Adrien
Pascal, Géraldine
Darbot, Vincent
Aymard, Patrick
Debrusse, Anne-Marie
Beaumont, Martin
Combes, Sylvie
author_facet Paës, Charlotte
Gidenne, Thierry
Bébin, Karine
Duperray, Joël
Gohier, Charly
Guené-Grand, Emeline
Rebours, Gwénaël
Barilly, Céline
Gabinaud, Béatrice
Cauquil, Laurent
Castinel, Adrien
Pascal, Géraldine
Darbot, Vincent
Aymard, Patrick
Debrusse, Anne-Marie
Beaumont, Martin
Combes, Sylvie
author_sort Paës, Charlotte
collection PubMed
description In mammals, the introduction of solid food is pivotal for the establishment of the gut microbiota. However, the effects of the first food consumed on long-term microbiota trajectory and host response are still largely unknown. This study aimed to investigate the influences of (i) the timing of first solid food ingestion and (ii) the consumption of plant polysaccharides on bacterial community dynamics and host physiology using a rabbit model. To modulate the first exposure to solid nutrients, solid food was provided to suckling rabbits from two different time points (3 or 15 days of age). In parallel, food type was modulated with the provision of diets differing in carbohydrate content throughout life: the food either was formulated with a high proportion of rapidly fermentable fibers (RFF) or was starch-enriched. We found that access to solid food as of 3 days of age accelerated the gut microbiota maturation. Our data revealed differential effects according to the digestive segment: precocious solid food ingestion influenced to a greater extent the development of bacterial communities of the appendix vermiformis, whereas life course polysaccharides ingestion had marked effects on the cecal microbiota. Greater ingestion of RFF was assumed to promote pectin degradation as revealed by metabolomics analysis. However, transcriptomic and phenotypic host responses remained moderately affected by experimental treatments, suggesting little outcomes of the observed microbiome modulations on healthy subjects. In conclusion, our work highlighted the timing of solid food introduction and plant polysaccharides ingestion as two different tools to modulate microbiota implantation and functionality. IMPORTANCE Our study was designed to gain a better understanding of how different feeding patterns affect the dynamics of gut microbiomes and microbe–host interactions. This research showed that the timing of solid food introduction is a key component of the gut microbiota shaping in early developmental stages, though with lower impact on settled gut microbiota profiles in older individuals. This study also provided in-depth analysis of dietary polysaccharide effects on intestinal microbiota. The type of plant polysaccharides reaching the gut through the lifetime was described as an important modulator of the cecal microbiome and its activity. These findings will contribute to better define the interventions that can be employed for modulating the ecological succession of young mammal gut microbiota.
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spelling pubmed-92392672022-06-29 Early Introduction of Plant Polysaccharides Drives the Establishment of Rabbit Gut Bacterial Ecosystems and the Acquisition of Microbial Functions Paës, Charlotte Gidenne, Thierry Bébin, Karine Duperray, Joël Gohier, Charly Guené-Grand, Emeline Rebours, Gwénaël Barilly, Céline Gabinaud, Béatrice Cauquil, Laurent Castinel, Adrien Pascal, Géraldine Darbot, Vincent Aymard, Patrick Debrusse, Anne-Marie Beaumont, Martin Combes, Sylvie mSystems Research Article In mammals, the introduction of solid food is pivotal for the establishment of the gut microbiota. However, the effects of the first food consumed on long-term microbiota trajectory and host response are still largely unknown. This study aimed to investigate the influences of (i) the timing of first solid food ingestion and (ii) the consumption of plant polysaccharides on bacterial community dynamics and host physiology using a rabbit model. To modulate the first exposure to solid nutrients, solid food was provided to suckling rabbits from two different time points (3 or 15 days of age). In parallel, food type was modulated with the provision of diets differing in carbohydrate content throughout life: the food either was formulated with a high proportion of rapidly fermentable fibers (RFF) or was starch-enriched. We found that access to solid food as of 3 days of age accelerated the gut microbiota maturation. Our data revealed differential effects according to the digestive segment: precocious solid food ingestion influenced to a greater extent the development of bacterial communities of the appendix vermiformis, whereas life course polysaccharides ingestion had marked effects on the cecal microbiota. Greater ingestion of RFF was assumed to promote pectin degradation as revealed by metabolomics analysis. However, transcriptomic and phenotypic host responses remained moderately affected by experimental treatments, suggesting little outcomes of the observed microbiome modulations on healthy subjects. In conclusion, our work highlighted the timing of solid food introduction and plant polysaccharides ingestion as two different tools to modulate microbiota implantation and functionality. IMPORTANCE Our study was designed to gain a better understanding of how different feeding patterns affect the dynamics of gut microbiomes and microbe–host interactions. This research showed that the timing of solid food introduction is a key component of the gut microbiota shaping in early developmental stages, though with lower impact on settled gut microbiota profiles in older individuals. This study also provided in-depth analysis of dietary polysaccharide effects on intestinal microbiota. The type of plant polysaccharides reaching the gut through the lifetime was described as an important modulator of the cecal microbiome and its activity. These findings will contribute to better define the interventions that can be employed for modulating the ecological succession of young mammal gut microbiota. American Society for Microbiology 2022-06-08 /pmc/articles/PMC9239267/ /pubmed/35674393 http://dx.doi.org/10.1128/msystems.00243-22 Text en Copyright © 2022 Paës et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Paës, Charlotte
Gidenne, Thierry
Bébin, Karine
Duperray, Joël
Gohier, Charly
Guené-Grand, Emeline
Rebours, Gwénaël
Barilly, Céline
Gabinaud, Béatrice
Cauquil, Laurent
Castinel, Adrien
Pascal, Géraldine
Darbot, Vincent
Aymard, Patrick
Debrusse, Anne-Marie
Beaumont, Martin
Combes, Sylvie
Early Introduction of Plant Polysaccharides Drives the Establishment of Rabbit Gut Bacterial Ecosystems and the Acquisition of Microbial Functions
title Early Introduction of Plant Polysaccharides Drives the Establishment of Rabbit Gut Bacterial Ecosystems and the Acquisition of Microbial Functions
title_full Early Introduction of Plant Polysaccharides Drives the Establishment of Rabbit Gut Bacterial Ecosystems and the Acquisition of Microbial Functions
title_fullStr Early Introduction of Plant Polysaccharides Drives the Establishment of Rabbit Gut Bacterial Ecosystems and the Acquisition of Microbial Functions
title_full_unstemmed Early Introduction of Plant Polysaccharides Drives the Establishment of Rabbit Gut Bacterial Ecosystems and the Acquisition of Microbial Functions
title_short Early Introduction of Plant Polysaccharides Drives the Establishment of Rabbit Gut Bacterial Ecosystems and the Acquisition of Microbial Functions
title_sort early introduction of plant polysaccharides drives the establishment of rabbit gut bacterial ecosystems and the acquisition of microbial functions
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9239267/
https://www.ncbi.nlm.nih.gov/pubmed/35674393
http://dx.doi.org/10.1128/msystems.00243-22
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