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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...
Autores principales: | , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Microbiology
2022
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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. |
format | Online Article Text |
id | pubmed-9239267 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
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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