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The diet rapidly and differentially affects the gut microbiota and host lipid mediators in a healthy population

BACKGROUND: Bioactive lipids produced by human cells or by the gut microbiota might play an important role in health and disease. Dietary intakes are key determinants of the gut microbiota, its production of short-chain (SCFAs) and branched-chain fatty acids (BCFAs), and of the host endocannabinoido...

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Autores principales: Bourdeau-Julien, Isabelle, Castonguay-Paradis, Sophie, Rochefort, Gabrielle, Perron, Julie, Lamarche, Benoît, Flamand, Nicolas, Di Marzo, Vincenzo, Veilleux, Alain, Raymond, Frédéric
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9921707/
https://www.ncbi.nlm.nih.gov/pubmed/36774515
http://dx.doi.org/10.1186/s40168-023-01469-2
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author Bourdeau-Julien, Isabelle
Castonguay-Paradis, Sophie
Rochefort, Gabrielle
Perron, Julie
Lamarche, Benoît
Flamand, Nicolas
Di Marzo, Vincenzo
Veilleux, Alain
Raymond, Frédéric
author_facet Bourdeau-Julien, Isabelle
Castonguay-Paradis, Sophie
Rochefort, Gabrielle
Perron, Julie
Lamarche, Benoît
Flamand, Nicolas
Di Marzo, Vincenzo
Veilleux, Alain
Raymond, Frédéric
author_sort Bourdeau-Julien, Isabelle
collection PubMed
description BACKGROUND: Bioactive lipids produced by human cells or by the gut microbiota might play an important role in health and disease. Dietary intakes are key determinants of the gut microbiota, its production of short-chain (SCFAs) and branched-chain fatty acids (BCFAs), and of the host endocannabinoidome signalling, which are all involved in metabolic diseases. This hypothesis-driven longitudinal fixed sequence nutritional study, realized in healthy participants, was designed to determine if a lead-in diet affects the host response to a short-term dietary intervention. Participants received a Mediterranean diet (MedDiet) for 3 days, a 13-day lead-in controlled diet reflecting the average Canadian dietary intake (CanDiet), and once again a MedDiet for 3 consecutive days. Fecal and blood samples were collected at the end of each dietary phase to evaluate alterations in gut microbiota composition and plasma levels of endocannabinoidome mediators, SCFAs, and BCFAs. RESULTS: We observed an immediate and reversible modulation of plasma endocannabinoidome mediators, BCFAs, and some SCFAs in response to both diets. BCFAs were more strongly reduced by the MedDiet when the latter was preceded by the lead-in CanDiet. The gut microbiota response was also immediate, but not all changes due to the CanDiet were reversible following a short dietary MedDiet intervention. Higher initial microbiome diversity was associated with reduced microbiota modulation after short-term dietary interventions. We also observed that BCFAs and 2-monoacylglycerols had many, but distinct, correlations with gut microbiota composition. Several taxa modulated by dietary intervention were previously associated to metabolic disorders, warranting the need to control for recent diet in observational association studies. CONCLUSIONS: Our results indicate that lipid mediators involved in the communication between the gut microbiota and host metabolism exhibit a rapid response to dietary changes, which is also the case for some, but not all, microbiome taxa. The lead-in diet influenced the gut microbiome and BCFA, but not the endocannabinoidome, response to the MedDiet. A higher initial microbiome diversity favored the stability of the gut microbiota in response to dietary changes. This study highlights the importance of considering the previous diet in studies relating the gut microbiome with lipid signals involved in host metabolism. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01469-2.
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spelling pubmed-99217072023-02-12 The diet rapidly and differentially affects the gut microbiota and host lipid mediators in a healthy population Bourdeau-Julien, Isabelle Castonguay-Paradis, Sophie Rochefort, Gabrielle Perron, Julie Lamarche, Benoît Flamand, Nicolas Di Marzo, Vincenzo Veilleux, Alain Raymond, Frédéric Microbiome Research BACKGROUND: Bioactive lipids produced by human cells or by the gut microbiota might play an important role in health and disease. Dietary intakes are key determinants of the gut microbiota, its production of short-chain (SCFAs) and branched-chain fatty acids (BCFAs), and of the host endocannabinoidome signalling, which are all involved in metabolic diseases. This hypothesis-driven longitudinal fixed sequence nutritional study, realized in healthy participants, was designed to determine if a lead-in diet affects the host response to a short-term dietary intervention. Participants received a Mediterranean diet (MedDiet) for 3 days, a 13-day lead-in controlled diet reflecting the average Canadian dietary intake (CanDiet), and once again a MedDiet for 3 consecutive days. Fecal and blood samples were collected at the end of each dietary phase to evaluate alterations in gut microbiota composition and plasma levels of endocannabinoidome mediators, SCFAs, and BCFAs. RESULTS: We observed an immediate and reversible modulation of plasma endocannabinoidome mediators, BCFAs, and some SCFAs in response to both diets. BCFAs were more strongly reduced by the MedDiet when the latter was preceded by the lead-in CanDiet. The gut microbiota response was also immediate, but not all changes due to the CanDiet were reversible following a short dietary MedDiet intervention. Higher initial microbiome diversity was associated with reduced microbiota modulation after short-term dietary interventions. We also observed that BCFAs and 2-monoacylglycerols had many, but distinct, correlations with gut microbiota composition. Several taxa modulated by dietary intervention were previously associated to metabolic disorders, warranting the need to control for recent diet in observational association studies. CONCLUSIONS: Our results indicate that lipid mediators involved in the communication between the gut microbiota and host metabolism exhibit a rapid response to dietary changes, which is also the case for some, but not all, microbiome taxa. The lead-in diet influenced the gut microbiome and BCFA, but not the endocannabinoidome, response to the MedDiet. A higher initial microbiome diversity favored the stability of the gut microbiota in response to dietary changes. This study highlights the importance of considering the previous diet in studies relating the gut microbiome with lipid signals involved in host metabolism. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01469-2. BioMed Central 2023-02-11 /pmc/articles/PMC9921707/ /pubmed/36774515 http://dx.doi.org/10.1186/s40168-023-01469-2 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Bourdeau-Julien, Isabelle
Castonguay-Paradis, Sophie
Rochefort, Gabrielle
Perron, Julie
Lamarche, Benoît
Flamand, Nicolas
Di Marzo, Vincenzo
Veilleux, Alain
Raymond, Frédéric
The diet rapidly and differentially affects the gut microbiota and host lipid mediators in a healthy population
title The diet rapidly and differentially affects the gut microbiota and host lipid mediators in a healthy population
title_full The diet rapidly and differentially affects the gut microbiota and host lipid mediators in a healthy population
title_fullStr The diet rapidly and differentially affects the gut microbiota and host lipid mediators in a healthy population
title_full_unstemmed The diet rapidly and differentially affects the gut microbiota and host lipid mediators in a healthy population
title_short The diet rapidly and differentially affects the gut microbiota and host lipid mediators in a healthy population
title_sort diet rapidly and differentially affects the gut microbiota and host lipid mediators in a healthy population
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9921707/
https://www.ncbi.nlm.nih.gov/pubmed/36774515
http://dx.doi.org/10.1186/s40168-023-01469-2
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