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

Diet Endocannabinoid Endocannabinoidome Gut microbiota Mediterranean Metabolomics Microbiome diversity Polyunsaturated fatty acids Short-chain fatty acids Western diet

Journal

Microbiome
ISSN: 2049-2618
Titre abrégé: Microbiome
Pays: England
ID NLM: 101615147

Informations de publication

Date de publication:
11 02 2023
Historique:
received: 21 03 2022
accepted: 16 01 2023
entrez: 11 2 2023
pubmed: 12 2 2023
medline: 15 2 2023
Statut: epublish

Résumé

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. 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. 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. Video Abstract.

Sections du résumé

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. Video Abstract.

Identifiants

pubmed: 36774515
doi: 10.1186/s40168-023-01469-2
pii: 10.1186/s40168-023-01469-2
pmc: PMC9921707
doi:

Substances chimiques

Fatty Acids 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

26

Subventions

Organisme : CIHR
Pays : Canada

Informations de copyright

© 2023. The Author(s).

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Auteurs

Isabelle Bourdeau-Julien (I)

Centre Nutrition, santé et société (NUTRISS), Institut sur la nutrition et les aliments fonctionnels (INAF), École de nutrition, Université Laval, 2440, boulevard Hochelaga, Québec, G1V 0A6, Canada.
Canada Excellence Research Chair in the Microbiome-Endocannabinoidome Axis in Metabolic Health, Quebec, Canada.

Sophie Castonguay-Paradis (S)

Centre Nutrition, santé et société (NUTRISS), Institut sur la nutrition et les aliments fonctionnels (INAF), École de nutrition, Université Laval, 2440, boulevard Hochelaga, Québec, G1V 0A6, Canada.
Canada Excellence Research Chair in the Microbiome-Endocannabinoidome Axis in Metabolic Health, Quebec, Canada.

Gabrielle Rochefort (G)

Centre Nutrition, santé et société (NUTRISS), Institut sur la nutrition et les aliments fonctionnels (INAF), École de nutrition, Université Laval, 2440, boulevard Hochelaga, Québec, G1V 0A6, Canada.
Canada Excellence Research Chair in the Microbiome-Endocannabinoidome Axis in Metabolic Health, Quebec, Canada.

Julie Perron (J)

Centre Nutrition, santé et société (NUTRISS), Institut sur la nutrition et les aliments fonctionnels (INAF), École de nutrition, Université Laval, 2440, boulevard Hochelaga, Québec, G1V 0A6, Canada.
Canada Excellence Research Chair in the Microbiome-Endocannabinoidome Axis in Metabolic Health, Quebec, Canada.

Benoît Lamarche (B)

Centre Nutrition, santé et société (NUTRISS), Institut sur la nutrition et les aliments fonctionnels (INAF), École de nutrition, Université Laval, 2440, boulevard Hochelaga, Québec, G1V 0A6, Canada.

Nicolas Flamand (N)

Canada Excellence Research Chair in the Microbiome-Endocannabinoidome Axis in Metabolic Health, Quebec, Canada.
Centre de recherche de l'Institut de cardiologie et de pneumologie de Québec, Faculté de médecine, Département de médecine, Université Laval, Québec, Canada.

Vincenzo Di Marzo (V)

Centre Nutrition, santé et société (NUTRISS), Institut sur la nutrition et les aliments fonctionnels (INAF), École de nutrition, Université Laval, 2440, boulevard Hochelaga, Québec, G1V 0A6, Canada.
Canada Excellence Research Chair in the Microbiome-Endocannabinoidome Axis in Metabolic Health, Quebec, Canada.
Centre de recherche de l'Institut de cardiologie et de pneumologie de Québec, Faculté de médecine, Département de médecine, Université Laval, Québec, Canada.
Unité Mixte Internationale en Recherche Chimique et Biomoléculaire sur le Microbiome et son Impact Sur la Santé Métabolique et la Nutrition (UMI-MicroMeNu), Université Laval and Consiglio Nazionale delle Ricerche, Istituto di Chimica Biomolecolare, Via Campi Flegrei 34, 80078, Pozzuoli, (NA), Italy.

Alain Veilleux (A)

Centre Nutrition, santé et société (NUTRISS), Institut sur la nutrition et les aliments fonctionnels (INAF), École de nutrition, Université Laval, 2440, boulevard Hochelaga, Québec, G1V 0A6, Canada.
Canada Excellence Research Chair in the Microbiome-Endocannabinoidome Axis in Metabolic Health, Quebec, Canada.

Frédéric Raymond (F)

Centre Nutrition, santé et société (NUTRISS), Institut sur la nutrition et les aliments fonctionnels (INAF), École de nutrition, Université Laval, 2440, boulevard Hochelaga, Québec, G1V 0A6, Canada. frederic.raymond@fsaa.ulaval.ca.
Canada Excellence Research Chair in the Microbiome-Endocannabinoidome Axis in Metabolic Health, Quebec, Canada. frederic.raymond@fsaa.ulaval.ca.

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