Western diet strongly influences gut microbiomes in nursing rat dams but translates modest long‐term consequences to offspring modulated by leptin supplementation during suckling

Abstract Early life conditions may influence the gut microbiome and contribute to health status in adulthood. We examined the impact of maternal obesity and/or obesogenic diet on the gut microbiome of mothers (at weaning) and their adult offspring, along with the effects of leptin supplementation du...

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Main Authors: Catalina A. Pomar, Tomeu Viver, Ana Valle, Juan F Gago, Pedro Castillo, Mariona Palou, Andreu Palou, Ramon Rossello‐Mora, Catalina Picó
Format: Article
Language:English
Published: Wiley 2024-01-01
Series:Food Frontiers
Subjects:
Online Access:https://doi.org/10.1002/fft2.322
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author Catalina A. Pomar
Tomeu Viver
Ana Valle
Juan F Gago
Pedro Castillo
Mariona Palou
Andreu Palou
Ramon Rossello‐Mora
Catalina Picó
author_facet Catalina A. Pomar
Tomeu Viver
Ana Valle
Juan F Gago
Pedro Castillo
Mariona Palou
Andreu Palou
Ramon Rossello‐Mora
Catalina Picó
author_sort Catalina A. Pomar
collection DOAJ
description Abstract Early life conditions may influence the gut microbiome and contribute to health status in adulthood. We examined the impact of maternal obesity and/or obesogenic diet on the gut microbiome of mothers (at weaning) and their adult offspring, along with the effects of leptin supplementation during suckling. Three groups of rats were studied: control (C) dams, fed with standard diet (SD); western diet (WD) dams, fed with WD (a high‐fat, high‐sucrose diet) before gestation and during gestation and lactation; and reversion (REV) dams, fed as WD‐dams but with SD during lactation. Offspring were supplemented throughout suckling with leptin/vehicle and weaned on an SD. WD‐dams showed lower microbial diversity and an altered microbiome compared to C‐ and REV‐dams, widely normalized by diet improvement during lactation. WD‐ and REV‐offspring (males) displayed lower microbiome diversity and greater dominance compared to C‐offspring. Taxonomic group differences (Proteobacteria phylum and Bacteroides, Parasutterella, and Phocea genera) were observed in WD‐ and REV‐offspring. WD‐offspring, but not REV‐offspring, had a greater abundance of the phylum Firmicutes and Lachnospiraceae family and a lower abundance of the family Tannerellaceae compared to C‐offspring. Leptin supplementation led to decreased abundance of the phylum Actinobacteria (family Eggerthellaceae and genera Enterorhabdus and Adlercreutzia (females)), and the genera Lachnospiraceae UCG‐008 group, Roseburia and Limosilactobacillus, and increased abundance of the genus Dellaglioa, compared to vehicle‐treated groups. Therefore, maternal consumption of an obesogenic diet during the perinatal period results in microbiome changes in dams, alleviated by dietary improvement during lactation. Maternal conditions and leptin supplementation during suckling modestly influenced the microbiome in adulthood, which might partially contribute to the adverse/beneficial effects, respectively, of these conditions on programmed metabolic health.
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spelling doaj.art-f0862c16e7d14893af8cd069eb19817e2024-01-10T05:26:21ZengWileyFood Frontiers2643-84292024-01-015110812910.1002/fft2.322Western diet strongly influences gut microbiomes in nursing rat dams but translates modest long‐term consequences to offspring modulated by leptin supplementation during sucklingCatalina A. Pomar0Tomeu Viver1Ana Valle2Juan F Gago3Pedro Castillo4Mariona Palou5Andreu Palou6Ramon Rossello‐Mora7Catalina Picó8Laboratory of Molecular Biology, Nutrition and Biotechnology (Nutrigenomics, Biomarkers and Risk Evaluation) University of the Balearic Islands Palma SpainMarine Microbiology Group, Department of Animal and Microbial Diversity IMEDEA (CSIC‐UIB) Esporles Balears SpainLaboratory of Molecular Biology, Nutrition and Biotechnology (Nutrigenomics, Biomarkers and Risk Evaluation) University of the Balearic Islands Palma SpainMarine Microbiology Group, Department of Animal and Microbial Diversity IMEDEA (CSIC‐UIB) Esporles Balears SpainLaboratory of Molecular Biology, Nutrition and Biotechnology (Nutrigenomics, Biomarkers and Risk Evaluation) University of the Balearic Islands Palma SpainLaboratory of Molecular Biology, Nutrition and Biotechnology (Nutrigenomics, Biomarkers and Risk Evaluation) University of the Balearic Islands Palma SpainLaboratory of Molecular Biology, Nutrition and Biotechnology (Nutrigenomics, Biomarkers and Risk Evaluation) University of the Balearic Islands Palma SpainMarine Microbiology Group, Department of Animal and Microbial Diversity IMEDEA (CSIC‐UIB) Esporles Balears SpainLaboratory of Molecular Biology, Nutrition and Biotechnology (Nutrigenomics, Biomarkers and Risk Evaluation) University of the Balearic Islands Palma SpainAbstract Early life conditions may influence the gut microbiome and contribute to health status in adulthood. We examined the impact of maternal obesity and/or obesogenic diet on the gut microbiome of mothers (at weaning) and their adult offspring, along with the effects of leptin supplementation during suckling. Three groups of rats were studied: control (C) dams, fed with standard diet (SD); western diet (WD) dams, fed with WD (a high‐fat, high‐sucrose diet) before gestation and during gestation and lactation; and reversion (REV) dams, fed as WD‐dams but with SD during lactation. Offspring were supplemented throughout suckling with leptin/vehicle and weaned on an SD. WD‐dams showed lower microbial diversity and an altered microbiome compared to C‐ and REV‐dams, widely normalized by diet improvement during lactation. WD‐ and REV‐offspring (males) displayed lower microbiome diversity and greater dominance compared to C‐offspring. Taxonomic group differences (Proteobacteria phylum and Bacteroides, Parasutterella, and Phocea genera) were observed in WD‐ and REV‐offspring. WD‐offspring, but not REV‐offspring, had a greater abundance of the phylum Firmicutes and Lachnospiraceae family and a lower abundance of the family Tannerellaceae compared to C‐offspring. Leptin supplementation led to decreased abundance of the phylum Actinobacteria (family Eggerthellaceae and genera Enterorhabdus and Adlercreutzia (females)), and the genera Lachnospiraceae UCG‐008 group, Roseburia and Limosilactobacillus, and increased abundance of the genus Dellaglioa, compared to vehicle‐treated groups. Therefore, maternal consumption of an obesogenic diet during the perinatal period results in microbiome changes in dams, alleviated by dietary improvement during lactation. Maternal conditions and leptin supplementation during suckling modestly influenced the microbiome in adulthood, which might partially contribute to the adverse/beneficial effects, respectively, of these conditions on programmed metabolic health.https://doi.org/10.1002/fft2.322leptinmaternal obesitymaternal overnutritionmetabolic programingmicrobiome
spellingShingle Catalina A. Pomar
Tomeu Viver
Ana Valle
Juan F Gago
Pedro Castillo
Mariona Palou
Andreu Palou
Ramon Rossello‐Mora
Catalina Picó
Western diet strongly influences gut microbiomes in nursing rat dams but translates modest long‐term consequences to offspring modulated by leptin supplementation during suckling
Food Frontiers
leptin
maternal obesity
maternal overnutrition
metabolic programing
microbiome
title Western diet strongly influences gut microbiomes in nursing rat dams but translates modest long‐term consequences to offspring modulated by leptin supplementation during suckling
title_full Western diet strongly influences gut microbiomes in nursing rat dams but translates modest long‐term consequences to offspring modulated by leptin supplementation during suckling
title_fullStr Western diet strongly influences gut microbiomes in nursing rat dams but translates modest long‐term consequences to offspring modulated by leptin supplementation during suckling
title_full_unstemmed Western diet strongly influences gut microbiomes in nursing rat dams but translates modest long‐term consequences to offspring modulated by leptin supplementation during suckling
title_short Western diet strongly influences gut microbiomes in nursing rat dams but translates modest long‐term consequences to offspring modulated by leptin supplementation during suckling
title_sort western diet strongly influences gut microbiomes in nursing rat dams but translates modest long term consequences to offspring modulated by leptin supplementation during suckling
topic leptin
maternal obesity
maternal overnutrition
metabolic programing
microbiome
url https://doi.org/10.1002/fft2.322
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