Maternal emulsifier consumption alters the offspring early-life microbiota and goblet cell function leading to long-lasting diseases susceptibility

Abstract Early-life acquisition of microbiota and, consequently, immune system development, both lastingly impacts health. Accordingly, we hypothesized that disturbing the microbiota of lactating mothers via consumption of dietary emulsifiers might alter the microbiota, and perhaps the immune system...

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Main Authors: Clara Delaroque, Héloïse Rytter, Erica Bonazzi, Marine Huillet, Sandrine Ellero-Simatos, Eva Chatonnat, Fuhua Hao, Andrew Patterson, Benoit Chassaing
Format: Article
Language:English
Published: Nature Portfolio 2025-07-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-62397-3
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author Clara Delaroque
Héloïse Rytter
Erica Bonazzi
Marine Huillet
Sandrine Ellero-Simatos
Eva Chatonnat
Fuhua Hao
Andrew Patterson
Benoit Chassaing
author_facet Clara Delaroque
Héloïse Rytter
Erica Bonazzi
Marine Huillet
Sandrine Ellero-Simatos
Eva Chatonnat
Fuhua Hao
Andrew Patterson
Benoit Chassaing
author_sort Clara Delaroque
collection DOAJ
description Abstract Early-life acquisition of microbiota and, consequently, immune system development, both lastingly impacts health. Accordingly, we hypothesized that disturbing the microbiota of lactating mothers via consumption of dietary emulsifiers might alter the microbiota, and perhaps the immune system, of their offspring, thereby increasing susceptibility to microbiota-mediated diseases, including colitis and metabolic syndrome. Here we report that, in mice, maternal consumption of carboxymethylcellulose and polysorbate-80 resulted in transient alterations in offspring microbiotas that were necessary and sufficient to increase proneness to colitis and metabolic syndrome in young adulthood. Offspring microbiome alterations induced by maternal emulsifier consumption resulted in elevated levels of pro-inflammatory flagellin, bacterial encroachment, and premature closure of goblet cell associated antigens passages (GAPs). The latter event was linked to phenotypic outcome in that pharmacologically preventing GAP closure eliminated the detrimental of maternal emulsifier consumption. Collectively, these results illustrate the potential of dietary emulsifiers to drive transgenerational microbiota alteration and, consequently, hastened immune development that increases susceptibility to inflammatory diseases.
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institution Kabale University
issn 2041-1723
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publishDate 2025-07-01
publisher Nature Portfolio
record_format Article
series Nature Communications
spelling doaj-art-1113fd9b9df743898e9c6a20b0b6c5f22025-08-20T04:03:01ZengNature PortfolioNature Communications2041-17232025-07-0116111510.1038/s41467-025-62397-3Maternal emulsifier consumption alters the offspring early-life microbiota and goblet cell function leading to long-lasting diseases susceptibilityClara Delaroque0Héloïse Rytter1Erica Bonazzi2Marine Huillet3Sandrine Ellero-Simatos4Eva Chatonnat5Fuhua Hao6Andrew Patterson7Benoit Chassaing8Microbiome-Host Interactions, Institut Pasteur, Université Paris Cité, INSERM U1306Microbiome-Host Interactions, Institut Pasteur, Université Paris Cité, INSERM U1306Microbiome-Host Interactions, Institut Pasteur, Université Paris Cité, INSERM U1306Toxalim (Research Centre in Food Toxicology), INRAE, ENVT, INP-Purpan, UPS, Université de ToulouseToxalim (Research Centre in Food Toxicology), INRAE, ENVT, INP-Purpan, UPS, Université de ToulouseMicrobiome-Host Interactions, Institut Pasteur, Université Paris Cité, INSERM U1306Department of Veterinary and Biomedical Sciences, Center for Molecular Toxicology and Carcinogenesis, Pennsylvania State UniversityDepartment of Veterinary and Biomedical Sciences, Center for Molecular Toxicology and Carcinogenesis, Pennsylvania State UniversityMicrobiome-Host Interactions, Institut Pasteur, Université Paris Cité, INSERM U1306Abstract Early-life acquisition of microbiota and, consequently, immune system development, both lastingly impacts health. Accordingly, we hypothesized that disturbing the microbiota of lactating mothers via consumption of dietary emulsifiers might alter the microbiota, and perhaps the immune system, of their offspring, thereby increasing susceptibility to microbiota-mediated diseases, including colitis and metabolic syndrome. Here we report that, in mice, maternal consumption of carboxymethylcellulose and polysorbate-80 resulted in transient alterations in offspring microbiotas that were necessary and sufficient to increase proneness to colitis and metabolic syndrome in young adulthood. Offspring microbiome alterations induced by maternal emulsifier consumption resulted in elevated levels of pro-inflammatory flagellin, bacterial encroachment, and premature closure of goblet cell associated antigens passages (GAPs). The latter event was linked to phenotypic outcome in that pharmacologically preventing GAP closure eliminated the detrimental of maternal emulsifier consumption. Collectively, these results illustrate the potential of dietary emulsifiers to drive transgenerational microbiota alteration and, consequently, hastened immune development that increases susceptibility to inflammatory diseases.https://doi.org/10.1038/s41467-025-62397-3
spellingShingle Clara Delaroque
Héloïse Rytter
Erica Bonazzi
Marine Huillet
Sandrine Ellero-Simatos
Eva Chatonnat
Fuhua Hao
Andrew Patterson
Benoit Chassaing
Maternal emulsifier consumption alters the offspring early-life microbiota and goblet cell function leading to long-lasting diseases susceptibility
Nature Communications
title Maternal emulsifier consumption alters the offspring early-life microbiota and goblet cell function leading to long-lasting diseases susceptibility
title_full Maternal emulsifier consumption alters the offspring early-life microbiota and goblet cell function leading to long-lasting diseases susceptibility
title_fullStr Maternal emulsifier consumption alters the offspring early-life microbiota and goblet cell function leading to long-lasting diseases susceptibility
title_full_unstemmed Maternal emulsifier consumption alters the offspring early-life microbiota and goblet cell function leading to long-lasting diseases susceptibility
title_short Maternal emulsifier consumption alters the offspring early-life microbiota and goblet cell function leading to long-lasting diseases susceptibility
title_sort maternal emulsifier consumption alters the offspring early life microbiota and goblet cell function leading to long lasting diseases susceptibility
url https://doi.org/10.1038/s41467-025-62397-3
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