Perinatal bisphenol A exposure impairs gut microbial colonization: Implications for offspring obesity and neurodevelopment

Exposure to plasticiser xenobiotics such as BPA has emerged as a significant health challenge due to globalised and industrial packaged food production. Toxicological approaches in animal models have revealed complex effects, using variable doses of BPA, on reproduction, development, obesity, immune...

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Main Authors: Ana López-Moreno, Alfonso Torres-Sánchez, Antonio Suárez, Alicia Ruiz-Rodríguez, Margarita Aguilera
Format: Article
Language:English
Published: Elsevier 2025-06-01
Series:Ecotoxicology and Environmental Safety
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Online Access:http://www.sciencedirect.com/science/article/pii/S0147651325006311
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author Ana López-Moreno
Alfonso Torres-Sánchez
Antonio Suárez
Alicia Ruiz-Rodríguez
Margarita Aguilera
author_facet Ana López-Moreno
Alfonso Torres-Sánchez
Antonio Suárez
Alicia Ruiz-Rodríguez
Margarita Aguilera
author_sort Ana López-Moreno
collection DOAJ
description Exposure to plasticiser xenobiotics such as BPA has emerged as a significant health challenge due to globalised and industrial packaged food production. Toxicological approaches in animal models have revealed complex effects, using variable doses of BPA, on reproduction, development, obesity, immune function, metabolic and systemic toxicity. Besides, gut microbiota has emerged as a key player in regulating the impact of xenobiotic exposure on host metabolism. The effect that BPA may exert on the gut microbiota and its consequences for the host's health remains unclear. Exposure to BPA during the perinatal period requires special attention and prevention approaches since it is a particularly vulnerable period and highly implicated in the metabolic health of childhood and adulthood. The aim of this study was to assess the effects of the BPA administration during the perinatal period on promoting obesity phenotypes, altering the composition of the gut microbiota and neurocognitive development of the offspring in a murine model. In this study, pregnant mice and their offspring were administered BPA, and the increase in weight and fat accumulation, the gut microbiota composition, and the cognitive development of the offspring were analyzed. In addition, a high-fat diet (HFD) was given to the mice to test for the synergistic obesogenic effect of BPA. Our results demonstrated that BPA exposure impaired the natural remodelling of the gut microbiota during pregnancy. For instance, Akkermansia and Prevotellaceae decreased during natural remodelling of the gut microbiota during pregnancy, but they did not change in the BPA-exposed pregnant mice. Conversely, several members of the Dubosiella genus increased during normal pregnancy but not in BPA-exposed pregnant mice. Moreover, BPA exposure and HFD differentially affect gut microbial transfer from mothers to offspring and both synergistically impact the gut microbiota's establishment in the offspring. Perinatal BPA exposure imprinted changes during colonisation and maturation process of the offspring gut microbiota, identifying Lactobacillus, Eubacterium and Acetatifactor as signature genera enriched in BPA and BPA-exposed mice fed with HFD, taxa involved in a more efficient at energy harvesting from the diet. Moreover, perinatal BPA exposure seemed to alter fat and lean percentages and triggered Muribaculacea taxa imbalance that appears to be associated with disrupted activity, spatial learning, and memory, mimicking impulsivity and hyperactivity-like behavior in the offspring. In conclusion, BPA exposure and HFD exert an influence on the vertical transfer of gut microbiota from mothers to offspring and drive towards an altered establishment of gut microbiota taxa in early life, contributing to enhancing susceptibility to obesity and behavioural disorders.
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spelling doaj-art-4405667a76cd48459ce7891d1e8d33ed2025-08-20T02:26:07ZengElsevierEcotoxicology and Environmental Safety0147-65132025-06-0129811829510.1016/j.ecoenv.2025.118295Perinatal bisphenol A exposure impairs gut microbial colonization: Implications for offspring obesity and neurodevelopmentAna López-Moreno0Alfonso Torres-Sánchez1Antonio Suárez2Alicia Ruiz-Rodríguez3Margarita Aguilera4Department of Microbiology, Faculty of Pharmacy, University of Granada, Granada 18071, Spain; Institute of Nutrition and Food Technology “José Mataix”. Center of Biomedical Research, University of Granada, Granada 18016, Spain; IBS: Instituto de Investigación Biosanitaria ibs, Granada 18012, SpainDepartment of Microbiology, Faculty of Pharmacy, University of Granada, Granada 18071, Spain; Institute of Nutrition and Food Technology “José Mataix”. Center of Biomedical Research, University of Granada, Granada 18016, SpainInstitute of Nutrition and Food Technology “José Mataix”. Center of Biomedical Research, University of Granada, Granada 18016, Spain; IBS: Instituto de Investigación Biosanitaria ibs, Granada 18012, Spain; Department of Biochemistry and Molecular Biology, Faculty of Pharmacy, University of Granada, Campus of Cartuja, Granada 18071, SpainDepartment of Microbiology, Faculty of Pharmacy, University of Granada, Granada 18071, Spain; Institute of Nutrition and Food Technology “José Mataix”. Center of Biomedical Research, University of Granada, Granada 18016, Spain; IBS: Instituto de Investigación Biosanitaria ibs, Granada 18012, Spain; Corresponding author at: Department of Microbiology, Faculty of Pharmacy, University of Granada, Granada 18071, Spain.Department of Microbiology, Faculty of Pharmacy, University of Granada, Granada 18071, Spain; Institute of Nutrition and Food Technology “José Mataix”. Center of Biomedical Research, University of Granada, Granada 18016, Spain; IBS: Instituto de Investigación Biosanitaria ibs, Granada 18012, SpainExposure to plasticiser xenobiotics such as BPA has emerged as a significant health challenge due to globalised and industrial packaged food production. Toxicological approaches in animal models have revealed complex effects, using variable doses of BPA, on reproduction, development, obesity, immune function, metabolic and systemic toxicity. Besides, gut microbiota has emerged as a key player in regulating the impact of xenobiotic exposure on host metabolism. The effect that BPA may exert on the gut microbiota and its consequences for the host's health remains unclear. Exposure to BPA during the perinatal period requires special attention and prevention approaches since it is a particularly vulnerable period and highly implicated in the metabolic health of childhood and adulthood. The aim of this study was to assess the effects of the BPA administration during the perinatal period on promoting obesity phenotypes, altering the composition of the gut microbiota and neurocognitive development of the offspring in a murine model. In this study, pregnant mice and their offspring were administered BPA, and the increase in weight and fat accumulation, the gut microbiota composition, and the cognitive development of the offspring were analyzed. In addition, a high-fat diet (HFD) was given to the mice to test for the synergistic obesogenic effect of BPA. Our results demonstrated that BPA exposure impaired the natural remodelling of the gut microbiota during pregnancy. For instance, Akkermansia and Prevotellaceae decreased during natural remodelling of the gut microbiota during pregnancy, but they did not change in the BPA-exposed pregnant mice. Conversely, several members of the Dubosiella genus increased during normal pregnancy but not in BPA-exposed pregnant mice. Moreover, BPA exposure and HFD differentially affect gut microbial transfer from mothers to offspring and both synergistically impact the gut microbiota's establishment in the offspring. Perinatal BPA exposure imprinted changes during colonisation and maturation process of the offspring gut microbiota, identifying Lactobacillus, Eubacterium and Acetatifactor as signature genera enriched in BPA and BPA-exposed mice fed with HFD, taxa involved in a more efficient at energy harvesting from the diet. Moreover, perinatal BPA exposure seemed to alter fat and lean percentages and triggered Muribaculacea taxa imbalance that appears to be associated with disrupted activity, spatial learning, and memory, mimicking impulsivity and hyperactivity-like behavior in the offspring. In conclusion, BPA exposure and HFD exert an influence on the vertical transfer of gut microbiota from mothers to offspring and drive towards an altered establishment of gut microbiota taxa in early life, contributing to enhancing susceptibility to obesity and behavioural disorders.http://www.sciencedirect.com/science/article/pii/S0147651325006311BPAPlasticiserEndocrine disruptor chemicalsGut microbiotaIntelliCageExposome
spellingShingle Ana López-Moreno
Alfonso Torres-Sánchez
Antonio Suárez
Alicia Ruiz-Rodríguez
Margarita Aguilera
Perinatal bisphenol A exposure impairs gut microbial colonization: Implications for offspring obesity and neurodevelopment
Ecotoxicology and Environmental Safety
BPA
Plasticiser
Endocrine disruptor chemicals
Gut microbiota
IntelliCage
Exposome
title Perinatal bisphenol A exposure impairs gut microbial colonization: Implications for offspring obesity and neurodevelopment
title_full Perinatal bisphenol A exposure impairs gut microbial colonization: Implications for offspring obesity and neurodevelopment
title_fullStr Perinatal bisphenol A exposure impairs gut microbial colonization: Implications for offspring obesity and neurodevelopment
title_full_unstemmed Perinatal bisphenol A exposure impairs gut microbial colonization: Implications for offspring obesity and neurodevelopment
title_short Perinatal bisphenol A exposure impairs gut microbial colonization: Implications for offspring obesity and neurodevelopment
title_sort perinatal bisphenol a exposure impairs gut microbial colonization implications for offspring obesity and neurodevelopment
topic BPA
Plasticiser
Endocrine disruptor chemicals
Gut microbiota
IntelliCage
Exposome
url http://www.sciencedirect.com/science/article/pii/S0147651325006311
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