Bisphenol A exposure affects specific gut taxa and drives microbiota dynamics in childhood obesity

mSystems. 2024 Mar 19;9(3):e0095723. doi: 10.1128/msystems.00957-23. Epub 2024 Mar 1.

Abstract

Cumulative xenobiotic exposure has an environmental and human health impact which is currently assessed under the One Health approach. Bisphenol A (BPA) exposure and its potential link with childhood obesity that has parallelly increased during the last decades deserve special attention. It stands during prenatal or early life and could trigger comorbidities and non-communicable diseases along life. Accumulation in the nature of synthetic chemicals supports the "environmental obesogen" hypothesis, such as BPA. This estrogen-mimicking xenobiotic has shown endocrine disruptive and obesogenic effects accompanied by gut microbiota misbalance that is not yet well elucidated. This study aimed to investigate specific microbiota taxa isolated and selected by direct BPA exposure and reveal its role on the overall children microbiota community and dynamics, driving toward specific obesity dysbiosis. A total of 333 BPA-resistant isolated species obtained through culturing after several exposure conditions were evaluated for their role and interplay with the global microbial community. The selected BPA-cultured taxa biomarkers showed a significant impact on alpha diversity. Specifically, Clostridium and Romboutsia were positively associated promoting the richness of microbiota communities, while Intestinibacter, Escherichia-Shigella, Bifidobacterium, and Lactobacillus were negatively associated. Microbial community dynamics and networks analyses showed differences according to the study groups. The normal-weight children group exhibited a more enriched, structured, and connected taxa network compared to overweight and obese groups, which could represent a more resilient community to xenobiotic substances. In this sense, subnetwork analysis generated with the BPA-cultured genera showed a correlation between taxa connectivity and more diverse potential enzymatic BPA degradation capacities.IMPORTANCEOur findings indicate how gut microbiota taxa with the capacity to grow in BPA were differentially represented within differential body mass index children study groups and how these taxa affected the overall dynamics toward patterns of diversity generally recognized in dysbiosis. Community network and subnetwork analyses corroborated the better connectedness and stability profiles for normal-weight group compared to the overweight and obese groups.

Keywords: BPA; amplicon-sequencing; culturomics; microbiota; obesity; xenobiotics.

MeSH terms

  • Benzhydryl Compounds*
  • Child
  • Clostridiaceae
  • Dysbiosis / chemically induced
  • Female
  • Humans
  • Microbiota*
  • Overweight
  • Pediatric Obesity* / epidemiology
  • Phenols*
  • Pregnancy
  • Xenobiotics

Substances

  • bisphenol A
  • Xenobiotics
  • Benzhydryl Compounds
  • Phenols