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

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          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.

          IMPORTANCE

          Our 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.

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          DADA2: High resolution sample inference from Illumina amplicon data

          We present DADA2, a software package that models and corrects Illumina-sequenced amplicon errors. DADA2 infers sample sequences exactly, without coarse-graining into OTUs, and resolves differences of as little as one nucleotide. In several mock communities DADA2 identified more real variants and output fewer spurious sequences than other methods. We applied DADA2 to vaginal samples from a cohort of pregnant women, revealing a diversity of previously undetected Lactobacillus crispatus variants.
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            Cutadapt removes adapter sequences from high-throughput sequencing reads

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              The SILVA ribosomal RNA gene database project: improved data processing and web-based tools

              SILVA (from Latin silva, forest, http://www.arb-silva.de) is a comprehensive web resource for up to date, quality-controlled databases of aligned ribosomal RNA (rRNA) gene sequences from the Bacteria, Archaea and Eukaryota domains and supplementary online services. The referred database release 111 (July 2012) contains 3 194 778 small subunit and 288 717 large subunit rRNA gene sequences. Since the initial description of the project, substantial new features have been introduced, including advanced quality control procedures, an improved rRNA gene aligner, online tools for probe and primer evaluation and optimized browsing, searching and downloading on the website. Furthermore, the extensively curated SILVA taxonomy and the new non-redundant SILVA datasets provide an ideal reference for high-throughput classification of data from next-generation sequencing approaches.
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                Author and article information

                Contributors
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – original draft
                Role: Data curationRole: Formal analysis
                Role: MethodologyRole: Resources
                Role: SupervisionRole: Visualization
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: SupervisionRole: Validation
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: Writing – review and editing
                Role: Editor
                Journal
                mSystems
                mSystems
                msystems
                mSystems
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                2379-5077
                March 2024
                01 March 2024
                01 March 2024
                : 9
                : 3
                : e00957-23
                Affiliations
                [1 ]Department of Microbiology, Faculty of Pharmacy, University of Granada, Campus of Cartuja; , Granada, Spain
                [2 ]Institute of Nutrition and Food Technology "José Mataix" (INYTA), Centre of Biomedical Research, University of Granada; , Granada, Spain
                [ ] 3Instituto de Investigación Biosanitaria ibs; , Granada, Spain
                [4 ]Quadram Institute Bioscience, Rosalind Franklin Road, Norwich Research Park; , Norwich, United Kingdom
                [5 ]Department of Biochemistry and Molecular Biology II, Faculty of Pharmacy, Campus of Cartuja, University of Granada; , Granada, Spain
                Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Université Évry, Université Paris-Saclay; , Evry, France
                Author notes
                Address correspondence to Margarita Aguilera, maguiler@ 123456ugr.es

                Margarita Aguilera and Alicia Ruiz-Rodriguez contributed equally to this article.

                The authors declare no conflict of interest.

                Author information
                https://orcid.org/0000-0003-3717-9852
                https://orcid.org/0000-0002-3204-9787
                Article
                00957-23 msystems.00957-23
                10.1128/msystems.00957-23
                10949422
                38426791
                8ebb80fd-9e94-46b3-b5c5-5cbdf04c10e1
                Copyright © 2024 Lopez-Moreno et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                History
                : 06 September 2023
                : 15 January 2024
                Page count
                supplementary-material: 0, authors: 6, Figures: 8, Tables: 1, References: 91, Pages: 20, Words: 11641
                Funding
                Funded by: European Food Safety Authority (EFSA);
                Award ID: EUFORA/GP/EFSA/ENCO/2021/01
                Award Recipient :
                Funded by: UGR | Vicerrectorado de Investigación y Transferencia, Universidad de Granada (Office of Vice-Rector for Research and Knowledge Transfer, University of Granada);
                Award ID: MARIA ZAMBRANO Next Generation EU
                Award Recipient :
                Funded by: Consejería de Universidad, Investigación e Innovación, Junta de Andalucía (Ministry of Knowledge, Research and University, Andalusia);
                Award ID: Proyectos-Excelencia: P21-00341 DiETOXµBio
                Award Recipient :
                Categories
                Research Article
                human-microbiome, Human Microbiome
                Custom metadata
                March 2024

                xenobiotics,bpa,obesity,microbiota,culturomics,amplicon-sequencing

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