Chlorpyrifos modulates the mouse gut microbiota and metabolic activity

The organophosphate chlorpyrifos is a commonly used pesticide for fruits and vegetables despite its association with neurotoxicity in humans. While some studies suggest that organophosphates may impact the gut microbiota, no studies to date have investigated the direct effect of chlorpyrifos on the...

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Main Authors: Robert G. Nichols, Bipin Rimal, Fuhua Hao, Jeffrey M. Peters, Emily R. Davenport, Andrew D. Patterson
Format: Article
Language:English
Published: Elsevier 2024-10-01
Series:Environment International
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0160412024006081
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author Robert G. Nichols
Bipin Rimal
Fuhua Hao
Jeffrey M. Peters
Emily R. Davenport
Andrew D. Patterson
author_facet Robert G. Nichols
Bipin Rimal
Fuhua Hao
Jeffrey M. Peters
Emily R. Davenport
Andrew D. Patterson
author_sort Robert G. Nichols
collection DOAJ
description The organophosphate chlorpyrifos is a commonly used pesticide for fruits and vegetables despite its association with neurotoxicity in humans. While some studies suggest that organophosphates may impact the gut microbiota, no studies to date have investigated the direct effect of chlorpyrifos on the gut microbiota with doses that approximate environmentally relevant dietary concentrations (EPA chronic reference dose: 0.3 µg/kg/day in humans and EPA acute reference dose: 5 µg/kg/day in humans). Thus, we examined the influence of chlorpyrifos on the gut microbiota by assessment of bacterial physiology and metabolism using flow cytometry, 1H NMR-based metabolomics, and changes in the cecal microbiota community with 16S rRNA amplicon sequencing and analysis. Chlorpyrifos did not directly damage bacteria but rather perturbed bacterial metabolism. Chlorpyrifos exposure to bacteria increased the concentration of amino acids, carbohydrates, and nucleic acids. The relative abundances of Lactobacillus, Allobaculum, Roseburia, and Butyricicoccus increased after exposure to chlorpyrifos. Analyses of the 16S rRNA gene amplicon data predicted decreased amino acid biosynthesis and nucleic acid degradation and increased glycolysis which was supported by 1H NMR-based metabolomics. Collectively, these results demonstrate that environmentally relevant doses of chlorpyrifos can impact the metabolic activity of isolated gut microbes which may result in an imbalance in overall gut metabolic activity.
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spelling doaj.art-99b50383e8e6472790e6e98410c299102024-10-23T04:26:52ZengElsevierEnvironment International0160-41202024-10-01192109022Chlorpyrifos modulates the mouse gut microbiota and metabolic activityRobert G. Nichols0Bipin Rimal1Fuhua Hao2Jeffrey M. Peters3Emily R. Davenport4Andrew D. Patterson5Department of Biology, The Pennsylvania State University, University Park, PA, USA; One Health Microbiome Center, Huck Life Sciences Institute, University Park, PA 16802, USAOne Health Microbiome Center, Huck Life Sciences Institute, University Park, PA 16802, USA; Department of Veterinary and Biomedical Sciences, Center for Molecular Toxicology and Carcinogenesis, The Pennsylvania State University, University Park, PA, USADepartment of Veterinary and Biomedical Sciences, Center for Molecular Toxicology and Carcinogenesis, The Pennsylvania State University, University Park, PA, USADepartment of Veterinary and Biomedical Sciences, Center for Molecular Toxicology and Carcinogenesis, The Pennsylvania State University, University Park, PA, USADepartment of Biology, The Pennsylvania State University, University Park, PA, USA; One Health Microbiome Center, Huck Life Sciences Institute, University Park, PA 16802, USAOne Health Microbiome Center, Huck Life Sciences Institute, University Park, PA 16802, USA; Department of Veterinary and Biomedical Sciences, Center for Molecular Toxicology and Carcinogenesis, The Pennsylvania State University, University Park, PA, USA; Corresponding author.The organophosphate chlorpyrifos is a commonly used pesticide for fruits and vegetables despite its association with neurotoxicity in humans. While some studies suggest that organophosphates may impact the gut microbiota, no studies to date have investigated the direct effect of chlorpyrifos on the gut microbiota with doses that approximate environmentally relevant dietary concentrations (EPA chronic reference dose: 0.3 µg/kg/day in humans and EPA acute reference dose: 5 µg/kg/day in humans). Thus, we examined the influence of chlorpyrifos on the gut microbiota by assessment of bacterial physiology and metabolism using flow cytometry, 1H NMR-based metabolomics, and changes in the cecal microbiota community with 16S rRNA amplicon sequencing and analysis. Chlorpyrifos did not directly damage bacteria but rather perturbed bacterial metabolism. Chlorpyrifos exposure to bacteria increased the concentration of amino acids, carbohydrates, and nucleic acids. The relative abundances of Lactobacillus, Allobaculum, Roseburia, and Butyricicoccus increased after exposure to chlorpyrifos. Analyses of the 16S rRNA gene amplicon data predicted decreased amino acid biosynthesis and nucleic acid degradation and increased glycolysis which was supported by 1H NMR-based metabolomics. Collectively, these results demonstrate that environmentally relevant doses of chlorpyrifos can impact the metabolic activity of isolated gut microbes which may result in an imbalance in overall gut metabolic activity.http://www.sciencedirect.com/science/article/pii/S0160412024006081ChlorpyrifosGut microbiomeFlow cytometryEPA acute reference doses
spellingShingle Robert G. Nichols
Bipin Rimal
Fuhua Hao
Jeffrey M. Peters
Emily R. Davenport
Andrew D. Patterson
Chlorpyrifos modulates the mouse gut microbiota and metabolic activity
Environment International
Chlorpyrifos
Gut microbiome
Flow cytometry
EPA acute reference doses
title Chlorpyrifos modulates the mouse gut microbiota and metabolic activity
title_full Chlorpyrifos modulates the mouse gut microbiota and metabolic activity
title_fullStr Chlorpyrifos modulates the mouse gut microbiota and metabolic activity
title_full_unstemmed Chlorpyrifos modulates the mouse gut microbiota and metabolic activity
title_short Chlorpyrifos modulates the mouse gut microbiota and metabolic activity
title_sort chlorpyrifos modulates the mouse gut microbiota and metabolic activity
topic Chlorpyrifos
Gut microbiome
Flow cytometry
EPA acute reference doses
url http://www.sciencedirect.com/science/article/pii/S0160412024006081
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