Metabolic Reprogramming in Gut Microbiota Exposed to Polystyrene Microplastics

<b>Background</b>: Microplastics (MPs) are small plastic fragments with diameters less than 5 mm in size and are prevalent in everyday essentials and consumables. Large global plastic production has now led to a flooding of MPs in our natural environment. Due to their detrimental impacts...

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Main Authors: Jinhua Chi, Jeffrey S. Patterson, Yan Jin, Kyle Joohyung Kim, Nicole Lalime, Daniella Hawley, Freeman Lewis, Lingjun Li, Xuan Wang, Matthew J. Campen, Julia Yue Cui, Haiwei Gu
Format: Article
Language:English
Published: MDPI AG 2025-02-01
Series:Biomedicines
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Online Access:https://www.mdpi.com/2227-9059/13/2/446
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author Jinhua Chi
Jeffrey S. Patterson
Yan Jin
Kyle Joohyung Kim
Nicole Lalime
Daniella Hawley
Freeman Lewis
Lingjun Li
Xuan Wang
Matthew J. Campen
Julia Yue Cui
Haiwei Gu
author_facet Jinhua Chi
Jeffrey S. Patterson
Yan Jin
Kyle Joohyung Kim
Nicole Lalime
Daniella Hawley
Freeman Lewis
Lingjun Li
Xuan Wang
Matthew J. Campen
Julia Yue Cui
Haiwei Gu
author_sort Jinhua Chi
collection DOAJ
description <b>Background</b>: Microplastics (MPs) are small plastic fragments with diameters less than 5 mm in size and are prevalent in everyday essentials and consumables. Large global plastic production has now led to a flooding of MPs in our natural environment. Due to their detrimental impacts on the planet’s ecosystems and potentially our health, MPs have emerged as a significant public health concern. In this pilot study, we hypothesize that MPs exposure will negatively affect gut microbiota composition and function, in which metabolic reprogramming plays an important role. <b>Methods</b>: Using in vitro experiments, three bacterial strains (<i>Escherichia coli</i> MG1655, Nissle 1917, and <i>Lactobacillus rhamnosus</i>) were selected to investigate the impacts of MPs exposure. The bacterial strains were individually cultured in an anaerobic chamber and exposed to 1 µm polystyrene MPs at various concentrations (0, 10, 20, 50, 100, and 500 µg/mL) in the culture medium. <b>Results</b>: MPs exposure reduced the growth of all three bacterial strains in a dose-dependent manner. Liquid chromatography mass spectrometry (LC-MS)-based untargeted metabolomics revealed significant differences in multiple metabolic pathways, such as sulfur metabolism and amino sugar and nucleotide sugar metabolism. In addition, we extracted gut microbiota from C57BL/6 mice, and 16S rRNA sequencing results showed a significant upregulation of <i>Lactobacillales</i> and a significant reduction in <i>Erysipelotrichales</i> due to MPs exposure. Furthermore, targeted and untargeted metabolomics corroborated the in vitro results and revealed alterations in microbial tryptophan metabolism and energy producing pathways, such as glycolysis/gluconeogenesis and the pentose phosphate pathway. <b>Conclusions</b>: These findings provide evidence that MPs exposure causes comprehensive changes to healthy gut microbiota, which may also provide insights into the mechanistic effects of MPs exposure in humans.
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spelling doaj-art-c2e5f5e07e7d4f9887ade60b4a0c00862025-08-20T02:44:45ZengMDPI AGBiomedicines2227-90592025-02-0113244610.3390/biomedicines13020446Metabolic Reprogramming in Gut Microbiota Exposed to Polystyrene MicroplasticsJinhua Chi0Jeffrey S. Patterson1Yan Jin2Kyle Joohyung Kim3Nicole Lalime4Daniella Hawley5Freeman Lewis6Lingjun Li7Xuan Wang8Matthew J. Campen9Julia Yue Cui10Haiwei Gu11College of Health Solutions, Arizona State University, Phoenix, AZ 85004, USACollege of Health Solutions, Arizona State University, Phoenix, AZ 85004, USACenter for Translational Science, Florida International University, Port St. Lucie, FL 34987, USADepartment of Environmental & Occupational Health Sciences, University of Washington, Seattle, WA 98195, USASchool of Biological and Health Systems Engineering, Arizona State University, Tempe, AZ 85287, USASchool of Life Sciences, Arizona State University, Tempe, AZ 85287, USAEnvironmental Health Sciences, Florida International University, Miami, FL 33199, USACollege of Health Solutions, Arizona State University, Phoenix, AZ 85004, USASchool of Life Sciences, Arizona State University, Tempe, AZ 85287, USADepartment of Pharmaceutical Sciences, College of Pharmacy, University of New Mexico Health Sciences, Albuquerque, NM 87106, USADepartment of Environmental & Occupational Health Sciences, University of Washington, Seattle, WA 98195, USACollege of Health Solutions, Arizona State University, Phoenix, AZ 85004, USA<b>Background</b>: Microplastics (MPs) are small plastic fragments with diameters less than 5 mm in size and are prevalent in everyday essentials and consumables. Large global plastic production has now led to a flooding of MPs in our natural environment. Due to their detrimental impacts on the planet’s ecosystems and potentially our health, MPs have emerged as a significant public health concern. In this pilot study, we hypothesize that MPs exposure will negatively affect gut microbiota composition and function, in which metabolic reprogramming plays an important role. <b>Methods</b>: Using in vitro experiments, three bacterial strains (<i>Escherichia coli</i> MG1655, Nissle 1917, and <i>Lactobacillus rhamnosus</i>) were selected to investigate the impacts of MPs exposure. The bacterial strains were individually cultured in an anaerobic chamber and exposed to 1 µm polystyrene MPs at various concentrations (0, 10, 20, 50, 100, and 500 µg/mL) in the culture medium. <b>Results</b>: MPs exposure reduced the growth of all three bacterial strains in a dose-dependent manner. Liquid chromatography mass spectrometry (LC-MS)-based untargeted metabolomics revealed significant differences in multiple metabolic pathways, such as sulfur metabolism and amino sugar and nucleotide sugar metabolism. In addition, we extracted gut microbiota from C57BL/6 mice, and 16S rRNA sequencing results showed a significant upregulation of <i>Lactobacillales</i> and a significant reduction in <i>Erysipelotrichales</i> due to MPs exposure. Furthermore, targeted and untargeted metabolomics corroborated the in vitro results and revealed alterations in microbial tryptophan metabolism and energy producing pathways, such as glycolysis/gluconeogenesis and the pentose phosphate pathway. <b>Conclusions</b>: These findings provide evidence that MPs exposure causes comprehensive changes to healthy gut microbiota, which may also provide insights into the mechanistic effects of MPs exposure in humans.https://www.mdpi.com/2227-9059/13/2/446gut microbiotamicroplasticsmass spectrometrymetabolomics16S rRNA
spellingShingle Jinhua Chi
Jeffrey S. Patterson
Yan Jin
Kyle Joohyung Kim
Nicole Lalime
Daniella Hawley
Freeman Lewis
Lingjun Li
Xuan Wang
Matthew J. Campen
Julia Yue Cui
Haiwei Gu
Metabolic Reprogramming in Gut Microbiota Exposed to Polystyrene Microplastics
Biomedicines
gut microbiota
microplastics
mass spectrometry
metabolomics
16S rRNA
title Metabolic Reprogramming in Gut Microbiota Exposed to Polystyrene Microplastics
title_full Metabolic Reprogramming in Gut Microbiota Exposed to Polystyrene Microplastics
title_fullStr Metabolic Reprogramming in Gut Microbiota Exposed to Polystyrene Microplastics
title_full_unstemmed Metabolic Reprogramming in Gut Microbiota Exposed to Polystyrene Microplastics
title_short Metabolic Reprogramming in Gut Microbiota Exposed to Polystyrene Microplastics
title_sort metabolic reprogramming in gut microbiota exposed to polystyrene microplastics
topic gut microbiota
microplastics
mass spectrometry
metabolomics
16S rRNA
url https://www.mdpi.com/2227-9059/13/2/446
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