Effects of Environmental Chemical Pollutants on Microbiome Diversity: Insights from Shotgun Metagenomics

Chemical exposure in the environment can adversely affect the biodiversity of living organisms, particularly when persistent chemicals accumulate over time and disrupt the balance of microbial populations. In this study, we examined how chemical contaminants influence microorganisms in sediment and...

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Main Authors: Seid Muhie, Aarti Gautam, John Mylroie, Bintu Sowe, Ross Campbell, Edward J. Perkins, Rasha Hammamieh, Natàlia Garcia-Reyero
Format: Article
Language:English
Published: MDPI AG 2025-02-01
Series:Toxics
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Online Access:https://www.mdpi.com/2305-6304/13/2/142
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author Seid Muhie
Aarti Gautam
John Mylroie
Bintu Sowe
Ross Campbell
Edward J. Perkins
Rasha Hammamieh
Natàlia Garcia-Reyero
author_facet Seid Muhie
Aarti Gautam
John Mylroie
Bintu Sowe
Ross Campbell
Edward J. Perkins
Rasha Hammamieh
Natàlia Garcia-Reyero
author_sort Seid Muhie
collection DOAJ
description Chemical exposure in the environment can adversely affect the biodiversity of living organisms, particularly when persistent chemicals accumulate over time and disrupt the balance of microbial populations. In this study, we examined how chemical contaminants influence microorganisms in sediment and overlaying water samples collected from the Kinnickinnic, Milwaukee, and Menomonee Rivers near Milwaukee, Wisconsin, USA. We characterized these samples using shotgun metagenomic sequencing to assess microbiome diversity and employed chemical analyses to quantify more than 200 compounds spanning 16 broad classes, including pesticides, industrial products, personal care products, and pharmaceuticals. Integrative and differential comparative analyses of the combined datasets revealed that microbial density, approximated by adjusted total sequence reads, declined with increasing total chemical concentrations. Protozoan, metazoan, and fungal populations were negatively correlated with higher chemical concentrations, whereas certain bacterial (particularly Proteobacteria) and archaeal populations showed positive correlations. As expected, sediment samples exhibited higher concentrations and a wider dynamic range of chemicals compared to water samples. Varying levels of chemical contamination appeared to shape the distribution of microbial taxa, with some bacterial, metazoan, and protozoan populations present only at certain sites or in specific sample types (sediment versus water). These findings suggest that microbial diversity may be linked to both the type and concentration of chemicals present. Additionally, this study demonstrates the potential roles of multiple microbial kingdoms in degrading environmental pollutants, emphasizing the metabolic versatility of bacteria and archaea in processing complex contaminants such as polyaromatic hydrocarbons and bisphenols. Through functional and resistance gene profiling, we observed that multi-kingdom microbial consortia—including bacteria, fungi, and protozoa—can contribute to bioremediation strategies and help restore ecological balance in contaminated ecosystems. This approach may also serve as a valuable proxy for assessing the types and levels of chemical pollutants, as well as their effects on biodiversity.
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spelling doaj-art-1c7d96cea3f94ccba3152a728e9d8ac32025-08-20T03:12:23ZengMDPI AGToxics2305-63042025-02-0113214210.3390/toxics13020142Effects of Environmental Chemical Pollutants on Microbiome Diversity: Insights from Shotgun MetagenomicsSeid Muhie0Aarti Gautam1John Mylroie2Bintu Sowe3Ross Campbell4Edward J. Perkins5Rasha Hammamieh6Natàlia Garcia-Reyero7Medical Readiness Systems Biology, Center for Military Psychiatry and Neuroscience, Walter Reed Army Institute of Research, Silver Spring, MD 20910, USAMedical Readiness Systems Biology, Center for Military Psychiatry and Neuroscience, Walter Reed Army Institute of Research, Silver Spring, MD 20910, USAU.S. Army Engineer Research and Development Center Environmental Laboratory, Vicksburg, MS 39180, USAMedical Readiness Systems Biology, Center for Military Psychiatry and Neuroscience, Walter Reed Army Institute of Research, Silver Spring, MD 20910, USAMedical Readiness Systems Biology, Center for Military Psychiatry and Neuroscience, Walter Reed Army Institute of Research, Silver Spring, MD 20910, USAU.S. Army Engineer Research and Development Center Environmental Laboratory, Vicksburg, MS 39180, USAMedical Readiness Systems Biology, Center for Military Psychiatry and Neuroscience, Walter Reed Army Institute of Research, Silver Spring, MD 20910, USAInstitute for Genomics, Biocomputing & Biotechnology, Mississippi State University, Starkville, MS 39759, USAChemical exposure in the environment can adversely affect the biodiversity of living organisms, particularly when persistent chemicals accumulate over time and disrupt the balance of microbial populations. In this study, we examined how chemical contaminants influence microorganisms in sediment and overlaying water samples collected from the Kinnickinnic, Milwaukee, and Menomonee Rivers near Milwaukee, Wisconsin, USA. We characterized these samples using shotgun metagenomic sequencing to assess microbiome diversity and employed chemical analyses to quantify more than 200 compounds spanning 16 broad classes, including pesticides, industrial products, personal care products, and pharmaceuticals. Integrative and differential comparative analyses of the combined datasets revealed that microbial density, approximated by adjusted total sequence reads, declined with increasing total chemical concentrations. Protozoan, metazoan, and fungal populations were negatively correlated with higher chemical concentrations, whereas certain bacterial (particularly Proteobacteria) and archaeal populations showed positive correlations. As expected, sediment samples exhibited higher concentrations and a wider dynamic range of chemicals compared to water samples. Varying levels of chemical contamination appeared to shape the distribution of microbial taxa, with some bacterial, metazoan, and protozoan populations present only at certain sites or in specific sample types (sediment versus water). These findings suggest that microbial diversity may be linked to both the type and concentration of chemicals present. Additionally, this study demonstrates the potential roles of multiple microbial kingdoms in degrading environmental pollutants, emphasizing the metabolic versatility of bacteria and archaea in processing complex contaminants such as polyaromatic hydrocarbons and bisphenols. Through functional and resistance gene profiling, we observed that multi-kingdom microbial consortia—including bacteria, fungi, and protozoa—can contribute to bioremediation strategies and help restore ecological balance in contaminated ecosystems. This approach may also serve as a valuable proxy for assessing the types and levels of chemical pollutants, as well as their effects on biodiversity.https://www.mdpi.com/2305-6304/13/2/142microbiomemetagenomicchemical pollutantstoxicitybiodiversity
spellingShingle Seid Muhie
Aarti Gautam
John Mylroie
Bintu Sowe
Ross Campbell
Edward J. Perkins
Rasha Hammamieh
Natàlia Garcia-Reyero
Effects of Environmental Chemical Pollutants on Microbiome Diversity: Insights from Shotgun Metagenomics
Toxics
microbiome
metagenomic
chemical pollutants
toxicity
biodiversity
title Effects of Environmental Chemical Pollutants on Microbiome Diversity: Insights from Shotgun Metagenomics
title_full Effects of Environmental Chemical Pollutants on Microbiome Diversity: Insights from Shotgun Metagenomics
title_fullStr Effects of Environmental Chemical Pollutants on Microbiome Diversity: Insights from Shotgun Metagenomics
title_full_unstemmed Effects of Environmental Chemical Pollutants on Microbiome Diversity: Insights from Shotgun Metagenomics
title_short Effects of Environmental Chemical Pollutants on Microbiome Diversity: Insights from Shotgun Metagenomics
title_sort effects of environmental chemical pollutants on microbiome diversity insights from shotgun metagenomics
topic microbiome
metagenomic
chemical pollutants
toxicity
biodiversity
url https://www.mdpi.com/2305-6304/13/2/142
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