Metabolomic-Based Assessment of Earthworm (<i>Eisenia fetida</i>) Exposure to Different Petroleum Fractions in Soils

<b>Background/Objectives:</b> Petroleum contamination in soil exerts toxic effects on earthworms (<i>Eisenia fetida</i>) through non-polar narcotic mechanisms. However, the specific toxicities of individual petroleum components remain insufficiently understood. <b>Metho...

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Main Authors: Meiyu Liu, Mutian Wang, Xiaowen Fu, Fanyong Song, Fangyuan Zhou, Tianyuan Li, Jianing Wang
Format: Article
Language:English
Published: MDPI AG 2025-02-01
Series:Metabolites
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Online Access:https://www.mdpi.com/2218-1989/15/2/97
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author Meiyu Liu
Mutian Wang
Xiaowen Fu
Fanyong Song
Fangyuan Zhou
Tianyuan Li
Jianing Wang
author_facet Meiyu Liu
Mutian Wang
Xiaowen Fu
Fanyong Song
Fangyuan Zhou
Tianyuan Li
Jianing Wang
author_sort Meiyu Liu
collection DOAJ
description <b>Background/Objectives:</b> Petroleum contamination in soil exerts toxic effects on earthworms (<i>Eisenia fetida</i>) through non-polar narcotic mechanisms. However, the specific toxicities of individual petroleum components remain insufficiently understood. <b>Methods:</b> This study investigates the effects of four petroleum components—saturated hydrocarbons, aromatic hydrocarbons, resins, and asphaltenes—on earthworms in artificially contaminated soil, utilizing a combination of biochemical biomarker analysis and metabolomics to uncover the underlying molecular mechanisms. <b>Results:</b> The results revealed that aromatic hydrocarbons are the most toxic fraction, with EC50 concentrations significantly lower than those of other petroleum fractions. All tested fractions triggered notable metabolic disturbances and immune responses in earthworms after 7 days of exposure, as evidenced by significant changes in metabolite abundance within critical pathways such as arginine synthesis, a-linolenic acid metabolism, and the pentose phosphate pathway. According to the KEGG pathway analysis, saturated hydrocarbon fractions induced marked changes in glycerophospholipid metabolism, and arginine and proline metabolism pathways, contributing to the stabilization of the protein structure and membrane integrity. Aromatic hydrocarbon fractions disrupted the arachidonic acid metabolic pathway, leading to increased myotube production and enhanced immune defense mechanisms. The TCA cycle and riboflavin metabolic pathway were significantly altered during exposure to the colloidal fraction, affecting energy production and cellular respiration. The asphaltene fraction significantly impacted glycolysis, accelerating energy cycling to meet stress-induced increases in energy demands. <b>Conclusions:</b> Aromatic hydrocarbons accounted for the highest level of toxicity among the four components in petroleum-contaminated soils. However, the contributions of other fractions to overall toxicity should not be ignored, as each fraction uniquely affects key metabolic pathways and biological functions. These findings emphasize the importance of monitoring metabolic perturbations caused by petroleum components in non-target organisms such as earthworms. They also reveal the specificity of the toxic metabolic effects of different petroleum components on earthworms.
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spelling doaj-art-5627ffc97df6463c8b28eb98fb56ade72025-08-20T03:12:05ZengMDPI AGMetabolites2218-19892025-02-011529710.3390/metabo15020097Metabolomic-Based Assessment of Earthworm (<i>Eisenia fetida</i>) Exposure to Different Petroleum Fractions in SoilsMeiyu Liu0Mutian Wang1Xiaowen Fu2Fanyong Song3Fangyuan Zhou4Tianyuan Li5Jianing Wang6Shandong Provincial Key Laboratory of Applied Microbiology, Ecology Institute, Qilu University of Technology (Shandong Academy of Sciences), Jinan 250100, ChinaEnviroCORE, Dargan Research Centre, South East Technological University, Carlow Campus, R93 V960 Carlow, IrelandShandong Provincial Key Laboratory of Applied Microbiology, Ecology Institute, Qilu University of Technology (Shandong Academy of Sciences), Jinan 250100, ChinaShandong Provincial Key Laboratory of Applied Microbiology, Ecology Institute, Qilu University of Technology (Shandong Academy of Sciences), Jinan 250100, ChinaShandong Provincial Key Laboratory of Applied Microbiology, Ecology Institute, Qilu University of Technology (Shandong Academy of Sciences), Jinan 250100, ChinaShandong Provincial Key Laboratory of Applied Microbiology, Ecology Institute, Qilu University of Technology (Shandong Academy of Sciences), Jinan 250100, ChinaShandong Provincial Key Laboratory of Applied Microbiology, Ecology Institute, Qilu University of Technology (Shandong Academy of Sciences), Jinan 250100, China<b>Background/Objectives:</b> Petroleum contamination in soil exerts toxic effects on earthworms (<i>Eisenia fetida</i>) through non-polar narcotic mechanisms. However, the specific toxicities of individual petroleum components remain insufficiently understood. <b>Methods:</b> This study investigates the effects of four petroleum components—saturated hydrocarbons, aromatic hydrocarbons, resins, and asphaltenes—on earthworms in artificially contaminated soil, utilizing a combination of biochemical biomarker analysis and metabolomics to uncover the underlying molecular mechanisms. <b>Results:</b> The results revealed that aromatic hydrocarbons are the most toxic fraction, with EC50 concentrations significantly lower than those of other petroleum fractions. All tested fractions triggered notable metabolic disturbances and immune responses in earthworms after 7 days of exposure, as evidenced by significant changes in metabolite abundance within critical pathways such as arginine synthesis, a-linolenic acid metabolism, and the pentose phosphate pathway. According to the KEGG pathway analysis, saturated hydrocarbon fractions induced marked changes in glycerophospholipid metabolism, and arginine and proline metabolism pathways, contributing to the stabilization of the protein structure and membrane integrity. Aromatic hydrocarbon fractions disrupted the arachidonic acid metabolic pathway, leading to increased myotube production and enhanced immune defense mechanisms. The TCA cycle and riboflavin metabolic pathway were significantly altered during exposure to the colloidal fraction, affecting energy production and cellular respiration. The asphaltene fraction significantly impacted glycolysis, accelerating energy cycling to meet stress-induced increases in energy demands. <b>Conclusions:</b> Aromatic hydrocarbons accounted for the highest level of toxicity among the four components in petroleum-contaminated soils. However, the contributions of other fractions to overall toxicity should not be ignored, as each fraction uniquely affects key metabolic pathways and biological functions. These findings emphasize the importance of monitoring metabolic perturbations caused by petroleum components in non-target organisms such as earthworms. They also reveal the specificity of the toxic metabolic effects of different petroleum components on earthworms.https://www.mdpi.com/2218-1989/15/2/97hydrocarbon series of petroleumsoilecotoxicityearthwormsmetabolismassessment
spellingShingle Meiyu Liu
Mutian Wang
Xiaowen Fu
Fanyong Song
Fangyuan Zhou
Tianyuan Li
Jianing Wang
Metabolomic-Based Assessment of Earthworm (<i>Eisenia fetida</i>) Exposure to Different Petroleum Fractions in Soils
Metabolites
hydrocarbon series of petroleum
soil
ecotoxicity
earthworms
metabolism
assessment
title Metabolomic-Based Assessment of Earthworm (<i>Eisenia fetida</i>) Exposure to Different Petroleum Fractions in Soils
title_full Metabolomic-Based Assessment of Earthworm (<i>Eisenia fetida</i>) Exposure to Different Petroleum Fractions in Soils
title_fullStr Metabolomic-Based Assessment of Earthworm (<i>Eisenia fetida</i>) Exposure to Different Petroleum Fractions in Soils
title_full_unstemmed Metabolomic-Based Assessment of Earthworm (<i>Eisenia fetida</i>) Exposure to Different Petroleum Fractions in Soils
title_short Metabolomic-Based Assessment of Earthworm (<i>Eisenia fetida</i>) Exposure to Different Petroleum Fractions in Soils
title_sort metabolomic based assessment of earthworm i eisenia fetida i exposure to different petroleum fractions in soils
topic hydrocarbon series of petroleum
soil
ecotoxicity
earthworms
metabolism
assessment
url https://www.mdpi.com/2218-1989/15/2/97
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AT fanyongsong metabolomicbasedassessmentofearthwormieiseniafetidaiexposuretodifferentpetroleumfractionsinsoils
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