Carbamazepine-exposed earthworms are characterized by tissue-specific accumulation patterns and transcriptional profiles
Pharmaceutically active compounds enter soils via wastewater reuse and biosolid application. A ubiquitous drug present in wastewater is carbamazepine, a frequently prescribed anti-convulsant. Its mode of action is not species-specific and affects the nervous system of non-target organisms, including...
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Elsevier
2025-04-01
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| Series: | Environment International |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S0160412025001084 |
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| author | Chubin Zhang Filipe Cabreiro Leon P. Barron Stephen R. Stürzenbaum |
| author_facet | Chubin Zhang Filipe Cabreiro Leon P. Barron Stephen R. Stürzenbaum |
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| description | Pharmaceutically active compounds enter soils via wastewater reuse and biosolid application. A ubiquitous drug present in wastewater is carbamazepine, a frequently prescribed anti-convulsant. Its mode of action is not species-specific and affects the nervous system of non-target organisms, including most likely the soil dwelling earthworms, which in turn has the potential to negatively impact soil quality. In this project, soils were amended with carbamazepine to explore uptake dynamics and resultant changes in molecular and life cycle endpoints of earthworms (Dendrobaena veneta). Earthworms were maintained, under laboratory conditions, for 28 days in soil spiked with either a solvent control, 0.6 mg/kg carbamazepine (encountered in the terrestrial system) or 10 mg/kg carbamazepine (significantly above an environmental hotspot). Carbamazepine concentrations were quantified in soils and worms by liquid chromatography tandem mass spectrometry (LC-MS/MS) which revealed tissue, dose and time-dependent differences in accumulation. Carbamazepine also modulated the make-up of the microbiome in the soil as well as the earthworm’s gut. De novo RNA sequencing identified novel transcripts and complex tissue-specific transcriptomic changes, where, for example, the expression of the tubulin polymerisation promoting protein (tppp) was inhibited (9-fold) in the gut but induced (11-fold) in the cerebral ganglion of exposed earthworms. However, the notable absence of a strong cytochrome P450 response across all conditions suggests that the terrestrial earthworm also relies on detoxification pathways that differ to those observed in well-studied aquatic models. The novel finding that carbamazepine exposure triggers tissue-specific impacts in non-target soil organisms highlights the value and need for a more comprehensive understanding of how contaminants of emerging concern behave within an ecotoxicological context. This, in turn, will lead to informed and reliable risk assessments defining the consequences of wastewater and biosolid amendment practices on soil ecology and ecosystem function. |
| format | Article |
| id | doaj-art-84671ece7ccc462196fc06f168b99eb7 |
| institution | OA Journals |
| issn | 0160-4120 |
| language | English |
| publishDate | 2025-04-01 |
| publisher | Elsevier |
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| series | Environment International |
| spelling | doaj-art-84671ece7ccc462196fc06f168b99eb72025-08-20T02:24:57ZengElsevierEnvironment International0160-41202025-04-0119810935710.1016/j.envint.2025.109357Carbamazepine-exposed earthworms are characterized by tissue-specific accumulation patterns and transcriptional profilesChubin Zhang0Filipe Cabreiro1Leon P. Barron2Stephen R. Stürzenbaum3Analytical, Environmental & Forensic Sciences Department, Institute of Pharmaceutical Sciences, School of Cancer and Pharmaceutical Sciences, Faculty of Life Sciences & Medicine, King’s College London, 150 Stamford Street, London SE1 9NH, United KingdomInstitute of Clinical Sciences, Imperial College London, Hammersmith Hospital Campus, Du Cane Road, London W12 0HS, United Kingdom; University of Cologne, Faculty of Mathematics and Natural Sciences, Institute of Genetics, Cluster of Excellence Cellular Stress Responses in Aging-associated Diseases (CECAD), Cologne, GermanyAnalytical, Environmental & Forensic Sciences Department, Institute of Pharmaceutical Sciences, School of Cancer and Pharmaceutical Sciences, Faculty of Life Sciences & Medicine, King’s College London, 150 Stamford Street, London SE1 9NH, United Kingdom; MRC Centre for Environment and Health, Environmental Research Group, School of Public Health, Faculty of Medicine, Imperial College London, 86 Wood Lane, London W12 0BZ, United KingdomAnalytical, Environmental & Forensic Sciences Department, Institute of Pharmaceutical Sciences, School of Cancer and Pharmaceutical Sciences, Faculty of Life Sciences & Medicine, King’s College London, 150 Stamford Street, London SE1 9NH, United Kingdom; Corresponding author.Pharmaceutically active compounds enter soils via wastewater reuse and biosolid application. A ubiquitous drug present in wastewater is carbamazepine, a frequently prescribed anti-convulsant. Its mode of action is not species-specific and affects the nervous system of non-target organisms, including most likely the soil dwelling earthworms, which in turn has the potential to negatively impact soil quality. In this project, soils were amended with carbamazepine to explore uptake dynamics and resultant changes in molecular and life cycle endpoints of earthworms (Dendrobaena veneta). Earthworms were maintained, under laboratory conditions, for 28 days in soil spiked with either a solvent control, 0.6 mg/kg carbamazepine (encountered in the terrestrial system) or 10 mg/kg carbamazepine (significantly above an environmental hotspot). Carbamazepine concentrations were quantified in soils and worms by liquid chromatography tandem mass spectrometry (LC-MS/MS) which revealed tissue, dose and time-dependent differences in accumulation. Carbamazepine also modulated the make-up of the microbiome in the soil as well as the earthworm’s gut. De novo RNA sequencing identified novel transcripts and complex tissue-specific transcriptomic changes, where, for example, the expression of the tubulin polymerisation promoting protein (tppp) was inhibited (9-fold) in the gut but induced (11-fold) in the cerebral ganglion of exposed earthworms. However, the notable absence of a strong cytochrome P450 response across all conditions suggests that the terrestrial earthworm also relies on detoxification pathways that differ to those observed in well-studied aquatic models. The novel finding that carbamazepine exposure triggers tissue-specific impacts in non-target soil organisms highlights the value and need for a more comprehensive understanding of how contaminants of emerging concern behave within an ecotoxicological context. This, in turn, will lead to informed and reliable risk assessments defining the consequences of wastewater and biosolid amendment practices on soil ecology and ecosystem function.http://www.sciencedirect.com/science/article/pii/S0160412025001084Contaminants of emerging concernInvertebratesRNA sequencingBiosolidsWastewaterDrug distribution |
| spellingShingle | Chubin Zhang Filipe Cabreiro Leon P. Barron Stephen R. Stürzenbaum Carbamazepine-exposed earthworms are characterized by tissue-specific accumulation patterns and transcriptional profiles Environment International Contaminants of emerging concern Invertebrates RNA sequencing Biosolids Wastewater Drug distribution |
| title | Carbamazepine-exposed earthworms are characterized by tissue-specific accumulation patterns and transcriptional profiles |
| title_full | Carbamazepine-exposed earthworms are characterized by tissue-specific accumulation patterns and transcriptional profiles |
| title_fullStr | Carbamazepine-exposed earthworms are characterized by tissue-specific accumulation patterns and transcriptional profiles |
| title_full_unstemmed | Carbamazepine-exposed earthworms are characterized by tissue-specific accumulation patterns and transcriptional profiles |
| title_short | Carbamazepine-exposed earthworms are characterized by tissue-specific accumulation patterns and transcriptional profiles |
| title_sort | carbamazepine exposed earthworms are characterized by tissue specific accumulation patterns and transcriptional profiles |
| topic | Contaminants of emerging concern Invertebrates RNA sequencing Biosolids Wastewater Drug distribution |
| url | http://www.sciencedirect.com/science/article/pii/S0160412025001084 |
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