Carbamazepine-exposed earthworms are characterized by  tissue-specific accumulation patterns and transcriptional profiles

Chubin Zhang; Filipe  Cabreiro; Leon Barron; Stephen Sturzenbaum

doi:10.1016/j.envint.2025.109357

Carbamazepine-exposed earthworms are characterized by tissue-specific accumulation patterns and transcriptional profiles

Chubin Zhang, Filipe Cabreiro, Leon Barron, Stephen Sturzenbaum

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Abstract

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.

Original language	English
Article number	109357
Journal	Environment International
Volume	198
Early online date	1 Mar 2025
DOIs	https://doi.org/10.1016/j.envint.2025.109357
Publication status	Published - Apr 2025

Keywords

contaminants of emerging concern; invertebrates; RNA sequencing; biosolids; wastewater; drug distribution

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This output contributes to the following UN Sustainable Development Goals (SDGs)

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Cite this

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title = "Carbamazepine-exposed earthworms are characterized by tissue-specific accumulation patterns and transcriptional profiles",

abstract = "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{\textquoteright}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.",

keywords = "contaminants of emerging concern; invertebrates; RNA sequencing; biosolids; wastewater; drug distribution",

author = "Chubin Zhang and Filipe Cabreiro and Leon Barron and Stephen Sturzenbaum",

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N2 - 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.

AB - 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.

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