Metabolic Regulation of Copper Toxicity during Marine Mussel Embryogenesis
The development of new tools for assessing the health of cultured shellfish larvae is crucial for aquaculture industries to develop and refine hatchery methodologies. We established a large-volume ecotoxicology/health stressor trial, exposing mussel (<i>Perna canaliculus</i>) embryos to...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2023-07-01
|
| Series: | Metabolites |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2218-1989/13/7/838 |
| _version_ | 1827732386840838144 |
|---|---|
| author | Tim Young Samantha L. Gale Norman L. C. Ragg Sylvia G. Sander David J. Burritt Billy Benedict Dung V. Le Silas G. Villas-Bôas Andrea C. Alfaro |
| author_facet | Tim Young Samantha L. Gale Norman L. C. Ragg Sylvia G. Sander David J. Burritt Billy Benedict Dung V. Le Silas G. Villas-Bôas Andrea C. Alfaro |
| author_sort | Tim Young |
| collection | DOAJ |
| description | The development of new tools for assessing the health of cultured shellfish larvae is crucial for aquaculture industries to develop and refine hatchery methodologies. We established a large-volume ecotoxicology/health stressor trial, exposing mussel (<i>Perna canaliculus</i>) embryos to copper in the presence of ethylenediaminetetraacetic acid (EDTA). GC/MS-based metabolomics was applied to identify potential biomarkers for monitoring embryonic/larval health and to characterise mechanisms of metal toxicity. Cellular viability, developmental abnormalities, larval behaviour, mortality, and a targeted analysis of proteins involved in the regulation of reactive oxygen species were simultaneously evaluated to provide a complementary framework for interpretative purposes and authenticate the metabolomics data. Trace metal analysis and speciation modelling verified EDTA as an effective copper chelator. Toxicity thresholds for <i>P</i>. <i>canaliculus</i> were low, with 10% developmental abnormalities in D-stage larvae being recorded upon exposure to 1.10 μg·L<sup>−1</sup> bioavailable copper for 66 h. Sublethal levels of bioavailable copper (0.04 and 1.10 μg·L<sup>−1</sup>) caused coordinated fluctuations in metabolite profiles, which were dependent on development stage, treatment level, and exposure duration. Larvae appeared to successfully employ various mechanisms involving the biosynthesis of antioxidants and a restructuring of energy-related metabolism to alleviate the toxic effects of copper on cells and developing tissues. These results suggest that regulation of trace metal-induced toxicity is tightly linked with metabolism during the early ontogenic development of marine mussels. Lethal-level bioavailable copper (50.3 μg·L<sup>−1</sup>) caused severe metabolic dysregulation after 3 h of exposure, which worsened with time, substantially delayed embryonic development, induced critical oxidative damage, initiated the apoptotic pathway, and resulted in cell/organism death shortly after 18 h of exposure. Metabolite profiling is a useful approach to (1) assess the health status of marine invertebrate embryos and larvae, (2) detect early warning biomarkers for trace metal contamination, and (3) identify novel regulatory mechanisms of copper-induced toxicity. |
| first_indexed | 2024-03-11T00:50:48Z |
| format | Article |
| id | doaj.art-5eab94d49b1c4a5097542bd486530b3f |
| institution | Directory Open Access Journal |
| issn | 2218-1989 |
| language | English |
| last_indexed | 2024-03-11T00:50:48Z |
| publishDate | 2023-07-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Metabolites |
| spelling | doaj.art-5eab94d49b1c4a5097542bd486530b3f2023-11-18T20:27:56ZengMDPI AGMetabolites2218-19892023-07-0113783810.3390/metabo13070838Metabolic Regulation of Copper Toxicity during Marine Mussel EmbryogenesisTim Young0Samantha L. Gale1Norman L. C. Ragg2Sylvia G. Sander3David J. Burritt4Billy Benedict5Dung V. Le6Silas G. Villas-Bôas7Andrea C. Alfaro8Aquaculture Biotechnology Research Group, Department of Environmental Science, School of Science, Auckland University of Technology, Auckland 1010, New ZealandCawthron Institute, Nelson 7010, New ZealandCawthron Institute, Nelson 7010, New ZealandDepartment of Chemistry, University of Otago, P.O. Box 56, Dunedin 9010, New ZealandDepartment of Botany, University of Otago, 464 Great King St, Dunedin 9016, New ZealandDepartment of Chemistry, University of Otago, P.O. Box 56, Dunedin 9010, New ZealandAquaculture Biotechnology Research Group, Department of Environmental Science, School of Science, Auckland University of Technology, Auckland 1010, New ZealandSchool of Biological Sciences, University of Auckland, Private Bag 92019, Auckland 1010, New ZealandAquaculture Biotechnology Research Group, Department of Environmental Science, School of Science, Auckland University of Technology, Auckland 1010, New ZealandThe development of new tools for assessing the health of cultured shellfish larvae is crucial for aquaculture industries to develop and refine hatchery methodologies. We established a large-volume ecotoxicology/health stressor trial, exposing mussel (<i>Perna canaliculus</i>) embryos to copper in the presence of ethylenediaminetetraacetic acid (EDTA). GC/MS-based metabolomics was applied to identify potential biomarkers for monitoring embryonic/larval health and to characterise mechanisms of metal toxicity. Cellular viability, developmental abnormalities, larval behaviour, mortality, and a targeted analysis of proteins involved in the regulation of reactive oxygen species were simultaneously evaluated to provide a complementary framework for interpretative purposes and authenticate the metabolomics data. Trace metal analysis and speciation modelling verified EDTA as an effective copper chelator. Toxicity thresholds for <i>P</i>. <i>canaliculus</i> were low, with 10% developmental abnormalities in D-stage larvae being recorded upon exposure to 1.10 μg·L<sup>−1</sup> bioavailable copper for 66 h. Sublethal levels of bioavailable copper (0.04 and 1.10 μg·L<sup>−1</sup>) caused coordinated fluctuations in metabolite profiles, which were dependent on development stage, treatment level, and exposure duration. Larvae appeared to successfully employ various mechanisms involving the biosynthesis of antioxidants and a restructuring of energy-related metabolism to alleviate the toxic effects of copper on cells and developing tissues. These results suggest that regulation of trace metal-induced toxicity is tightly linked with metabolism during the early ontogenic development of marine mussels. Lethal-level bioavailable copper (50.3 μg·L<sup>−1</sup>) caused severe metabolic dysregulation after 3 h of exposure, which worsened with time, substantially delayed embryonic development, induced critical oxidative damage, initiated the apoptotic pathway, and resulted in cell/organism death shortly after 18 h of exposure. Metabolite profiling is a useful approach to (1) assess the health status of marine invertebrate embryos and larvae, (2) detect early warning biomarkers for trace metal contamination, and (3) identify novel regulatory mechanisms of copper-induced toxicity.https://www.mdpi.com/2218-1989/13/7/838metabolomicsecotoxicologycopper speciationaquacultureshellfishmollusc physiology |
| spellingShingle | Tim Young Samantha L. Gale Norman L. C. Ragg Sylvia G. Sander David J. Burritt Billy Benedict Dung V. Le Silas G. Villas-Bôas Andrea C. Alfaro Metabolic Regulation of Copper Toxicity during Marine Mussel Embryogenesis Metabolites metabolomics ecotoxicology copper speciation aquaculture shellfish mollusc physiology |
| title | Metabolic Regulation of Copper Toxicity during Marine Mussel Embryogenesis |
| title_full | Metabolic Regulation of Copper Toxicity during Marine Mussel Embryogenesis |
| title_fullStr | Metabolic Regulation of Copper Toxicity during Marine Mussel Embryogenesis |
| title_full_unstemmed | Metabolic Regulation of Copper Toxicity during Marine Mussel Embryogenesis |
| title_short | Metabolic Regulation of Copper Toxicity during Marine Mussel Embryogenesis |
| title_sort | metabolic regulation of copper toxicity during marine mussel embryogenesis |
| topic | metabolomics ecotoxicology copper speciation aquaculture shellfish mollusc physiology |
| url | https://www.mdpi.com/2218-1989/13/7/838 |
| work_keys_str_mv | AT timyoung metabolicregulationofcoppertoxicityduringmarinemusselembryogenesis AT samanthalgale metabolicregulationofcoppertoxicityduringmarinemusselembryogenesis AT normanlcragg metabolicregulationofcoppertoxicityduringmarinemusselembryogenesis AT sylviagsander metabolicregulationofcoppertoxicityduringmarinemusselembryogenesis AT davidjburritt metabolicregulationofcoppertoxicityduringmarinemusselembryogenesis AT billybenedict metabolicregulationofcoppertoxicityduringmarinemusselembryogenesis AT dungvle metabolicregulationofcoppertoxicityduringmarinemusselembryogenesis AT silasgvillasboas metabolicregulationofcoppertoxicityduringmarinemusselembryogenesis AT andreacalfaro metabolicregulationofcoppertoxicityduringmarinemusselembryogenesis |