Abstract
Chemical pollution in coastal waters, particularly from agricultural runoff organophosphates, poses a significant threat to marine ecosystems, including coral reefs. Pollutants such as chlorpyrifos (CPF) are widely used in agriculture and have adverse effects on marine life and humans. In this paper, we investigate the impact of CPF on the metamorphosis of a coral reef fish model, the clownfish Amphiprion ocellaris, focusing on the disruption of thyroid hormone (TH) signalling pathways. Our findings reveal that by reducing TH levels, CPF exposure impairs the formation of characteristic white bands in clownfish larvae, indicative of metamorphosis progression. Interestingly, TH treatment can rescue these effects, establishing a direct causal link between CPF effect and TH disruption. The body shape changes occurring during metamorphosis are also impacted by CPF exposure, shape changes are less advanced in CPF-treated larvae than in control conditions. Moreover, transcriptomic analysis elucidates CPF’s effects on all components of the TH signalling pathway. Additionally, CPF induces systemic effects on cholesterol and vitamin D metabolism, DNA repair, and immunity, highlighting its broader TH-independent impacts. Pollutants are often overlooked in marine ecosystems, particularly in coral reefs. Developing and enhancing coral reef fish models, such as Amphiprion ocellaris, offers a more comprehensive understanding of how chemical pollution affects these ecosystems. This approach provides new insights into the complex mechanisms underlying CPF toxicity during fish metamorphosis, shedding light on the broader impact of environmental pollutants on marine organisms.
Highlights
Chlorpyrifos (CPF) is an insecticide widely used in agriculture for the past five decades and has adverse effects on marine life and humans
CPF exposure impairs the formation of characteristic white bands in clownfish larvae, indicative of metamorphosis progression
During metamorphosis, clownfish larvae lose their elongated body shape and transform into miniature ovoid-shaped adults, these shape changes are less advanced in CPF-treated larvae
CPF induces systemic effects on cholesterol and vitamin D metabolism, DNA repair, and immunity, highlighting its broader TH-independent impacts
Competing Interest Statement
The authors have declared no competing interest.
Footnotes
The methods section has been clarified and the order of presentation changed.
Data Availability
Raw reads of bulkRNAseq datasets are available to download under NCBI BioProject accession number PRJNA1138483 (https://www.ncbi.nlm.nih.gov/bioproject/PRJNA1138483)
Counts matrix and code to reproduce the transcriptomics analysis is available at: https://github.com/StefanoVianello/ReynaudVianello_AoceCPF. Lists of all genes in each treatment intersection, as indicated in the text, are also made available.
Acknowledgments
We thank the High Throughput Genomics Core of the Biodiversity Research Center at Academia Sinica for performing the NGS experiments. The core facility is funded by Academia Sinica Core Facility and Innovative Instrument Project (AS-CFII-108-114). We further thank Dr. Mei-Yeh Lu and Ms. Pei-Lin Chao for their assistance and discussion troubleshooting quality-control metrics. We also thank the staff of the ICOB Marine Research Station for superb help for fish husbandry. Work from our laboratory is supported by a Grand Challenge Grant from Academia Sinica and JSPS KAKENHI grant 22H02678 at OIST. L.B. and D.L. have been supported by a grant from Agence Nationale de la Recherche SENSO (ANR19-CE14-0010).