Sains Malaysiana 53(8)(2024): 1729-1739

http://doi.org/10.17576/jsm-2024-5308-01

 

Synergistic Developmental Toxicity and Apoptosis of BPA and Zn Co-Exposure in Daphnia magna

 (Ketoksikan Perkembangan Sinergi dan Apoptosis Pendedahan BPA dan Zn Co dalam Daphnia magna)

 

NAIMA HAMID1,2,*, AISHAH BINTI ARIFIN1 & ONG MENG CHUAN1,2

 

1Faculty of Science and Marine Environment, Universiti Malaysia Terengganu, 21030 Kuala Nerus, Terengganu, Malaysia

2Ocean Pollution and Ecotoxicology (OPEC) Research Group, Universiti Malaysia Terengganu, 21030 Kuala Nerus, Terengganu, Malaysia

 

Received: 21 March 2024/Accepted: 28 June 2024

 

Abstract

The combined effects of chemical pollutants in the aqueous environment create inevitable impacts on aquatic ecosystems. Bisphenol A (BPA) is identified as a chemical pollutant of significant concern, primarily owing to its pronounced toxicity in the freshwater environment. Similarly, essential elements like zinc (Zn) may induce toxic effects upon alterations in their metal speciation, leading to increased bioavailability. Therefore, the present study aimed to elucidate the developmental toxicity effects using fresh water model Daphnia magna. Using environment-relevant BPA (10 µg/L and 20 µg/L) and Zn (10 µg/L and 30 µg/L) levels were exposed to Daphnia magna for 48 h to determine the acute toxicity. Results showed that maximum mortality (40%) was observed at a high exposure dose of BPA and Zn at 48 h. Similarly, a significant dose-dependent reduction in heartbeat and body weight was found in all samples. Blood clotting, broken antenna, missing tail changes in the carapace, and bioaccumulation, were the dominant morphological changes in all treatments. These findings were confirmed with the elevated apoptosis at the second antenna, gut, and post-abdominal regions after high-dose treatment. Spearman correlation analysis showed a significant positive correlation (R2 = 0.86) between mortality and deformity ratio indicating high joint toxicity of BPA and Zn. Lastly, more in-depth studies are required to highlight the combined toxicity of the BPA and Zn and ensure ecological integrity.

 

Keywords: Acute toxicity; Bisphenol A; Daphnia magna; emerging pollutants; heavy metals

 

Abstrak

Kesan gabungan pencemar kimia dalam persekitaran akuatik memberi kesan yang tidak dapat dielakkan terhadap ekosistem akuatik. Bisfenol A (BPA) dikenal pasti sebagai pencemar kimia yang memberi perhatian utama, terutamanya disebabkan ketoksikan yang ketara dalam persekitaran air tawar. Demikian juga, unsur-unsur penting seperti zink (Zn) boleh menyebabkan kesan toksik apabila terdapat perubahan dalam spesiasi logam mereka, mengakibatkan peningkatan bioketersediaan. Oleh itu, kajian ini bertujuan untuk menerangkan kesan ketoksikan perkembangan dengan menggunakan model air tawar Daphnia magna. Dengan menggunakan tahap BPA (10 µg/L dan 20 µg/L) dan Zn (10 µg/L dan 30 µg/L) yang relevan dengan alam sekitar, Daphnia magna terdedah selama 48 jam untuk menentukan ketoksikan akut. Keputusan menunjukkan bahawa kematian maksimum (40%) diperhatikan pada dos pendedahan tinggi BPA dan Zn pada 48 jam. Begitu juga, pengurangan berdasarkan dos yang signifikan dalam kadar degupan jantung dan berat badan ditemui dalam semua sampel. Pengerutan darah, patah antena, perubahan ekor yang hilang dalam karapas, dan bioakumulasi, adalah perubahan morfologi dominan dalam semua rawatan. Penemuan ini disahkan dengan peningkatan apoptosis pada antena kedua, usus dan kawasan post-abdomen selepas rawatan dos tinggi. Analisis korelasi Spearman mendedahkan korelasi positif yang signifikan (R2 = 0.86) antara kadar kematian dan nisbah kecacatan, menunjukkan ketoksikan gabungan yang tinggi bagi BPA dan Zn. Kesimpulannya, kajian yang lebih mendalam diperlukan untuk menonjolkan ketoksikan gabungan BPA dan Zn serta memastikan integriti ekologi.

 

Kata kunci: Bisfenol A; Daphnia magna; kemunculan bahan pencemar; ketoksikan akut; logam berat

 

REFERENCES

Chen, L., Hu, C., Guo, Y., Shi, Q. & Zhou, B. 2019. TiO2 nanoparticles and BPA are combined to impair the development of offspring zebrafish after parental coexposureChemosphere 217: 732-741.

Chen, Q., Yin, D., Jia, Y., Schiwy, S., Legradi, J., Yang, S. & Hollert, H. 2017. Enhanced uptake of BPA in the presence of nanoplastics can lead to neurotoxic effects in adult zebrafish.  Science of the Total Environment 609: 1312-1321.

Chen, S., Li, X., Li, H., Yuan, S., Li, J. & Liu, C. 2021. Greater toxic potency of bisphenol AF than bisphenol A in growth, reproduction, and transcription of genes in Daphnia magnaEnvironmental Science and Pollution Research 28(20): 25218-25227.

Grzesiuk, M., Pijanowska, J., Markowska, M. & Bednarska, A. 2020. Morphological deformation of Daphnia magna embryos caused by prolonged exposure to ibuprofen. Environmental Pollution 261: 114135.

Hamid, N., Junaid, M., Manzoor, R., Jia, P-P. & Pei, D-S. 2020. Prioritizing phthalate esters (PAEs) using experimental in vitro/vivo toxicity assays and computational in silico approaches.  Journal of Hazardous Materials 398: 122851.

Heijerick, D.G., Janssen, C.R. & De Coen, W.M. 2003. The combined effects of hardness, pH, and dissolved organic carbon on the chronic toxicity of Zn to D. magna: Development of a surface response model. Archives of Environmental Contamination and Toxicology 44: 0210-0217.

Houde, M., Douville, M., Giraudo, M., Jean, K., Lépine, M., Spencer, C. & O De Silva, A. 2016. Endocrine-disruption potential of perfluoroethylcyclohexane sulfonate (PFECHS) in chronically exposed Daphnia magna. Environmental Pollution 218: 950-956.

Hyne, R.V., Pablo, F., Julli, M. & Markich, S.J. 2005. Influence of water chemistry on the acute toxicity of copper and zinc to the cladoceran Ceriodaphnia cf dubiaEnvironmental Toxicology and Chemistry: An International Journal 24(7): 1667-1675.

Kari, S., Subramanian, K., Altomonte, I.A., Murugesan, A., Yli-Harja, O. & Kandhavelu, M. 2022. Programmed cell death detection methods: A systematic review and a categorical comparison. Apoptosis 27(7-8): 482-508. doi: 10.1007/s10495-022-01735-y

Kundu, S., Biswas, A., Ray, A., Roy, S., Das Gupta, S., Ramteke, M.H., Kumar, V. & Das, B.K. 2024. Bisphenol A contamination in Hilsa shad and assessment of potential health hazard: A pioneering investigation in the national river Ganga, India.  Journal of Hazardous Materials 461: 132532. https://doi.org/10.1016/j.jhazmat.2023.132532

Labine, L.M., Oliveira Pereira, E.A., Kleywegt, S., Jobst, K.J., Simpson, A.J. & Simpson, M.J. 2023. Environmental metabolomics uncovers oxidative stress, amino acid dysregulation, and energy impairment in Daphnia magna with exposure to industrial effluents. Environmental Research 234: 116512.

Li, D., Chen, H., Bi, R., Xie, H., Zhou, Y., Luo, Y. & Xie, L. 2018. Individual and binary mixture effects of bisphenol A and lignin-derived bisphenol in Daphnia magna under chronic exposure. Chemosphere 191: 779-786.

Liang, R., He, J., Shi, Y., Li, Z., Sarvajayakesavalu, S., Baninla, Y., Guo, F., Chen, J., Xu, X. & Lu, Y. 2017. Effects of Perfluorooctane sulfonate on immobilization, heartbeat, reproductive and biochemical performance of Daphnia magna. Chemosphere 168: 1613-1618.

Liang, X., Xie, R., He, Y., Li, W., Du, B. & Zeng, L. 2023. Broadening the lens on bisphenols in coastal waters: Occurrence, partitioning, and input fluxes of multiple novel bisphenol S derivatives along with BPA and BPA analogues in the Pearl River Delta, China. Environmental Pollution 322: 121194. https://doi.org/10.1016/j.envpol.2023.121194

Liu, J., Shen, J., Lu, G., Xu, X., Yang, H., Yan, Z. & Chen, W. 2020. Multilevel ecotoxicity assessment of environmentally relevant bisphenol F concentrations in Daphnia magna. Chemosphere 240: 124917.

Liu, J., Zhang, L., Lu, G., Jiang, R., Yan, Z. & Li, Y. 2021. Occurrence, toxicity and ecological risk of Bisphenol A analogues in aquatic environment - A review.  Ecotoxicology and Environmental Safety 208: 111481.

Metruccio, F., Battistoni, M., Di Renzo, F., Bacchetta, R., Santo, N. & Menegola, E. 2024. Teratogenic and neuro-behavioural toxic effects of bisphenol A (BPA) and B (BPB) on Xenopus laevisdevelopment. Reproductive Toxicology 123: 108496. doi: https://doi.org/10.1016/j.reprotox.2023.108496

Miglioli, A., Balbi, T., Besnardeau, L., Dumollard, R. & Canesi, L. 2021. Bisphenol A interferes with first shell formation and development of the serotoninergic system in early larval stages of Mytilus galloprovincialis. Science of The Total Environment 758: 144003. https://doi.org/10.1016/j.scitotenv.2020.144003

Naveira, C., Rodrigues, N., Santos, F.S., Santos, L.N. & Neves, R.A.F. 2021. Acute toxicity of Bisphenol A (BPA) to tropical marine and estuarine species from different trophic groups. Environmental Pollution 268: 115911. https://doi.org/10.1016/j.envpol.2020.115911

Park, H.S., Tayemeh, M.B., Yu, I.J. & Johari, S.A. 2021. Evaluation of silver nanowires (AgNWs) toxicity on reproductive success of Daphnia magna over two generations and their teratogenic effect on embryonic development. Journal of Hazardous Materials 412: 125339.

Price, G.A.V., Stauber, J.L., Jolley, D.F., Koppel, D.J., Van Genderen, E.J., Ryan, A.C. & Holland, A. 2023. Natural organic matter source, concentration, and pH influences the toxicity of zinc to a freshwater microalga. Environmental Pollution 318: 120797. https://doi.org/10.1016/j.envpol.2022.120797

Scopel, C.F.V., Sousa, C., Machado, M.R.F. & Dos Santos, W.G. 2020. BPA toxicity during development of zebrafish embryo. Brazilian Journal of Biology 81: 437-447.

Seyoum, A., Pradhan, A., Jass, J. & Olsson, P-E. 2020. Perfluorinated alkyl substances impede growth, reproduction, lipid metabolism and lifespan in Daphnia magna. Science of The Total Environment 737: 139682. https://doi.org/10.1016/j.scitotenv.2020.139682

Usman, A., Ikhlas, S. & Ahmad, M. 2019. Occurrence, toxicity and endocrine disrupting potential of Bisphenol-B and Bisphenol-F: A mini-review. Toxicology Letters 312: 222-227.

Wang, Q., Chang, Q., Sun, M., Liu, C., Fan, J., Xie, Y. & Deng, X. 2021. The combined toxicity of ultra-small SiO2 nanoparticles and bisphenol A (BPA) in the development of zebrafish. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 248: 109125. https://doi.org/10.1016/j.cbpc.2021.109125

Xie, X., Jin, Y., Ma, Z., Tang, S., Peng, H., Giesy, J.P. & Liu, H. 2019. Underlying mechanisms of reproductive toxicity caused by multigenerational exposure of 2, bromo-4, 6-dinitroaniline (BDNA) to Zebrafish (Danio rerio) at environmental relevant levels. Aquatic Toxicology 216: 105285.

Zhan, C., Zhang, Y., Li, W., Zhang, S., Liu, J., Zhao, Y. & Peng, Y. 2023. Effects of the toxic metal zinc on the growth, development, and reproduction of the wolf spider Pardosa laura through its food Drosophila melanogaster. Chemosphere 344: 140425. https://doi.org/10.1016/j.chemosphere.2023.140425

Zhang, Y., Liu, J., Jing, C., Lu, G., Jiang, R., Zheng, X., He, C. & Ji, W. 2023. Life history traits of low-toxicity alternative bisphenol S on Daphnia magna with short breeding cycles: A multigenerational study. Ecotoxicology and Environmental Safety 253: 114682.

 

*Corresponding author; email: naima@umt.edu.my

 

 

 

 

 

 

 

 

 

 

 

 

 

 

  next