COPPER AND MICROPLASTIC EXPOSURE AFFECTS THE GILL GENE EXPRESSION OF COMMON CARP DURING SALTWATER CHALLENGE
DOI:
https://doi.org/10.25271/sjuoz.2024.12.3.1335Keywords:
gene expression, water contamination, carp rearing, osmotic challenge, co-exposureAbstract
The aim of the present study was to assess if pre-exposure to water copper and/or polyvinyl chloride microparticles affects the transcriptional responses of common carp, Cyprinus carpio, to saltwater exposure. Fish were exposed to 0.25 mg/L copper alone (Cu) or in the presence of 0.5 mg/L polyvinyl chloride microparticles (Cu-MPVC) for 14 days, followed by 72 hours of salt water exposure (0 to 13 ppt NaCl). The copper content in the gills and the expression of heat shock protein (hsp70) and cytochrome P450 family 1 (cyp1a) transcripts were examined. The results showed that gill copper levels increased significantly (P = 0.008) in the Cu and Cu-MPVC treatments after 14 days of exposure, compared to the control fish; the Cu and Cu-MPVC treatments had similar gill copper levels. After 14 days of exposure, branchial expression of the hsp70 and cyp1a genes was significantly up-regulated in the Cu and Cu-MPVC treatments. Exposure to salt water led to a significant down-regulation of the gene transcripts in all treatments after 24 h of exposure. At this point, the Cu and Cu-MPVC treatments showed transcripts similar to those of the control fish prior to saltwater exposure. The fish treated with Cu-MPVC showed significantly higher hsp70 expression 72 h after saltwater exposure than the other treatments. At this time point, the control and Cu fish had significantly lower cyp1a expression than before saltwater exposure. In conclusion, the present data suggest that copper exposure induces stress in the fish gills, and the presence of MPCV in the water hampers normal transcriptomic responses of the fish gills to saltwater exposure.
References
Altun, S., Özdemir, S. & Arslan, H. (2017). Histopathological effects, responses of oxidative stress, inflammation, apoptosis biomarkers and alteration of gene expressions related to apoptosis, oxidative stress, and reproductive system in chlorpyrifos-exposed common carp (Cyprinus et al.). Environmental Pollution, 230, 432-443.
Aluru, N. & Vijayan, M. M. (2009). Stress transcriptomics in fish: A role for genomic cortisol signalling. General and Comparative Endocrinology, 164, 142-150.
Banaee, M., Soltanian, S., Sureda, A., Gholamhosseini, A., Haghi, B. N., Akhlaghi, M. & Derikvandy, A. (2019). Evaluation of single and combined effects of cadmium and micro-plastic particles on biochemical and immunological parameters of common carp (Cyprinus carpio). Chemosphere, 236, 124335.
Barus, V., Peaz, M. & Kohlmann, K. (2001) Cyprinus carpio (Linnaeus, 1758). In: The freshwater fishes of Europe (ed. by Banarescu P, Paepke H). Aula Verlag GmbH, Wiebelsheim, Germany, pp. 85-179.
Bengtson Nash, S., Dawson, A., Burkhard, M., Waugh, C. & Huston, W. (2014). Detoxification enzyme activities (CYP1A1 and GST) in the skin of humpback whales as a function of organochlorine burdens and migration status. Aquatic Toxicology, pp. 155, 207–212.
Brun, N. R., van Hage, P., Hunting, E. R., Haramis, A.-P. G., Vink, S. C., Vijver, M. G., Schaaf, M. J. M. & Tudorache, C. (2019) Polystyrene nanoplastics disrupt glucose metabolism and cortisol levels with a possible link to behavioural changes in larval zebrafish. Communications Biology, 2, 382.
Bystriansky, J., Richards, J., Schulte, P. & Ballantyne, J. (2006). Reciprocal expression of gill Na+/K+-ATPaseα-subunit isoforms α1a and α1b during seawater acclimation of three salmonid fishes that vary in their salinity tolerance. Journal of Experimental Biology, p. 209, 1848-1858.
Chao Dang, Z., Flik, G., Ducouret, B., Hogstrand, C., E. Wendelaar Bonga, S. & A.C. Lock, R. (2000). Effects of copper on cortisol receptor and metallothionein expression in gills of Oncorhynchus mykiss. Aquatic Toxicology, 51, 45–54.
Choi, C. Y. (2010). Environmental stress-related gene expression and blood physiological responses in olive flounder (Paralichthys olivaceus) exposed to osmotic and thermal stress. Animal Cells and Systems, pp. 14, 17–23.
Eissa, N., Wang, H.-P., Yao, H., Shen, Z.-G., Shaheen, A. A. & Abou-ElGheit, E. N. (2017). Expression of Hsp70, Igf1, and three oxidative stress biomarkers in response to handling and salt treatment at different water temperatures in yellow perch, Perca flavescens. Frontiers in Physiology, 8, 1-15.
Espinosa, C., Esteban, M. Á. & Cuesta, A. (2019). Dietary administration of PVC and PE microplastics produces histological damage, oxidative stress and immunoregulation in European sea bass (Dicentrarchus labrax L.). Fish & Shellfish Immunology, 95, 574-583.
Eyckmans, M., Tudorache, C., Darras, V. M., Blust, R. & De Boeck, G. (2010). Hormonal and ion regulatory response in three freshwater fish species following waterborne copper exposure. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, pp. 152, 270–278.
Eyckmans, M., Celis, N., Horemans, N., Blust, R. & De Boeck, G. (2011). Exposure to waterborne copper reveals differences in oxidative stress response in three freshwater fish species. Aquatic Toxicology, 103, 112-120.
Ghelichpour, M., Taheri Mirghaed, A. & Zargar, A. (2020). The response of lufenuron‐ and flonicamid‐exposed Cyprinus carpio to saltwater challenge: Study on ion‐regulation and stress genes expression and plasma antioxidant characteristics. Aquaculture Research, 51, 4829-4837.
Ghelichpour, M., Mirghaed, A. T., Mirzargar, S. S., Joshaghani, H. & Mousavi, H. E. (2018). Modification of saltwater stress response in Cyprinus carpio (Linnaeus, 1758) pre-exposed to pesticide indoxacarb. Ecotoxicology and Environmental Safety, 147, 139-143.
Ghelichpour, M., Mirghaed, A. T., Hoseinifar, S. H., Khalili, M., Yousefi, M., Van Doan, H. & Jimenez, A. P. (2019). Expression of immune, antioxidant and stress-related genes in different organs of common carp exposed to indoxacarb. Aquatic Toxicology, 208, 208-216.
Gopi, N., Vijayakumar, S., Thaya, R., Govindarajan, M., Alharbi, N. S., Kadaikunnan, S., Khaled, J. M., Al-Anbr, M. N. & Vaseeharan, B. (2019). Chronic exposure of Oreochromis niloticus to sub-lethal copper concentrations: Effects on growth, antioxidant, non-enzymatic antioxidant, oxidative stress and non-specific immune responses. Journal of Trace Elements in Medicine and Biology, 55, 170-179.
Hoseini, S. M., Khosraviani, K., Hosseinpour Delavar, F., Arghideh, M., Zavvar, F., Hoseinifar, S. H., Van Doan, H., Zabihi, E. & Reverter, M. (2022). Hepatic transcriptomic and histopathological responses of common carp, Cyprinus carpio, to copper and microplastic exposure. Marine Pollution Bulletin, 175, 113401.
Jinhui, S., Sudong, X., Yan, N., Xia, P., Jiahao, Q. & Yongjian, X. (2019). Effects of microplastics and attached heavy metals on growth, immunity, and heavy metal accumulation in the yellow seahorse, Hippocampus kuda Bleeker. Marine Pollution Bulletin, 149, 110510.
Kim, J.-H., Yu, Y.-B. & Choi, J.-H. (2021) Toxic effects on bioaccumulation, haematological parameters, oxidative stress, immune responses and neurotoxicity in fish exposed to microplastics: A review. Journal of Hazardous Materials, 413, 125423.
Kumari, K., Pathakota, G.-B., Kumar, S. & Krishna, G. (2018). Gene structure and comparative and phylogenetic analyses of Catla catla CYP1A full-length cDNA and its responsiveness to benzo(a)pyrene and copper sulphate at early developmental stages. Fish Physiology and Biochemistry, pp. 44, 95–108.
Lavado, R., Aparicio-Fabre, R. & Schlenk, D. (2014). Effects of salinity acclimation on the expression and activity of Phase I enzymes (CYP450 and FMOs) in coho salmon (Oncorhynchus kisutch). Fish Physiology and Biochemistry, 40, 267-278.
Leguen, I., Odjo, N., Le Bras, Y., Luthringer, B., Baron, D., Monod, G. & Prunet, P. (2010) Effect of seawater transfer on CYP1A gene expression in rainbow trout gills. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 156, 211-217.
Lu, K., Qiao, R., An, H. & Zhang, Y. (2018). Influence of microplastics on the accumulation and chronic toxic effects of cadmium in zebrafish (Danio rerio). Chemosphere, pp. 202, 514-520.
Malhotra, N., Ger, T.-R., Uapipatanakul, B., Huang, J.-C., Chen, K. H. C. & Hsiao, C.-D. (2020). Review of copper and copper nanoparticle toxicity in fish. Nanomaterials, 10.
McCormick, S. D., Regish, A. & Christensen, A. (2009). Distinct freshwater and seawater isoforms of Na+/K+-ATPase in gill chloride cells of Atlantic salmon. Journal of Experimental Biology, pp. 212, 3994–4001.
McCormick, S. D., Regish, A., O'Dea, M. F. & Shrimpton, J. M. (2008). Are we missing a mineralocorticoid in teleost fish? Effects of cortisol, deoxycorticosterone and aldosterone on osmoregulation, gill Na+, K+-ATPase activity and isoform mRNA levels in Atlantic salmon. General and Comparative Endocrinology, 157, 35–40.
Naz, S., Hussain, R., Ullah, Q., Chatha, A. M. M., Shaheen, A. & Khan, R. U. (2021). Toxic effect of some heavy metals on haematology and histopathology of major carp (Catla catla). Environmental Science and Pollution Research, pp. 28, 6533–6539.
Nguyen, T. V., Jung, H., Nguyen, T. M., Hurwood, D. & Mather, P. (2016). Evaluation of potential candidate genes involved in salinity tolerance in striped catfish (Pangasianodon hypophthalmus) using an RNA-Seq approach. Marine Genomics, pp. 25, 75-88.
Niu, C. J., Rummer, J. L., Brauner, C. J. & Schulte, P. M. (2008). Heat shock protein (Hsp70) induced by a mild heat shock slightly moderates plasma osmolarity increases upon salinity transfer in rainbow trout (Oncorhynchus mykiss). Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 148, 437-444.
Rahman, M. S. & Thomas, P. (2012). Effects of hypoxia exposure on hepatic cytochrome P450 1A (CYP1A) expression in Atlantic croaker: molecular mechanisms of CYP1A down-regulation. PloS One, 7, e40825.
Roberts, R. J., Agius, C., Saliba, C., Bossier, P. & Sung, Y. Y. (2010). Heat shock proteins (chaperones) in fish and shellfish and their potential role in relation to fish health: a review. Journal of Fish Diseases, 33, 789–801.
Roda, J. F. B., Lauer, M. M., Risso, W. E. & Bueno dos Reis Martinez, C. (2020). Microplastics and copper effects on the neotropical teleost Prochilodus lineatus: Is there any interaction? Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 242, 110659.
Romano, N., Renukdas, N., Fischer, H., Shrivastava, J., Baruah, K., Egnew, N. & Sinha, A. K. (2020). Differential modulation of oxidative stress, antioxidant defence, histomorphology, ion-regulation and growth marker gene expression in goldfish (Carassius auratus) following exposure to different doses of virgin microplastics. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 238, 108862.
Smith, T. R., Tremblay, G. C. & Bradley, T. M. (1999). Hsp70 and a 54 kDa protein (Osp54) are induced in salmon (Salmo salar) in response to hyperosmotic stress. Journal of Experimental Zoology Part A: Ecological and Integrative Physiology, pp. 284, 286–298.
Sonone, S. S., Jadhav, S., Sankhla, M. S. & Kumar, R. (2020). Water contamination by heavy metals and their toxic effect on aquaculture and human health through the food Chain. Letters in applied NanoBioScience, pp. 10, 2148–2166.
Sung, Y., Roberts, R. & Bossier, P. (2012). Enhancement of Hsp70 synthesis protects common carp, Cyprinus carpio L., against lethal ammonia toxicity. Journal of Fish Diseases, 35, 563-568.
Wang, T., Long, X., Liu, Z., Cheng, Y. & Yan, S. (2015). Effect of copper nanoparticles and copper sulphate on oxidation stress, cell apoptosis and immune responses in the intestines of juvenile Epinephelus coioides. Fish & Shellfish Immunology, 44, 674-682.
Wen, B., Jin, S.-R., Chen, Z.-Z., Gao, J.-Z., Liu, Y.-N., Liu, J.-H. & Feng, X.-S. (2018) Single and combined effects of microplastics and cadmium on the cadmium accumulation, antioxidant defence and innate immunity of the discus fish (Symphysodon aequifasciatus). Environmental Pollution, 243, 462-471.
Yu, Z., Dai, Z.-Y., Qin, G.-X., Li, M.-Y. & Wu, L.-F. (2020) Alleviative effects of dietary microbial floc on copper-induced inflammation, oxidative stress, intestinal apoptosis and barrier dysfunction in Rhynchocypris lagowski Dybowski. Fish & Shellfish Immunology, 106, 120–132.
Published
How to Cite
Issue
Section
License
Copyright (c) 2024 Seyyed M. Hoseini, Basim S.A. Al Sulivany2
![Creative Commons License](http://i.creativecommons.org/l/by/4.0/88x31.png)
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License [CC BY-NC-SA 4.0] that allows others to share the work with an acknowledgment of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work, with an acknowledgment of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online.