Potential genotoxicity impacts of a co-exposure of polypropylene microplastic and antibiotics to freshwater pearl mussel Hyriopsis cumingii (Lea, 1852)

Ngoc Tuan Nguyen; Danh Thien Nguyen; Gia Minh Tu Pham; Huong Mai

doi:10.15625/2525-2518/19276

Author affiliations

Authors

Ngoc Tuan Nguyen Vietnam National University of Agriculture, Trau Quy, Gia Lam, Ha Noi, Viet Nam
Danh Thien Nguyen University of Science and Technology of Hanoi, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, Cau Giay, Ha Noi, Viet Nam https://orcid.org/0000-0002-0386-0538
Gia Minh Tu Pham University of Science and Technology of Hanoi, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, Cau Giay, Ha Noi, Viet Nam https://orcid.org/0009-0000-2458-4010
Huong Mai University of Science and Technology of Hanoi, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, Cau Giay, Ha Noi, Viet Nam https://orcid.org/0000-0001-6791-1050

DOI:

https://doi.org/10.15625/2525-2518/19276

Keywords:

polypropylene, sulfamethoxazole, oxytetracycline, genotoxicity, Hyriopsis cumingii

Abstract

Microplastics (MPs) are becoming ubiquitous, and their environmental fate is becoming an issue concern. MPs can adsorb antibiotics to coexist and accumulate in the aquatic environment in the form of complexes, resulting in unforeseeable adverse consequences. Herein, we investigated the genotoxic effects of coexist of polypropylene (PP) microplastic and two antibiotics of sulfamethoxazole (SMX) and oxytetracycline (OTC) at environmental concentrations on gill and gastrointestinal tract (GIT) cells of freshwater pearl mussel Hyriopsis cumingii. Results showed that coexist of PP and antibiotics SMX and OTC at environmental concentrations can cause the DNA damage (5.0 – 8.7% in gill and 4.5 7.9 % in GIT) and micronucleus (10.8 – 20.9 ‰ in gill and 11.9 – 18.6 ‰ in GIT) for H. cumingii. By principal component analysis, we found that there was a strong relationship between microplastic accumulation in the GIT and biomarkers, including DNA damage and micronucleus, for H. cumingii co-exposed to PP microplatics in combination with only OTC antibiotic. Meanwhile, only a strong correlation was detected between microplatic accumulation in gill or GIT and DNA damage in those tisues, when H. cumingii was exposed to mixing anibiotics OTC and SMX along with PP microplastic. Our study contributed to improve the understanding of the adverse genetic impacts of coexistance of PP microplastics and antibiotics (SMX and OTC) in the environment as well as to provided essential information for ecological risk assessment of MPs and antibiotics pollution.

Downloads

Download data is not yet available.

References

Avio C. G., Gorbi S., Milan M., Benedetti M., Fattorini D., d'Errico G., Pauletto M., Bargelloni L., Regoli F. - Pollutants bioavailability and toxicological risk from microplastics to marine mussels. Environmental Pollution 198 (2015) 211-222. https://doi.org/10.1016/j.envpol.2014.12.021

2. Berber A. A. - Genotoxic evaluation of polystyrene microplastic. Sakarya University Journal of Science 23 (2019) 358-367. 10.16984/saufenbilder.455574

3. Bobori D. C., Dimitriadi A., Feidantsis K., Samiotaki A., Fafouti D., Sampsonidis I., Kalogiannis S., Kastrinaki G., Lambropoulou D. A., Kyzas G. Z., Koumoundouros G., Bikiaris D. N., Kaloyianni M. - Differentiation in the expression of toxic effects of polyethylene-microplastics on two freshwater fish species: Size matters. Science of The Total Environment 830 (2022) 154603. https://doi.org/10.1016/j.scitotenv.2022.154603

4. Choi J. S., Hong S. H., Park J.-W. - Evaluation of microplastic toxicity in accordance with different sizes and exposure times in the marine copepod Tigriopus japonicus. Marine Environmental Research 153 (2020) 104838. https://doi.org/10.1016/j.marenvres.2019.104838

5. Wang F., Shih K. M., Li X. Y. - The partition behavior of perfluorooctanesulfonate (PFOS) and perfluorooctanesulfonamide (FOSA) on microplastics. Chemosphere 119 (2015) 841-847. https://doi.org/10.1016/j.chemosphere.2014.08.047

6. Wu C., Zhang K., Huang X., Liu J. - Sorption of pharmaceuticals and personal care products to polyethylene debris. Environmental Science and Pollution Research 23 (2016) 8819-8826. 10.1007/s11356-016-6121-7

7. Yu Z., Yan C., Qiu D., Zhang X., Wen C., Dong S. - Accumulation and ecotoxicological effects induced by combined exposure of different sized polyethylene microplastics and oxytetracycline in zebrafish. Environmental Pollution 319 (2023) 120977. https://doi.org/10.1016/j.envpol.2022.120977

8. Granby K., Rainieri S., Rasmussen R. R., Kotterman M. J. J., Sloth J. J., Cederberg T. L., Barranco A., Marques A., Larsen B. K. - The influence of microplastics and halogenated contaminants in feed on toxicokinetics and gene expression in European seabass (Dicentrarchus labrax). Environmental Research 164 (2018) 430-443. https://doi.org/10.1016/j.envres.2018.02.035

9. Le Bihanic F., Clérandeau C., Cormier B., Crebassa J.-C., Keiter S. H., Beiras R., Morin B., Bégout M.-L., Cousin X., Cachot J. - Organic contaminants sorbed to microplastics affect marine medaka fish early life stages development. Marine Pollution Bulletin 154 (2020) 111059. https://doi.org/10.1016/j.marpolbul.2020.111059

10. Zhang J., Meng H., Kong X., Cheng X., Ma T., He H., Du W., Yang S., Li S., Zhang L. - Combined effects of polyethylene and organic contaminant on zebrafish (Danio rerio): Accumulation of 9-Nitroanthracene, biomarkers and intestinal microbiota. Environmental Pollution 277 (2021) 116767. https://doi.org/10.1016/j.envpol.2021.116767

11. Li X., Luo J., Zeng H., Zhu L., Lu X. - Microplastics decrease the toxicity of sulfamethoxazole to marine algae (Skeletonema costatum) at the cellular and molecular levels. Science of The Total Environment 824 (2022) 153855. https://doi.org/10.1016/j.scitotenv.2022.153855

12. Doan Thi O., Duong Thi T., Nguyen Thi Nhu H., Hoang Thi Q., Le Thi Phuong Q., Duong Hong P., Le Phuong T., Bui Huyen T. - Preliminary results on microplastics in surface water from the downstream of the Day River. Vietnam Journal of Earth Sciences, (2021)10.15625/2615-9783/16504

13. Egessa R., Nankabirwa A., Ocaya H., Pabire W. G. - Microplastic pollution in surface water of Lake Victoria. Science of The Total Environment 741 (2020) 140201. https://doi.org/10.1016/j.scitotenv.2020.140201

14. Hwang J., Choi D., Han S., Choi J., Hong J. - An assessment of the toxicity of polypropylene microplastics in human derived cells. Science of The Total Environment 684 (2019) 657-669. https://doi.org/10.1016/j.scitotenv.2019.05.071

15. Rodriguez-Mozaz S., Vaz-Moreira I., Varela Della Giustina S., Llorca M., Barceló D., Schubert S., Berendonk T. U., Michael-Kordatou I., Fatta-Kassinos D., Martinez J. L., Elpers C., Henriques I., Jaeger T., Schwartz T., Paulshus E., O'Sullivan K., Pärnänen K. M. M., Virta M., Do T. T., Walsh F., Manaia C. M. - Antibiotic residues in final effluents of European wastewater treatment plants and their impact on the aquatic environment. Environment International 140 (2020) 105733. https://doi.org/10.1016/j.envint.2020.105733

16. Danner M.-C., Robertson A., Behrends V., Reiss J. - Antibiotic pollution in surface fresh waters: Occurrence and effects. Science of The Total Environment 664 (2019) 793-804. https://doi.org/10.1016/j.scitotenv.2019.01.406

17. Nguyen Dang Giang C., Sebesvari Z., Renaud F., Rosendahl I., Hoang Minh Q., Amelung W. - Occurrence and Dissipation of the Antibiotics Sulfamethoxazole, Sulfadiazine, Trimethoprim, and Enrofloxacin in the Mekong Delta, Vietnam. PLOS ONE 10 (2015) e0131855. 10.1371/journal.pone.0131855

18. Van Hoi B., Vu C.-T., Phung-Thi L.-A., Thi Nguyen T., Nguyen P. T., Mai H., Le P.-T., Nguyen T.-H., Thanh Duong D., Nguyen Thi H., Le-Van D., Chu D. B. - Determination of Pharmaceutical Residues by UPLC-MS/MS Method: Validation and Application on Surface Water and Hospital Wastewater. Journal of Analytical Methods in Chemistry 2021 (2021) 6628285. 10.1155/2021/6628285

19. Binh V. N., Dang N., Anh N. T. K., Ky L. X., Thai P. K. - Antibiotics in the aquatic environment of Vietnam: Sources, concentrations, risk and control strategy. Chemosphere 197 (2018) 438-450. https://doi.org/10.1016/j.chemosphere.2018.01.061

20. Zhu W., Yang D., Chang L., Zhang M., Zhu L., Jiang J. - Animal gut microbiome mediates the effects of antibiotic pollution on an artificial freshwater system. Journal of Hazardous Materials 425 (2022) 127968. https://doi.org/10.1016/j.jhazmat.2021.127968

21. Chen H., Liu S., Xu X.-R., Zhou G.-J., Liu S.-S., Yue W.-Z., Sun K.-F., Ying G.-G. - Antibiotics in the coastal environment of the Hailing Bay region, South China Sea: Spatial distribution, source analysis and ecological risks. Marine Pollution Bulletin 95 (2015) 365-373. https://doi.org/10.1016/j.marpolbul.2015.04.025

22. Cardoso O., Porcher J.-M., Sanchez W. - Factory-discharged pharmaceuticals could be a relevant source of aquatic environment contamination: Review of evidence and need for knowledge. Chemosphere 115 (2014) 20-30. https://doi.org/10.1016/j.chemosphere. 2014.02.004

23. Chen S., Shen Z., Ding J., Qu M., Li T., Tong M., Di Y. - Sulfamethoxazole induced systematic and tissue-specific antioxidant defense in marine mussels (Mytilus galloprovincialis): Implication of antibiotic’s ecotoxicity. Chemosphere 279 (2021) 130634. https://doi.org/10.1016/j.chemosphere.2021.130634

24. Iftikhar N., Zafar R., Hashmi I. - Multi-biomarkers approach to determine the toxicological impacts of sulfamethoxazole antibiotic on freshwater fish Cyprinus carpio. Ecotoxicology and Environmental Safety 233 (2022) 113331. https://doi.org/10.1016/j.ecoenv.2022.113331

25. Rutkoski C. F., Grott S. C., Israel N. G., Carneiro F. E., de Campos Guerreiro F., Santos S., Horn P. A., Trentini A. A., Barbosa da Silva E., Coelho de Albuquerque C. A., Alves T. C., Alves de Almeida E. - Hepatic and blood alterations in Lithobates catesbeianus tadpoles exposed to sulfamethoxazole and oxytetracycline. Chemosphere 307 (2022) 136215. https://doi.org/10.1016/j.chemosphere.2022.136215

26. Xu X., Xu Y., Xu N., Pan B., Shu F., Ni J. - Bioaccumulation of pharmaceuticals and personal care products (PPCPs) in freshwater pearl mussels Hyriopsis cumingii in Poyang Lake. Marine Pollution Bulletin 193 (2023) 115221. https://doi.org/10.1016/j.marpolbul.2023.115221

27. Li Z., Lu T., Li M., Mortimer M., Guo L.-H. - Direct and gut microbiota-mediated toxicities of environmental antibiotics to fish and aquatic invertebrates. Chemosphere, 329 (2023) 138692. https://doi.org/10.1016/j.chemosphere.2023.138692

28. Qu M., Xu J., Yang Y., Li R., Li T., Chen S., Di Y. - Assessment of sulfamethoxazole toxicity to marine mussels (Mytilus galloprovincialis): Combine p38-MAPK signaling pathway modulation with histopathological alterations. Ecotoxicology and Environmental Safety 249 (2023) 114365. https://doi.org/10.1016/j.ecoenv.2022.114365

29. Yu Z., Zhang L., Huang Q., Dong S., Wang X., Yan C. - Combined effects of micro-/nano-plastics and oxytetracycline on the intestinal histopathology and microbiome in zebrafish (Danio rerio). Science of The Total Environment 843 (2022) 156917. https://doi.org/10.1016/j.scitotenv.2022.156917

30. Li X., Luo J., Han C., Lu X. - Nanoplastics enhance the intestinal damage and genotoxicity of sulfamethoxazole to medaka juveniles (Oryzias melastigma) in coastal environment. Science of The Total Environment 894 (2023) 164943. https://doi.org/10.1016/j.scitotenv.2023.164943

31. Lien L. T., Hoa N. Q., Chuc N. T., Thoa N. T., Phuc H. D., Diwan V., Dat N. T., Tamhankar A. J., Lundborg C. S. - Antibiotics in Wastewater of a Rural and an Urban Hospital before and after Wastewater Treatment, and the Relationship with Antibiotic Use-A One Year Study from Vietnam. Int J Environ Res Public Health 13 (2016)10.3390/ijerph13060588

32. Mai H., Cachot J., Brune J., Geffard O., Belles A., Budzinski H., Morin B. - Embryotoxic and genotoxic effects of heavy metals and pesticides on early life stages of Pacific oyster (Crassostrea gigas). Marine Pollution Bulletin 64 (2012) 2663-2670. https://doi.org/10.1016/j.marpolbul.2012.10.009

33. Le Bihanic F., Clérandeau C., Le Menach K., Morin B., Budzinski H., Cousin X., Cachot J. - Developmental toxicity of PAH mixtures in fish early life stages. Part II: adverse effects in Japanese medaka. Environmental Science and Pollution Research 21 (2014) 13732-13743. 10.1007/s11356-014-2676-3

34. Collins A. R. - The comet assay for DNA damage and repair. Molecular Biotechnology 26 (2004) 249-261. 10.1385/MB:26:3:249

35. Kissling G. E., Dertinger S. D., Hayashi M., MacGregor J. T. - Sensitivity of the erythrocyte micronucleus assay: Dependence on number of cells scored and inter-animal variability. Mutation Research/Genetic Toxicology and Environmental Mutagenesis 634 (2007) 235-240. https://doi.org/10.1016/j.mrgentox.2007.07.010

36. Juan C. A., Pérez de la Lastra J. M., Plou F. J., Pérez-Lebeña E. - The Chemistry of Reactive Oxygen Species (ROS) Revisited: Outlining Their Role in Biological Macromolecules (DNA, Lipids and Proteins) and Induced Pathologies. International Journal of Molecular Sciences 22 (2021) 4642.

37. Kovalakova P., Cizmas L., McDonald T. J., Marsalek B., Feng M., Sharma V. K. - Occurrence and toxicity of antibiotics in the aquatic environment: A review. Chemosphere 251 (2020) 126351. https://doi.org/10.1016/j.chemosphere.2020.126351