Korean Journal of Environmental Biology (환경생물)

Korean Society of Environmental Biology (한국환경생물학회)
권호 표지
DOI QR코드

DOI QR Code

Combined toxic effects of water temperature and polystyrene beads in the brackish water flea

기수산 물벼룩에서 수온과 polystyrene beads의 복합 독성

  • Youn-Ha Lee (Department of Biotechnology, College of Convergence Engineering, Sangmyung University) ;
  • Jong-Seok Park (Department of Biotechnology, College of Convergence Engineering, Sangmyung University) ;
  • Chaerin Park (Department of Biotechnology, College of Convergence Engineering, Sangmyung University) ;
  • Sang-Hyun Cho (Department of Biotechnology, College of Convergence Engineering, Sangmyung University) ;
  • Je-Won Yoo (Department of Biotechnology, College of Convergence Engineering, Sangmyung University) ;
  • Young-Mi Lee (Department of Biotechnology, College of Convergence Engineering, Sangmyung University)
  • 이윤하 (상명대학교 융합공과대학 생명공학전공) ;
  • 박종석 (상명대학교 융합공과대학 생명공학전공) ;
  • 박채린 (상명대학교 융합공과대학 생명공학전공) ;
  • 조상현 (상명대학교 융합공과대학 생명공학전공) ;
  • 유제원 (상명대학교 융합공과대학 생명공학전공) ;
  • 이영미 (상명대학교 융합공과대학 생명공학전공)
  • Received : 2023.08.08
  • Accepted : 2023.11.08
  • Published : 2023.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

Microplastics and nanoplastics (NMPs) are considered one of hazardous contaminants in marine ecosystems due to their toxic effects, such as reproduction disorder and oxidative stress, on marine organisms. Although water temperature is rising due to global climate change, little information on the toxicological interaction between NMPs and temperature is available. Therefore, in this study, we confirmed the toxicity of NMPs (polystyrene [PS] beads; 0.05- and 6-㎛) on brackish water fleas (Diaphanosoma celebensis) depending on increased temperature (30℃ and 35℃) at individual and molecular levels. In the chronic toxicity test, the group exposed to high temperatures showed an earlier first reproduction time compared to the normal temperatures group, but it was delayed by co-exposure to NMPs at 35℃. Notably, the total reproduction decreased significantly only after 0.05-㎛ PS beads exposure at 30℃. Interaction analysis showed that first reproduction time, modulation of the antioxidant-related gene (GSTS1), heat shock gene (Hsp70), and ecdysteroid pathway-related genes (EcR_A, EcR_B, and CYP314A1) were closely related to temperature and PS beads size. These results indicate that microplastics have size-dependent toxicity, and their toxicity can be enhanced at high temperatures. In addition, higher temperatures and PS beads exposure may have negative effects on reproduction. This study suggests that various factors such as water temperature should be considered when evaluating the toxicity of microplastics in marine ecosystems, and provides an understanding of the complex toxic interaction between water temperature and microplastics for marine zooplankton.

미세플라스틱과 나노플라스틱(NMPs)은 해양생물에 대한 생식 방해, 산화적 스트레스 등의 부정적 영향을 줄 수 있어 해양생태계의 유해오염물질 중 하나로 간주된다. 전 지구적 기후변화로 해수 온도가 상승하고 있음에도 불구하고 미세플라스틱과 온도변화 간의 독성학적 상호 작용에 대한 연구는 제한적이다. 따라서, 본 연구에서는 기수산 물벼룩 Diaphanosoma celebensis에 대한 NMPs(polystyrene beads; 0.05-, 6-㎛)의 온도 상승에 따른 독성을 개체 및 유전자 수준에서 확인하였다. 개체 수준에서의 첫 생식 시점은 온도 상승에 의해 빨라지는 양상을 보였으나 35℃ 온도 조건에서 PS beads에 노출된 경우 유의하게 지연되었다. 총 산란 수는 30℃, 0.05-㎛ PS beads에 노출된 경우에서만 유의하게 감소하였다. 상호작용 분석결과 첫번째 생식 시점과 항산화 및 열충격 단백질 유전자(GSTS1 및 Hsp70) 및 ecdysteroid 경로 관련 유전자(EcR_A, EcR_B, 및 CYP314A1)가 온도 및 PS 입자 크기에 주로 영향을 받는 것으로 나타났다. 이러한 결과는 미세플라스틱이 크기 의존적인 독성을 가지고 있음을 보여줌과 동시에 온도 증가로 인해 독성이 강화될 수 있음을 의미한다. 본 연구는 미세플라스틱의 독성을 평가할 때 수온 등 다양한 요소 또한 고려되어야 한다는 점을 제시하였으며, 해양동물 플랑크톤에 대한 수온과 미세플라스틱의 복합적 독성 상호작용에 대한 이해를 제공할 수 있을 것이다.

Keywords

References

  1. Bae E, P Samanta, J Yoo and J Jung. 2016. Effects of multigenerational exposure to elevated temperature on reproduction, oxidative stress, and Cu toxicity in Daphnia magna. Ecotox. Environ. Safe. 132:366-371. https://doi.org/10.1016/j.ecoenv.2016.06.034
  2. Cao SS and RJ Kaufman. 2014. Endoplasmic reticulum stress and oxidative stress in cell fate decision and human disease. Antioxid. Redox Signal. 21:396-413. https://doi.org/10.1089/ars.2014.5851
  3. Cho H, CB Jeong and YM Lee. 2022. Modulation of ecdysteroid and juvenile hormone signaling pathways by bisphenol analogues and polystyrene beads in the brackish water flea Diaphanosoma celebensis. Comp. Biochem. Physiol. C-Toxicol. Pharmacol. 262:109462. https://doi.org/10.1016/j.cbpc.2022.109462
  4. Cole M, P Lindeque, E Fileman, C Halsband and TS Galloway. 2015. The impact of polystyrene microplastics on feeding, function and fecundity in the marine copepod Calanus helgolandicus. Environ. Sci. Technol. 49:1130-1137. https://doi.org/10.1021/es504525u
  5. Cozar A, F Echevarria, JI Gonzalez-Gordillo, X Irigoien, B Ubeda, S Hernandez-Leon, AT Palma, S Navarro, J Garcia-de-Lomas, A Ruiz, ML Fernandez-de-Puelles and CM Duarte. 2014. Plastic debris in the open ocean. Proc. Natl. Acad. Sci. U.S.A. 111:10239-10244. https://doi.org/10.1073/pnas.1314705111
  6. Frias JPGL and R Nash. 2019. Microplastics: Finding a consensus on the definition. Mar. Pollut. Bull. 138:145-147. https://doi.org/10.1016/j.marpolbul.2018.11.022
  7. Geyer R, JR Jambeck and KL Law. 2017. Production, use, and fate of all plastics ever made. Sci. Adv. 3:e1700782. https://doi.org/10.1126/sciadv.1700782
  8. Han J, CB Jeong, E Byeon and JS Lee. 2018. Effects of temperature changes on the generation of reactive oxygen species and the expression and activity of glutathione-S transferases in two congeneric copepods Tigriopus japonicus and Tigriopus kingsejongensis. Fish. Sci. 84:815-823. https://doi.org/10.1007/s12562-018-1224-3
  9. Haque MN, SE Nam, BM Kim, K Kim and JS Rhee. 2020. Temperature elevation stage-specifically increases metal toxicity through bioconcentration and impairment of antioxidant defense systems in juvenile and adult marine mysids. Comp. Biochem. Physiol. C-Toxicol. Pharmacol. 237:108831. https://doi.org/10.1016/j.cbpc.2020.108831
  10. Hasan J, MA Siddik, AK Ghosh, SB Mesbah, MA Sadat and M Shahjahan. 2023. Increase in temperature increases ingestion and toxicity of polyamide microplastics in Nile tilapia. Chemosphere 327:138502. https://doi.org/10.1016/j.chemosphere.2023.138502
  11. Huang CH, TW Chu, CH Kuo, MC Hong, YY Chen and B Chen. 2022. Effects of microplastics on reproduction and growth of freshwater live feeds Daphnia magna. Fishes 7:181. https://doi.org/10.3390/fishes7040181
  12. Jaikumar G, J Baas, NR Brun, MG Vijver and T Bosker. 2018. Acute sensitivity of three Cladoceran species to different types of microplastics in combination with thermal stress. Environ. Pollut. 239:733-740. https://doi.org/10.1016/j.envpol.2018.04.069
  13. Jambeck JR, R Geyer, C Wilcox, TR Siegler, M Perryman, A Andrady, R Narayan and KL Law. 2015. Plastic waste inputs from land into the ocean. Science 347:768-771. https://doi.org/10.1126/science.1260352
  14. Jang SW, HS Kang, DY Kang and KS Cho. 2022. Effect of rearing water temperature on growth and physiological response of juvenile chum salmon(Oncorhynchus keta). Korean J. Environ. Biol. 40:651-659. https://doi.org/10.11626/KJEB.2022.40.4.651
  15. Jeon MJ, JW Yoo, KW Lee, EJ Won and YM Lee. 2023. Micro-plastics disrupt energy metabolism in the brackish water flea Diaphanosoma celebensis. Comp. Biochem. Physiol. C-Toxicol. Pharmacol. 271:109680. https://doi.org/10.1016/j.cbpc.2023.109680
  16. Jeong CB, EJ Won, HM Kang, MC Lee, DS Hwang, UK Hwang, B Zhou, S Souissi, SJ Lee and JS Lee. 2016. Microplastic size-dependent toxicity, oxidative stress induction, and p-JNK and p-p38 activation in the monogonont rotifer (Brachionus koreanus). Environ. Sci. Technol. 50:8849-8857. https://doi.org/10.1021/acs.est.6b01441
  17. Juan CA, JM Perez de la Lastra, FJ Plou and E Perez-Lebena. 2021. The chemistry of reactive oxygen species (ROS) revisited: outlining their role in biological macromolecules (DNA, lipids and proteins) and induced pathologies. Int. J. Mol. Sci. 22:4642. https://doi.org/10.3390/ijms22094642
  18. Khan Q and M Khan. 2008. Effect of temperature on waterflea Daphnia magna (Crustacea: Cladocera). Nat. Prec. https://doi.org/10.1038/npre.2008.1909.1
  19. Kim H, JH Kim, SH Kim, Z Suonan and KS Lee. 2022. Photosynthetic and respiratory responses of the surfgrass, Phyllospadix japonicus, to the rising water temperature. Korean J. Environ. Biol. 40:352-362. https://doi.org/10.11626/KJEB.2022.40.3.352
  20. Kumar N, NK Chandan, GC Wakchaure and NP Singh. 2020. Synergistic effect of zinc nanoparticles and temperature on acute toxicity with response to biochemical markers and histopathological attributes in fish. Comp. Biochem. Physiol. C-Toxicol. Pharmacol. 229:108678. https://doi.org/10.1016/j.cbpc.2019.108678
  21. Lafont R and M Mathieu. 2007. Steroids in aquatic invertebrates. Ecotoxicology 16:109-130. https://doi.org/10.1007/s10646-006-0113-1
  22. Lee KW, WJ Shim, OY Kwon and JH Kang. 2013. Size-dependent effects of micro polystyrene particles in the marine copepod Tigriopus japonicus. Environ. Sci. Technol. 47:11278-11283. https://doi.org/10.1021/es401932b
  23. Liu T, CK Daniels and S Cao. 2012. Comprehensive review on the HSC70 functions, interactions with related molecules and involvement in clinical diseases and therapeutic potential. Pharmacol. Ther. 136:354-374. https://doi.org/10.1016/j.pharmthera.2012.08.014
  24. Liu Z, M Cai, P Yu, M Chen, D Wu, M Zhang and Y Zhao. 2018. Age-dependent survival, stress defense, and AMPK in Daphnia pulex after short-term exposure to a polystyrene nanoplastic. Aquat. Toxicol. 204:1-8. https://doi.org/10.1016/j.aquatox.2018.08.017
  25. Livak KJ and TD Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402-408. https://doi.org/10.1006/meth.2001.1262
  26. Lu Y, Y Zhang, Y Deng, W Jiang, Y Zhao, J Geng, L Din and H Ren. 2016. Uptake and accumulation of polystyrene microplastics in zebrafish (Danio rerio) and toxic effects in liver. Environ. Sci. Technol. 50:4054-4060. https://doi.org/10.1021/acs.est.6b00183
  27. Luo S, S Jin, L Su and J Wang. 2017. Effect of water temperature on reproductive performance and offspring quality of rare minnow, Gobiocypris rarus. J. Therm. Biol. 67:59-66. https://doi.org/10.1016/j.jtherbio.2017.05.002
  28. Magnani F and A Mattevi. 2019. Structure and mechanisms of ROS generation by NADPH oxidases. Curr. Opin. Struct. Biol. 59:91-97. https://doi.org/10.1016/j.sbi.2019.03.001
  29. Mailloux RJ. 2020. An update on mitochondrial reactive oxygen species production. Antioxidants 9:472. https://doi.org/10.3390/antiox9060472
  30. Marcial HS and A Hagiwara. 2007. Multigenerational effects of 17β-estradiol and nonylphenol on euryhaline cladoceran Diaphanosoma celebensis. Fish. Sci. 73:324-330. https://doi.org/10.1111/j.1444-2906.2007.01338.x
  31. Mayer MP and B Bukau. 2005. Hsp70 chaperones: cellular functions and molecular mechanism. Cell. Mol. Life Sci. 62:670-684. https://doi.org/10.1007/s00018-004-4464-6
  32. Niwa YS and R Niwa. 2016. Transcriptional regulation of insect steroid hormone biosynthesis and its role in controlling timing of molting and metamorphosis. Dev. Growth Diff. 58:94-105. https://doi.org/10.1111/dgd.12248
  33. Oghbaei H, L Hosseini, F Farajdokht, SR Aghsan, A Majdi, S Sadigh-Eteghad, SS Shotorani and J Mahmoudi. 2021. Heat stress aggravates oxidative stress, apoptosis, and endoplasmic reticulum stress in the cerebellum of male C57 mice. Mol. Biol. Rep. 48:5881-5887. https://doi.org/10.1007/s11033-021-06582-9
  34. Pandi P, J Madhuvandhi, KK Priya, R Thiagarajan, S Gopalakrishnan, S Elumalai and H Thilagam. 2022. Weathered polyethylene microplastics exposure leads to modulations in glutathione-S-transferase activity in fish. Front. Mar. Sci. 9:990351. https://doi.org/10.3389/fmars.2022.990351
  35. Park JC and HG Park. 2010. Optimum salinity and temperature condition for mass culture of the brackish water flea, Diaphanosoma celebensis. Korean J. Fish. Aquat. Sci. 43:139-145. https://doi.org/10.5657/kfas.2010.43.2.139
  36. Park K and IS Kwak. 2014. The effect of temperature gradients on endocrine signaling and antioxidant gene expression during Chironomus riparius development. Sci. Total Environ. 470:1003-1011. https://doi.org/10.1016/j.scitotenv.2013.10.052
  37. Patra RW, JC Chapman, RP Lim, PC Gehrke and RM Sunderam. 2015. Interactions between water temperature and contaminant toxicity to freshwater fish. Environ. Toxicol. Chem. 34:1809-1817. https://doi.org/10.1002/etc.2990
  38. Rahman MS and MS Rahman. 2021. Effects of elevated temperature on prooxidant-antioxidant homeostasis and redox status in the American oyster: Signaling pathways of cellular apoptosis during heat stress. Environ. Res. 196:110428. https://doi.org/10.1016/j.envres.2020.110428
  39. Rico-Martinez R and SI Dodson. 1992. Culture of the rotifer Brachionus calyciflorus Pallas. Aquaculture 105:191-199. https://doi.org/10.1016/0044-8486(92)90130-D
  40. Serra T, A Barcelona, N Pous, V Salvado and J Colomer. 2020. Synergistic effects of water temperature, microplastics and ammonium as second and third order stressors on Daphnia magna. Environ. Pollut. 267:115439. https://doi.org/10.1016/j.envpol.2020.115439
  41. Sussarellu R, M Suquet, Y Thomas, C Lambert, C Fabioux, MEJ Pernet, NL Goic, V Quillien, C Mingant, Y Epelboin, C Corporeau, J Guyomarch, J Robbens, I Paul-Pont, P Soudant and A Huvet. 2016. Oyster reproduction is affected by exposure to polystyrene microplastics. Proc. Natl. Acad. Sci. U. S. A. 113:2430-2435. https://doi.org/10.1073/pnas.1519019113
  42. Trestrail C, D Nugegoda and J Shimeta. 2020. Invertebrate responses to microplastic ingestion: Reviewing the role of the antioxidant system. Sci. Total Environ. 734:138559. https://doi.org/10.1016/j.scitotenv.2020.138559
  43. Wong LL and DT Do. 2017. The role of heat shock proteins in response to extracellular stress in aquatic organisms. pp. 247-274. In: Heat Shock Proteins in Veterinary Medicine and Sciences(Asea A and P Kaur, eds.). Springer. Berlin, Germany. https://doi.org/10.1007/978-3-319-73377-7_9
  44. Xie SP, C Deser, GA Vecchi, J Ma, H Teng and AT Wittenberg. 2010. Global warming pattern formation: Sea surface temperature and rainfall. J. Clim. 23:966-986. https://doi.org/10.1175/2009JCLI3329.1
  45. Xu DX, S Zhou and H Yang. 2018. RNA-seq based transcriptional analysis reveals dynamic genes expression profiles and immune-associated regulation under heat stress in Apostichopus japonicus. Fish Shellfish Immunol. 78:169-176. https://doi.org/10.1016/j.fsi.2018.04.037
  46. Yoo JW, H Cho, MJ Jeon, CB Jeong, JH Jung and YM Lee. 2021. Effects of polystyrene in the brackish water flea Diaphanosoma celebensis: Size-dependent acute toxicity, ingestion, egestion, and antioxidant response. Aquat. Toxicol. 235:105821. https://doi.org/10.1016/j.aquatox.2021.105821
  47. Yoo JW, MJ Jeon, KW Lee, JH Jung, CB Jeong and YM Lee. 2022. The single and combined effects of mercury and polystyrene plastic beads on antioxidant-related systems in the brackish water flea: Toxicological interaction depending on mercury species and plastic bead size. Aquat. Toxicol. 252:106325. https://doi.org/10.1016/j.aquatox.2022.106325
  48. Yoon SJ and JH Park. 2022. Behavioral responses and tolerance limits of wild goldeye rockfish Sebastes thompsoni to high temperature exposure. Korean J. Environ. Biol. 40:247-254. https://doi.org/10.11626/KJEB.2022.40.3.247
  49. Yu H, L Shi, P Fan, B Xi and W Tan. 2022. Effects of conventional versus biodegradable microplastic exposure on oxidative stress and gut microorganisms in earthworms: A comparison with two different soils. Chemosphere 307:135940. https://doi.org/10.1016/j.chemosphere.2022.135940
  50. Zbyszewski M, PL Corcoran and A Hockin. 2014. Comparison of the distribution and degradation of plastic debris along shorelines of the Great Lakes, North America. J. Gt. Lakes Res. 40:288-299. https://doi.org/10.1016/j.jglr.2014.02.012
  51. Zhang C, J Wang, Z Pan, S Wang, L Zhang, Q Wang, Q Ye, A Zhou, S Xie, F Zeng, G Xu and J Zou. 2021. A dosage-effect assessment of acute toxicology tests of microplastic exposure in filter-feeding fish. Fish Shellfish Immunol. 113:154-161. https://doi.org/10.1016/j.fsi.2021.04.010
  52. Zhou J, L Wang, Y Xin, WN Wang, WY He, AL Wang and Y Liu. 2010. Effect of temperature on antioxidant enzyme gene expression and stress protein response in white shrimp, Litopenaeus vannamei. J. Therm. Biol. 35:284-289. https://doi.org/10.1016/j.jtherbio.2010.06.004
  53. Zhu J, L Chen, G Sun and AS Raikhel. 2006. The competence factor βFtz-F1 potentiates ecdysone receptor activity via recruiting a p160/SRC coactivator. Mol. Cell. Biol. 26:9402-9412. https://doi.org/10.1128/MCB.01318-06