The impact of morphology and size of zinc oxide nanoparticles on its toxicity to the freshwater microalga, Raphidocelis subcapitata

Abstract

Microalgae are key test organisms to assess the effects of chemicals on aquatic ecosystems. Zinc oxide nanoparticles (ZnO NPs) as a widely used metal oxide is considered a potential threat to these primary producers at the base of the food chain. This study investigates the toxicity of ZnO NPs, bulk ZnO, and Zn2+ to the representative of freshwater microalgae, Raphidocelis subcapitata. To examine the effect of shape and size of nanoparticles, two types of spherical ZnO NPs with different sizes (20 and 40 nm) and two types of rod-shaped ZnO NPs with different lengths (100 and 500 nm) were synthesized. Microalgal cells were exposed to eight concentrations of each ZnO NP type from 0.01 to 0.7 mg/L for 96 h. The results showed that 0.7 mg/L of ZnO NP could completely inhibit algal growth. Size did not interfere with toxicity in spherical ZnO NPs, but the toxicity decreased by increasing the size of rod-shaped ZnO NPs. Spherical ZnO NPs acted more destructive to microalgal cells than nanorod shape. The addition of 0.7 mg/L of ZnO nanorods to samples caused 30% cell death, while 50% cell death was observed by adding the same concentration of nanospherical ZnO. Nano ZnO revealed to be more toxic than bulk ZnO and Zn2+. The Zn2+ released from dissolution of ZnO NPs was one of the sources of toxicity, but the ZnO nanostructures were also an important factor in the toxicity.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

References

  1. Adams L, Lyon D, McIntosh A, Alvarez P (2006) Comparative toxicity of nano-scale TiO2, SiO2 and ZnO water suspensions. Water Sci Technol 54:327–334

    Article  CAS  Google Scholar 

  2. Aruoja V, Dubourguier H-C, Kasemets K, Kahru A (2009) Toxicity of nanoparticles of CuO, ZnO and TiO2 to microalgae Pseudokirchneriella subcapitata. Sci Total Environ 407:1461–1468

    Article  CAS  Google Scholar 

  3. Bhuvaneshwari M, Iswarya V, Archanaa S, Madhu GM, Kumar GKS, Nagarajan R, Chandrasekaran N, Mukherjee A (2015) Cytotoxicity of ZnO NPs towards fresh water algae Scenedesmus obliquus at low exposure concentrations in UV-C, visible and dark conditions. Aquat Toxicol 162:29–38

    Article  CAS  Google Scholar 

  4. Blaise C, Férard J-F (2005) Small-scale freshwater toxicity investigations volume 1-toxicity test methods. Springer, Netherlands

    Google Scholar 

  5. Blinova I, Ivask A, Heinlaan M, Mortimer M, Kahru A (2010) Ecotoxicity of nanoparticles of CuO and ZnO in natural water. Environ Pollut 158:41–47

    Article  CAS  Google Scholar 

  6. Bondarenko O, Juganson K, Ivask A, Kasemets K, Mortimer M, Kahru A (2013) Toxicity of Ag, CuO and ZnO nanoparticles to selected environmentally relevant test organisms and mammalian cells in vitro: a critical review. Arch Toxicol 87:1181–1200

    Article  CAS  Google Scholar 

  7. Bondarenko OM, Heinlaan M, Sihtmäe M, Ivask A, Kurvet I, Joonas E, Jemec A, Mannerström M, Heinonen T, Rekulapelly R, Singh S, Zou J, Pyykkö I, Drobne D, Kahru A (2016) Multilaboratory evaluation of 15 bioassays for (eco)toxicity screening and hazard ranking of engineered nanomaterials: FP7 project NANOVALID. Nanotoxicology 10:1229–1242

    Article  CAS  Google Scholar 

  8. Brayner R, Dahoumane SA, Yéprémian C, Djediat C, Meyer M, Couté A, Fiévet F (2010) ZnO nanoparticles: synthesis, characterization, and ecotoxicological studies. Langmuir 26:6522–6528

    Article  CAS  Google Scholar 

  9. Chen P, Powell BA, Mortimer M, Ke PC (2012) Adaptive interactions between zinc oxide nanoparticles and Chlorella sp. Environ Sci Technol 46:12178–12185

    Article  CAS  Google Scholar 

  10. Chen X, O’Halloran J, Jansen MA (2016) The toxicity of zinc oxide nanoparticles to Lemna minor (L.) is predominantly caused by dissolved Zn. Aquat Toxicol 174:46–53

    Article  CAS  Google Scholar 

  11. Debenest T, Petit A-N, Gagné F, Kohli M, Nguyen N, Blaise C (2011) Comparative toxicity of a brominated flame retardant (tetrabromobisphenol a) on microalgae with single and multi-species bioassays. Chemosphere 85:50–55

    Article  CAS  Google Scholar 

  12. Franklin NM, Rogers NJ, Apte SC, Batley GE, Gadd GE, Casey PS (2007) Comparative toxicity of nanoparticulate ZnO, bulk ZnO, and ZnCl2 to a freshwater microalga (Pseudokirchneriella subcapitata): the importance of particle solubility. Environ Sci Technol 41:8484–8490

    Article  CAS  Google Scholar 

  13. Ghaffari S-B, Sarrafzadeh M-H, Fakhroueian Z, Shahriari S, Khorramizadeh MR (2017) Functionalization of ZnO nanoparticles by 3-mercaptopropionic acid for aqueous curcumin delivery: synthesis, characterization, and anticancer assessment. Mater Sci Eng C 79:465–472

    Article  CAS  Google Scholar 

  14. Hajimahmoodi M, Faramarzi MA, Mohammadi N, Soltani N, Oveisi MR, Nafissi-Varcheh N (2010) Evaluation of antioxidant properties and total phenolic contents of some strains of microalgae. J Appl Phycol 22:43–50

    Article  CAS  Google Scholar 

  15. Hou J, Wang X, Hayat T, Wang X (2017) Ecotoxicological effects and mechanism of CuO nanoparticles to individual organisms. Environ Pollut 221:209–217

    Article  CAS  Google Scholar 

  16. Hou J, Liu H, Wang L, Duan L, Li S, Wang X (2018a) Molecular toxicity of metal oxide nanoparticles in Danio rerio. Environ Sci Technol 52:7996–8004

    Article  CAS  Google Scholar 

  17. Hou J, Wu Y, Li X, Wei B, Li S, Wang X (2018b) Toxic effects of different types of zinc oxide nanoparticles on algae, plants, invertebrates, vertebrates and microorganisms. Chemosphere 193:852–860

    Article  CAS  Google Scholar 

  18. Hsiao I-L, Huang Y-J (2011) Effects of various physicochemical characteristics on the toxicities of ZnO and TiO2 nanoparticles toward human lung epithelial cells. Sci Total Environ 409:1219–1228

    Article  CAS  Google Scholar 

  19. Ivask A, Juganson K, Bondarenko O, Mortimer M, Aruoja V, Kasemets K, Blinova I, Heinlaan M, Slaveykova V, Kahru A (2014) Mechanisms of toxic action of ag, ZnO and CuO nanoparticles to selected ecotoxicological test organisms and mammalian cells in vitro: a comparative review. Nanotoxicology 8:57–71

    Article  CAS  Google Scholar 

  20. Juganson K, Ivask A, Blinova I, Mortimer M, Kahru A (2015) NanoE-Tox: new and in-depth database concerning ecotoxicity of nanomaterials. Beilstein J Nanotechnol 6:1788–1804

    Article  CAS  Google Scholar 

  21. Khare P, Sonane M, Pandey R, Ali S, Gupta KC, Satish A (2011) Adverse effects of TiO2 and ZnO nanoparticles in soil nematode, Caenorhabditis elegans. J Biomed Nanotechnol 7:116–117

    Article  CAS  Google Scholar 

  22. Lee W-M, An Y-J (2013) Effects of zinc oxide and titanium dioxide nanoparticles on green algae under visible, UVA, and UVB irradiations: no evidence of enhanced algal toxicity under UV pre-irradiation. Chemosphere 91:536–544

    Article  CAS  Google Scholar 

  23. Li M, Luo Z, Yan Y, Wang Z, Chi Q, Yan C, Xing B (2016) Arsenate accumulation, distribution, and toxicity associated with titanium dioxide nanoparticles in Daphnia magna. Environ Sci Technol 50:9636–9643

    Article  CAS  Google Scholar 

  24. Li J, Schiavo S, Rametta G, Miglietta ML, La Ferrara V, Wu C, Manzo S (2017) Comparative toxicity of nano ZnO and bulk ZnO towards marine algae Tetraselmis suecica and Phaeodactylum tricornutum. Environ Sci Pollut Res 24:6543–6553

    Article  CAS  Google Scholar 

  25. Liu N, Wang Y, Ge F, Liu S, Xiao H (2018) Antagonistic effect of nano-ZnO and cetyltrimethyl ammonium chloride on the growth of Chlorella vulgaris: dissolution and accumulation of nano-ZnO. Chemosphere 196:566–574

    Article  CAS  Google Scholar 

  26. Luo Z, Wang Z, Yan Y, Li J, Yan C, Xing B (2018) Titanium dioxide nanoparticles enhance inorganic arsenic bioavailability and methylation in two freshwater algae species. Environ Pollut 238:631–637

    Article  CAS  Google Scholar 

  27. Machado MD, Soares EV (2015) Use of a fluorescence-based approach to assess short-term responses of the alga Pseudokirchneriella subcapitata to metal stress. J Appl Phycol 27:805–813

    Article  CAS  Google Scholar 

  28. Manzo S, Miglietta ML, Rametta G, Buono S, Di Francia G (2013) Toxic effects of ZnO nanoparticles towards marine algae Dunaliella tertiolecta. Sci Total Environ 445:371–376

    Article  CAS  Google Scholar 

  29. Manzo S, Buono S, Rametta G, Miglietta M, Schiavo S, Di Francia G (2015) The diverse toxic effect of SiO2 and TiO2 nanoparticles toward the marine microalgae Dunaliella tertiolecta. Environ Sci Pollut Res 22:15941–15951

    Article  CAS  Google Scholar 

  30. Miao AJ, Zhang XY, Luo Z, Chen CS, Chin WC, Santschi PH, Quigg A (2010) Zinc oxide–engineered nanoparticles: dissolution and toxicity to marine phytoplankton. Environ Toxicol Chem 29:2814–2822

    Article  CAS  Google Scholar 

  31. Miller WE, Greene JC, Shiroyama T (1978) The Selenastrum capricornutum Printz Algal Assay Bottle Test: Experimental Design, Application, and Data Interpretation Protocol, EPA-600/9–78-018, Corvallis, OR

  32. Miller RJ, Lenihan HS, Muller EB, Tseng N, Hanna SK, Keller AA (2010) Impacts of metal oxide nanoparticles on marine phytoplankton. Environ Sci Technol 44:7329–7334

    Article  CAS  Google Scholar 

  33. Nowack B, Bucheli TD (2007) Occurrence, behavior and effects of nanoparticles in the environment. Environ Pollut 150:5–22

    Article  CAS  Google Scholar 

  34. OECD (2006) OECD Guideline for the Testing of Chemicals no. 201. Freshwater Alga and Cyanobacteria, Growth Inhibition Test

  35. Oukarroum A, Bras S, Perreault F, Popovic R (2012) Inhibitory effects of silver nanoparticles in two green algae, Chlorella vulgaris and Dunaliella tertiolecta. Ecotoxicol Environ Saf 78:80–85

    Article  CAS  Google Scholar 

  36. Peng X, Palma S, Fisher NS, Wong SS (2011) Effect of morphology of ZnO nanostructures on their toxicity to marine algae. Aquat Toxicol 102:186–196

    Article  CAS  Google Scholar 

  37. Raghupathi KR, Koodali RT, Manna AC (2011) Size-dependent bacterial growth inhibition and mechanism of antibacterial activity of zinc oxide nanoparticles. Langmuir 27:4020–4028

    Article  CAS  Google Scholar 

  38. Schiavo S, Oliviero M, Li J, Manzo S (2018) Testing ZnO nanoparticle ecotoxicity: linking time variable exposure to effects on different marine model organisms. Environ Sci Pollut Res 25:4871–4880

    Article  CAS  Google Scholar 

  39. Suman TY, Radhika Rajasree SR, Kirubagaran R (2015) Evaluation of zinc oxide nanoparticles toxicity on marine algae chlorella vulgaris through flow cytometric, cytotoxicity and oxidative stress analysis. Ecotoxicol Environ Saf 113:23–30

    Article  CAS  Google Scholar 

  40. Talebian N, Amininezhad M, Doudi M (2013) Controllable synthesis of ZnO nanoparticles and their morphology-dependent antibacterial and optical properties. J Photochem Photobiol B 120:66–73

    Article  CAS  Google Scholar 

  41. Wong SW, Leung PT, Djurišić A, Leung KM (2010) Toxicities of nano zinc oxide to five marine organisms: influences of aggregate size and ion solubility. Anal Bioanal Chem 396:609–618

    Article  CAS  Google Scholar 

  42. Xiang L, Zhao HM, Li YW, Huang XP, Wu XL, Zhai T, Yuan Y, Cai QY, Mo CH (2015) Effects of the size and morphology of zinc oxide nanoparticles on the germination of Chinese cabbage seeds. Environ Sci Pollut Res 22:10452–10462

    Article  CAS  Google Scholar 

  43. Zhang C, Wang J, Tan L, Chen X (2016) Toxic effects of nano-ZnO on marine microalgae Skeletonema costatum: attention to the accumulation of intracellular Zn. Aquat Toxicol 178:158–164

    Article  CAS  Google Scholar 

  44. Zhou H, Wang X, Zhou Y, Yao H, Ahmad F (2014) Evaluation of the toxicity of ZnO nanoparticles to Chlorella vulgaris by use of the chiral perturbation approach. Anal Bioanal Chem 406:3689–3695

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The results were extracted from the PhD thesis of Mahya Samei (Faculty of Chemical Engineering, University of Tehran, Tehran, Iran).

Funding

This study was financially supported by grants from University of Tehran and Tehran University of Medical Sciences, Tehran, Iran.

Author information

Affiliations

Authors

Corresponding authors

Correspondence to Mohammad-Hossein Sarrafzadeh or Mohammad Ali Faramarzi.

Additional information

Responsible editor: Thomas D. Bucheli

Electronic supplementary material

ESM 1

(DOCX 165 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Samei, M., Sarrafzadeh, M. & Faramarzi, M.A. The impact of morphology and size of zinc oxide nanoparticles on its toxicity to the freshwater microalga, Raphidocelis subcapitata. Environ Sci Pollut Res 26, 2409–2420 (2019). https://doi.org/10.1007/s11356-018-3787-z

Download citation

Keywords

  • Toxicity
  • Flow cytometry
  • ZnO nanoparticle
  • Pseudokirchneriella
  • Microalgae
  • Cell viability