Abstract
The wide use of ZnO nanoparticles in a number of products implies an increasing release into the marine environment, resulting in the need to evaluate the potential effects upon organisms, and particularly phytoplankton, being at the base of the throphic chain. To this aim, dose–response curves for the green alga Tetraselmis suecica and the diatom Phaeodactylum tricornutum derived from the exposure to nano ZnO (100 nm) were evaluated and compared with those obtained for bulk ZnO (200 nm) and ionic zinc. The toxic effects to both algae species were reported as no observable effect concentration (NOEC) of growth inhibition and as 1, 10, and 50% effect concentrations (EC1, EC10, and EC50). The toxicity decreased in the order nano ZnO > Zn2+ > bulk ZnO. EC50 values for nano ZnO were 3.91 [3.66–4.14] mg Zn/L towards the green microalgae and 1.09 [0.96–1.57] mg Zn/L towards the diatom, indicating a higher sensitivity of P. tricornutum. The observed diverse effects can be ascribed to the interaction occurring between different algae and ZnO particles. Due to algae motility, ZnO particles were intercepted in different phases of aggregation and sedimentation processes, while algae morphology and size can influence the level of entrapment by NP aggregates.
This underlines the need to take into account the peculiarity of the biological system in the assessment of NP toxicity.
Similar content being viewed by others
References
Angel BM, Simpson SL, Chariton AA, Stauber JL, Jolley DF (2015) Time-averaged copper concentrations from continuous exposures predicts pulsed exposure toxicity to the marine diatom, Phaeodactylum tricornutum: importance of uptake and elimination. Aquat Toxicol 164:1–9
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
ASTM (1998) Standard guide for acute toxicity test with the rotifer Brachionus. In: RF A (ed) Annual book of ASTM standards. Section II-Water and Environmental Technology, West Conshohocken, pp 837–843
Batley GE, Halliburton B, Kirby JK, Doolette CL, Navarro D, McLaughlin MJ, Veitch C (2013) Characterization and ecological risk assessment of nanoparticulate CeO2 as a diesel fuel catalyst. Environ Toxicol Chem 32:1896–1905
Bian SW, Mudunkotuwa IA, Rupasinghe T, Grassian VH (2011) Aggregation and dissolution of 4 nm ZnO nanoparticles in aqueous environments: influence of pH, ionic strength, size, and adsorption of humic acid. Langmuir 27:6059–6068
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
Castro-Bugallo A, González-Fernández Á, Guisande C, Barreiro A (2014) Comparative responses to metal oxide nanoparticles in marine phytoplankton. Arch Environ Contam Toxicol 67:483–493
Clément L, Hurel C, Marmier N (2013) Toxicity of TiO2 nanoparticles to cladocerans, algae, rotifers and plants–effects of size and crystalline structure. Chemosphere 90:1083–1090
Fairbairn EA, Keller AA, Mädler L, Zhou D, Pokhrel S, Cherr GN (2011) Metal oxide nanomaterials in seawater: linking physicochemical characteristics with biological response in sea urchin development. J Hazard Mater 192:1565–1571
Francius G, Tesson B, Dague E, Martin-Jézéquel V, Dufrêne YF (2008) Nanostructure and nanomechanics of live Phaeodactylum tricornutum morphotypes. Environ Microbiol 10:1344–1356
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
Gong N, Shao K, Feng W, Lin Z, Liang C, Sun Y (2011) Biotoxicity of nickel oxide nanoparticles and bio-remediation by microalgae Chlorella vulgaris. Chemosphere 83:510–516
Gottschalk F, Sonderer T, Scholz RW, Nowack B (2009) Modeled environmental concentrations of engineered nanomaterials (TiO2, ZnO, Ag, CNT, fullerenes) for different regions. Environ Sci Technol 43:9216–9222
Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Culture of marine invertebrate animals. Springer, pp 29–60
Hotze EM, Bottero JY, Wiesner MR (2010) Theoretical framework for nanoparticle reactivity as a function of aggregation state. Langmuir 26:11170–11175
Ji J, Long Z, Lin D (2011) Toxicity of oxide nanoparticles to the green algae Chlorella sp. Chem Eng J 170:525–530
Kadar E, Rooks P, Lakey C, White DA (2012) The effect of engineered iron nanoparticles on growth and metabolic status of marine microalgae cultures. Sci Total Environ 439:8–17
Keller AA, Vosti W, Wang H, Lazareva A (2014) Release of engineered nanomaterials from personal care products throughout their life cycle. J Nanopart Res 16:1–10
Lee AK, Lewis DM, Ashman PJ (2013) Force and energy requirement for microalgal cell disruption: an atomic force microscope evaluation. Bioresour Technol 128:199–206. doi:10.1016/j.biortech.2012.10.032
Li F, Liang Z, Zheng X, Zhao W, Wu M, Wang Z (2015) Toxicity of nano-TiO2 on algae and the site of reactive oxygen species production. Aquat Toxicol 158:1–13
Li M, Lin D, Zhu L (2013) Effects of water chemistry on the dissolution of ZnO nanoparticles and their toxicity to Escherichia coli. Environ Pollut 173:97–102
Ma HB, Williams PL, Diamond SA (2013) Ecotoxicity of manufactured ZnO nanoparticles—a review. Environ Pollut 172:76–85. doi:10.1016/j.envpol.2012.08.011
Mafuné F, J-y K, Takeda Y, Kondow T, Sawabe H (2000) Structure and stability of silver nanoparticles in aqueous solution produced by laser ablation. J Phys Chem B 104:8333–8337
Manzo S, Miglietta ML, Rametta G, Buono S, Di Francia G (2013a) Toxic effects of ZnO nanoparticles towards marine algae Dunaliella tertiolecta. Sci Total Environ 445-446:371–376. doi:10.1016/j.scitotenv.2012.12.051
Manzo S, Miglietta ML, Rametta G, Buono S, Di Francia G (2013b) Embryotoxicity and spermiotoxicity of nanosized ZnO for Mediterranean Sea urchin Paracentrotus lividus. J Hazard Mater 254:1–9
Miao A-J, Quigg A, Schwehr K, Xu C, Santoschi P (2009) The algal toxicity of silver engineered nanoparticles and detoxification by exopolymeric substances. Environ Pollut 11:3034–3041
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
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
Navarro E, Piccapietra F, Wagner B, Marconi F, Kaegi R, Odzak N, Sigg L, Behra R (2008a) Toxicity of silver nanoparticles to Chlamydomonas reinhardtii. Environ Sci Technol 42:8959–8964
Navarro E, Baun A, Behra R, Hartmann NB, Filser J, Miao A-J, Quigg A, Santschi PH, Sigg L (2008b) Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi. Ecotoxicology 17:372–386
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
PROSPEcT (2009) Toxicology Review of Nano Zinc Oxide
Schiavo S, Oliviero M, Miglietta M, Rametta G, Manzo S (2016) Genotoxic and cytotoxic effects of ZnO nanoparticles for Dunaliella tertiolecta and comparison with SiO 2 and TiO 2 effects at population growth inhibition levels. Sci Tot Environ 550:619–627
Scholze M, Boedeker W, Faust M, Backhaus T, Altenburger R, Grimme LH (2001) A general best-fit method for concentration-response curves and the estimation of low-effect concentrations. Environ Toxicol Chem 20:448–457
Seoane M, Rioboo C, Herrero C, Cid Á (2014) Toxicity induced by three antibiotics commonly used in aquaculture on the marine microalga Tetraselmis suecica (Kylin) Butch. Mar Environ Res 101:1–7
Soldo D, Hari R, Sigg L, Behra R (2005) Tolerance of Oocystis nephrocytioides to copper: intracellular distribution and extracellular complexation of copper. Aquat Toxicol 71:307–317
Tesson B, Genet MJ, Fernandez V, Degand S, Rouxhet PG, Martin-Jézéquel V (2009) Surface chemical composition of diatoms. Chembiochem 10:2011–2024
US-EPA (1989) EPA 600/4–89/001 Dunnett’s test
US EPA (1993) A linear interpolation method for sub lethal toxicity: the inhibition concentration (ICp) approach. National Effluent Toxicity Assessment Center Technical Report 03-93. Environmental Research Laboratory, Duluth, Minnesota
Xia B, Chen B, Sun X, Qu K, Ma F, Du M (2015) Interaction of TiO2 nanoparticles with themarine microalga Nitzschia closterium: growth inhibition, oxidative stress and internalization. Sci Total Environ 508:525–533
Wang J, Zhang X, Chen Y, Sommerfeld M, Hu Q (2008) Toxicity assessment of manufactured nanomaterials using the unicellular green alga Chlamydomonas reinhardtii. Chemosphere 73:1121–1128
Wang L, Zheng B (2008) Toxic effects of fluoranthene and copper on marine diatom Phaeodactylum tricornutum. J Environ Sci 20:1363–1372
Wong SWY, Leung PTY, Djurišić AB, Leung KMY (2010) Toxicities of nano zinc oxide to five marine organisms: influences of aggregate size and ion solubility. Anal Bioanal Chem 396:609–618
Yung MM, Wong SW, Kwok KW, Liu F, Leung Y, Chan W, Li X, Djurišić A, Leung KM (2015) Salinity-dependent toxicities of zinc oxide nanoparticles to the marine diatom Thalassiosira pseudonana. Aquat Toxicol 165:31–40
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by: Markus Hecker
Rights and permissions
About this article
Cite this article
Li, J., Schiavo, S., Rametta, G. et al. Comparative toxicity of nano ZnO and bulk ZnO towards marine algae Tetraselmis suecica and Phaeodactylum tricornutum . Environ Sci Pollut Res 24, 6543–6553 (2017). https://doi.org/10.1007/s11356-016-8343-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-016-8343-0