Abstract
Commercial usage of ZnO nanoparticles has increased recently due to its versatile applications, raising serious environmental concern because of its ultimate release of nanoparticles in aquatic ecosystem. Therefore, it is important to understand the impact of ZnO nanoparticle toxicity especially on algal flora, which is the primary producer in the aquatic food chain. In the current study, algal growth kinetics was assessed after the exposure of zinc oxide nanoparticles and its bulk counterpart to Coelastrella terrestris (Chlorophyceae). Zinc oxide nanoparticles were found to be more toxic (y = 34.673x, R2 = − 0.101, 1 mg L−1 nanoparticle (NP)) than bulk (y = 50.635x, R2 = 0.173, 1 mg L−1 bulk) by entrapping the algal cell surface. Higher toxicity may be due to oxidative stress within the algal cell as confirmed through biochemical analysis. Biochemical parameters revealed stressful physiological condition in the alga under nanoparticle exposure, as lactate dehydrogenase release (18.89 ± 0.2 NP; 13.67 ± 0.2 bulk), lipid peroxidation (0.9147 ± 1.2 NP; 0.7480 ± 0.8 bulk), and catalase activity (4.77 ± 0.1 NP; 3.32 ± 0.1 bulk) were found higher at 1 mg L−1 in the case of nano-form. Surface adsorptions of nanoparticles were observed by SEM. Cell organelle damage, cell wall breakage, and cytoplasm shrinkage were found as responses under toxic condition through SEM and TEM. Toxicity was found to be influenced by dose concentration and exposure period. This study indicates that nano-form of ZnO is found to be more toxic than bulk form to freshwater alga.
Similar content being viewed by others
Abbreviations
- ANOVA:
-
Analysis of variance
- BG-11:
-
Blue Green-11
- BSA:
-
Bovine serum albumin
- CAT:
-
Catalase
- CDH:
-
Central drug house
- FTIR:
-
Fourier-transform infrared spectroscopy
- LDH:
-
Lactate dehydrogenase
- MDA:
-
Malondialdehyde assay
- NADH:
-
Nicotinamide adenine dinucleotide hydrogen
- NCBI:
-
National Center for Biotechnology Information
- NP:
-
Nanoparticle
- PBS :
-
Phosphate-buffered saline
- PDI:
-
Polydispersity index
- SD:
-
Standard deviation
- SEM:
-
Scanning electron microscopy
- SOD:
-
Superoxide dismutase
- TEM:
-
Transmission electron microscopy
- UV:
-
Ultraviolet
- ZnO:
-
Zinc oxide
References
Alswat AA, Ahmad MB, Saleh TA, Hussein MZB, Ibrahim NA (2016) Effect of zinc oxide amounts on the properties and antibacterial activities of zeolite/zinc oxide nanocomposite. Mater Sci Eng C 68:505–511
Angel BM, Batley GE, Jarolimek CV, Rogers NJ, (2013) The impact of size on the fate and toxicity of nanoparticulate silver in aquatic systems. Chemosphere 93(2):359–365
Aruoja V, Dubourguier HC, Kasemets K, Kahru A (2009) Toxicity of nanoparticles of CuO, ZnO and TiO2 to microalgae Pseudokirchneriella subcapitata. Sci Total Environ 407:1461–1468
Bergtold M, Dohmen GP (2011) Biomass or growth rate endpoint for algae and aquatic plants: relevance for the aquatic risk assessment of herbicides. Integr Environ Assess Manag 7:237–247
Bhattacharya P, Lin S, Turner JP, Ke PC (2010) Physical adsorption of charged plastic nanoparticles affects algal photosynthesis. J Phys Chem C 114:16556–16561
Bhuvaneshwari M, Iswarya V, Vishnu S, Chandrasekaran N, Mukherjee A (2018) Dietary transfer of zinc oxide particles from algae (Scenedesmus obliquus) to daphnia (Ceriodaphnia dubia). Environ Res 164:395–404
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
Cattaneo AG (2018) Nanotoxicological evaluation in marine water ecosystem: a detailed review. In: Kumar V, Dasgupta N, Ranjan S (eds) Environmental toxicity of nanomaterials, 1st edn. CRC Press, pp 61–90
Chen P, Powell BA, Mortimer M, Ke PC (2012) Adaptive interactions between zinc oxide nanoparticles and Chlorella sp. Environ Sci Technol 46:12178–12185
Chen F, Xiao Z, Yue L, Wang J, Feng Y, Zhu X, Wang Z, Xing B (2019) Algae response to engineered nanoparticles: current understanding, mechanisms and implications. Environ Sci Nano 6:1026–1042. https://doi.org/10.1039/C8EN01368C
Dash A, Singh AP, Chaudhary BR, Singh SK, Dash D (2012) Silver nanoparticles on growth of eukaryotic green algae. Nano Micro Lett 4:158–165
Ejaz M, Arfat YA, Mulla M, Ahmed J (2018) Zinc oxide nanorods/clove essential oil incorporated type B gelatin composite films and its applicability for shrimp packaging. Food Pack Shelf 15:113–121
Espinasse BP, Geitner NK, Schierz A, Therezien M, Richardson CJ, Lowry GV, Ferguson L, Wiesner MR (2018) Comparative persistence of engineered nanoparticles in a complex aquatic ecosystem. Environ Sci Technol 52:4072–4078
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
Fu PP, Xia Q, Hwang HM, Ray PC, Yu H (2014) Mechanisms of nanotoxicity: generation of reactive oxygen species. J Food Drug Anal 22(1):64–75
Ghaffari SB, Sarrafzadeh MH, 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
Gong N, Shao KS, Feng W, Lin ZZ, Liang CH, Sun YQ (2011) Biotoxicity of nickel oxide nanoparticles and bio-remediation by microalgae Chlorella vulgaris. Chemosphere 83:510–516
Harish, Sundaramoorthy S, Kumar D, Vaijapurkar SG (2008) A new chlorophycean nickel hyperaccumulator. Bioresour Technol 99(9):3930–3934
Hazeem LJ, Bououdina M, Rashdan S, Brunet L, Slomianny C, Boukherroub R (2016) Cumulative effect of zinc oxide and titanium oxide nanoparticles on growth and chlorophyll a content of Picochlorum sp. Environ Sci Pollut Res 23:2821–2830
Herbert D, Phipps PJ, Strange RE (1971) The chemical analysis of microbial cell. In: Norris JR, Ribbons DW (eds) Methods in microbiology, volume VB. London Academic Press, London, pp 209–344
Horie M, Nishio K, Fujita K, Endoh S, Miyauchi A, Saito Y et al (2009) Protein adsorption of ultrafine metal oxide and its influence on cytotoxicity toward cultured cells. Chem Res Toxicol 22(3):543–553
Houimli SIM, Denden M, Mouhandes BM (2010) Effects of 24-epibrassinolide on growth, chlorophyll, electrolyte leakage and proline by pepper plants under NaCl-stress. Eur Asia J Biosci 4:96–104
Huang CP, Cha DK, Ismat SS (2005) Progress report: short-term chronic toxicity of photocatalytic nanoparticles to bacteria, algae, and zooplankton. EPA Grant number: R831721./http://cfpub.epa.gov/ncer_abstracts/indexcfm/fuseaction/display.abstractDetail/abstract/7384/report/0S
Ji J, Long Z, Lin D (2011) Toxicity of oxide nanoparticles to the green algae Chlorella sp. Chem Eng J 170:525–530
Kim DY, Vijayan D, Praveenkumar R, Han JI, Lee K, Park JY, Chang WS, Lee JS, Oh YK (2016) Cell-wall disruption and lipid/astaxanthin extraction from microalgae: Chlorella and Haematococcus. Bioresour Technol 199:300–310
Klaine SJ, Alvarez PJJ, Batley GE, Fernandes TF, Handy RD, Lyon DY, Mahendra S, McLaughlin MJ, Lead JR (2008) Nanomaterials in the environment: behavior, fate, bioavailability, and effects. Environ Toxicol Chem 27:1825–1851
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
Lowry OH, Rosenbrough NJ, Farr AL, Randall RJ (1951) Protein measurement with folin reagent. J Biol Chem 193:265–275
Lu PJ, Huang SC, Chen YP, Chiueh LC, Shih DYC (2015) Analysis of titanium dioxide and zinc oxide nanoparticles in cosmetics. Food Compos Anal 23:587–594
Lupan O, Cretu V, Postica V, Ahmadi M, Cuenya BR, Chow L, Adelung R (2016) Silver-doped zinc oxide single nanowire multifunctional nanosensor with a significant enhancement in response. Sensors Actuators B Chem 223:893–903
Ma H, Williams PL, Diamond SA (2013) Ecotoxicity of manufactured ZnO nanoparticles–a review. Environ Pollut 172:76–85
Mackinney G (1941) Absorption of light by chlorophyll solution. J Biol Chem 140:315–322
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
Merdzan V, Domingos RF, Monteiro CE, Hadioui M, Wilkinson KJ (2014) The effects of different coatings on zinc oxide nanoparticles and their influence on dissolution and bioaccumulation by the green alga, C. reinhardtii. Sci Total Environ 488:316–324
Metzler DM, Li M, Erdem A, Huang CP (2011) Responses of algae to photocatalytic nano-TiO2 particles with an emphasis on the effect of particle size. Chem Eng J 170:538–546
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
Mishra PK, Mishra H, Ekielski A, Talegaonkar S, Vaidya B (2017) Zinc oxide nanoparticles: a promising nanomaterial for biomedical applications. Drug Discov Today 22:1825–1834
Navarro E, Baun A, Behra R, Hartmann NB, Filser J, Miao A-J, Quigg A, Santschi PH, Sigg L (2008) Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi. Ecotoxicology 17:372–386
Nikookar K, Moradshahi A, Hosseini L (2005) Physiological responses of Dunaliella salina and Dunaliella tertiolecta to copper toxicity. Biomol Eng 22:141–146
Nowack B, Bucheli TD (2007) Occurrence, behavior and effects of nanoparticles in the environment. Environ Pollut 150:5–22
Pakrashi S, Dalai S, Prathna TC, Trivedi S, Myneni R, Raichur AM, Chandrasekaran N, Mukherjee A (2013) Cytotoxicity of aluminium oxide nanoparticles towards fresh water algal isolate at low exposure concentrations. Aquat Toxicol 132:34–45
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
Piccinno F, Gottschalk F, Seeger S, Nowack B (2012) Industrial production quantities and uses of ten engineered nanomaterials in Europe and the world. J Nanopart Res 14:1109
Rai UN, Tripathi RD, Kumar N (1992) Bioaccumulation of chromium and toxicity on growth, photosynthetic pigments, photosynthesis, in vivo nitrate reductase activity and protein content in a chlorococcalean green alga Glaucocystis nostochinearum Itzigsohn. Chemosphere 25(11):1721–1732
Raliya R, Saharan V, Dimkpa C, Biswas P (2017) Nanofertilizer for precision and sustainable agriculture: current state and future perspectives. Agric Food Chem 66:6487–6503
Rasmussen JW, Martinez E, Louka P, Wingett DG (2010) Zinc oxide nanoparticles for selective destruction of tumor cells and potential for drug delivery applications. Expert Opin Drug Deliv 7(9):1063–1077
Rippka R, Derelies J, Waterbury JB, Herdman M, Stainer RV (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61
Roy R, Parashar A, Bhuvaneshwari M, Chandrasekaran N, Mukherjee A (2016) Differential effects of P25 TiO2 nanoparticles on freshwater green microalgae: Chlorella and Scenedesmus species. Aquat Toxicol 176:161–171
Samei M, Sarrafzadeh MH, Faramarzi MA (2019) 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
Sayeed I, Parvez S, Pandey S, Bin-Hafeez B, Haque R, Raisuddin S (2003) Oxidative stress biomarkers of exposure to deltamethrin in freshwater fish, Channa punctatus Bloch. Ecotoxicol Environ Saf 56:295–301
Schiavo S, Oliviero M, Miglietta M, Rametta G, Manzo S, (2016) Genotoxic and cytotoxic effects of ZnO nanoparticles for Dunaliella tertiolecta and comparison with SiO2 and TiO2 effects at population growth inhibition levels. Sci Total Environ 550:619–627
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
Sharma N, Jha R, Baghel S, Sharma D (2017) Study on photocatalyst zinc oxide annealed at different temperatures for photodegradation of eosin Y dye. J Alloys Compd 695:270–279
Suman TY, 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
Sun TY, Bornhöft NA, Hungerbühler K, Nowack B (2016) Dynamic probabilistic modeling of environmental emissions of engineered nanomaterials. Environ Sci Technol 50:4701–4711
Taylor NS, Merrifield R, Williams TD, Chipman JK, Lead JR, Viant MR (2016) Molecular toxicity of cerium oxide nanoparticles to the freshwater alga Chlamydomonas reinhardtii is associated with supra-environmental exposure concentrations. Nanotoxicology 10:32–41
Tripathi DK, Tripathi A, Shweta SS, Singh Y, Vishwakarma K, Yadav G, Sharma S, Singh VK, Mishra RK, Upadhyay RG, Dubey NK, Lee Y, Chauhan DK (2017) Uptake, accumulation and toxicity of silver nanoparticle in autotrophic plants, and heterotrophic microbes: a concentric review. Front Microbiol 8:7
Turhani D, Cvikl B, Watzinger E, Weißenböck M, Yerit K, Thurnher D, Lauer G, Ewers R (2005) In vitro growth and differentiation of osteoblast-like cells on hydroxyapatite ceramic granule calcified from red algae. J Oral Maxillofac Surg 63(6):793–799
Wacker WE, Ulmer DD, Vallee BL (1956) Metalloenzymes and myocardial infarction: malic and lactic dehydrogenase activities and zinc concentrations in serum. N Engl J Med 255:449–456
Wang ZL (2004) Zinc oxide nanostructures: growth, properties and applications. J Phys Condens Matter 16:R829–R858
Wang GH, Hao ZJ, Huang ZB, Chen LZ, Li XY, Hu CX, Liu YD (2010) Raman spectroscopic analysis of a desert cyanobacterium Nostoc sp. in response to UV-B radiation. Astrobiology 10:783–788
Wang ZY, Li J, Zhao J, Xing BS (2011) Toxicity and internalization of CuO nanoparticles to prokaryotic alga Microcystis aeruginosa as affected by dissolved organic matter. Environ Sci Technol 45:6032–6040
Wang Z, Vijver MG, Peijnenburg WJ (2018) Multiscale coupling strategy for nano ecotoxicology prediction. Environ Sci Technol 52(14):7598–7600
Xia B, Chen B, Sun X, Qu K, Ma F, Du M (2015) Interaction of TiO2 nanoparticles with the marine microalga Nitzschia closterium: growth inhibition, oxidative stress and internalization. Sci Total Environ 508:525–533
Yang H, Liu C, Yang D, Zhang H, Xi Z (2009) Comparative study of cytotoxicity, oxidative stress and genotoxicity induced by four typical nanomaterials: the role of particle size, shape and composition. J Appl Toxicol 29:69–78
Yilancioglu K, Cokol M, Pastirmaci I, Erman B, Cetiner S (2014) Oxidative stress is a mediator for increased lipid accumulation in a newly isolated Dunaliella salina strain. PLoS One 9:e91957
Zhang H, Ji Z, Xia T, Meng H, Low-Kam C, Liu R, Pokhrel S, Lin S, Wang X, Liao YP, Wang M (2012) Use of metal oxide nanoparticle band gap to develop a predictive paradigm for oxidative stress and acute pulmonary inflammation. ACS Nano 6:4349–4368
Acknowledgments
We are thankful to the anonymous reviewers for the critical reading of the manuscript and improvement. We wish to acknowledge SAIF, New Delhi, for extending electron microscopy facilities. We are also thankful to Dr. Vinod Saharan, RCA, Udaipur, and Dr. Prabhat Baroliya, MLSU, Udaipur, for providing us DLS and FTIR facilities, respectively.
Funding
Pallavi Saxena received financial support from the University Grants Commission (UGC), New Delhi, India, in the form of BSR Meritorious Fellowship (F.25-a/2013-14(BSR)/7-125/2007(BSR)).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible editor: Philippe Garrigues
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(PPT 282 kb)
Rights and permissions
About this article
Cite this article
Saxena, P., Harish Toxicity assessment of ZnO nanoparticles to freshwater microalgae Coelastrella terrestris. Environ Sci Pollut Res 26, 26991–27001 (2019). https://doi.org/10.1007/s11356-019-05844-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-019-05844-1