Skip to main content
Log in

Ecotoxicity of a mixture of nanoparticles on algal species Scendesmus obliquus in OECD growth media, wastewater, and pond water

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

The possible impact of ZnO and CuO nanoparticles (NPs) (individually and in binary mixture) was investigated using the freshwater microalgae, Scenedesmus obliquus. The present study shows the effect of nanoparticles on algae in OECD growth media, wastewater, and pond water during a 96-h toxicity test. At 0.1 mg/L concentration of the mixture of NPs, the reduction in the chlorophyll a content was 13.61 ± 1.34% (OECD media), 28.83 ± 1.85% (wastewater), and 31.81 ± 2.23% (pond water). Values of reduction in biomass were observed to be 42.13 ± 1.38, 39.96 ± 1.03, and 33.10 ± 1.29% for OECD media, wastewater, and pond water, respectively. The highest increase in lipid values was observed in the case of pond water (6.3 ± 1.31%). A significant increase in the value of EPS-generated protein was observed in the wastewater sample. EPS-generated carbohydrate values were increased in OECD media but decreased in the wastewater matrix. The transmission electron microscope images showed structural damage to algae cells due to the exposure to a mixture of nanoparticles at higher concentrations. Fourier transform infrared analysis showed an addition of bonds and differences in the peak and its intensity during exposure to high concentrations of NPs. Overall, this study gives fundamental insights into the interaction and toxicity of a mixture of NPs to algal species in different water matrices.

Highlights

  • Higher toxicity to S. obliquus due to ZnO nanoparticles (NPs) in pond water than CuO NPs.

  • Order of toxicity (high to low): ZnO NPs alone> CuO NPs alone> ZnO+ CuO NPs.

  • Highest generation of EPS-generated protein in wastewater due to the mixture of NPs.

  • Less toxicity to algae in field water matrixes due to the OECD toxicity test 201 procedure.

  • The important role of water chemistry on the toxicity of a mixture of NPs to algae.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • Adjei IM, Sharma B, Labhasetwar V (2014) Nanoparticles: cellular uptake and cytotoxicity. Nanomaterial: impacts on cell biology and medicine Springer, p 73–91

  • Ahmad M, Gani A, Hassan I, Huang Q, Shabbir H (2020) Production and characterization of starch nanoparticles by mild alkali hydrolysis and ultra-sonication process. Sci Rep 10(1):3533

    Article  CAS  Google Scholar 

  • American Public Health Association (APHA) (2005) Standard Methods for the Examination of Water and Wastewater 21st ed. American Public Health Association, Washington DC, p 1220.

  • 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(4):1461–1468

    Article  CAS  Google Scholar 

  • Badireddy AR, Chellam S, Gassman PL, Engelhard MH, Lea AS, Rosso KM (2010) Role of extracellular polymeric substances in bioflocculation of activated sludge microorganisms under glucose-controlled conditions. Water Res 44(15):4505–4516

    Article  CAS  Google Scholar 

  • Bhuvaneshwari M, Iswarya V, Archanaa S, Madhu GM, Kumar GS, 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 

  • Bundschuh M, Filser J, Lüderwald S, McKee MS, Metreveli G, Schaumann GE, Schulz R, Wagner S (2018) Nanoparticles in the environment: where do we come from, where do we go to? Environ Sci Eur 30(1):1–17

    Article  CAS  Google Scholar 

  • Chen CY, Zhao XQ, Yen HW, Ho SH, Cheng CL, Lee DJ, Bai FW, Chang JS (2013) Microalgae-based carbohydrates for biofuel production. Biochem Eng J 78:1–10

    Article  CAS  Google Scholar 

  • Chang YN, Zhang M, Xia L, Zhang J, Xing G (2012) The toxic effects and mechanisms of CuO and ZnO nanoparticles. Materials 5(12):2850–2871

    Article  CAS  Google Scholar 

  • Chen X, Zhang C, Tan L, Wang J (2018) Toxicity of Co nanoparticles on three species of marine microalgae. Environ Pollut 236:454–461

    Article  CAS  Google Scholar 

  • Dalai S, Pakrashi S, Nirmala MJ, Chaudhri A, Chandrasekaran N, Mandal AB, Mukherjee A (2013) Cytotoxicity of TiO2 nanoparticles and their detoxification in a freshwater system. Aquat Toxicol 138:1–11

    Article  Google Scholar 

  • Fang H, Bai SL, Wong CP (2017) Thermal, mechanical and dielectric properties of flexible BN foam and BN nanosheets reinforced polymer composites for electronic packaging application. Compos Part A Appl Sci Manuf 100:71–80

    Article  CAS  Google Scholar 

  • Fitzgerald MG, Keen H (1964) Diagnostic classification of diabetes. British Medical Journal 1(5397):1568

    Article  Google Scholar 

  • Foladori P, Velho VF, Costa RHR, Bruni L, Quaranta A, Andreottola G (2015) Concerning the role of cell lysis-cryptic growth in anaerobic side-stream reactors: the single-cell analysis of viable, dead and lysed bacteria. Water Res 74:132–142

    Article  CAS  Google Scholar 

  • 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(24):8484–8490

    Article  CAS  Google Scholar 

  • Gao X, Middepogu A, Deng R, Liu J, Hao Z, Lin D (2019) Adsorption of extracellular polymeric substances from two microbes by TiO2 nanoparticles. Sci Total Environ 694:133778

    Article  CAS  Google Scholar 

  • Guillard RR, Kilham P, Jackson TA (1973) Kinetics of silicon-limited growth in the marine diatom thalassiosira pseudonana hasle and heimdal (= cyclotella nana hustedt) 1, 2. J Phycol 9(3):233–237

    CAS  Google Scholar 

  • APHA (1998) Standards Methods for the Examination of Water and Wastewater, 20th edition. American Public Health Association, Washington, DC

    Google Scholar 

  • Hessler CM, Wu MY, Xue Z, Choi H, Seo Y (2012) The influence of capsular extracellular polymeric substances on the interaction between TiO2 nanoparticles and planktonic bacteria. Water Res 46(15):4687–4696

    Article  CAS  Google Scholar 

  • Hou D, Zhou W, Liu X, Zhou K, Xie J, Li G, Chen S (2015) Pt nanoparticles/MoS2 nanosheets/carbon fibers as efficient catalyst for the hydrogen evolution reaction. Electrochimica Acta 166:26–31

    Article  CAS  Google Scholar 

  • Huang B, Wei ZB, Yang LY, Pan K, Miao AJ (2019) Combined toxicity of silver nanoparticles with hematite or plastic nanoparticles toward two freshwater algae. Environ Sci Technol 53(7):3871–3879

    Article  CAS  Google Scholar 

  • Iswarya V, Bhuvaneshwari M, Alex SA, Iyer S, Chaudhuri G, Chandrasekaran PT, Bhalerao GM, Chakravarty S, Raichur AM, Chandrasekaran N, Mukherjee A (2015) Combined toxicity of two crystalline phases (anatase and rutile) of Titania nanoparticles towards freshwater microalgae: Chlorella sp. Aquat Toxicol 161:154–169

    Article  CAS  Google Scholar 

  • Jeon S, Hurley KR, Bischof JC, Haynes CL, Hogan CJ (2016) Quantifying intra-and extracellular aggregation of iron oxide nanoparticles and its influence on specific absorption rate. Nanoscale 8(35):16053–16064

    Article  CAS  Google Scholar 

  • Ji J, Long Z, Lin D (2011) Toxicity of oxide nanoparticles to the green algae Chlorella sp. Chemical Engineering Journal 170(2–3):525–530

    Article  CAS  Google Scholar 

  • Kang H, Zuo K, Wang Z, Zhang L, Liu L, Guo B (2014) Using a green method to develop graphene oxide/elastomers nanocomposites with combination of high barrier and mechanical performance. Compos Sci Technol 92:1–8

    Article  CAS  Google Scholar 

  • Kazbar A, Cogne G, Urbain B, Marec H, Le-Gouic B, Tallec J, Takache H, Ismail A, Pruvost J (2019) Effect of dissolved oxygen concentration on microalgal culture in photobioreactors. Algal Res 39:101432

    Article  Google Scholar 

  • Keller AA, McFerran S, Lazareva A, Suh S (2013) Global life cycle releases of engineered nanomaterials. J Nanopart Res 15:1–17

    Article  Google Scholar 

  • Ko KS, Koh DC, Kong IC (2018) Toxicity evaluation of individual and mixtures of nanoparticles based on algal chlorophyll content and cell count. Materials 11(1):121

    Article  Google Scholar 

  • Lin D, Ji J, Long Z, Yang K, Wu F (2012) The influence of dissolved and surface-bound humic acid on the toxicity of TiO2 nanoparticles to Chlorella sp. Water Res 46(14):4477–4487

    Article  CAS  Google Scholar 

  • Li Z, Chen Z, Zhu Q, Song J, Li S, Liu X (2020) Improved performance of immobilized laccase on Fe3O4@C-Cu2+ nanoparticles and its application for biodegradation of dyes. J Hazard Mater 399:123088

    Article  CAS  Google Scholar 

  • Liu S, Wang C, Hou J, Wang P, Miao L, Fan X, You G, Xu Y (2018) Effects of Ag and Ag2S nanoparticles on denitrification in sediments. Water Res 137:28–36

    Article  CAS  Google Scholar 

  • Llop J, Estrela‐Lopis I, Ziolo RF, González A, Fleddermann J, Dorn M, Vallejo VG, Simon‐Vazquez R, Donath E, Mao Z, Gao C (2014) Uptake, biological fate, and toxicity of metal oxide nanoparticles. Part Part Syst Charact 31(1):24–35

    Article  CAS  Google Scholar 

  • Ma H, Williams PL, Diamond SA (2013) Ecotoxicity of manufactured ZnO nanoparticles–a review. Environ Pollut 172:76–85

    Article  CAS  Google Scholar 

  • Mao Y, Yu Y, Ma Z, Li H, Yu W, Cao L, He Q (2021) Azithromycin induces dual effects on microalgae: Roles of photosynthetic damage and oxidative stress. Ecotoxicol Environ Saf 222:112496

    Article  CAS  Google Scholar 

  • Metzler DM, Erdem A, Tseng YH, Huang CP (2012) Responses of algal cells to engineered nanoparticles measured as algal cell population, chlorophyll a, and lipid peroxidation: effect of particle size and type. J Nanotechnol 2012:237284

    Article  Google Scholar 

  • Miller MA, Kudela RM, Mekebri A, Crane D, Oates SC, Tinker MT, Staedler M, Miller WA, Toy-Choutka S, Dominik C, Hardin D (2010) Evidence for a novel marine harmful algal bloom: cyanotoxin (microcystin) transfer from land to sea otters. PLoS One 5(9):e12576

    Article  Google Scholar 

  • Navarro E, Baun A, Behra R, Hartmann NB, Filser J, Miao AJ, Quigg A, Santschi PH, Sigg L (2008) Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi. Ecotoxicology 17(5):372–386

    Article  CAS  Google Scholar 

  • Nel A, Xia T, Madler L, Li N (2006) Toxic potential of materials at the nanolevel. Science 311(5761):622–627

    Article  CAS  Google Scholar 

  • Ostermeyer AK, Kostigen Mumuper C, Semprini L, Radniecki T (2013) Influence of bovine serum albumin and alginate on silver nanoparticle dissolution and toxicity to Nitrosomonas europaea. Environ Sci Technol 47(24):14403–14410

    Article  CAS  Google Scholar 

  • Parsai T, Kumar A (2019) Understanding effect of solution chemistry on heteroaggregation of zinc oxide and copper oxide nanoparticles. Chemosphere 235:457–469

    Article  CAS  Google Scholar 

  • Perreault F, Oukarroum A, Melegari SP, Matias WG, Popovic R (2012) Polymer coating of copper oxide nanoparticles increases nanoparticles uptake and toxicity in the green alga Chlamydomonas reinhardtii. Chemosphere 87(11):1388–1394

    Article  CAS  Google Scholar 

  • Planas Gisbert M (2013) Production, characterization and evaluation of potential cosmetic uses of Arthospira Platensis exopolysaccharides (Bachelor’s thesis, Universitat Politècnica de Catalunya)

  • Planchon M, Jittawuttipoka T, Cassier-Chauvat C, Guyot F, Gelabert A, Benedetti MF, Chauvat F, Spalla O (2013) Exopolysaccharides protect Synechocystis against the deleterious effects of titanium dioxide nanoparticles in natural and artificial waters. J Colloid Interface Sci 405:35–43

    Article  CAS  Google Scholar 

  • Rai GS, Shovlin C, Wesnes KA (1991) A double-blind, placebo controlled study of Ginkgo biloba extract (‘tanakan’) in elderly outpatients with mild to moderate memory impairment. Curr Med Res Opin 12(6):350–355

    Article  CAS  Google Scholar 

  • Razack SA, Duraiarasan S, Mani V (2016) Biosynthesis of silver nanoparticle and its application in cell wall disruption to release carbohydrate and lipid from C. vulgaris for biofuel production. Biotechnol Rep 11:70–76

    Article  Google Scholar 

  • Sheng Z, Liu Y (2011) Effects of silver nanoparticles on wastewater biofilms. Water Res 45(18):6039–6050

    Article  CAS  Google Scholar 

  • Shi AM, Li D, Wang LJ, Li BZ, Adhikari B (2011) Preparation of starch-based nanoparticles through high-pressure homogenization and miniemulsion cross-linking: Influence of various process parameters on particle size and stability. Carbohydr Polym 83(4):1604–1610

    Article  CAS  Google Scholar 

  • Shin KS (2004) The role of enzymes produced by white-rot fungus Irpex lacteus in the decolorization of the textile industry effluent. J Microbiol 42(1):37–41

    CAS  Google Scholar 

  • Trenkenshu RP, Avsiyan AL (2009) Dark respiration as a biomass loss factor of microalgae (a review). Ekologiya Morya (79):63

  • Wang D, Lin Z, Wang T, Yao Z, Qin M, Zheng S, Lu W (2016) Where does the toxicity of metal oxide nanoparticles come from: the nanoparticles, the ions, or a combination of both? J hazardous mat 308:328–334

    Article  CAS  Google Scholar 

  • Wang Q, Wangjin X, Zhang Y, Wang N, Wang Y, Meng G, Chen Y (2020) The toxicity of virgin and UV-aged PVC microplastics on the growth of freshwater algae Chlamydomonas reinhardtii. Sci Total Environ 749:141603

    Article  CAS  Google Scholar 

  • Wang WY, Wang WL, Boynton JE, Gillham NW (1974) Genetic control of chlorophyll biosynthesis in Chlamydomonas: analysis of mutants at two loci mediating the conversion of protoporphyrin-IX to magnesium protoporphyrin. J Cell Biol 63(3):806–823

    Article  CAS  Google Scholar 

  • Wang Z, Li J, Zhao J, Xing B (2011) Toxicity and internalization of CuO nanoparticles to prokaryotic alga Microcystis aeruginosa as affected by dissolved organic matter. Environ Sci Technol 45(14):6032–6040

    Article  CAS  Google Scholar 

  • Wilde KL, Stauber JL, Markich SJ, Franklin NM, Brown PL (2006) The effect of pH on the uptake and toxicity of copper and zinc in a tropical freshwater alga (Chlorella sp.). Arch Environ Contam Toxicol 51(2):174–185

    Article  CAS  Google Scholar 

  • Xu H, Jiang H (2015) Effects of cyanobacterial extracellular polymeric substances on the stability of ZnO nanoparticles in eutrophic shallow lakes. Environ Pollut 197:231–239

    Article  CAS  Google Scholar 

  • Xu J, Sheng GP, Ma Y, Wang LF, Yu HQ (2013) Roles of extracellular polymeric substances (EPS) in the migration and removal of sulfamethazine in activated sludge system. Water Res 47(14):5298–5306

    Article  CAS  Google Scholar 

  • Ye N, Wang Z, Wang S, Peijnenburg WJ (2018) Toxicity of mixtures of zinc oxide and graphene oxide nanoparticles to aquatic organisms of different trophic level: particles outperform dissolved ions. Nanotoxicology 12(5):423–438

    Article  CAS  Google Scholar 

  • You G, Hou J, Xu Y, Wang C, Wang P, Miao L, Ao Y, Li Y, Lv B (2015) Effects of CeO2 nanoparticles on production and physicochemical characteristics of extracellular polymeric substances in biofilms in sequencing batch biofilm reactor. Bioresour Technol 194:91–98

    Article  CAS  Google Scholar 

  • Zhang X, Zhang Q, Zhang Z, Chen Y, Xie Z, Wei J, Zhou Z (2015) Rechargeable Li–CO 2 batteries with carbon nanotubes as air cathodes. Chem Commun 51(78):14636–14639

    Article  CAS  Google Scholar 

  • Zhang XF, Liu ZG, Shen W, Gurunathan S (2016) Silver nanoparticles: synthesis, characterization, properties, applications, and therapeutic approaches. Int J Mol Sci 17(9):1534

    Article  Google Scholar 

  • Zhao X, Ren X, Zhu R, Luo Z, Ren B (2016) Zinc oxide nanoparticles induce oxidative DNA damage and ROS-triggered mitochondria-mediated apoptosis in zebrafish embryos. Aquat Toxicol 180:56–70

    Article  CAS  Google Scholar 

  • Zhou M, Vigouroux C, Langerock B, Wang P, Dutton G, Hermans C, Kumps N, Metzger JM, Toon G, De Mazière M (2016) CFC-11, CFC-12 and HCFC-22 ground-based remote sensing FTIR measurements at Réunion Island and comparisons with MIPAS/ENVISAT data. Atmos Measurement Tech 9(11):5621–5636

    Article  CAS  Google Scholar 

  • Zhu L, Qi HY, Kong Y, Yu YW, Xu XY (2012) Component analysis of extracellular polymeric substances (EPS) during aerobic sludge granulation using FTIR and 3D-EEM technologies. Bioresour Technol 124:455–459

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by the Department of Civil Engineering, IIT Delhi (India) and experiments were performed in the Environmental Engineering Lab, IIT Delhi, and Central Research Facility, IIT Delhi (FTIR, TEM, and ICP-MS).

Author information

Authors and Affiliations

Authors

Contributions

SR: Conceptualization, Investigation, Methodology, Writing-original draft, Data curation, Validation. AK: Conceptualization, Methodology, Validation, Writing-review, and editing.

Corresponding author

Correspondence to Arun Kumar.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rana, S., Kumar, A. Ecotoxicity of a mixture of nanoparticles on algal species Scendesmus obliquus in OECD growth media, wastewater, and pond water. Ecotoxicology 32, 1257–1271 (2023). https://doi.org/10.1007/s10646-023-02718-8

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-023-02718-8

Keywords

Navigation