Skip to main content
SpringerLink
Log in

Assessing the toxicity of copper oxide nanoparticles and copper sulfate in a tropical Chlorella

  • 8th Asian Pacific Phycological Forum
  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Copper (Cu) in the form of copper sulfate (CuSO4) and copper oxide nanoparticles (CuO NP), arising mainly from agro-industrial activities, is known to have an adverse impact on algae. This study aimed to compare the toxicity of CuSO4 and CuO NP in Chlorella sp., which was isolated from a farmland in Cameron Highlands, Malaysia. Toxicity testing (96 h) based on chlorophyll-a concentration was conducted on cultures grown in Bold’s Basal Medium (BBM) added with CuSO4 ranging from 0 (control) to 200 μM or CuO NP ranging from 0 to 2 mM. In addition, the effects of CuSO4 and CuO NP at EC10 and EC50 on the pigmentation, oxidative stress response, and cell morphology of Chlorella sp. were assessed. Results showed that Chlorella sp. was more sensitive to CuSO4 (EC50 = 150 μM) than CuO NP (EC50 = 1.30 mM). Exposure to CuSO4 at EC50 but not CuO NP reduced the chlorophyll-a, chlorophyll-b, and carotenoid contents of the algal cells. At 96 h, CuSO4 at EC50 induced significant increase in the production of reactive oxygen species (ROS) and degree of lipid peroxidation. Agglomerates of nanoparticles and algal cells were seen in cultures treated with CuO NP, whereas clumping of cells occurred in cultures exposed to CuSO4. Some CuO NP were found to penetrate the cell wall and be internalized into the algal cells. In conclusion, the toxicity of CuSO4 and CuO NP in Chlorella sp. differed in terms of their effects on growth, pigmentation, and oxidative stress response.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Ahsanullah M, Williams AR (1991) Sublethal effects and bioaccumulation of cadmium, chromium, copper and zinc in the marine amphipod Allorchestes compressa. Mar Biol 108:59–65

    Article  CAS  Google Scholar 

  • Aravantinou AF, Tsarpali V, Dailianis S, Manariotis ID (2015) Effect of cultivation media on the toxicity of ZnO nanoparticles to freshwater and marine microalgae. Ecotoxicol Environ Saf 114:109–116

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Auffan M, Rose J, Bottero JY, Lowry GV, Jolivet JP, Wiesner MR (2009) Towards a definition of inorganic nanoparticles from an environmental, health and safety perspective. Nat Nanotechnol 4:634–641

    Article  CAS  Google Scholar 

  • BCC Research (2012) Global nanotechnology market to reach $48.9 billion in 2017. https://www.bccresearch.com/pressroom/nan/global-nanotechnology-market-reach-$48.9-billion-2017. Accessed 17 October 2017

  • Buffet PE, Tankoua OF, Pan JF, Berhanu D, Herrenknecht C, Poirier L, Guibbolini M (2011) Behavioural and biochemical responses of two marine invertebrates Scrobicularia plana and Hediste diversicolor to copper oxide nanoparticles. Chemosphere 84:166–174

    Article  CAS  Google Scholar 

  • Canning-Clode J, Fofonoff P, Riedel GF, Torchin M, Ruiz GM (2011) The effects of copper pollution on fouling assemblage diversity: a tropical-temperate comparison. PLoS One 6:e18026

    Article  CAS  Google Scholar 

  • Cardeilhac PT, Simpson CF, Lovelock RL, Yosha SF, Calderwood HW, Gudat JC (1979) Failure of osmoregulation with apparent potassium intoxication in marine teleosts: a primary toxic effect of copper. Aquaculture 17:231–239

    Article  CAS  Google Scholar 

  • Chen Z, Song S, Wen Y, Zou Y, Liu H (2016) Toxicity of Cu (II) to the green alga Chlorella vulgaris: a perspective of photosynthesis and oxidant stress. Environ Sci Pollut Res 23:17910–17918

    Article  CAS  Google Scholar 

  • Collado S, Laca A, Díaz M (2010) Catalytic wet oxidation of thiocyanate with homogeneous copper (II) sulphate catalyst. J Hazard Mater 177:183–189

    Article  CAS  Google Scholar 

  • Conway JR, Adeleye AS, Gardea-Torresdey J, Keller AA (2015) Aggregation, dissolution, and transformation of copper nanoparticles in natural waters. Environ Sci Technol 49:2749–2756

    Article  CAS  Google Scholar 

  • Cronholm P, Karlsson HL, Hedberg J, Lowe TA, Winnberg L, Elihn K, Wallinder IO, Möller L (2013) Intracellular uptake and toxicity of Ag and CuO nanoparticles: a comparison between nanoparticles and their corresponding metal ions. Small 9:970–982

    Article  CAS  Google Scholar 

  • Dauda S, Chia MA, Bako SP (2017) Toxicity of titanium dioxide nanoparticles to Chlorella vulgaris Beyerinck (Beijerinck) 1890 (Trebouxiophyceae, Chlorophyta) under changing nitrogen conditions. Aquat Toxicol 187:108–114

    Article  CAS  Google Scholar 

  • Expósito N, Kumar V, Sierra J, Schuhmacher M, Papiol GG (2017) Performance of Raphidocelis subcapitata exposed to heavy metal mixtures. Sci Total Environ 601:865–873

    Article  Google Scholar 

  • Fishel (2015) Pesticide toxicity profile: copper-based pesticides. https://edis.ifas.ufl.edu/pi103. Accessed 4 December 2017

  • Franklin NM, Stauber JL, Apte SC, Lim RP (2002) Effect of initial cell density on the bioavailability and toxicity of copper in microalgal bioassays. Environ Toxicol Chem 21:742–751

    Article  CAS  Google Scholar 

  • Frentz G, Teilum D (1980) Cutaneous eruptions and intrauterine contraceptive copper device. Acta Derm Venereol 60:69–71

  • Garcı́a-Villada L, Rico M, Altamirano M, Sánchez-Martı́n L, López-Rodas V, Costas E (2004) Occurrence of copper resistant mutants in the toxic cyanobacteria Microcystis aeruginosa: characterisation and future implications in the use of copper sulphate as algaecide. Water Res 38:2207–2213

    Article  Google Scholar 

  • Goswami L, Kim KH, Deep A, Das P, Bhattacharya SS, Kumar S, Adelodun AA (2017) Engineered nano particles: nature, behavior, and effect on the environment. J Environ Manag 196:297–315

    Article  CAS  Google Scholar 

  • Hanna SK, Miller RJ, Lenihan HS (2014) Accumulation and toxicity of copper oxide engineered nanoparticles in a marine mussel. Nano 4:535–547

    Google Scholar 

  • Hoecke KV, Quik JT, Mankiewicz-Boczek J, Schamphelaere KA, Elsaesser A, Meeren PV, Barnes C, McKerr G, Howard CV, Meent DV, Rydzynski K (2009) Fate and effects of CeO2 nanoparticles in aquatic ecotoxicity tests. Environ Sci Technol 43:4537–4546

    Article  Google Scholar 

  • Ingle AP, Duran N, Rai M (2014) Bioactivity, mechanism of action, and cytotoxicity of copper-based nanoparticles: a review. Appl Microbiol Biotechnol 98:1000–1009

    Article  Google Scholar 

  • Jiang Y, Zhu Y, Hu Z, Lei A, Wang J (2016) Towards elucidation of the toxic mechanism of copper on the model green alga Chlamydomonas reinhardtii. Ecotoxicology 25:1417–1425

    Article  CAS  Google Scholar 

  • Jianrong XI, Qiran TI (2009) Early stage toxicity of excess copper to photosystem II of Chlorella pyrenoidosa–OJIP chlorophyll a fluorescence analysis. J Environ Sci 21:1569–1574

    Article  Google Scholar 

  • Jing X, Park JH, Peters TM, Thorne PS (2015) Toxicity of copper oxide nanoparticles in lung epithelial cells exposed at the air–liquid interface compared with in vivo assessment. Toxicol in Vitro 29:502–511

  • Johnson HL, Stauber JL, Adams MS, Jolley DF (2007) Copper and zinc tolerance of two tropical microalgae after copper acclimation. Environ Toxicol 22:234–244

    Article  CAS  Google Scholar 

  • Karlsson HL, Cronholm P, Gustafsson J, Moller L (2008) Copper oxide nanoparticles are highly toxic: a comparison between metal oxide nanoparticles and carbon nanotubes. Chem Res Toxicol 21:1726–1732

    Article  CAS  Google Scholar 

  • Kiaune L, Singhasemanon N (2011) Pesticidal copper (I) oxide: environmental fate and aquatic toxicity. Rev Environ Contam Toxicol 213:1–26

    CAS  PubMed  Google Scholar 

  • Knauert S, Knauer K (2008) The role of reactive oxygen species in copper toxicity to two freshwater green algae. J Phycol 44:311–319

    Article  CAS  Google Scholar 

  • Levy JL, Angel BM, Stauber JL, Poon WL, Simpson SL, Cheng SH, Jolley DF (2008) Uptake and internalisation of copper by three marine microalgae: comparison of copper-sensitive and copper-tolerant species. Aquat Toxicol 89:82–93

    Article  CAS  Google Scholar 

  • Levy JL, Stauber JL, Jolley DF (2007) Sensitivity of marine microalgae to copper: the effect of biotic factors on copper adsorption and toxicity. Sci Total Environ 387:141–154

    Article  CAS  Google Scholar 

  • Li M, Hu C, Zhu Q, Chen L, Kong Z, Liu Z (2006) Copper and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in the microalga Pavlova viridis (Prymnesiophyceae). Chemosphere 62:565–572

    Article  CAS  Google Scholar 

  • Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. Current Protocols in Food Analytical Chemistry. F:F4:F4.3

    Google Scholar 

  • Lim CY, Yoo YH, Sidharthan M, Ma CW, Bang IC, Kim JM, Shin HW (2006) Effects of copper(I) oxide on growth and biochemical compositions of two marine microalgae. J Environ Biol 27:461–466

  • Macfie SM, Tarmohamed Y, Welbourn PM (1994) Effects of cadmium, cobalt, copper, and nickel on growth of the green alga Chlamydomonas reinhardtii: the influences of the cell wall and pH. Arch Environ Contam Toxicol 27:454–458

    Article  CAS  Google Scholar 

  • Melegari SP, Perreault F, Costa RH, Popovic R, Matias WG (2013) Evaluation of toxicity and oxidative stress induced by copper oxide nanoparticles in the green alga Chlamydomonas reinhardtii. Aquat Toxicol 142:431–440

    Article  Google Scholar 

  • Muller E, Behra R, Sigg L (2015) Toxicity of engineered copper (CuO) nanoparticles to the green alga Chlamydomonas reinhardtii. Environ Chem 13:457–463

    Article  Google Scholar 

  • Nagalakshmi N, Prasad MN (1998) Copper-induced oxidative stress in Scenedesmus bijugatus: protective role of free radical scavengers. Bull Environ Contam Toxicol 61:623–628

    Article  CAS  Google Scholar 

  • Nichols HW, Bold HC (1965) Trichosarcina polymorpha gen. et sp. nov. J Phycol 1:34–38

    Article  Google Scholar 

  • Norberg-King TJ (1993) A linear interpolation method for sublethal toxicity: the inhibition concentration (ICP) approach. Version 2.0. National Effluent Toxicity Assessment Center technical report 03-93. Environmental Research Laboratory, Duluth, MN 55804, USA

  • 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 

  • Oukarroum A, Zaidi W, Samadani M, Dewez D (2017) Toxicity of nickel oxide nanoparticles on a freshwater green algal strain of Chlorella vulgaris. BioMed Res Int. https://doi.org/10.1155/2017/9528180

    Article  Google Scholar 

  • Qian H, Zhu K, Lu H, Lavoie M, Chen S, Zhou Z, Fu Z (2016) Contrasting silver nanoparticle toxicity and detoxification strategies in Microcystis aeruginosa and Chlorella vulgaris: new insights from proteomic and physiological analyses. Sci Total Environ 572:1213–1221

    Article  CAS  Google Scholar 

  • Rana S, Kalaichelvan PT (2013) Ecotoxicity of nanoparticles. ISRN Toxicol. https://doi.org/10.1155/2013/574648, 1, 11

    Article  Google Scholar 

  • Repetto M, Boveris A, Semprine J (2012) Lipid peroxidation: chemical mechanism, biological implications and analytical determination. In: Catala A (ed) Lipid peroxidation. INTECH Open, Riejeka, pp 3–30

    Google Scholar 

  • Richardson HW (1997) Handbook of copper compounds and applications. Wiley, New York

    Book  Google Scholar 

  • Rocha GS, Parrish CC, Lombardi AT, da GG Melão M (2016) Copper affects biochemical and physiological responses of Selenastrum gracile (Reinsch). Ecotoxicology 25:1468–1477

    Article  CAS  Google Scholar 

  • Rugnini L, Costa G, Congestri R, Bruno L (2017) Testing of two different strains of green microalgae for Cu and Ni removal from aqueous media. Sci Total Environ 601:959–967

    Article  Google Scholar 

  • Sadiq IM, Pakrashi S, Chandrasekaran N, Mukherjee A (2011) Studies on toxicity of aluminum oxide (Al2O3) nanoparticles to microalgae species: Scenedesmus sp. and Chlorella sp. J Nanopart Res 13:3287–3299

  • Saison C, Perreault F, Daigle JC, Fortin C, Claverie J, Morin M, Popovic R (2010) Effect of core-shell copper oxide nanoparticles on cell culture morphology and photosynthesis (photosystem II energy distribution) in the green alga, Chlamydomonas reinhardtii. Aquat Toxicol 96:109–114

    Article  CAS  Google Scholar 

  • Samadani M, Perreault F, Oukarroum A, Dewez D (2017) Effect of cadmium accumulation on green algae Chlamydomonas reinhardtii and acid-tolerant Chlamydomonas CPCC 121. Chemosphere 191:174–182

    Article  Google Scholar 

  • Sandberg J, Odnevall Wallinder I, Leygraf C, Virta M (2007) Release and chemical speciation of copper from anti-fouling paints with different active copper compounds in artificial seawater. Mater Corros 58:165–172

    Article  CAS  Google Scholar 

  • Scholes GD, Fleming GR, Olaya-Castro A, van Grondelle R (2011) Lessons from nature about solar light harvesting. Nat Chem 3:763–774

    Article  CAS  Google Scholar 

  • Schwab F, Bucheli TD, Lukhele LP, Magrez A, Nowack B, Sigg L, Knauer K (2011) Are carbon nanotube effects on green algae caused by shading and agglomeration? Environ Sci Technol 45:6136–6144

    Article  CAS  Google Scholar 

  • Singh N, Turner A (2009) Leaching of copper and zinc from spent antifouling paint particles. Environ Pollut 157:371–376

    Article  CAS  Google Scholar 

  • Soto P, Gaete H, Hidalgo ME (2011) Assessment of catalase activity, lipid peroxidation, chlorophyll-a, and growth rate in the freshwater green algae Pseudokirchneriella subcapitata exposed to copper and zinc. Lat Am J Aquat Res 39:280–285

    Article  Google Scholar 

  • Stauber JL, Florence TM (1987) Mechanism of toxicity of ionic copper and copper complexes to algae. Mar Biol 94:511–519

    Article  CAS  Google Scholar 

  • Tsai KP (2016) Management of target algae by using copper-based algaecides: effects of algal cell density and sensitivity to copper. Water Air Soil Pollut 227:1–11

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Wang Y, Zhu X, Lao Y, Lv X, Tao Y, Huang B, Wang J, Zhou J, Cai Z (2016) TiO2 nanoparticles in the marine environment: physical effects responsible for the toxicity on algae Phaeodactylum tricornutum. Sci Total Environ 565:818–826

    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 45:6032–6040

    Article  CAS  Google Scholar 

  • Wang H, Sathasivam R, Ki JS (2017) Physiological effects of copper on the freshwater alga Closterium ehrenbergii Meneghini (Conjugatophyceae) and its potential use in toxicity assessments. Algae 32:131–137

    Article  CAS  Google Scholar 

  • Yamamoto M, Kurihara I, Kawano S (2005) Late type of daughter cell wall synthesis in one of the Chlorellaceae, Parachlorella kessleri (Chlorophyta, Trebouxiophyceae). Planta 221:766–775

    Article  CAS  Google Scholar 

  • Zhao J, Cao X, Liu X, Wang Z, Zhang C, White JC, Xing B (2016) Interactions of CuO nanoparticles with the algae Chlorella pyrenoidosa: adhesion, uptake, and toxicity. Nanotoxicology 10:1297–1305

    Article  CAS  Google Scholar 

  • Zhu Y, Xu J, Lu T, Zhang M, Ke M, Fu Z, Qian H (2017) A comparison of the effects of copper nanoparticles and copper sulfate on Phaeodactylum tricornutum physiology and transcription. Environ Toxicol Pharmacol 56:43–49

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to acknowledge the International Medical University for providing the funding (Grant No. BMS I-02/2015(1)) to support this research project.

Author information

Authors and Affiliations

  1. School of Postgraduate Studies, International Medical University, 126 Jalan Jalil Perkasa 19, Bukit Jalil, 57000, Kuala Lumpur, Malaysia

    Jun-Kit Wan & Wan-Loy Chu

  2. Applied Biomedical Science and Biotechnology Division, School of Health Sciences, International Medical University, 126 Jalan Jalil Perkasa 19, Bukit Jalil, 57000, Kuala Lumpur, Malaysia

    Yih-Yih Kok

  3. Department of Pharmaceutical Chemistry, School of Pharmacy, International Medical University, 126 Jalan Jalil Perkasa 19, Bukit Jalil, 57000, Kuala Lumpur, Malaysia

    Kok-Whye Cheong

Authors
  1. Jun-Kit Wan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wan-Loy Chu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yih-Yih Kok
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kok-Whye Cheong
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wan-Loy Chu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wan, JK., Chu, WL., Kok, YY. et al. Assessing the toxicity of copper oxide nanoparticles and copper sulfate in a tropical Chlorella. J Appl Phycol 30, 3153–3165 (2018). https://doi.org/10.1007/s10811-018-1408-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-018-1408-3

Keywords

Search

Navigation