Skip to main content
Log in

Toxicological effects of copper oxide nanoparticles on the growth rate, photosynthetic pigment content, and cell morphology of the duckweed Landoltia punctata

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Recently, the application of copper oxide nanoparticles (CuO-NPs) has increased considerably, primarily in scientific and industrial fields. However, studies to assess their health risks and environmental impacts are scarce. Therefore, the present study aims to evaluate the toxicological effects of CuO-NPs on the duckweed species Landoltia punctata, which was used as a test organism. To accomplish this, duckweed was grown under standard procedures according to ISO DIS 20079 and exposed to three different concentrations of CuO-NPs (0.1, 1.0, and 10.0 g L−1), with one control group (without CuO-NPs). The toxicological effects were measured based on growth rate inhibition, changes in the plant’s morphology, effects on ultrastructure, and alterations in photosynthetic pigments. The morphological and ultrastructural effects were evaluated by electronic, scanning and light microscopic analysis, and CuO-NPs were characterized using transmission electron microscopy (TEM), zeta potential, and superficial area methods of analysis. This analysis was performed to evaluate nanoparticle size and form in solution and sample stability. The results showed that CuO-NPs affected morphology more significantly than growth rate. L. punctata also showed the ability to remove copper ions. However, for this plant to be representative within the trophic chain, the biomagnification of effects must be assessed.

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

Similar content being viewed by others

References

  • Appenroth KJ, Luther A, Jetschke G, Gabrys H (2008) Modification of chromate toxicity by sulphate in duckweeds (Lemnaceae). Aquat Toxicol 89:167–171

    Article  CAS  PubMed  Google Scholar 

  • Appenroth KJ, Krech K, Keresztes Á, Fischer W, Koloczek H (2010) Effects of nickel on the chloroplasts of the duckweeds Spirodela polyrhiza and Lemna minor and their possible use in biomonitoring and phytoremediation. Chemosphere 78:216–223

    Article  CAS  PubMed  Google Scholar 

  • Axtell NR, Sternberg SP, Claussen K (2003) Lead and nickel removal using microspora and Lemna minor. Bioresour Technol 89:41–48

    Article  CAS  PubMed  Google Scholar 

  • Chiang CY, Aroh K, Ehrman SH (2012) Copper oxide nanoparticle made by flame spray pyrolysis for photoelectrochemical water splitting e Part I. CuO nanoparticle preparation. Int J Hydrogen Energ 37:4871–4879

    Article  CAS  Google Scholar 

  • Crosera M, Bovenzi M, Maina G, Adami G, Zanette C, Florio C, Larese FF (2009) Nanoparticle dermal absorption and toxicity: a review of the literature. Int Arch Occup Environ Health. doi:10.1007/s00420-009-0458-x

    PubMed  Google Scholar 

  • Das D, Nath BC, Phukon P, Dolui SK (2013) Synthesis and evaluation of antioxidant and antibacterial behavior of CuO nanoparticles. Colloids Surf B: Biointerfaces 101:430–433

    Article  CAS  PubMed  Google Scholar 

  • Drost W, Matzke M, Backhaus T (2007) Heavy metal toxicity to Lemna minor: studies on the time dependence of growth inhibition and the recovery after exposure. Chemosphere 67:36–43

    Article  CAS  PubMed  Google Scholar 

  • Fernandes JC, Henriques FS (1991) Biochemical, physiological, and structural effects of excess copper in plants. Bot Rev. doi:10.1007/BF02858564

  • Gouveia C, Kreusch M, Schmidt EC, Felix MRL, Osorio LKP, Pereira DT, Santos R, Ouriques LC, Martins RP, Latini A, Ramlov F, Carvalho TJG, Chow F, Maraschin M, Bouzon ZL (2013) The effects of lead and copper on the cellular architecture and metabolism of the red alga gracilaria domingensis. Microsc Microanal 19:513–524

  • Gubbins EJ, Batty LC, Lead JR (2011) Phytotoxicity of silver nanoparticles to Lemna minor L. Environ Pollut 159:1551–1559

    Article  CAS  PubMed  Google Scholar 

  • Hiscox JD, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1334

  • Hou W, Chen X, Song G, Wang Q, Chang CC (2007) Effects of copper and cadmium on heavy metal polluted waterbody restoration by duckweed (Lemna minor). Plant Physiol Biochem 45:62–69

    Article  CAS  PubMed  Google Scholar 

  • ISO 20079 (2005) Water quality—determination of toxic effect of water constituents and waste water to duckweed (Lemna minor)—Duckweed growth inhibition test. DRAFT INTERNATIONAL STANDARD

  • Juhel G, Batisse E, Hugues Q, Daly D, van Pelt FNAM, O’Halloran J, Jansen MAK (2011) Alumina nanoparticles enhance growth of L. minor. Aquat Toxicol 105:328–336

    Article  CAS  PubMed  Google Scholar 

  • Khellaf N, Zerdaoui M (2010) Growth, photosynthesis and respiratory response to copper in Lemna minor: a potential use of duckweed in biomonitoring. Iran J Environ Health Sci Eng 7(4):299–306

    CAS  Google Scholar 

  • Li L, Sillanp M, Tuominen M, Lounatmaa K, Schultz E (2013) Behavior of titanium dioxide nanoparticles in Lemna minor growth test conditions. Ecotoxicol Environ Saf 88:89–94

    Article  CAS  PubMed  Google Scholar 

  • Marchand L, Mench M, Marchand C, Le Coustumer P, Kolbas A, Maalouf JP (2011) Phytotoxicity testing of lysimeter leachates from aided phytostabilized Cu-contaminated soils using duckweed (Lemna minor L.). Sci Total Environ 410–411:146–153

    Article  PubMed  Google Scholar 

  • Miao AJ, Schwehr KA, Xu C, Zhang SJ, Luo Z, Quigg A, Santschi PH (2009) The algal toxicity of silver engineered nanoparticles and detotoxification by exopolymeric substances. Environ Pollut. doi:10.1016/j.envpol.2009.05.047

  • Naumann B, Eberius M, Appenroth KJ (2007) Growth rate based dose–response relationships and EC-values of ten heavy metals using the duckweed growth inhibition test (ISO 20079) with Lemna minor L. clone St. J Plant Physiol 164:1656–1664

    Article  CAS  PubMed  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. Ecotoxicol. doi:10.1007/s10646-008-0214-0

  • OECD (2002) Guidelines for the testing of chemicals: revised proposal for a new guideline 221—Lemna sp. Growth Inhibition Test. http://www.oecd.org/chemicalsafety/testing/1948054.pdf. Accessed 26 Sept 2013

  • Patsikka E, Kairavuo M, Sersen F, Aro EM, Tyystjarvi E (2002) Excess copper predisposes photosystem II to photoinhibition in vivo by outcompeting iron and causing decrease in leaf chlorophyll. Plant Physiol. doi:10.1104/pp.004788

  • Perreault F, Oukarroum A, Pirastru L, Sirois L, Matias WG, Popovic R (2010) Evaluation of copper oxide nanoparticles toxicity using chlorophyll a fluorescence imaging in Lemna gibba. J Bot. doi:10.1155/2010/763142

    Google Scholar 

  • Perreault F, Samadani M, Dewez D (2013) Effect of soluble copper released from copper oxide nanoparticles solubilisation on growth and photosynthetic processes of Lemna gibba L. Nanotoxicology. doi:10.3109/17435390.2013.789936

    PubMed  Google Scholar 

  • Powers KW, Palazuelos M, Moudgil BM, Roberts SM (2007) Characterization of the size, shape, and state of dispersion of nanoparticles for toxicological studies. Nanotoxicology. doi:10.1080/17435390701314902

    Google Scholar 

  • Prasad MNV, Malec P, Waloszek A, Bojko M, Strzalka K (2001) Physiological responses of Lemna trisulca L. (duckweed) to cadmium and copper bioaccumulation. Plant Sci. doi:10.1016/S0168-9452(01)00478-2

  • Quina FH (2004) Nanotecnologia e o meio ambiente: perspectivas e riscos. Quim Nova. doi:10.1590/S0100-40422004000600031

    Google Scholar 

  • Radić S, Babić M, Skobić D, Roje V, Pevalek-Kozlina B (2010) Ecotoxicological effects of aluminum and zinc on growth and antioxidants in Lemna minor L. Ecotoxicol Environ Saf 73:336–342

    Article  PubMed  Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212

  • Rosseto ALOF (2012) Estudo comparativo entre os efeitos tóxicos agudos e crônicos do óxido de cobre na forma de nanopartícula e micropartícula. Dissertation, Universidade Federal de Santa Catarina

  • Schmidt ÉC, Rover T, Scariot L, Bouzon ZL (2009) Changes in ultrastructure and histochemistry of two red macroalgae strains of Kappaphycus alvarezii (Rhodophyta, Gigartinales), as a consequence of ultraviolet B radiation exposure. Micron 40:860–869

    Article  CAS  PubMed  Google Scholar 

  • Schmidt ÉC, Maraschin M, Bouzon ZL (2010a) Effects of UVB radiation on the carragenophyte Kappaphycus alvarezii (Rhodophyta, Gigartinales): changes in ultrastructure, growth, and photosynthetic pigments. Hydrobiologia 649:171–182

    Article  CAS  Google Scholar 

  • Schmidt ÉC, Nunes BG, Maraschin M, Bouzon ZL (2010b) Effect of ultraviolet-B radiation on growth, photosynthetic pigments, and cell biology of Kappaphycus alvarezii (Rhodophyta, Gigartinales) macroalgae brown strain. Photosynthetica 48:161–172

    Article  CAS  Google Scholar 

  • Schmidt ÉC, Santos R, Horta PA, Maraschin M, Bouzon ZL (2010c) Effects of UVB radiation on the agarophyte Gracilaria domingensis (Rhodophyta, Gracilariales): changes in cell organization, growth and photosynthetic performance. Micron 41:919–930

    Article  CAS  PubMed  Google Scholar 

  • Schmidt ÉC, Pereira B, Santos R, Gouveia C, Costa GB, Faria GSM, Scherner F, Horta PA, Paula MR, Latini A, Ramlov F, Maraschin M, Bouzon ZL (2012) Responses of the macroalgae Hypnea musciformis after in vitro exposure to UV-B. Aquat Bot 100:8–17

    Article  CAS  Google Scholar 

  • Sharma SS, Gaur JP (1995) Potential of Lemna polyrrhiza for removal of heavy metals. Ecol Eng 4:37–43

    Article  Google Scholar 

  • Shaw AJ (1989) Heavy metal tolerance in plants: evolutionary aspects. CRC Press, New York, 355p

    Google Scholar 

  • Shi J, Abid AD, Kennedy IM, Hristova KR, Silk WK (2011) To duckweeds (Landoltia punctata), nanoparticulate copper oxide is more inhibitory than the soluble copper in the bulk solution? Environ Pollut 159:1277–1282

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Upadhyay R, Panda SK (2010) Zinc reduces copper toxicity induced oxidative stress by promoting antioxidant defense in freshly grown aquatic duckweed Spirodela polyrhiza L. J Hazard Mater 175:1081–1084

    Article  CAS  PubMed  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  PubMed  Google Scholar 

  • Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313

  • Zha LY, Xu ZR, Wang MQ, Gu LY (2007) Chromium nanoparticle exhibits higher absorption efficiency than chromium picolinate and chromium chloride in Caco-2 cell monolayers. J Anim Physiol Anim Nutr. doi:10.1111/j.1439-0396.2007.00718

    Google Scholar 

Download references

Acknowledgments

This work was supported by research grants from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Brazil. The authors thank the LCME (Central Laboratory of Electronic Microscopy at Federal University of Santa Catarina) and Dr. José Julio Barrios Restrepo (Federal University of Santa Catarina) for their kind assistance.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to William Gerson Matias.

Additional information

Handling Editor: DAMJANA Drobne

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lalau, C.M., Mohedano, R.d.A., Schmidt, É.C. et al. Toxicological effects of copper oxide nanoparticles on the growth rate, photosynthetic pigment content, and cell morphology of the duckweed Landoltia punctata . Protoplasma 252, 221–229 (2015). https://doi.org/10.1007/s00709-014-0671-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-014-0671-7

Keywords

Navigation