Toxicity of engineered copper (Cu0) nanoparticles to the green alga Chlamydomonas reinhardtii
Emanuel Müller A B , Renata Behra A B and Laura Sigg A B C
+ Author Affiliations
- Author Affiliations
A Eawag, Swiss Federal Institute of Aquatic Science and Technology, CH-8600 Dübendorf, Switzerland.
B ETH (Eidgenössische Technische Hochschule) Zürich, Swiss Federal Institute of Technology, Institute of Biogeochemistry and Pollutant Dynamics, CH-8092 Zürich, Switzerland.
C Corresponding author: laura.sigg@eawag.ch
Environmental Chemistry 13(3) 457-463 https://doi.org/10.1071/EN15132
Submitted: 24 June 2015 Accepted: 18 September 2015 Published: 30 November 2015
Environmental context. Engineered copper nanoparticles are presently under development for various uses and may thus be finally released into the aquatic environment. Copper is well known to be both an essential and a toxic element for aquatic organisms. Here, we investigate the toxicity of copper nanoparticles to a green alga and compare it with the toxicity of dissolved copper.
Abstract. The toxicity of carbon-coated copper nanoparticles (CuNPs) to the unicellular green alga Chlamydomonas reinhardtii was investigated and compared with effects of dissolved Cu2+. The CuNPs with an original size of 6–7 nm rapidly agglomerated in the medium to average particle sizes of 140–200 nm. Dissolved Cu from CuNPs increased over 2 h to 1–2 % of total Cu. The photosynthetic yield of C. reinhardtii strongly decreased after exposure for 1 or 2 h to dissolved CuII in the concentration range 0.1–10 μM, whereas this decrease occurred in the total Cu concentration range 1–100 μM after exposure to CuNPs. Effects of CuNPs were compared with those of dissolved CuII on the basis of dissolution experiments. CuNP effects on photosynthetic yield were similar or somewhat stronger for the same dissolved Cu2+ concentration. Addition of EDTA as a strong ligand for CuII suppressed the toxicity of dissolved CuII and of CuNPs. These results thus indicate effects on the algae are mostly from free Cu2+.
References
[1] B. Nowack, T. D. Bucheli, Occurrence, behavior and effects of nanoparticles in the environment. Environ. Pollut. 2007, 150, 5.| Occurrence, behavior and effects of nanoparticles in the environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtF2mt7vJ&md5=ae29f6a198dd4bed1462903d23740273CAS | 17658673PubMed |
[2] B. Nowack, J. F. Ranville, S. Diamond, J. A. Gallego-Urrea, C. Metcalfe, J. Rose, N. Horne, A. A. Koelmans, S. J. Klaine, Potential scenarios for nanomaterial release and subsequent alteration in the environment. Environ. Toxicol. Chem. 2012, 31, 50.
| Potential scenarios for nanomaterial release and subsequent alteration in the environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1yktr7M&md5=687c136c137b531bcb52bbf6c458ec45CAS | 22038832PubMed |
[3] S. J. Klaine, P. J. J. Alvarez, G. E. Batley, T. F. Fernandes, R. D. Handy, D. Y. Lyon, S. Mahendra, M. J. McLaughlin, J. R. Lead, Nanomaterials in the environment: behavior, fate, bioavailability, and effects. Environ. Toxicol. Chem. 2008, 27, 1825.
| Nanomaterials in the environment: behavior, fate, bioavailability, and effects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVersLjJ&md5=db8b539a7b7c8782cda2e5885df35098CAS | 19086204PubMed |
[4] K. C. Anyaogu, A. V. Fedorov, D. C. Neckers, Synthesis, characterization, and antifouling potential of functionalized copper nanoparticles. Langmuir 2008, 24, 4340.
| Synthesis, characterization, and antifouling potential of functionalized copper nanoparticles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtlOju7g%3D&md5=91506f868f2a5a249f4c2c148c88d2c8CAS | 18341370PubMed |
[5] N. Cioffi, L. Torsi, N. Ditaranto, G. Tantillo, L. Ghibelli, L. Sabbatini, T. Bleve-Zacheo, M. D’Alessio, P. G. Zambonin, E. Traversa, Copper nanoparticle/polymer composites with antifungal and bacteriostatic properties. Chem. Mater. 2005, 17, 5255.
| Copper nanoparticle/polymer composites with antifungal and bacteriostatic properties.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVWnurvL&md5=33e20ba8d92bf8d6429e07d59a296c3cCAS |
[6] N. Odzak, D. Kistler, R. Behra, L. Sigg, Dissolution of metal and metal oxide nanoparticles in aqueous media. Environ. Pollut. 2014, 191, 132.
| Dissolution of metal and metal oxide nanoparticles in aqueous media.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXpslKqsL8%3D&md5=3d7500cc099b1f1e9ce4ec33d4ff9aa7CAS | 24832924PubMed |
[7] I. A. Mudunkotuwa, J. M. Pettibone, V. H. Grassian, Environmental implications of nanoparticle aging in the processing and fate of copper-based nanomaterials. Environ. Sci. Technol. 2012, 46, 7001.
| Environmental implications of nanoparticle aging in the processing and fate of copper-based nanomaterials.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XovFehsg%3D%3D&md5=37aead724dc2a301090ac8e824870a27CAS | 22280489PubMed |
[8] W. Sunda, R. R. L. Guillard, The relationship between cupric ion activity and the toxicity of copper to phytoplankton. J. Mar. Res. 1976, 34, 511.
| 1:CAS:528:DyaE2sXjvVaqtA%3D%3D&md5=b1aac45dd2dc7e5e4633a80b59af77daCAS |
[9] F. M. M. Morel, N. M. Price, The biogeochemical cycles of trace metals in the oceans. Science 2003, 300, 944.
| The biogeochemical cycles of trace metals in the oceans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjsVyjsLk%3D&md5=c9e39d3fdfa28c650219e4b0f457a654CAS |
[10] W. G. Sunda, S. A. Huntsman, Regulation of copper concentration in the oceanic nutricline by phytoplankton uptake and regeneration cycles. Limnol. Oceanogr. 1995, 40, 132.
| Regulation of copper concentration in the oceanic nutricline by phytoplankton uptake and regeneration cycles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmtFaitbs%3D&md5=32b851111d2c6719e3e4b5674e252bddCAS |
[11] E. Rue, K. W. Bruland, Domoic acid binds iron and copper: a possible role for the toxin produced by the marine diatom Pseudo-nitzschia. Mar. Chem. 2001, 76, 127.
| Domoic acid binds iron and copper: a possible role for the toxin produced by the marine diatom Pseudo-nitzschia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXntlKns7g%3D&md5=55597fc7ef3181436ebcfa66ceaf4514CAS |
[12] P. L. Croot, B. Karlson, J. T. Van Elteren, J. J. Kroon, Uptake of 64Cu-oxine by marine phytoplankton. Environ. Sci. Technol. 1999, 33, 3615.
| Uptake of 64Cu-oxine by marine phytoplankton.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlslOms7c%3D&md5=b15038268cf2cab4bde1649472c0debbCAS |
[13] K. Knauer, R. Behra, L. Sigg, Effects of free Cu2+ and Zn2+ on growth and metal accumulation in freshwater algae. Environ. Toxicol. Chem. 1997, 16, 220.
| Effects of free Cu2+ and Zn2+ on growth and metal accumulation in freshwater algae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhsFahsbw%3D&md5=a8959e44d6454f7b65ed1678a13a8036CAS |
[14] P. G. C. Campbell, O. Errécalde, C. Fortin, V. P. Hiriart-Baer, B. Vigneault, Metal bioavailability to phytoplankton – applicability of the biotic ligand model. Comp. Biochem. Physiol. C 2002, 133, 189.
[15] A.-J. Miao, W.-X. Wang, P. Juneau, Comparison of Cd, Cu, and Zn toxic effects on four marine phytoplankton by pulse-amplitude-modulated fluorometry. Environ. Toxicol. Chem. 2005, 24, 2603.
| Comparison of Cd, Cu, and Zn toxic effects on four marine phytoplankton by pulse-amplitude-modulated fluorometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVKqt7bM&md5=b0cea26c2ffa858920dd693fd33b5c8eCAS | 16268163PubMed |
[16] H. Küpper, I. Setlik, E. Setlikova, N. Ferimazova, M. Spiller, F. C. Kupper, Copper-induced inhibition of photosynthesis: limiting steps of in vivo copper chlorophyll formation in Scenedesmus quadricauda. Funct. Plant Biol. 2003, 30, 1187.
| Copper-induced inhibition of photosynthesis: limiting steps of in vivo copper chlorophyll formation in Scenedesmus quadricauda.Crossref | GoogleScholarGoogle Scholar |
[17] C. Saison, F. Perreault, J.-C. Daigle, C. Fortin, J. Claverie, M. Morin, R. Popovic, 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. 2010, 96, 109.
| Effect of core-shell copper oxide nanoparticles on cell culture morphology and photosynthesis (photosystem II energy distribution) in the green alga, Chlamydomonas reinhardtii.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtValt7w%3D&md5=51c59222fb0231c730cf6730ee4b67ddCAS | 19883948PubMed |
[18] Z. Wang, J. Li, J. Zhao, B. Xing, Toxicity and internalization of CuO nanoparticles to prokaryotic alga Microcystis aeruginosa as Affected by dissolved organic matter. Environ. Sci. Technol. 2011, 45, 6032.
| Toxicity and internalization of CuO nanoparticles to prokaryotic alga Microcystis aeruginosa as Affected by dissolved organic matter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXotVOns7w%3D&md5=c2a66347baa9f4fcb02345b6de6d1e1fCAS | 21671609PubMed |
[19] L. Manusadžianas, C. Caillet, L. Fachetti, B. Gylyte, R. Grigutyte, S. Jurkoniene, R. Karitonas, K. Sadauskas, F. Thomas, R. Vitkus, J.-F. Ferard, Toxicity of copper oxide nanoparticle suspensions to aquatic biota. Environ. Toxicol. Chem. 2012, 31, 108.
| Toxicity of copper oxide nanoparticle suspensions to aquatic biota.Crossref | GoogleScholarGoogle Scholar | 22020877PubMed |
[20] F. Perreault, A. Oukarroum, S. P. Melegari, W. G. Matias, R. Popovic, Polymer coating of copper oxide nanoparticles increases nanoparticles uptake and toxicity in the green alga Chlamydomonas reinhardtii. Chemosphere 2012, 87, 1388.
| Polymer coating of copper oxide nanoparticles increases nanoparticles uptake and toxicity in the green alga Chlamydomonas reinhardtii.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XkvVGksLs%3D&md5=7254e610ce6f83cdbe6cd4392bd1893aCAS | 22445953PubMed |
[21] O. Bondarenko, K. Juganson, A. Ivask, K. Kasemets, M. Mortimer, A. Kahru, Toxicity of Ag, CuO and ZnO nanoparticles to selected environmentally relevant test organisms and mammalian cells in vitro: a critical review. Arch. Toxicol. 2013, 87, 1181.
| Toxicity of Ag, CuO and ZnO nanoparticles to selected environmentally relevant test organisms and mammalian cells in vitro: a critical review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXosFyqsbo%3D&md5=4e6f4a2168f79bb15343a1d4c2933412CAS | 23728526PubMed |
[22] F. Perreault, M. Samadani, D. Dewez, Effect of soluble copper released from copper oxide nanoparticles solubilisation on growth and photosynthetic processes of Lemna gibba L. Nanotoxicology 2014, 8, 374.
| Effect of soluble copper released from copper oxide nanoparticles solubilisation on growth and photosynthetic processes of Lemna gibba L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvFemtLnP&md5=f74d53fefccab06b85db08b545eaec94CAS | 23521766PubMed |
[23] V. Aruoja, H. C. Dubourguier, K. Kasemets, A. Kahru, Toxicity of nanoparticles of CuO, ZnO and TiO2 to microalgae Pseudokirchneriella subcapitata. Sci. Total Environ. 2009, 407, 1461.
| Toxicity of nanoparticles of CuO, ZnO and TiO2 to microalgae Pseudokirchneriella subcapitata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVOmsrvP&md5=42a41a4bac8c7f46db50240492642105CAS | 19038417PubMed |
[24] L. Song, M. Connolly, M. L. Fernández-Cruz, M. G. Vijver, M. Fernández, E. Conde, G. R. de Snoo, W. J. G. M. Peijnenburg, J. M. Navas, Species-specific toxicity of copper nanoparticles among mammalian and piscine cell lines. Nanotoxicology 2014, 8, 383.
| Species-specific toxicity of copper nanoparticles among mammalian and piscine cell lines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvFemtLbP&md5=cbc1804665a5cd2cb6ab3aabede78fcbCAS | 23600739PubMed |
[25] F. Piccapietra, C. Gil-Allué, L. Sigg, R. Behra, Intracellular silver accumulation in Chlamydomonas reinhardtii upon exposure to carbonate-coated silver nanoparticles and silver nitrate. Environ. Sci. Technol. 2012, 46, 7390.
| Intracellular silver accumulation in Chlamydomonas reinhardtii upon exposure to carbonate-coated silver nanoparticles and silver nitrate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XnvF2ktrc%3D&md5=3678fdf489dcc8b89dbc71d3ea77801eCAS | 22667990PubMed |
[26] E. Navarro, F. Piccapietra, B. Wagner, F. Marconi, R. Kaegi, N. Odzak, L. Sigg, R. Behra, Toxicity of silver nanoparticles to Chlamydomonas reinhardtii. Environ. Sci. Technol. 2008, 42, 8959.
| Toxicity of silver nanoparticles to Chlamydomonas reinhardtii.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFOqt7nO&md5=755432a47d7e3de51aa8c899bb99feb3CAS | 19192825PubMed |
[27] K. Groh, T. Dalkvist, F. Piccapietra, R. Behra, M. Suter, K. Schirmer, Critical influence of chloride ions on silver ion-mediated acute toxicity of silver nanoparticles to zebrafish embryos. Nanotoxicology 2015, 9, 81.
| Critical influence of chloride ions on silver ion-mediated acute toxicity of silver nanoparticles to zebrafish embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXltFehsLY%3D&md5=b9fc0fd84c8c0b6507f534b732f650acCAS | 24625062PubMed |
[28] X. Yang, A. P. Gondikas, S. M. Marinakos, M. Auffan, J. Liu, H. Hsu-Kim, J. N. Meyer, Mechanism of silver nanoparticle toxicity is dependent on dissolved silver and surface coating in Caenorhabditis elegans. Environ. Sci. Technol. 2012, 46, 1119.
| Mechanism of silver nanoparticle toxicity is dependent on dissolved silver and surface coating in Caenorhabditis elegans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFygt7vN&md5=405a52bb51aca60821dd3899ce3aa76fCAS | 22148238PubMed |
[29] Y. Yue, R. Behra, L. Sigg, P. Fernandez Freire, S. Pillai, K. Schirmer, Toxicity of silver nanoparticles to a fish gill cell line: role of medium composition. Nanotoxicology 2015, 9, 54.
| Toxicity of silver nanoparticles to a fish gill cell line: role of medium composition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXltFehs7k%3D&md5=949a3242412ff59292287388e360e7b6CAS | 24621324PubMed |
[30] S. Pillai, R. Behra, H. Nestler, M. J. F. Suter, L. Sigg, K. Schirmer, Linking toxicity and adaptive responses across the transcriptome, proteome, and phenotype of Chlamydomonas reinhardtii exposed to silver. Proc. Natl. Acad. Sci. USA 2014, 111, 3490.
| Linking toxicity and adaptive responses across the transcriptome, proteome, and phenotype of Chlamydomonas reinhardtii exposed to silver.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjtlyrurY%3D&md5=fc5b731cd6a8df2ed2cfed43bc9c28dfCAS | 24550482PubMed |
[31] S. Gass, J. M. Cohen, G. Pyrgiotakis, G. A. Sotiriou, S. E. Pratsinis, P. Demokritou, Safer formulation concept for flame-generated engineered nanomaterials. ACS Sustain. Chem.& Eng. 2013, 1, 843.
| 1:CAS:528:DC%2BC3sXltVCltL0%3D&md5=2f5834d881969d5866628a3f62338c07CAS |
[32] M. L. Eggersdorfer, S. E. Pratsinis, Agglomerates and aggregates of nanoparticles made in the gas phase. Adv. Powder Technol. 2014, 25, 71.
| Agglomerates and aggregates of nanoparticles made in the gas phase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVagtrzL&md5=e772d852a03a9a77d56ea57cb2f9b8e5CAS |
[33] S. Le Faucheur, R. Behra, L. Sigg, Phytochelatin induction, cadmium accumulation and algal sensitivity to free cadmium ions in Scenedesmus vacuolatus. Environ. Toxicol. Chem. 2005, 24, 1731.
| Phytochelatin induction, cadmium accumulation and algal sensitivity to free cadmium ions in Scenedesmus vacuolatus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlslWrsrs%3D&md5=5d74a14b0d0eb0f5beff15c7e842ba28CAS | 16050590PubMed |
[34] E. Navarro, A. Baun, R. Behra, N. B. Hartmann, J. Filser, A. J. Miao, A. Quigg, P. H. Santschi, L. Sigg, Environmental behaviour and ecotoxicity of engineered nanoparticles to algae, plants and fungi. Ecotoxicology 2008, 17, 372.
| Environmental behaviour and ecotoxicity of engineered nanoparticles to algae, plants and fungi.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmsVKrsLc%3D&md5=bd0c43cd3b40073839874f44ea37a2a8CAS | 18461442PubMed |
[35] C. Nickel, J. Angelstorf, R. Bienert, C. Burkart, S. Gabsch, S. Giebner, A. Haase, B. Hellack, H. Hollert, K. Hund-Rinke, D. Jungmann, H. Kaminski, A. Luch, H. Maes, A. Nogowski, M. Oetken, A. Schaeffer, A. Schiwy, K. Schlich, M. Stintz, F. von der Kammer, T. J. Kuhlbusch, Dynamic light-scattering measurement comparability of nanomaterial suspensions. J. Nanopart. Res. 2014, 16, 2260.
| Dynamic light-scattering measurement comparability of nanomaterial suspensions.Crossref | GoogleScholarGoogle Scholar |
[36] N. Odzak, D. Kistler, R. Behra, L. Sigg, Dissolution of metal and metal oxide nanoparticles under natural freshwater conditions. Environ. Chem. 2015, 12, 138.
| Dissolution of metal and metal oxide nanoparticles under natural freshwater conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXltVWmsr0%3D&md5=58809246df1b22f3b5f17b17057c0e16CAS |
[37] F. Schwab, T. D. Bucheli, L. P. Lukhele, A. Magrez, B. Nowack, L. Sigg, K. Knauer, Are carbon nanotube effects on green algae caused by shading and agglomeration? Environ. Sci. Technol. 2011, 45, 6136.
| Are carbon nanotube effects on green algae caused by shading and agglomeration?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvF2js7s%3D&md5=0ba2c2848739dec0710edf1612448bfdCAS | 21702508PubMed |
[38] E. Navarro, B. Wagner, N. Odzak, L. Sigg, R. Behra, Effects of differently coated silver nanoparticles on photosynthesis in Chlamydomonas reinhardtii. Environ. Sci. Technol. 2015, 49, 8041.
| Effects of differently coated silver nanoparticles on photosynthesis in Chlamydomonas reinhardtii.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXovF2qs7w%3D&md5=add0735c0b0d5cf681c7c34ac4126d09CAS | 26018638PubMed |
[39] M. Vaara, Agents that increase the permeability of the outer membrane. Microbiol. Rev. 1992, 56, 395.
| 1:CAS:528:DyaK3sXjsFCktQ%3D%3D&md5=8800c04f01e8ef6d08b4a34250fd0b7fCAS | 1406489PubMed |
[40] C. S. Hassler, V. I. Slaveykova, K. J. Wilkinson, Discriminating between intra- and extracellular metals using chemical extractions. Limnol. Oceanogr. Methods 2004, 2, 237.
| Discriminating between intra- and extracellular metals using chemical extractions.Crossref | GoogleScholarGoogle Scholar |
[41] L. Sigg, Metals as water quality parameters – role of speciation and bioavailability, in Comprehensive Water Quality and Purification (Ed. S. Ahuja) 2014, pp. 315–329 (Elsevier: Oxford, UK).
