Abstract
The aim of this study was to investigate the effect of pH 4 and 7 on the cellular toxicity impact of silver nanoparticles (AgNPs) on the green alga Chlamydomonas acidophila. Changes in chlorophyll content, cellular viability, and reactive oxygen species (ROS) formation were determined permitting the characterization of the toxicity of AgNPs. Chemical characterization of AgNPs in suspension showed that nanoparticle size distribution was dependent to the pH of the culture medium, and a higher solubility was observed at pH 4 compared to that at pH 7. After 24 h of exposure, results indicated that the chlorophyll content and cellular viability decreased significantly, while the intracellular ROS production increased significantly, in relation to the increasing concentration of AgNPs (0.1–100 mg/L). Therefore, our results demonstrated that AgNP-induced toxicity was pH dependent as indicated by the cytotoxicity mediated through the induction of oxidative stress. In conclusion, the characterization of the physicochemical properties of AgNPs in aqueous solution having different pH is essential for the understanding of their toxicity impact on algal cells.
Similar content being viewed by others
References
AshaRani, P. V., Mun, G. L. K., Hande, M. P., & Valiyaveettil, S. (2009). Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano, 32, 79–290.
Baalousha, M., Manciulea, A., Cumberland, S., & Kendall, K. (2008). Aggregation and surface properties of iron oxide nanoparticles: influence of pH and natural organic matter. Environmental Toxicology and Chemistry, 27, 1875–1882.
Campbell, P. G. C., & Stokes, P. M. (1985). Acidification and toxicity of metals to aquatic biota. Canadian Journal of Fisheries and Aquatic Sciences, 42, 2034–2049.
Carlson, C., Hussain, S. M., Schrand, A. M., Braydich-Stolle, L. K., Hess, K. L., Jones, R. L., et al. (2008). Unique cellular interaction of silver nanoparticles: size-dependent generation of reactive oxygen species. Journal of Physical Chemistry B, 112, 13608–13619.
Choi, O., & Hu, Z. (2008). Size dependent and reactive oxygen species related nanosilver toxicity to nitrifying bacteria. Environmental Science and Technology, 42, 4583–4588.
Dewez, D., & Oukarroum, A. (2012). Alteration of photosystem II photochemistry induced by silver nanoparticles on the green alga Chlamydomonas reinhardtii indicated by chlorophyll a fluorescence. Toxicological and Environmental Chemistry, 94, 1536–1546.
Fabrega, J., Luoma, S. N., Tyler, C. R., Galloway, T. S., & Lead, J. R. (2011). Silver nanoparticles: behaviour and effects in the aquatic environment. Environment International, 37, 517–531.
Franklin, N. M., Stauber, J. L., Markich, S. J., & Lim, R. P. (2000). pH-dependent toxicity of copper and uranium to a tropical freshwater alga (Chlorella sp.). Aquatic Toxicology, 48, 275–289.
Franklin, N. M., Rogers, N. J., Apte, S. C., Batley, G., Gadd, G. E., & Casey, P. S. (2007). Comparative toxicity of nanoparticulate ZnO, bulk ZnO and ZnCl2 to a freshwater microalga (Pseudokirchneriella subcapitata): the importance of particle solubility. Environmental Science and Technology, 41, 8484–8490.
Ghosh, S., Mashayekhi, H., Pan, B., Bhowmik, P., & Xing, B. (2008). Colloidal behavior of aluminum oxide nanoparticles as affected by pH and natural organic matter. Langmuir, 24, 12385–12391.
Jiang, J., Oberdörster, G., & Biswas, P. (2009). Characterization of size, surface charge, and agglomeration state of nanoparticle dispersions for toxicological studies. Journal of Nanoparticle Research, 11, 77–89.
Keller, A. A., Wang, H. T., Zhou, D. X., Lenihan, H. S., Cherr, G., Cardinale, B. J., et al. (2010). Stability and aggregation of metal oxide nanoparticles in natural aqueous matrices. Environmental Science and Technology, 44, 1962–1967.
Kim, E., Kim, S. H., Kim, H. C., Lee, S. G., Lee, S. J., & Jeong, S. W. (2011). Growth inhibition of aquatic plant caused by silver and titanium oxide nanoparticles. Toxicology and Environmental Health Sciences, 3, 1–6.
Lessmann, D., Fyson, A., & Nixdorf, B. (2000). Phytoplankton of the extremely acidic mining lakes of Lusatia (Germany) with pH < 3. Hydrobiologia, 433, 123–128.
Levard, C., Hotze, E. M., Lowry, G. V., & Brown, G. E., Jr. (2012). Environmental transformations of silver nanoparticles: impact on stability and toxicity. Environmental Science and Technology, 46, 6900–6914.
Macfie, S. M., Tarmohamed, Y., & Welbourn, P. M. (1994). Effects of cadmium, cobalt, copper, and nickel on growth of the green alga Chlamydomonas reinhardtii: the influences of the cell wall and pH. Archives of Environmental Contamination and Toxicology, 27, 454–458.
Mayer, P., Kuhel, R., & Nyholm, N. (1997). A simple in vitro fluorescence method for biomass measurements in algal growth inhibition tests. Water Research, 31, 2525–2531.
Meador, J. P. (1991). The interaction of pH, dissolved organic carbon and total copper in the determination of ionic copper and toxicity. Aquatic Toxicology, 19, 13–32.
Miao, A. J., Schwehr, K. A., Xu, C., Zhang, S. J., Luo, Z., Quigg, A., et al. (2009). The algal toxicity of silver engineered nanoparticles and detoxification by exopolymeric substances. Environmental Pollution, 157, 3034–3041.
Navarro, E., Piccapietra, F., Wagner, B., Marconi, F., Kaegi, R., Odzak, N., et al. (2008). Toxicity of silver nanoparticles to Chlamydomonas reinhardtii. Environmental Science and Technology, 42, 8959–8964.
Nel, A., Xia, T., Mädler, L., & Li, N. (2006). Toxic potential of materials at the nanolevel. Science, 311, 622–627.
Olaveson, M. M., & Stokes, P. M. (1989). Responses of the acidophilic alga Euglena mutabilis (Euglenophyceae) to carbon enrichment at pH 3. Journal of Phycology, 25, 529–539.
Oukarroum, A., Polchtchikov, S., Perreault, F., & Popovic, R. (2012a). Temperature influence on silver nanoparticles inhibitory on photosystem II photochemistry in two green algae, Chlorella vulgaris and Dunaliella tertiolecta. Environmental Science and Pollution Research, 19, 1755–1762.
Oukarroum, A., Bras, S., Perreault, F., & Popovic, R. (2012b). Inhibitory effects of silver nanoparticles in two green algae, Chlorella vulgaris and Dunaliella tertiolecta. Ecotoxicology and Environmental Safety, 78, 80–85.
Oukarroum, A., Barhoumi, L., Pirastru, L., & Dewez, D. (2013). Silver nanoparticles toxicity effect on growth and cellular viability of the aquatic plant Lemna gibba. Environmental Toxicology and Chemistry, 32, 902–907.
Panessa-Warren, B. J., Maye, M. M., Warren, J. B., & Crosson, K. M. (2009). Single walled carbon nanotube reactivity and cytotoxicity following extended aqueous exposure. Environmental Pollution, 157, 1140–1151.
Petit, A. N., Eullaffroy, P., Debenest, T., & Gagné, F. (2010). Toxicity of PAMAM dendrimers to Chlamydomonas reinhardtii. Aquatic Toxicology, 100, 187–193.
Petit, A. N., Debenest, T., Eullaffroy, P., & Gagné, F. (2012). Effects of a cationic PAMAM dendrimer on photosynthesis and ROS production of Chlamydomonas reinhardtii. Nanotoxicology, 6, 315–326.
Regel, R. H., Ferris, J. M., Ganf, G. G., & Brookes, J. D. (2002). Algal esterase activity as a biomeasure of environmental degradation in a freshwater creek. Aquatic Toxicology, 59, 209–223.
Sager, T. M., Porter, D. W., Robinson, V. A., Lindsley, W. G., Schwegler-Berry, D. E., & Castranova, V. (2007). Improved method to disperse nanoparticles for in vitro and in vivo investigation of toxicity. Nanotoxicology, 1, 118–129.
Schubauer-Berigan, M. K., Dierkes, J. R., Monson, P. D., & Ankley, G. T. (1993). pH-dependent toxicity of Cd, Cu, Ni, Pb, and Zn to Ceriodaphnia dubia, Pimephales promelas, Hyalella azteca, and Lumbriculus variegatus. Environmental Toxicology and Chemistry, 12, 1261–1266.
Szivák, I., Behra, R., & Sigg, L. (2009). Metal-induced reactive oxygen species production in Chlamydomonas reinhardtii (Chlorophyceae). Journal of Phycology, 45, 427–435.
Turner, A., Brice, D., & Brown, M. T. (2012). Interactions of silver nanoparticles with the marine macroalga, Ulva lactuca. Ecotoxicology, 21, 148–154.
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.
Wellburn, R. (1994). The spectral determination of chlorophyll a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Journal of Plant Physiology, 144, 307–313.
Wetzel, R. G. (2001). Limnology-Lake and River Ecosystems. San Diego: Academic.
Xia, T., Kovochich, M., Liong, M., Madler, L., Gilbert, B., Shi, H., et al. (2008). Comparison of the mechanism of toxicity of zinc oxide and cerium oxide nanoparticles based on dissolution and oxidative stress properties. ACS Nano, 2, 2121–2134.
Acknowledgments
This research was financially supported by the Natural Sciences and Engineering Research Council of Canada (NSERC).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Oukarroum, A., Samadani, M. & Dewez, D. Influence of pH on the Toxicity of Silver Nanoparticles in the Green Alga Chlamydomonas acidophila . Water Air Soil Pollut 225, 2038 (2014). https://doi.org/10.1007/s11270-014-2038-2
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11270-014-2038-2