Water, Air, & Soil Pollution

, 227:450 | Cite as

Environmentally Relevant Concentrations of TiO2 Nanoparticles Affected Cell Viability and Photosynthetic Yield in the Chlorophyceae Scenedesmus bijugus

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Abstract

The impact of nanoparticles (NPs) in phytoplankton is understudied, particularly with respect to the organism’s physiology and environmentally relevant concentrations. In the present research, we investigated the effects of titanium dioxide nanoparticles (nano-TiO2) in the physiology of Scenedesmus bijugus, a freshwater cosmopolitan phytoplankter, exposed to concentrations ranging from 3.30 × 10−9 mol L−1 (log −8.48) to 3.70 × 10−7 mol L−1 (log −6.43), which includes environmentally relevant values. The nano-TiO2 concentrations in the medium and in the cells were determined in experiments that lasted 96 h. Controlled environmental conditions were used throughout and a variety of endpoints were monitored. These included cell density, cell viability, chlorophyll a concentration, growth rates, maximum quantum yield of photosystem II (ΦM), intracelular proteins and carbohydrates, and proteins:carbohydrates ratios. The results showed that cell viability was the most sensitive parameter for the detection of the nano-TiO2 effects, being followed by ΦM. At the concentration of 3.90 × 10−8 mol L−1 (log −7.40), there was an increase of nano-TiO2 injured cells, and at 3.70 × 10−7 mol L−1 (log −6.43) 24%, ΦM decrease in comparison with the controls was obtained. Different from several literature results, we showed that nano-TiO2 particles at environmentally relevant concentrations affected microalgae physiology, and this was dependent on the endpoint used to evaluate the effect.

Keywords

Phytoplankton Microalgae Photosynthesis Toxicity Proteins Carbohydrates 

References

  1. AFNOR (1980). Association Française Normalisation. Norme experimentale. T90-304. Essais deseaux Determination de I’inhibition de Scenesdesmus subspicatus par une substance, Paris, France (1980).Google Scholar
  2. Agustí, S., & Sánchez, C. (2002). Cell viability in natural phytoplankton communities quantified by a membrane permeability probe. Limnology and Oceanography, 47, 818–828.CrossRefGoogle Scholar
  3. Aruoja, V., Dubourguier, H. C., Kasemets, K., & Kahru, A. (2009). Toxicity of nanoparticles of CuO, ZnO and TiO2 to microalgae Pseudokirchneriella subcapitata. Science of the Total Environment, 407, 1461–1468. doi:10.1016/j.scitotenv.2008.10.053.CrossRefGoogle Scholar
  4. Baker, T. J., Tyler, C. R., & Galloway, T. S. (2013). Impacts of metal and metal oxide nanoparticles on marine organisms. Environmental Pollution, 186, 257–71. doi:10.1016/j.envpol.2013.11.014.CrossRefGoogle Scholar
  5. Bottero, J. Y., Auffan, M., Borschnek, D., Chaurand, P., Labille, J., Levard, C., Masion, A., Tella, M., Rose, J., & Wiesner, M. R. (2015). Nanotechnology, global development in the frame of environmental risk forecasting. a necessity of interdisciplinary researches. Comptes Rendus Geoscience, 347, 35–42. doi:10.1016/j.crte.2014.10.004.CrossRefGoogle Scholar
  6. Bradford, M. (1976). A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 243–254.CrossRefGoogle Scholar
  7. Brunauer, S., Emmet, P. H., & Teller, E. (1938). Absorption of gases in multimolecular layers. Journal of the American Chemical Society, 60, 309–319.CrossRefGoogle Scholar
  8. Cardinale, B. J., Bier, R., & Kwan, C. (2012). Effects of TiO2 nanoparticles on the growth and metabolism of three species of freshwater algae. Journal of Nanoparticle Research. doi:10.1007/s11051-012-0913-6.Google Scholar
  9. Cherchi, C. (2012). Ecotoxicity and environmental implications of nano titanium dioxide revealed through primary producers surrogates—cyanobacteria. Civil Engineering Dissertations. Paper 16. Northeastern University, Department of Civil and Environmental Engineering (http://hdl.handle.net/2047/d20002839).
  10. Dalai, S., Pakrashi, S., Nirmala, M. J., Chaudhri, A., Chandrasekaran, N., Mandal, A. B., & Mukherjee, A. (2013). Cytotoxicity of TiO2 nanoparticles and their detoxification in a freshwater system. Aquatic Toxicology, 138–139, 1–11. doi:10.1016/j.aquatox.2013.04.005.CrossRefGoogle Scholar
  11. Echeveste, P., Sánchez, A. T., & Agustí, S. (2014). Tolerance of polar phytoplankton communities to metals. Environmental Pollution, 185, 188–195. doi:10.1016/j.envpol.2013.10.029.CrossRefGoogle Scholar
  12. Ganf, G. G., Stone, S. J. L., & Oliver, R. L. (1986). Use of protein to carbohydrate ratios to analyse for nutrient deficiency in phytoplankton. Australian Journal Marine Freshwater Reserve, 37, 183–197. doi:10.1071/MF9860183.CrossRefGoogle Scholar
  13. Garrido, M., Cecchi, P., Vaquer, A., & Pasqualini, V. (2013). Effects of sample conservation on assessments of the photosynthetic efficiency of phytoplankton using PAM fluorometry. Deep Sea Research Pt. I, 71, 38–48. doi:10.1016/j.dsr.2012.09.004.CrossRefGoogle Scholar
  14. Gorelik, S., Rastorguev, L., & Skakov, Y.U. (1963). X-ray diffraction and electro-optic analysis of metals. Metallurgizdat 256.Google Scholar
  15. Govorov, A. O., & Carmeli, I. (2007). Hybrid structures composed of photosynthetic system and metal nanoparticles: plasmon enhancement effect. Nanotechnology Letter, 7, 620–625. doi:10.1021/nl062528t.Google Scholar
  16. Gubbins, E. J., Batty, L. C., & Lead, J. R. (2011). Phytotoxicity of silver nanoparticles to Lemna minor L. Environmental Pollution, 159(6), 1551–9. doi:10.1016/j.envpol.2011.03.002.CrossRefGoogle Scholar
  17. Hartmann, N. B., Kammer, F. V., Hofmann, T., Baalousha, M., Ottofuelling, S., & Baun, A. (2010). Algal testing of titanium dioxide nanoparticles-testing considerations, inhibitory effects and modification of cadmium bioavailability. Toxicology, 296, 190–197. doi:10.1016/j.tox.2009.08.008.CrossRefGoogle Scholar
  18. Hassellöv, M., Readman, J. W., Ranville, J. F., & Tiede, K. (2008). Nanoparticle analysis and characterization methodologies in environmental risk assessment of engineered nanoparticles. Ecotoxicology, 17, 344–361. doi:10.1007/s10646-008-0225-x.CrossRefGoogle Scholar
  19. He, D., Dorantes-Aranda, J. J., & Waite, T. D. (2012). Silver nanoparticle-algae interactions: oxidative dissolution, reactive oxygen species generation and synergistic toxic effects. Environmental Science & Technology, 46, 8731–8738. doi:10.1021/es300588a.CrossRefGoogle Scholar
  20. Joner, E.J., Hartnik, T., & Amundsen, C.E. (2008). Environmental fate and ecotoxicity of engineered nanoparticles. http://www.nanotechia.org/global-news/norwegian-authorities-assess-environmental-fate-an. Accessed 5 January 2016. ISBN 978-82-7655-540-0.
  21. Juhel, G., Batisse, E., Hugues, Q., Daly, D., Van Pelt, F. N., O’halloran, J., & Jansen, M. A. (2011). Alumina nanoparticles enhance growth of Lemna minor. Aquatic Toxicology, 105(3-4), 328–36. doi:10.1016/j.aquatox.2011.06.019.CrossRefGoogle Scholar
  22. Juneau, P., Qiu, B., & Deblois, C. P. (2007). Use of chlorophyll fluorescence as a tool for determination of herbicide toxic effect: review. Environmental Toxicology & Chemistry, 89, 609–625. doi:10.1080/02772240701561569.CrossRefGoogle Scholar
  23. Kadar, E., Rooks, P., Lakey, C., & White, D. A. (2012). The effect of engineered nanoparticles on growth and metabolic status of marine microalgae cultures. Science of the Total Environment, 439, 8–17.CrossRefGoogle Scholar
  24. Kilham, S., Kreeger, D. A., Gouldern, C. E., & Lynn, S. G. (1997). Effects of nutrient limitation on biochemical constituents of Ankistrodesmus falcatus. Freshwater Biology, 38, 591–59. doi:10.1046/j.1365-2427.1997.00231.x.CrossRefGoogle Scholar
  25. Krajnik, B., Gajda-rączka, M., Piątkowski, D., Nyga, P., Jankiewicz, B., Hofmann, E., & Mackowski, S. (2013). Silica nanoparticles as a tool for fluorescence collection efficiency enhancement. Nanoscale Research Letters, 8, 146. doi:10.1186/1556-276X-8-146.CrossRefGoogle Scholar
  26. Kulacki, K. J., & Cardinale, B. J. (2012). Effects of nano-titanium dioxide on freshwater algal population dynamics. PLoS One, 7(10), e47130. doi:10.1371/journal.pone.0047130.CrossRefGoogle Scholar
  27. Kulacki, K. J., Cardinale, B. J., Keller, A. A., Bier, R., & Dickson, H. (2012). How do stream organisms respond to, and influence, the concentration of titanium dioxide nanoparticles? A mesocosm study with algae and herbivores. Environmental Toxicology & Chemistry, 31, 2414–2422. doi:10.1002/etc.1962.CrossRefGoogle Scholar
  28. Liu, D., Wong, P. T. S., & Dutka, B. J. (1973). Determination of carbohydrate in lake sediment by a modified phenol-sulfuric acid method. Water Research, 7, 741–46. doi:10.1016/0043-1354(73)90090-0.CrossRefGoogle Scholar
  29. Liu, Y., Wang, W., Zhang, M., Xing, P., & Yang, Z. (2010). PSII-efficiency, polysaccharide production, and phenotypic plasticity of Scenedesmus obliquus in response to changes in metabolic carbon flux. Biochemical System Ecology, 38, 292–299. doi:10.1016/j.bse.2010.02.003.CrossRefGoogle Scholar
  30. Lombardi, A. T., & Maldonado, M. T. (2011). The effects of copper on the photosynthetic response of Phaeocystis cordata. Photosynthesis Research, 108, 77–78. doi:10.1007/s11120-011-9655-z.CrossRefGoogle Scholar
  31. Lombardi, A. T., Vieira, A. A. H., & Sartori, L. A. (2002). Mucilacinous capsule adsorption and intracellular uptake of copper by Kirchneriella aperta (Chlorococcales). Journal of Phycology, 38, 332–337. doi:10.1046/j.1529-8817.2002.00126.x.CrossRefGoogle Scholar
  32. Melegari, S. P., Perreault, P., Costa, R. H. R., Popovic, R., & Matias, W. G. (2013). Evaluation of toxicity and oxidative stress induced by copper oxide nanoparticles in the green alga Chlamydomonas reinhardtii. Aquatic Toxicology, 142–143, 431–440. doi:10.1016/j.aquatox.2013.09.015.CrossRefGoogle Scholar
  33. Mueller, N. C., & Nowack, B. (2008). Exposure modeling of engineered nanoparticles in the environment. Environmental Science & Technology, 42, 4447–4453. doi:10.1021/es7029637.CrossRefGoogle Scholar
  34. Navarro, E., Piccapietra, F., Wagner, B., Marconi, F., Kaegi, R., Odzak, N., Sigg, L., & Behra, R. (2008a). Toxicity of silver nanoparticles to Chlamydomonas reinhardtii. Environmental Science & Technology, 42, 8959–8964. doi:10.1021/es801785m.CrossRefGoogle Scholar
  35. Navarro, E., Baun, A., Behra, R., Hartmann, N. B., Filser, J., Miao, A. J., Quigg, A., Santschi, P. H., & Sigg, L. (2008b). Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi. Ecotoxicology, 17, 372–386. doi:10.1007/s10646-008-0214-0.CrossRefGoogle Scholar
  36. Perron, M.-C., Qiu, B., Boucher, N., Bellemare, F., & Juneau, P. (2012). Use of chlorophyll a fluorescence to detect the effect of microcystins on photosynthesis and photosystem II energy fluxes of green algae. Toxicon, 59, 567–577. doi:10.1016/j.toxicon.2011.12.005.CrossRefGoogle Scholar
  37. Rausch, T. (1981). The estimation of micro-algal protein content and its meaning to the evaluation of algal biomass I. comparison of methods for extracting protein. Hydrobiologia, 78, 237–251.CrossRefGoogle Scholar
  38. Ribeiro, F., Gallego-Urrea, J. A., Jurkschat, K., Crossley, A., Hassellöv, M., Taylor, C., Soares, A. M. V. M., & Loureiro, S. (2014). Silver nanoparticles and silver nitrate induce high toxicity to Pseudokirchneriella subcapitata, Daphnia magna and Danio rerio. Science of the Total Environment, 466–467, 232–241. doi:10.1016/j.scitotenv.2013.06.101.CrossRefGoogle Scholar
  39. Rocha, G. S., Pinto, F. H. V., Melao, M. G. G., & Lombardi, A. T. (2014). Growing Scenedesmus quadricauda in used culture media: is it viable? Journal of Applied Phycology. doi:10.1007/s10811-014-0320-8.Google Scholar
  40. Sadiq, I. M., Swayamprava, D. N., & Chandrasekaran, A. M. (2011). Ecotoxicity study of titania (TiO2) NPs on two microalgae species: Scenedesmus sp. and Chlorella sp. Ecotox. Environmental Safety, 74, 1180–1187. doi:10.1016/j.ecoenv.2011.03.006.CrossRefGoogle Scholar
  41. Saison, C., Perreault, F., Daigle, J. C., 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. Aquatic Toxicology, 96, 109–114. doi:10.1016/j.aquatox.2009.10.002.CrossRefGoogle Scholar
  42. Shang, L., Nienhaus, K., & Nienhaus, G. U. (2014). Engineered nanoparticles interacting with cells: size matters. Journal of Nanbiotechnology, 12, 5–16. doi:10.1186/1477-3155-12-5.CrossRefGoogle Scholar
  43. Singsaas, E. L., Ort, D. R., & DeLucia, E. H. (2001). Variation in measured values of photosynthetic quantum yield in ecophysiological studies. Oecologia, 128, 15–23. doi:10.1007/s004420000624.CrossRefGoogle Scholar
  44. Tang, Y. Z., & Dobbs, F. C. (2007). Green autofluorescence in Dinoflagellates, Diatoms, and other microalgae and its implications for vital staining and morphological studies. Applied and Environmental Microbiology, 73, 2306–2313. doi:10.1128/AEM.01741-06.CrossRefGoogle Scholar
  45. Tang, Y., Li, S., Qiao, J., Wang, H., & Li, L. (2013). Synergistic effects of nano-sized titanium dioxide and zinc on the photosynthetic capacity and survival of Anabaena sp. International Journal of Molecular Sciences, 14, 14395–14407. doi:10.3390/ijms140714395.CrossRefGoogle Scholar
  46. Yeung, K. L., Leung, W. K., Yao, N., & Cao, S. (2009). Reactivity and antimicrobial properties of nanostructured titanium dioxide. Catalysis Today, 143, 218–224. doi:10.1016/j.cattod.2008.09.036.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Daniela Mariano Barreto
    • 1
  • Ana Teresa Lombardi
    • 1
  1. 1.Department of Botany, Programa de Pós-Graduação em Ecologia e Recursos Naturais Rodovia Washington LuisFederal University of São CarlosSão CarlosBrazil

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