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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.

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References

  • AFNOR (1980). Association Française Normalisation. Norme experimentale. T90-304. Essais deseaux Determination de I’inhibition de Scenesdesmus subspicatus par une substance, Paris, France (1980).

  • Agustí, S., & Sánchez, C. (2002). Cell viability in natural phytoplankton communities quantified by a membrane permeability probe. Limnology and Oceanography, 47, 818–828.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Brunauer, S., Emmet, P. H., & Teller, E. (1938). Absorption of gases in multimolecular layers. Journal of the American Chemical Society, 60, 309–319.

    Article  CAS  Google Scholar 

  • 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 

  • 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).

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Gorelik, S., Rastorguev, L., & Skakov, Y.U. (1963). X-ray diffraction and electro-optic analysis of metals. Metallurgizdat 256.

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Liu, Y., Wang, W., Zhang, M., **ng, 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Mueller, N. C., & Nowack, B. (2008). Exposure modeling of engineered nanoparticles in the environment. Environmental Science & Technology, 42, 4447–4453. doi:10.1021/es7029637.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Prof. Dr. Edson Roberto Leite and collaborators for NP characterization, and Prof. Dr. Joaquim A. Nobrega and Dr. Clarisse D. B. Amaral for Ti determinations. ATL thanks Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq—Brazil) (302175/2015-6) for financial support and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Demanda Social (Capes-DM) for a scholarship.

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Correspondence to Daniela Mariano Barreto.

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Barreto, D.M., Lombardi, A.T. Environmentally Relevant Concentrations of TiO2 Nanoparticles Affected Cell Viability and Photosynthetic Yield in the Chlorophyceae Scenedesmus bijugus . Water Air Soil Pollut 227, 450 (2016). https://doi.org/10.1007/s11270-016-3139-x

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