Skip to main content
SpringerLink
Log in

Effects of Titanium Dioxide Nanoparticles in Different Metabolic Pathways in the Freshwater Microalga Chlorella sorokiniana (Trebouxiophyceae)

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

Abstract

The products that employ nanoparticles (NPs) in their composition have increased since the beginning of NP production; hence, their availability in the environment, especially in aquatic ecosystems, tends to increase. In these ecosystems, the phytoplankton is immersed in a complex matrix of nutrients, excreted materials, and other chemical compounds, which can influence the metabolic strategy of microalgae. One of the metabolic ways is mixotrophy, a situation whereby microalgae perform photosynthesis and use dissolved organic carbon at the same time. Most toxicity evaluations do not consider such a metabolic route, but this can represent a preferential metabolism in natural environments. The present study aimed at evaluating the effects of NP-TiO2 at a log concentration range of − 3.10 to 0.89, on photosynthesis, growth, viability, and biochemical composition of the microalgae Chlorella sorokiniana during photoautotrophic and mixotrophic growth (glucose as the organic carbon source). The results showed lower chlorophyll a and photosynthetic activity in mixotrophy than in photoautotrophy, which can be due to a decreased need for photosynthesis in mixotrophy. Photoautotrophy cultures were sensitive to NPs, reaching 39% of viability at log 0.89, while in mixotrophy, cell viability was not affected by NPs. The biochemical composition and cell density changed as a function of NP concentrations, with increase in the protein/carbohydrate ratio in both treatments. The results showed that C. sorokiniana is more resistant to NPs during mixotrophic growth, but with changes in biochemical composition, whereas the photoautotrophic cultures were more sensitive to the increase in NP concentrations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Albalasmeh, A. A., Berhe, A. A., & Ghezzehei, T. A. (2013). A new method for rapid determination of carbohydrate and total carbon concentration using UV spectrophotometry. Carbohydrate Polymers, 97, 253–261.

    Article  CAS  Google Scholar 

  • Alkhamis, Y., & Qin, J. G. (2016). Comparison of pigment and proximate composition of Tisochrysis lutea in phototrophic and mixotrophic cultures. Journal of Applied Phycology, 25, 35–42.

    Article  Google Scholar 

  • Araujo, C. F. C., & Souza-Santos, L. P. (2013). Use of the microalgae Thalassiosira weissflogii to assess water toxicity in the Suape industrial-port complex of Pernambuco, Brazil. Ecotoxicology and Environmental Safety, 89, 212–221.

    Article  CAS  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.

    Article  CAS  Google Scholar 

  • Baldisserotto, C., Giovanardi, M., Ferrori, L., & Pancaldi, S. (2014). Growth, morphology and photosynthetic responses of Neochloris oleoabundans during cultivation in a mixotrophic brackish medium and subsequent starvation. Acta Physiologiae Plantarum, 36, 461–472.

    Article  CAS  Google Scholar 

  • Barreto, D. M., & Lombardi, A. T. (2016). Environmentally relevant concentrations of TiO2 nanoparticles affected cell viability and photosynthetic yield in the Chlorophyceae Scenedesmus bijugus. Water, Air, & Soil Pollution, 227, 450.

    Article  Google Scholar 

  • Beer, C., Foldbjerg, R., Hayashi, Y., Sutherland, D. S., & Autrup, H. (2012). Toxicity of silver nanoparticles—nanoparticle or silver ion? Toxicology Letters, 208, 286–292.

    Article  CAS  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 

  • 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 Nano Research, 14, 913.

    Article  Google Scholar 

  • Cherchi, C., Miljkovic, M., Diem, M., & Gu, A. Z. (2015). nTiO2 induced changes in intracellular composition and nutrient stoichiometry in primary producer—Cyanobacteria. Science of the Total Environment, 512-513, 345–352.

    Article  CAS  Google Scholar 

  • Chia, M. A., Lombardi, A. T., Melão, M. G. G., & Parrish, C. C. (2013). Combined nitrogen limitation and cadmium stress stimulate total carbohydrates, lipids, protein and amino acid accumulation in Chlorella vulgaris (Trebouxiophyceae). Aquatic Toxicology, 160, 87–95.

    Article  Google Scholar 

  • Dalaia, S., Pakrashia, S., Nirmalaa, M. J., Chaudhria, A., Chandrasekarana, N., Mandalb, A. B., & Mukherjeea, A. (2013). Cytotoxicity of TiO2 nanoparticles and their detoxification in a freshwater system. Aquatic Toxicology, 138-139, 1–11.

    Article  Google Scholar 

  • Franklin, N. M., Rogers, N. J., Apte, S. C., Batley, G. E., Gadd, G. E., & Casey, P. S. (2007). Comparative toxicity of nanoparticles ZnO, bulk ZnO, and ZnCl2 to a freshwater microalga (Pseudokirchneriella subcapitata): the importance of particle solubility. Environmental Science & Technology, 41, 8484–8490.

    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 of Marine and Freshwater Research, 37(2), 183–197.

    Article  Google Scholar 

  • Giovanardi, M., Baldisserotto, C., Ferrori, L., Longoni, P., Cella, R., & Pancaldi, S. (2014). Growth and lipid synthesis promotion in mixotrophic Neochloris oleoabundans (Chlorophyta) cultivated with glucose. Protoplasma, 251, 115–125.

    Article  CAS  Google Scholar 

  • Gottschalk, F., Sonderer, T., Scholz, R. W., & Nowack, B. (2009). Modeled environmental concentrations of engineered nanomaterials (TiO2, ZnO, Ag, CNT, fullerenes) for different regions. Environmental Science and Technology, 43, 9216–9222.

    Article  CAS  Google Scholar 

  • Granum, E., Kirkvold, S., & Myklestad, S. M. (2002). Cellular and extracellular production of carbohydrates and amino acids by the marine diatom Skeletonema costatum: diel variations and effects of N depletion. Marine Ecology Progress Series, 242, 83–94.

    Article  CAS  Google Scholar 

  • Hartmann, N. B., Der 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, 269, 190–197.

    Article  CAS  Google Scholar 

  • Hund-Rinke, K., & Simon, M. (2006). Ecotoxic effect of photocatalytic active nanoparticles (TiO2) on algae and daphnids. Environmental Science and Pollution Research, 13, 225–232.

    Article  CAS  Google Scholar 

  • Juntila, D. J., Bautista, M. A., & Monotilla, W. (2015). Biomass and lipid production of a local isolate Chlorella sorokiniana under mixotrophic growth conditions. Bioresource Technology, 191, 395–398.

    Article  CAS  Google Scholar 

  • Kadar, E., Rooks, P., Lakey, C., & White, D. A. (2012). The effect of engineered iron nanoparticles on growth and metabolic status of marine microalgae cultures. Environmental Science and Technology, 439, 8–17.

    CAS  Google Scholar 

  • Kaegi, R., Ulrich, A., Sinnet, B., Banbank, R., Wichser, A., Zuleeg, S., Simmler, H., Brunner, S., Vonmont, H., Burkhardt, M., & Boller, M. (2008). Synthetic TiO2 nanoparticle emission from exterior facades into the aquatic environment. Environmental Pollution, 156, 233–239.

    Article  CAS  Google Scholar 

  • Kahru, A., & Dubourguier, H. C. (2010). From ecotoxicology to nanoecotoxicology. Toxicology, 269, 105–119.

    Article  CAS  Google Scholar 

  • Kaplan, D., Heimer, Y. M., Abeliovich, A., & Goldsbrough, P. B. (1995). Cadmium toxicity and resistance in Chlorella sp. Plant Science, 109, 129–137.

    Article  CAS  Google Scholar 

  • Kilham, S. S., Kreeger, D. A., Goulden, C. E., & Lynn, S. G. (1997). Effects of nutrient limitation on biochemical constituents of Ankistrodesmus falcatus. Freshwater Biology, 38, 591–596.

    Article  CAS  Google Scholar 

  • Komor, E., & Tanner, W. (1974). The hexose-proton symport system of Chlorella vulgaris: specificity, stoichiometry and energetics of sugar-induced proton uptake. European Journal of Biochemistry, 44, 219–223.

    Article  CAS  Google Scholar 

  • Kong, W., Song, H., Cao, Y., Yang, H., Hua, S., & Xia, C. (2011). The characteristics of biomass production, lipid accumulation and chlorophyll biosynthesis of Chlorella vulgaris under mixotrophic cultivation. African Journal of Biotechnology, 10, 11620–11630.

    CAS  Google Scholar 

  • Kulacki, K. J., & Cardinale, B. J. (2012). Effects of nano-titanium dioxide on freshwater algal population dynamics. PLoS One, 7(10), e47130.

    Article  CAS  Google Scholar 

  • Kumar, K. S., Dahms, H. U., Lee, J. S., Kim, H. C., Lee, W. C., & Shin, K. H. (2014). Algal photosynthetic responses to toxic metals and herbicides assessed by chlorophyll a fluorescence. Ecotoxicology and Environmental Safety, 104, 51–71.

    Article  Google Scholar 

  • Li, T., Zheng, Y., Yu, L., & Chen, S. (2014). Mixotrophic cultivation of a Chlorella sorokiniana strain for enhanced biomass and lipid production. Biomass & Bioenergy, 66, 204–213.

    Article  CAS  Google Scholar 

  • Liang, Y., Sarkany, N., & Cui, Y. (2009). Biomass and lipid productivities of Chlorella vulgaris under autotrophic, heterotrophic and mixotrophic growth conditions. Biotechnology Letters, 31, 1043–1049.

    Article  CAS  Google Scholar 

  • Linkous, C. A., Carter, G. L., Locuson, D. B., Ouellette, A. J., Slattery, D. K., & Smitha, L. A. (2000). Photocatalytic inhibition of algae growth using TiO2, WO3, and cocatalyst modifications. Environmental Science and Technology, 34, 4754–4758.

    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.

    Article  CAS  Google Scholar 

  • Melegari, S. P., Perreault, F., Costa, R. H. R., Popovic, R., & Matias, W. G. (2013). Evaluation of toxicity and oxidative stress induced by cooper oxide nanoparticles in the green alga Chlamydomonas reinharstii. Aquatic Toxicology, 142-143, 431–440.

    Article  CAS  Google Scholar 

  • Miao, A. J., Schwehr, K. A., Xu, C., Zhang, S. J., Luo, Z., Quigg, A., & Santschi, P. H. (2009). The algal toxicity of silver engineered nanoparticles and detoxification by exopolymeric substances. Environmental Pollution, 157, 3034–3041.

    Article  CAS  Google Scholar 

  • Mueller, N. C., & Nowack, B. (2008). Exposure modeling of engineered nanoparticles in the environment. Environmental Pollution, 157, 3034–3041.

    Google Scholar 

  • Navarro, E., Baun, A., Behra, R., Hartmann, N. B., Filser, J., Miao, A. J., Quigg, A., Santschi, P. H., & Sigg, L. (2008). Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi. Ecotoxicology, 17, 372–386.

    Article  CAS  Google Scholar 

  • Nel, A., Xia, T., Madler, L., & Li, N. (2006). Toxic potential of materials at the nanolevel. Science, 311, 622–627.

    Article  CAS  Google Scholar 

  • Nowack, B., & Bucheli, T. D. (2007). Occurrence, behavior and effects of nanoparticles in the environment. Environmental Pollution, 150, 5–22.

    Article  CAS  Google Scholar 

  • Perales-Vela, H. V., Peña-Castro, J. M., & Cañizares-Villanueva, R. O. (2006). Heavy metal detoxification in eukaryotic microalgae. Chemosphere, 64, 1–10.

    Article  CAS  Google Scholar 

  • Perez-Garcia, O., Escalante, F. M. E., de-Bashan, L. E., & Bashan, Y. (2011). Heterotrophic cultures of microalgae: metabolism and potential products. Water Research, 45, 11–36.

    Article  CAS  Google Scholar 

  • Piccinno, F., Gottschalk, F., Seeger, S., & Nowack, B. (2012). Industrial production quantities and uses of ten engineered nanomaterials for Europe and the world. Journal of Nano Research, 14, 1109–1120.

    Article  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 

  • Reynolds, C. S. (2006). The ecology of phytoplankton (p. 551). Cambridge: Cambridge University Press.

    Book  Google Scholar 

  • Ridley, M. K., Hackley, V. A., & Machesky, M. L. (2006). Characterization and surface-reactivity of nanocrystalline anatase in aqueous solutions. Langmuir, 22, 10972–10982.

    Article  CAS  Google Scholar 

  • Robichaud, C. O., Uyar, A. E., Darby, M. R., Zucker, L. G., & Wiesner, M. R. (2009). Estimates of upper bounds and trends in nano-TiO2 production as a basis for exposure assessment. Environmental Science and Technology, 43(12), 4227–4233.

    Article  CAS  Google Scholar 

  • Rocha, G. S., Pinto, F. H. V., Melão, M. G. G., & Lombardi, A. T. (2015). Growing Scenedesmus quadricauda in used culture media: is it viable? Journal of Applied Phycology, 27, 171–178.

    Article  Google Scholar 

  • Rosemberg, J. N., Kobayashi, N., Barnes, A., Noel, E. A., Betenbaugh, M. J., & Oyler, G. A. (2014). Comparative analyses of three Chlorella species in response to light and sugar reveal distinctive lipid accumulation patterns in the microalga C. sorokiniana. PLoS One, 9(4), e92460.

    Article  Google Scholar 

  • Sadiq, I. M., Pakrashi, S., Chandrasekaran, A. M., & Mukherjee, A. (2011). Studies on toxicity of aluminum oxide (Al2O3) nanoparticles to microalgae species: Scendesmus sp. and Chlorella sp. Journal of Nanoparticle Research, 13, 3287–3299.

    Article  CAS  Google Scholar 

  • Sharma, V. K. (2009). Aggregation and toxicity of titanium dioxide nanoparticles in aquatic environment—a review. Journal of Environmental Science and Health, 44, 1485–1495.

    Article  CAS  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(7), 2306–2313.

    Article  CAS  Google Scholar 

  • USEPA (2012). Ecological effects test guidelines—OCSPP 850.4500: Algal Toxicity (pp. 28). Washington, DC.

  • Yang, W. W., Miao, A. J., & Yang, L. Y. (2012b). Cd2+ toxicity to a green alga Chlamydomonas reinhardtii as influenced by its adsorption on TiO2 engineered nanoparticles. PLoS One, 7(3), e32300.

    Article  CAS  Google Scholar 

  • Yang, Z., Geng, L., Wang, W., & Zhang, J. (2012a). Combined effects of temperature, light intensity, and nitrogen concentration on the growth and polysaccharide content of Microcystis aeruginosa in batch culture. Biochemical Systematics and Ecology, 41, 130–135.

    Article  CAS  Google Scholar 

  • Zhan, W. X. (2003). Nanoscale iron particles for environmental remediation: an overview. Journal of Nanoparticle Research, 5, 323–332.

    Article  Google Scholar 

  • Zhu, X., Zhou, J., & Cai, Z. (2011). TiO2 nanoparticles in the marine environment: Impact on the toxicity of tributyltin to abalone (Haliotis diversicolor supertexta) embryos. Environmental Science and Technology, 45, 3753–3758.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank the Brazilian agency FAPESP (Proc. No. 2014/15894-0) and CNPq (Proc. No. 302175/2015-6) for financial support.

Author information

Authors and Affiliations

  1. Laboratory of Algal Biotechnology, Department of Botany, Federal University of São Carlos, Rodovia Washington Luis, km 235, SP 310, São Carlos, 13565-905, Brazil

    Adriano Evandir Marchello, Daniela Mariano Barreto & Ana Teresa Lombardi

  2. Post-graduate in Ecology and Natural Resources, Center for Biological and Health Sciences, Federal University of São Carlos, Rodovia Washington Luis, km 235, SP 310, São Carlos, 13565-905, Brazil

    Adriano Evandir Marchello & Daniela Mariano Barreto

Authors
  1. Adriano Evandir Marchello
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniela Mariano Barreto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ana Teresa Lombardi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Adriano Evandir Marchello.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Marchello, A.E., Barreto, D.M. & Lombardi, A.T. Effects of Titanium Dioxide Nanoparticles in Different Metabolic Pathways in the Freshwater Microalga Chlorella sorokiniana (Trebouxiophyceae). Water Air Soil Pollut 229, 48 (2018). https://doi.org/10.1007/s11270-018-3705-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11270-018-3705-5

Keywords

Search

Navigation