Skip to main content

Advertisement

SpringerLink
Log in

Toxicity of TiO2 nanoparticles to the marine microalga Chaetoceros muelleri Lemmermann, 1898 under long-term exposure

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Titanium dioxide nanoparticles (TiO2NPs) have been extensively used in industry, raising many concerns about their release into the aquatic environments. In marine ecosystems, microalgae are major primary producers; among them, Chaetoceros muelleri is an important microalga in the aquaculture industry as live feed. The impacts of TiO2NPs on the growth, photosynthetic pigments, protein and lipid contents, and the interaction of TiO2NPs with the cell wall of C. muelleri were investigated in the present study. Algal cells were exposed to concentrations of 5, 10, 50, 100, 200, and 400 mg/L TiO2NPs for 10 days. There was a significant difference in the growth between the control and TiO2NPs treatments on each day. The half-maximal inhibitory concentration (IC50) of TiO2NPs on algal cells was found to be 10.08 and 5.01 mg/L on the 3rd and 10th days, respectively. The contents of chlorophyll a and c reduced significantly in the TiO2NPs-treated microalgae. TiO2NPs also reduced the protein and lipid contents in the treated microalgae, up to 13.02% and 47.6% respectively, at the highest concentration. The interaction of TiO2NPs with the C. muelleri cells was obvious based on Fourier transform infrared spectroscopy, microscopic images, EDS, and Mapping analyses. Toxic effects of the released TiO2NPs can damage the stocks of C. muelleri as an important live feed in mariculture.

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
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13

Similar content being viewed by others

Data availability

The authors can confirm that all relevant data are included in the article.

References

  • Abdi V, Sourinejad I, Yousefzadi M, Ghasemi Z (2018) Mangrove-mediated synthesis of silver nanoparticles using native Avicennia marina plant extract from southern Iran. Chem Eng Commun 205:1069–1076

    Article  CAS  Google Scholar 

  • Al-Ammari A, Zhang L, Yang J, Wei F, Chen C, Sun D (2021) Toxicity assessment of synthesized titanium dioxide nanoparticles in fresh water algae Chlorella pyrenoidosa and a zebrafish liver cell line. Ecotoxicol Environ Saf 211:111948

    Article  CAS  Google Scholar 

  • Amini M, Younesi H, Bahramifar N (2013) Biosorption of U(VI) from Aqueous Solution by Chlorella vulgaris: Equilibrium, Kinetic, and Thermodynamic Studies. J Environ Eng 139:410–421

    Article  CAS  Google Scholar 

  • Batley GE, Kirby JK, McLaughlin MJ (2013) Fate and Risks of Nanomaterials in Aquatic and Terrestrial Environments. Acc Chem Res 46:854–862

    Article  CAS  Google Scholar 

  • BehzadiTayemeh M, Esmailbeigi M, Shirdel I, Joo HS, Johari SA, Banan A, Nourani H, Mashhadi H, Jami MJ, Tabarrok M (2020) Perturbation of fatty acid composition, pigments, and growth indices of Chlorella vulgaris in response to silver ions and nanoparticles: A new holistic understanding of hidden ecotoxicological aspect of pollutants. Chemosphere 238:124576

    Article  CAS  Google Scholar 

  • Bhuvaneshwari M, Thiagarajan V, Nemade P, Chandrasekaran N, Mukherjee A (2018) Toxicity and trophic transfer of P25 TiO2 NPs from Dunaliella salina to Artemia salina: Effect of dietary and waterborne exposure. Environ Res 160:39–46

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Chen L, Zhou L, Liu Y, Deng S, Wu H, Wang G (2012) Toxicological effects of nanometer titanium dioxide (nano-TiO2) on Chlamydomonas reinhardtii. Ecotoxicol Environ Saf 84:155–162

    Article  CAS  Google Scholar 

  • Das K, Roychoudhury A, 2014. Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Frontiers in Environmental Science 2

  • Dauda S, Chia MA, Bako SP (2017) Toxicity of titanium dioxide nanoparticles to Chlorella vulgaris Beyerinck (Beijerinck) 1890 (Trebouxiophyceae, Chlorophyta) under changing nitrogen conditions. Aquat Toxicol 187:108–114

    Article  CAS  Google Scholar 

  • Deng X-Y, Cheng J, Hu X-L, Wang L, Li D, Gao K (2017) Biological effects of TiO2 and CeO2 nanoparticles on the growth, photosynthetic activity, and cellular components of a marine diatom Phaeodactylum tricornutum. Sci Total Environ 575:87–96

    Article  CAS  Google Scholar 

  • Fazelian N, Movafeghi A, Yousefzadi M, Rahimzadeh M (2019) Cytotoxic impacts of CuO nanoparticles on the marine microalga Nannochloropsis oculata. Environ Sci Pollut Res Int 26:17499–17511

    Article  CAS  Google Scholar 

  • Fazelian N, Movafeghi A, Yousefzadi M, Rahimzadeh M, Zarei M (2020a) Impact of silver nanoparticles on the growth, fatty acid profile, and antioxidative response of Nannochloropsis oculata. Acta Physiol Plant 42:126

    Article  CAS  Google Scholar 

  • Fazelian N, Yousefzadi M, Movafeghi A (2020b) Algal Response to Metal Oxide Nanoparticles: Analysis of Growth, Protein Content, and Fatty Acid Composition. BioEnergy Research 13:944–954

    Article  CAS  Google Scholar 

  • Finney DJ (1971) Probit Analysis, 3rd edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Ghasemi Z, Abdi V, Sourinejad I (2020) Single-step biosynthesis of Ag/AgCl@TiO2 plasmonic nanocomposite with enhanced visible light photoactivity through aqueous leaf extract of a mangrove tree. Appl Nanosci 10:507–516

    Article  CAS  Google Scholar 

  • Gong N, Shao K, Feng W, Lin Z, Liang C, Sun Y (2011) Biotoxicity of nickel oxide nanoparticles and bio-remediation by microalgae Chlorella vulgaris. Chemosphere 83:510–516

    Article  CAS  Google Scholar 

  • Hadjoudja S, Deluchat V, Baudu M (2010) Cell surface characterisation of Microcystis aeruginosa and Chlorella vulgaris. J Colloid Interface Sci 342:293–299

    Article  CAS  Google Scholar 

  • Haghighat F, Kim Y, Sourinejad I, Yu IJ, Johari SA (2021) Titanium dioxide nanoparticles affect the toxicity of silver nanoparticles in common carp (Cyprinus carpio). Chemosphere 262:127805

    Article  CAS  Google Scholar 

  • Jeevanandam J, Barhoum A, Chan YS, Dufresne A, Danquah MK (2018) Review on nanoparticles and nanostructured materials: history, sources, toxicity and regulations. Beilstein J Nanotechnol 9:1050–1074

    Article  CAS  Google Scholar 

  • Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167:191–194

    Article  CAS  Google Scholar 

  • Johari SA, Sarkheil M, Behzadi Tayemeh M, Veisi S (2018) Influence of salinity on the toxicity of silver nanoparticles (AgNPs) and silver nitrate (AgNO(3)) in halophilic microalgae, Dunaliella salina. Chemosphere 209:156–162

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kang NK, Lee B, Choi G-G, Moon M, Park MS, Lim J, Yang J-W (2014) Enhancing lipid productivity of Chlorella vulgaris using oxidative stress by TiO2 nanoparticles. Korean J Chem Eng 31:861–867

    Article  CAS  Google Scholar 

  • Kumaran J, Jose B, Joseph V, Bright Singh IS (2017) Optimization of growth requirements of marine diatom Chaetoceros muelleri using Response Surface Methodology. Aquac Res 48:1513–1524

    Article  CAS  Google Scholar 

  • Kumaran J, Singh ISB, Joseph V (2021) Effective biomass harvesting of marine diatom Chaetoceros muelleri by chitosan-induced flocculation, preservation of biomass, and recycling of culture medium for aquaculture feed application. J Appl Phycol 33:1605–1619

    Article  CAS  Google Scholar 

  • Kuwabara JS, Davis JA, Chang CCY (1986) Algal growth response to particle-bound orthophosphate and zinc. Limnol Oceanogr 31:503–511

    Article  CAS  Google Scholar 

  • Li F, Liang Z, Zheng X, Zhao W, Wu M, Wang Z (2015) Toxicity of nano-TiO2 on algae and the site of reactive oxygen species production. Aquat Toxicol 158:1–13

    Article  CAS  Google Scholar 

  • Liu Y, Wang S, Wang Z, Ye N, Fang H, Wang D (2018) TiO2, SiO2 and ZrO2 Nanoparticles Synergistically Provoke Cellular Oxidative Damage in Freshwater Microalgae. Nanomaterials (basel, Switzerland) 8:95

    Article  CAS  Google Scholar 

  • Mansouri B, Maleki A, Johari SA, Shahmoradi B, Mohammadi E, Shahsavari S, Davari B (2016) Copper Bioaccumulation and Depuration in Common Carp (Cyprinus carpio) Following Co-exposure to TiO2 and CuO Nanoparticles. Arch Environ Contam Toxicol 71:541–552

    Article  CAS  Google Scholar 

  • Matouke MM, Elewa DT, Abdullahi K (2018) Binary effect of titanium dioxide nanoparticles (nTio2) and phosphorus on microalgae (Chlorella ‘Ellipsoides Gerneck, 1907). Aquat Toxicol 198:40–48

    Article  CAS  Google Scholar 

  • Matranga V, Corsi I (2012) Toxic effects of engineered nanoparticles in the marine environment: Model organisms and molecular approaches. Mar Environ Res 76:32–40

    Article  CAS  Google Scholar 

  • Middepogu A, Hou J, Gao X, Lin D (2018) Effect and mechanism of TiO2 nanoparticles on the photosynthesis of Chlorella pyrenoidosa. Ecotoxicol Environ Saf 161:497–506

    Article  CAS  Google Scholar 

  • Miller RJ, Lenihan HS, Muller EB, Tseng N, Hanna SK, Keller AA (2010) Impacts of Metal Oxide Nanoparticles on Marine Phytoplankton. Environ Sci Technol 44:7329–7334

    Article  CAS  Google Scholar 

  • Morelli E, Salvadori E, Bizzarri R, Cioni P, Gabellieri E (2013) Interaction of CdSe/ZnS quantum dots with the marine diatom Phaeodactylum tricornutum and the green alga Dunaliella tertiolecta: A biophysical approach. Biophys Chem 182:4–10

    Article  CAS  Google Scholar 

  • Nigro M, Bernardeschi M, Costagliola D, Della Torre C, Frenzilli G, Guidi P, Lucchesi P, Mottola F, Santonastaso M, Scarcelli V, Monaci F, Corsi I, Stingo V, Rocco L (2015) n-TiO2 and CdCl2 co-exposure to titanium dioxide nanoparticles and cadmium: Genomic, DNA and chromosomal damage evaluation in the marine fish European sea bass (Dicentrarchus labrax). Aquat Toxicol 168:72–77

    Article  CAS  Google Scholar 

  • OECD, 2011. Test No. 201: Freshwater Alga and Cyanobacteria, Growth Inhibition Test.

  • Ozkaleli M, Erdem A (2018) Biotoxicity of TiO2 Nanoparticles on Raphidocelis subcapitata Microalgae Exemplified by Membrane Deformation. Int J Environ Res Public Health 15:416

    Article  CAS  Google Scholar 

  • Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349

    Article  CAS  Google Scholar 

  • Parmar TK, Rawtani D, Agrawal YK (2016) Bioindicators: the natural indicator of environmental pollution. Frontiers in Life Science 9:110–118

    Article  CAS  Google Scholar 

  • Pikula K, Mintcheva N, Kulinich SA, Zakharenko A, Markina Z, Chaika V, Orlova T, Mezhuev Y, Kokkinakis E, Tsatsakis A, Golokhvast K (2020) Aquatic toxicity and mode of action of CdS and ZnS nanoparticles in four microalgae species. Environmental Research 186:109513

    Article  CAS  Google Scholar 

  • Reis Batista I, Garcia AB, van Dalen P, Kamermans P, Verdegem M, Smaal AC (2015) Culturing Chaetoceros muelleri using simplified media with different N sources: effects on production and lipid content. Eur J Phycol 50:92–99

    Article  CAS  Google Scholar 

  • Rosenfeldt RR, Seitz F, Schulz R, Bundschuh M (2014) Heavy Metal Uptake and Toxicity in the Presence of Titanium Dioxide Nanoparticles: A Factorial Approach Using Daphnia magna. Environ Sci Technol 48:6965–6972

    Article  CAS  Google Scholar 

  • Sadiq IM, Dalai S, Chandrasekaran N, Mukherjee A (2011) Ecotoxicity study of titania (TiO2) NPs on two microalgae species: Scenedesmus sp. and Chlorella sp. Ecotoxicol Environ Saf 74:1180–1187

    Article  CAS  Google Scholar 

  • Sarkheil M, Sourinejad I, Mirbakhsh M, Kordestani D, Johari SA (2017) Antibacterial activity of immobilized silver nanoparticles on TEPA-Den-SiO2 against shrimp pathogen, Vibrio sp. Persian1. Aquac Res 48:2120–2132

    Article  CAS  Google Scholar 

  • Schwab F, Bucheli TD, Lukhele LP, Magrez A, Nowack B, Sigg L, Knauer K (2011) Are Carbon Nanotube Effects on Green Algae Caused by Shading and Agglomeration? Environ Sci Technol 45:6136–6144

    Article  CAS  Google Scholar 

  • Sendra M, Moreno-Garrido I, Yeste MP, Gatica JM, Blasco J (2017a) Toxicity of TiO(2), in nanoparticle or bulk form to freshwater and marine microalgae under visible light and UV-A radiation. Environ Pollut 227:39–48

    Article  CAS  Google Scholar 

  • Sendra M, Yeste MP, Gatica JM, Moreno-Garrido I, Blasco J (2017b) Direct and indirect effects of silver nanoparticles on freshwater and marine microalgae (Chlamydomonas reinhardtii and Phaeodactylum tricornutum). Chemosphere 179:279–289

    Article  CAS  Google Scholar 

  • Shahin Lefteh M, Sourinejad I, Ghasemi Z (2021) Avicennia marina mediated synthesis of TiO2 nanoparticles: its antibacterial potential against some aquatic pathogens. Inorganic and Nano-Metal Chemistry 51:1775–1785

    CAS  Google Scholar 

  • Sukarni S, Hamidi N, Yanuhar U, Wardana ING (2014) Potential and properties of marine microalgae Nannochloropsis oculata as biomass fuel feedstock. Int J Energy Environ Eng 5:279–290

    Article  CAS  Google Scholar 

  • Takagi M, Karseno Y, T., (2006) Effect of salt concentration on intracellular accumulation of lipids and triacylglyceride in marine microalgae Dunaliella cells. J Biosci Bioeng 101:223–226

    Article  CAS  Google Scholar 

  • Tiong IKR, Nagappan T, Abdul Wahid ME, Tengku Muhammad TS, Tatsuki T, Satyantini WH, Mahasri G, Sorgeloos P, Sung YY (2020) Antioxidant capacity of five microalgae species and their effect on heat shock protein 70 expression in the brine shrimp Artemia. Aquaculture Reports 18:100433

    Article  Google Scholar 

  • Waghmode MS, Gunjal AB, Mulla JA, Patil NN, Nawani NN (2019) Studies on the titanium dioxide nanoparticles: biosynthesis, applications and remediation. SN Applied Sciences 1:310

    Article  CAS  Google Scholar 

  • Wang Y, Zhu X, Lao Y, Lv X, Tao Y, Huang B, Wang J, Zhou J, Cai Z (2016) TiO2 nanoparticles in the marine environment: Physical effects responsible for the toxicity on algae Phaeodactylum tricornutum. Sci Total Environ 565:818–826

    Article  CAS  Google Scholar 

  • Wiesner MR, Lowry GV, Alvarez P, Dionysiou D, Biswas P (2006) Assessing the Risks of Manufactured Nanomaterials. Environ Sci Technol 40:4336–4345

    Article  CAS  Google Scholar 

  • Xia B, Chen B, Sun X, Qu K, Ma F, Du M (2015) Interaction of TiO2 nanoparticles with the marine microalga Nitzschia closterium: growth inhibition, oxidative stress and internalization. Sci Total Environ 508:525–533

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Special thanks are due to University of Hormozgan for providing the facilities.

Author information

Authors and Affiliations

  1. Department of Fisheries, Faculty of Marine Science and Technology, University of Hormozgan, Bandar Abbas, Iran

    Leila Bameri, Iman Sourinejad & Zahra Ghasemi

  2. Department of Marine Biology, Faculty of Marine Science and Technology, University of Hormozgan, Bandar Abbas, Iran

    Nasrin Fazelian

Authors
  1. Leila Bameri
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Iman Sourinejad
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zahra Ghasemi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nasrin Fazelian
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Leila Bameri performed the experiments and helped with the data analysis. Iman Sourinejad was the supervisor, contributed to the conception and design of the work and revised the final manuscript version. Zahra Ghasemi was the adviser and contributed to the data analysis. Nasrin Fazelian contributed to the design of the work and interpretation of data.

Corresponding author

Correspondence to Iman Sourinejad.

Ethics declarations

Ethics approval

The authors confirm that all experiments were performed in accordance with relevant guidelines and regulations.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Conflict of interest

The authors declare no competing interests.

Additional information

Responsible Editor: Bruno Nunes

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bameri, L., Sourinejad, I., Ghasemi, Z. et al. Toxicity of TiO2 nanoparticles to the marine microalga Chaetoceros muelleri Lemmermann, 1898 under long-term exposure. Environ Sci Pollut Res 29, 30427–30440 (2022). https://doi.org/10.1007/s11356-021-17870-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-17870-z

Keywords

Search

Navigation