Toxic Effects of Colloidal Silver Particles Biosynthesized using Gamma-irradiated Propolis Extract and Silver Nitrate Salts on Microalgae Chlorella vulgaris

Document Type : Research Paper

Authors

1 Professor, Medical Radiation Engineering, Shahid Beheshti University, Tehran, Iran

2 Associate professor, Nuclear Science and Technology Research Institute, Tehran, Iran

3 Assistant Professor in the Department of Basic Sciences, Faculty of Veterinary Medicine, Semnan University, Semnan, Iran

4 DVM, Faculty of Veterinary Medicine, Semnan University, Semnan, Iran

10.22059/jfisheries.2023.355590.1371

Abstract

The discharge of nanoparticles, including silver nanoparticles used in various industries into the environment, and their potential toxic effects on plants, animals and humans has raised global concerns, highlighting the need for more research on this topic. The aim of this study was to investigate the toxicity of silver nitrate salt (AgNO3), γ-irradiated (10 kGy) (AgNPs-γ) and non-irradiated (AgNPs) silver particles synthesized by the alcoholic extract of bee propolis at different concentrations (10, 50, 100, 200 μg/l) on Chlorella vulgaris microalgae. The results demonstrated that exposure to AgNPs-γ and AgNPs and silver nitrate salts increased growth inhibition (%) in a dose-dependent manner (P<0.05). Moreover, cell viability (VC %), microalgal cell density/biomass (μ/L) and chlorophyll-a concentration decreased. In contrast, electrolyte conductivity/living cells (electrolyte leakage (EL %) increased in the exposed groups, compared with the control group (P<0.05). These results showed the following trend in inducing toxicity, inhibiting growth and photosynthesis in Chlorella vulgaris: AgNO3 < AgNPs < AgNPs-γ.

Keywords

Main Subjects


Arunakumara, K.K.I.U., Zhang, X., 2008. Heavy metal bioaccumulation and toxicity with special reference to microalgae. Journal of Ocean University of China 7(1), 60-64.DOI:10.1007/s11802-008-0060-y.
Aruoja, V., Dubourguier, H.C., Kasemets, K., Kahru, A., 2009. Toxicity of nanoparticles of CuO, ZnO and TiO2 to microal-gae Pseudokirchneriella subcapitata. Science of the Total Environment 407(4), 1461-1468. DOI :10.1016/j.scitotenv.2008.10.053
Banerjee, S., Hew Khatoon, W.E.H., Shariffi, M., 2011. Growth and proximate composition of tropical marine Chaetoceros calcitrans and Nannochloropsis oculata cultured outdoors and under laboratory condition. African Journal of Biotechnology 10(8), 1375-1383. DOI: 10.5897/AJB10.1748
Barbosa, V.T., Souza, J.K.C., Alvino, V., Meneghetti, M.R., Florez-Rodriguez, P.P., Moreira, R.E., Paulino, G.V.B., Landell, M.F., Basílio-Júnior, I.D., do Nascimento, T.G., Luciano A. M. Grillo, L.A.M., Camila B. Dornelas, C.B., 2019. Biogenic synthesis of silver nanoparticles using Brazilian propolis. Biotechnology Progress 35(7), e2888. DOI: 10.1002/btpr.2888
Bhuyan, U., Handique, J.G., 2022. Chapter 6 - Plant polyphenols as potent antioxidants: Highlighting the mechanism of antioxidant activity and synthesis/development of some polyphenol conjugates, Editor(s):  Atta-ur-Rahman, Studies in Natural Products Chemistry, Elsevier 75, 243-266.
Bosio, K., Avanzini, C., Avolio, A.D., Ozino, O., Savoia D., 2000. In vitro activity of propolis against Streptococcus pyogenes. Letters in Applied Microbiology 31(2), 174-177. DOI: 10.1046/j.1365-2672.2000.00785.x
Deres, S., Gunes, T., Sivaci, R., 1998. Spectrophotometric determination of chlorophyll a, b and total carotenoid content of some algae species using different solvent. Turkish Journal of Botany 22(1), 13-17.
Ebrahimzadeh, Z., Salehzadeh, A., Naeemi, A.S., Jalali A., 2020. Silver nanoparticles biosynthesized by Anabaena flosaquae enhance the apoptosis in breast cancer cell line. Bulletin of Materials Science 43(1), 1-7. DOI: 10.1007/s12034-020-2064-1
Ghanizadeh, F., 1401. Biosynthesis of silver nanoparticles using gamma irradiated of Iranian propolis. MSc Thesis, Faculty of Nuclear Engineering, Shahid Beheshti University, Tehran, Iran. DOI:10.21203/rs.3.rs-2012454/v1
Gong, N., Shao, K., Feng, W., Lin, Z., Liang, C., Sun, Y., 2011. Biotoxicity of nickel oxide nanoparticles and bioremediation by microalgae Chlorella vulgaris. Chemosphere 83(4), 510-516. DOI: 10.1016/j.chemosphere.2010.12.059
Gruyer, N., Dorais, M., Bastien, C., Dassylva, N., Triffault-Bouchet, G., 2013. Interaction between silver nanoparticles and plant growth. In International Symposium on New Technologies for Environment Control, Energy-Saving and Crop Production in Greenhouse and Plant 1037, 795-800. DOI:10.17660/ActaHortic.2014.1037.105
Hedayati, S.A., Farsani, H.G., Naserabad, S.S., Hoseinifar, S.H., Van Doan, H., 2019. Protective effect of dietary vitamin E on immunological and biochemical induction through silver
nanoparticles (AgNPs) inclusion in diet and silver salt (AgNO3) exposure on Zebrafish (Danio rerio). Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 222, 100-107. DOI: 10.1016/j.cbpc.2019.04.004
Heidarieh, M., Chakoli Nabipour, A., Shahbazi, S., Shawrang, P., Zhang, B., 2021. Effect of gamma irradiation processing on total phenol and antioxidant capacities of the Iranian extract of propolis. Radiochimica Acta 109(8), 635-641. DOI: 10.1515/ract-2021-1042
Huang, S.J., Mau, J.L., 2007. Antioxidant properties of methanolic extracts from Antrodia camphorata with various doses of γ-irradiation. Food Chemistry 105(4), 1702-1710. DOI: 10.1016/j.foodchem.2007.04.046
Jiang, H.S., Li, M., Chang, F.Y., Li, W., Yin, L.Y., 2012. Physiological analysis of silver
nanoparticles and AgNO3 toxicity to Spirodela polyrhiza. Environmental Toxicology and Chemistry 31(8), 1880-1886. DOI:10.1002/etc.1899
Johari, S.A., Sarkheil, M., Tayemeh, M.B., Veisi, S., 2018. Influence of salinity on the toxicity of silver nanoparticles (AgNPs) and silver nitrate (AgNO3) in halophilic microalgae, Dunaliella salina. Chemosphere 209(C), 156-162. DOI: 10.1016/j.chemosphere.2018.06.098
Karimi, R., Norastehnia, A., Abbaspour, H. Saeidi Sar, S., Naeemi, A.S., 2018. Evaluation of copper oxide nanoparticle toxicity to cyanobacteria Anabaena sp. in Guilan wetlands. Aquatics Physiology and Biotechnology 6(1), 1-20. DOI:10.22124/japb.2018.7224.1157
Karimi, R., Norastehnia, A., Abbaspour, H., Saeidi Sar, S., Naeemi, A.S., 2017. Effects of copper oxide nanoparticles on the growth of Chlorella vulgaris. Progress in Biological Sciences 7(1), 11-20. DOI: 10.22059/pbs.2018.226951.1253
Kastori, R., Plesnicar, M., Sakac, Z., Pankovic, D., Arsenijevic Maksimovic, I., 1998. Effect of excess lead on sunflower growth and photosynthesis. Journal of Plant Nutrition 21(1), 75-85. DOI: 10.1080/01904169809365384
Khan, I., Raza, M.A., Khalid, M.H.B., Awan, S.A., Raja, N.I., Zhang, X., Min, S., Wu, B.C., Hassan, M.J., Huang, L., 2019. Physiological and biochemical responses of pearl millet (Pennisetum glaucum L.) seedlings exposed to silver nitrate (AgNO3) and silver nanoparticles (AgNPs). International Journal of Environmental Research and Public Health 16(13), 2261. DOI: 10.3390/ijerph16132261
Khristo Forova, N.K., Aizdaicher, N.A., Berezovskaya, O., 1996. The effect of copper ions and a detergent of green microalge Dunaliella tertiolecta and Platymonas sp. Russian Journal of Marine Biology 22, 109-114.
Kitada, K., Machmudah, S., Sasaki, M., Goto, M., Nakashima, Y., Kumamoto, S., Hasegawa, T., 2009. Supercritical CO2 extraction of pigment components with pharmaceutical importance from Chlorella vulgaris. Journal of Chemical Technology & Biotechnology: International Research in Process, Environmental & Clean Technology 84(5), 657-661. DOI:10.1002/jctb.2096
Kumar, P., Senthamil Selvi, S., Govindaraju, M., 2012a. Seaweed-mediated biosynthesis of silver nanoparticles using Gracilaria corticata for its antifungal activity against Candida spp. Applied Nanoscience 3(6), 495-500. DOI: 10.1007/s13204-012-0151-3
Kumar, P., Senthamil Selvi, S., Lakshmi Prabha, A., Prem Kumar, K., Ganeshkumar, R.S., Govindaraju, M., 2012b. Synthesis of silver nanoparticles from Sargassum tenerrimum and screening phytochemicals for its antibacterial activity. Nano Biomedicine and Engineering 4(1), 2-16. DOI: 10.5101/nbe. V4i1.p12-16
Kumar, P., Senthamil Selvi, S., Lakshmi Prabha, A., Selvaraj, M., Macklin Rani, L., Suganthi, P., Sarojini D., Govindaraju, M., 2012c. Antibacterial activity and in-vitro cytotoxicity assay against brine shrimp using silver nanoparticles synthesized from Sargassum ilicifolium. Digest Journal of Nanomaterials and Biostructures 7(4), 1447-1455.
Li, X., Schirmer, K., Bernard, L., Sigg, L., Pillai, S., Behra, R., 2015. Silver nanoparticle toxicity and
association with the alga Euglena gracilis. Environmental Science: Nano 2(6), 594-602. DOI: 10.1039/C5EN00093A.
Liu, C., Liu, Y., Guo, K., Fan, D., Li, G., Zheng, Y., 2011. Effect of drought on pigments, osmotic adjustment and antioxidant enzymes in six woody plant species in karst habitats of southwestern China. Environmental and Experimental Botany 71(2), 174-183. DOI: 10.1016/j.envexpbot.2010.11.012
Liu, J., Wang, W., Wang, L., Sun, Y., 2015. Exogenous melatonin improves seedling health index and drought tolerance in tomato. Journal of Plant Growth Regulation 77(3), 317-326. DOI: 10.1007/s10725-015-0066-6
Martınez, M., Sánchez, S., Jimenez, J., El Yousfi, F., Munoz, L., 2000. Nitrogen and phosphorus removal from urban wastewater by the microalga Scenedesmus obliquus. Bioresource Technology 73(3), 263-272. DOI: 10.1016/S0960-8524(99)00121-2.
Naeemi, A.S., Sarmad, J., Mohseni, N., Kehtari, F., 2018. The effects of different concentrations of lead on the growth, photosynthetic pigments and malondialdehyde content of the unicellular green algae Chlorella Vulgaris. Journal of Plant Research (Iranian Journal of Biology) 30(4), 940-947. DOI: 20.1001.1.23832592.1396.30.4.19.4
Parker, M.S., Mock, T., Armbrust, E.V., 2008. Genomic insights into marine microalgae. Annual Review of Genetics 42(1), 619-645. DOI: 10.1146/annurev.genet.42.110807.091417.
Pham, T.L., 2019. Effect of silver nanoparticles on tropical freshwater and marine microalgae.
Journal of Chemistry 9658386. DOI:10.1155/2019/9658386.
Rossa, M.M., oliveira, M.C., Okamoto, O.K., lopes, P.F., Colepicolo, P., 2002. Effect of visible light on super oxidase dismutase SOD activity in the red Alga Gracilariopsis tenuifrons (Gracilarials, Rhodophyta). Journal of applied phycology 14(3), 151-157. DOI: 10.1023/A: 1019985722808
Shanab, S.M.M., Partila, A.M., Ali, H.E.A., Abdullah, M.A., 2021. Impact of gamma-irradiated
silver nanoparticles biosynthesized from Pseudomonas aeruginosa on growth, lipid, and
carbohydrates of Chlorella vulgaris and Dictyochloropsis splendida. Journal of Radiation Research
and Applied Sciences
14(1), 70-81. DOI:10.1080/16878507.2020.1856599
Sumi, Y., 2009. Microalgae pioneering the future-application and utilization. Science and Technology Trends 34, 9-21
Vishwakarma, K., Upadhyay, N., Singh, J., Liu, S., Singh, V.P., Prasad, S.M., Chauhan, D.K., Tripathi, D.K., Sharma, S., 2017. Differential phytotoxic impact of plant mediated silver nanoparticles (AgNPs) and silver nitrate (AgNO3) on Brassica Sp. Frontiers in Plant Science 8, 1501. DOI:10.3389/fpls.2017.01501.
Wang, L., Cui, Y.R., Lee, H.G., Fu, X., Wang, K., Xu, J., Gao, X., Jeon, Y.J., 2022. Fucoidan isolated from fermented Sargassum fusiforme suppresses oxidative stress through stimulating the expression of superoxidase dismutase and catalase by regulating Nrf2 signaling pathway. International Journal of Biological Macromolecules 209 (part A), 935-941. DOI: 10.1016/j.ijbiomac.2022.04.083
Wang, L., Wang, M., Peng, C., Pan, J., 2013. Toxic Effects of Nano-CuO, Micro-CuO and Cu2+ on Chlorella Sp. Journal of Environmental Protection 4(1B), 86-91. DOI: 10.4236/jep.2013.41B016
Zuliani, L., Frison, N., Jelic, A., Fatone, F., Bolzonella, D., Ballottari, M., 2016. Microalgae cultivation on anaerobic digestate of municipal wastewater, sewage sludge and agro-waste. International Journal of Molecular Sciences 17(10), E1692. DOI: 10.3390/ijms17101692