2507000997
  • Open Access
  • Article
Bioaccumulation and Ecotoxicity of Silver Nanoparticles in Simple Food Chain Algae-Microcrustaceans in the Presence of Natural Organic Matter 
  • Cláudia Hitomi Watanabe 1, 2, *,   
  • Rute Ferreira Domingos 2,   
  • Marc F. Benedetti 3,   
  • André Henrique Rosa 1, *

Received: 01 May 2025 | Revised: 18 Jun 2025 | Accepted: 15 Jul 2025 | Published: 23 Jul 2025

Abstract

The rapid growth of nanotechnology has resulted in widespread use of nanoparticles (NP) in various commercial products. Consequently, these NP may enter aquatic environments, where they can interact with natural organic matter (NOM) such as humic substances and extracellular polymeric substances (EPS). The present work aims to evaluate the toxicity of manufactured coated silver nanoparticles (AgNP) in the presence of NOM on the microalgae Raphidocelis subcapitata and the microcrustacean Daphnia similis, both individually and within a simple food chain. By investigating the influence of NOM on the bioavailability and toxicity of AgNP, this research seeks to understand the potential environmental risks associated with these nanomaterials. The test-organisms, individually and simple food chain, were exposed to AgNP manufactured coated (citrate and poly(ethylene glycol), respectively Cit and PEG) and ionic silver solution (AgNO3) in the absence and presence of NOM, represented by humic substances (HS) and natural EPS (excreted by algae). Algae growth inhibition was assessed, and the toxic effect of silver ions remained unchanged in the presence of NOM. However, the toxicity of the highest of AgCit was reduced by HS. NOM enhanced silver bioaccumulation in algae, likely due to surface binding of HS-Ag complexes. HS exposure to AgCit decreased silver bioaccumulation, correlating with reduced toxicity. Microcrustaceans exhibited greater sensitivity to silver toxicity compared to algae. The toxic effects on Daphnia similis were evaluated through mortality (EC₅₀) and reproduction (number of neonates). The toxicity ranking was AgNO3 > AgCit > AgPeg, indicating higher toxicity for ionic silver. Daphnia reproduction was observed at environmentally permitted concentrations. Different toxic effects of AgNP were observed between neonate and adult microcrustaceans, suggesting age-dependent sensitivity. These findings highlight the need for bioassays considering the influence of NOM and capping agents to better understand the environmental impact of nanomaterials.

References 

  • 1.
    Lead, J.R.; Batley, G.E.; Alvarez, P.J.; et al. Nanomaterials in the environment: Behavior, fate, bioavailability, and effects-An updated review. Environ. Toxicol. Chem. 2018, 37, 2029–2063.
  • 2.
    Puri, M.; Gandhi, K.; Kumar, M.S. Emerging environmental contaminants: A global perspective on policies and regulations. J. Environ. Manag. 2023, 332, 117344.
  • 3.
    Wiesner, M.; Bottero, J.Y. Environmental Nanotechnology: Applications and Impacts of Nanomaterials; Mcgraw-Hill: New York, NY, USA, 2007.
  • 4.
    Jeremiah, S.S.; Miyakawa, K.; Morita, T.; et al. Potent antiviral effect of silver nanoparticles on SARS-CoV-2. Biochem. Biophys. Res. Commun. 2020, 533, 195–200.
  • 5.
    Sikder, M.; Croteau, M.N.; Poulin, B.A.; et al. Effect of Nanoparticle Size and Natural Organic Matter Composition on the Bioavailability of Polyvinylpyrrolidone-Coated Platinum Nanoparticles to a Model Freshwater Invertebrate. Environ. Sci. Technol. 2021, 55, 2452–2461.
  • 6.
    Dolganyuk, V.; Belova, D.; Babich, O.; et al. Microalgae: A Promising Source of Valuable Bioproducts. Biomolecules 2020, 10, 1153. https://doi.org/10.3390/biom10081153.
  • 7.
    Manahan, S.E. Environmental Chemistry, 8th ed.; New Age International: New York, NY, USA, 2005.
  • 8.
    Hoffman, D.J.; Rattner, B.A.; Burton, G.A., Jr.; et al. Handbook of Ecotoxicology, 1st ed.; CRC Press: Boca Raton, FL, USA, 1995.
  • 9.
    Ratte, H.T. Bioaccumulation and toxicity of silver compounds: A Review. Environ. Toxicol. Chem. 1999, 18, 89–108.
  • 10.
    Mackay, D.; Celsie AK, D.; Powellc, D.E.; et al. Bioconcentration, bioaccumulation, biomagnification and trophic magnification: A modelling perspective. Environ. Sci. Process. Impacts 2018, 20, 221–228.
  • 11.
    Rajewicz, W.; Romano, D.; Schmickl, T.; et al. Daphnia’s phototaxis as an indicator in ecotoxicological studies: A review. Aquat. Toxicology. 2023, 265, 106762.
  • 12.
    Costa, C.R.; Olivi, P.; Botta, C.M.R.; et al. Toxicity in Aquatic Environments: Discussion and Evaluation Methods. Química Nova 2008, 31, 1820–1830.
  • 13.
    Kalman, J.; Paul, K.B.; Khan, F.R.; et al. Characterisation of bioaccumulation dynamics of three differently coated silver nanoparticles and aqueous silver in a simple freshwater food chain. Environ. Chem. 2015, 12, 662–672.
  • 14.
    Grillo, R.; Rosa, A.H.; Fraceto, L.F. Engineered nanoparticles and organic matter: A review of the state-of-the-art. Chemosphere 2015, 119, 608–619.
  • 15.
    Popa, D.G.; Lupu, C.; Constantinescu-Aruxandei, D.; et al. Humic Substances as Microalgal Biostimulants-Implications for Microalgal Biotechnology. Mar. Drugs 2022, 20, 327.
  • 16.
    Alt, V.; Bechert, T.; Steinrücke, P.; et al. An in vitro assessment of the antibacterial properties and cytotoxicity of nanoparticulate silver bone cement. Biomaterials 2004, 25, 4383–4391.
  • 17.
    Li, L.; Wu, H.; Peijnenburg, W.J.; et al. Both released silver ions and particulate Ag contribute to the toxicity of AgNPs to earthworm Eisenia fetida. Nanotoxicology 2015, 9, 792–801.
  • 18.
    Watanabe, C.H.; Domingos, R.F.; Benedetti, M.F.; et al. Dissolution and fate of silver nanoparticles in the presence of natural aquatic organic matter. J. Environ. Expo. Assess. 2023, 2, 6.
  • 19.
    Aiken, G.R. Isolation and concentration techniques for aquatic humic substances. In Humic Substances in Soil, Sediment and Water: Geochemistry and Isolation; Wiley-Interscience, New York, NY, USA, 1985.
  • 20.
    Thurman, E.M.; Malcolm, R.L. Preparative isolation of aquatic humic substances. Environ. Sci. Technol. 1981, 15, 463–466.
  • 21.
    Abbt-Braun, G.; Lankes, U.; Frimmel, F.H. Structural characterization of aquatic humic substances—The need for a multiple method approach. Aquat. Sci. 2004, 66, 151–170.
  • 22.
    OECD. Test No. 201: Freshwater Alga and Cyanobacteria, Growth Inhibition Test. 2011. Available online: https://www.oecd-ilibrary.org/content/publication/9789264069923-en (accessed on 1 January 2015).
  • 23.
    Short-Term Methods for Estimating the Chronic Toxicity of Effluents and Receiving Waters to Freshwater Organisms; USEPA: Washington, DC, USA, 2002.
  • 24.
    Aquatic Ecotoxicology—Chronic Toxicity—Test Algae (Chlorophyceae); ABNT: Rio de Janeiro, Brazil, 2018.
  • 25.
    Assumpção, R.M.V.; Morita, T. Manual de Soluções, Reagentes e Solventes: Padronização-Preparação-Purificação. 1968. Available online: https://books.google.com.br/books?id=crdcAAAAMAAJ (accessed on 1 June 2015).
  • 26.
    APHA. Standard Methods for the Examination of Water and Wastewater; American Public Health Association Inc.: New York, NY, USA, 1995.
  • 27.
    OECD. Test No. 202: Daphnia sp. Acute Immobilisation Test. 2004. Available online: https://www.oecd-ilibrary.org/content/publication/9789264069947-en (accessed on 1 January 2015).
  • 28.
    OECD. Test No. 211: Daphnia Magna Reproduction Test. 2012. Available online: https://www.oecd-ilibrary.org/content/publication/9789264185203-en (accessed on 1 January 2015).
  • 29.
    Aquatic Ecotoxicology—Acute Toxicity—Test with Daphnia spp (Cladocera, Crustacea); ABNT: Rio de Janeiro, Brazil, 2016.
  • 30.
    Hamilton, M.; Russo, R.; Thurston, R. Trimmed Spearman-Karber Method for Estimating Median Lethal Concentrations in Toxicity Bioassays; U.S. Environmental Protection Agency: Washington, DC, USA, 1977.
  • 31.
    West, I.; Gulley, D. Toxstat 3.5; University of Wyoming: Laramie, WY, USA, 1996.
  • 32.
    Ribeiro, F.; Gallego-Urrea, J.A.; Jurkschat, K.; et al. Silver nanoparticles and silver nitrate induce high toxicity to Pseudokirchneriella subcapitata, Daphnia magna and Danio rerio. Sci. Total Environ. 2014, 466, 232–241.
  • 33.
    Zheng, X.; Xu, Z.; Zhao, D.; et al. Double-dose responses of Scenedesmus capricornus microalgae exposed to humic acid. Sci. Total Environ. 2022, 806, 150547.
  • 34.
    Lee, J.; Park, J.H.; Shin, Y.S.; et al. Effect of dissolved organic matter on the growth of algae, Pseudokirchneriella subcapitata, in Korean lakes: The importance of complexation reactions. Ecotoxicol. Environ. Saf. 2009, 72, 335–343. https://doi.org/10.1016/j.ecoenv.2008.01.013.
  • 35.
    Domingos, R.F.; Franco, C.; Pinheiro, J.P. Stability of core/shell quantum dots—Role of pH and small organic ligands. Environ. Sci. Pollut. Res. 2013, 20, 4872–4880.
  • 36.
    Nasser, F.; Constantinou, J.; Lynch, I. Nanomaterials in the Environment Acquire an “Eco-Corona” Impacting their Toxicity to Daphnia Magna-a Call for Updating Toxicity Testing Policies. Proteomics 2020, 20, e1800412. https://doi.org/10.1002/pmic.201800412.
  • 37.
    Baalousha, M.; Manciulea, A.; Cumberland, S.; et al. Aggregation and surface properties of iron oxide nanoparticles: Influence of pH and natural organic matter. Environ. Toxicol. Chem. 2008, 27, 1875–1882.
  • 38.
    Gunsolus, I.L.; Mousavi, M.P.; Hussein, K.; et al. Effects of Humic and Fulvic Acids on Silver Nanoparticle Stability, Dissolution, and Toxicity. Environ. Sci. Technol. 2015, 49, 8078–8086.
  • 39.
    Sharma, V.K.; Siskova, K.M.; Zboril, R.; et al. Organic-coated silver nanoparticles in biological and environmental conditions: Fate, stability and toxicity. Adv. Colloid Interface Sci. 2014, 204, 15–34.
  • 40.
    Yu, Q.; Wang, Z.; Zhai, Y.; et al. Effects of humic substances on the aqueous stability of cerium dioxide nanoparticles and their toxicity to aquatic organisms. Sci. Total Environ. 2021, 781, 146583.
  • 41.
    Domingos, R.F.; Baalousha, M.A.; Ju-Nam, Y.; et al. Characterizing Manufactured Nanoparticles in the Environment: Multimethod Determination of Particle Sizes. Environ. Sci. Technol. 2009, 43, 7277–7284.
  • 42.
    Maurer-Jones, M.A.; Gunsolus, I.L.; Murphy, C.J.; et al. Toxicity of Engineered Nanoparticles in the Environment. Anal. Chem. 2013, 85, 3036–3049.
  • 43.
    Hiriart-Baer, V.P.; Fortin, C.; Lee, D.Y.; et al. Toxicity of silver to two freshwater algae, Chlamydomonas reinhardtii and Pseudokirchneriella subcapitata, grown under continuous culture conditions: Influence of thiosulphate. Aquat. Toxicol. 2006, 78, 136–148.
  • 44.
    Navarro, E.; Baun, A.; Behra, R.; et al. Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi. Ecotoxicology 2008, 17, 372–386.
  • 45.
    Handy, R.D.; Cornelis, G.; Fernandes, T.; et al. Ecotoxicity test methods for engineered nanomaterials: Practical experiences and recommendations from the bench. Environ. Toxicol. Chem. 2012, 31, 15–31.
  • 46.
    Aruoja, V.; Dubourguier, H.C.; Kasemets, K.; et al. Toxicity of nanoparticles of CuO, ZnO and TiO2 to microalgae Pseudokirchneriella subcapitata. Sci. Total Environ. 2009, 407, 1461–1468.
  • 47.
    Chen, Z.; Porcher, C.; Campbell, P.G.; et al. Influence of Humic Acid on Algal Uptake and Toxicity of Ionic Silver. Environ. Sci. Technol. 2013, 47, 8835–8842.
  • 48.
    Naguyen, M.; Moon, J.Y.; Lee, Y.C. Microalgal ecotoxicity of nanoparticles: An updated review. Ecotoxicol. Environ. Saf. 2020, 201, 110781.
  • 49.
    Campbell, P.G.C.; Twiss, M.R.; Wilkinson, K.J. Accumulation of natural organic matter on the surfaces of living cells: Implications for the interaction of toxic solutes with aquatic biota. Can. J. Fish. Aquat. Sci. 1997, 54, 2543–2554.
  • 50.
    Knauer, K.; Buffle, J. Adsorption of Fulvic Acid on Algal Surfaces and Its Effect on Carbon Uptake. J. Phycol. 2001, 37, 47–51.
  • 51.
    Zhao, C.-M.; Wang, W.-X. Comparison of acute and chronic toxicity of silver nanoparticles and silver nitrate to Daphnia magna. Environ. Toxicol. Chem. 2011, 30, 885–892.
  • 52.
    Serwatowska, K.; Nederstigt, T.A.; Peijnenburg, W.J.; et al. Chronic toxicity of core–shell SiC/TiO2 (nano)-particles to Daphnia magna under environmentally relevant food rations in the presence of humic acid. Nanotoxicology 2024, 18, 107–118. https://doi.org/10.1080/17435390.2024.2321873.
  • 53.
    Gao, J.I.E.; Youn, S.; Hovsepyan, A.; et al. Dispersion and Toxicity of Selected Manufactured Nanomaterials in Natural River Water Samples: Effects of Water Chemical Composition. Environ. Sci. Technol. 2009, 43, 3322–3328.
  • 54.
    Mohammed, A. Why are Early Life Stages of Aquatic Organisms more Sensitive to Toxicants than Adults? In New Insights into Toxicity and Drug Testing; InTech: London, UK, 2013.
  • 55.
    Huang, B.; Li, D.; Yang, Y. Joint Toxicity of Two Phthalates with Waterborne Copper to Daphnia magna and Photobacterium phosphoreum. Bull. Environ. Contam. Toxicol. 2016, 97, 380–386.
  • 56.
    Zhao, C.M.; Wang, W.X. Size-Dependent Uptake of Silver Nanoparticles in Daphnia magna. Environ. Sci. Technol. 2012, 46, 11345–11351.
  • 57.
    Souza, M.B. Avaliação da toxicidade aguda de um herbicida comercial e dos componentes químicos Diuron e Hexazinona em Ceriodaphnia dubia. PhD Thesis, Universidade de Ribeirão Preto, Ribeirão Preto, Brazil, 2012.
Share this article:
How to Cite
Watanabe, C. H.; Domingos, R. F.; Benedetti, M. F.; Rosa, A. H. Bioaccumulation and Ecotoxicity of Silver Nanoparticles in Simple Food Chain Algae-Microcrustaceans in the Presence of Natural Organic Matter . Environmental Contamination: Causes and Solutions 2025, 1 (1), 3. https://doi.org/10.53941/eccs.2025.100003.
RIS
BibTex
Copyright & License
article copyright Image
Copyright (c) 2025 by the authors.