Abstract
Gold nanoparticles (AuNPs) are nowadays used in many areas of science, particularly in medicine as drug release and gene carriers. The extensive use of these materials makes imperative the study of their effects on the environment after their disposal, that mostly affects the aquatic media. The present work explores the bioaccumulation and toxicity of chitosan-functionalized and non-functionalized gold nanoparticles, with primary producers (Lemna valdiviana) and primary consumers (Daphnia pulex) aquatic organisms. Bioaccumulation of 27.4 nm AuNPs and 43.1 nm chitosan-gold nanoparticles (CO-AuNPs) was evaluated in both microorganisms, finding accumulation of AuNPs and inhomogeneous aggregation of CO-AuNPs in Daphnia pulex gut, and internalization of both types of nanoparticles in Lemna valdiviana cell walls. The effective concentration of nanomaterial for 50% survival (LC50) of Daphnia pulex organisms was 1.13 mg/L for AuNPs and 0.96 mg/L for CO-AuNPs in the acute test. In Lemna valdiviana 7-day test, the EC50 for area and frond number were 1.19 mg/L and 1.26 mg/L, respectively, for AuNPs, 1.53 mg/L and 1.44 mg/L, respectively, for CO-AuNPs, finding higher toxicity of CO-AuNPs to Daphnia pulex, and AuNPs to Lemna valdiviana. The obtained results suggest that the effects of nanomaterials on the growth and survival of key organisms deserve further study, as this may lead to the development of appropriate environmental regulations.
Similar content being viewed by others
Availability of data and material
Raw data and materials are available if required by the reviewers.
Code availability
Not applicable.
References
Luoma SN, Rainbow PS (2005) Why is metal bioaccumulation so variable? Biodynamics as a unifying concept. Environ Sci Technol 39:1921–1931. https://doi.org/10.1021/es048947e
Park S, Woodhall J, Ma G et al (2014) Regulatory ecotoxicity testing of engineered nanoparticles: are the results relevant to the natural environment? Nanotoxicology 8:583–592. https://doi.org/10.3109/17435390.2013.818173
Yuan L, Richardson CJ, Ho M et al (2018) Stress responses of aquatic plants to silver nanoparticles. Environ Sci Technol 52:2558–2565. https://doi.org/10.1021/acs.est.7b05837
Klaine SJ, Alvarez PJJ, Batley GE et al (2008) Nanomaterials in the environment: behavior, fate, bioavailability, and effects. Environ Toxicol Chem 27:1825. https://doi.org/10.1897/08-090.1
Hochella MF, Mogk DW, Ranville J, et al. (2019) Natural, incidental, and engineered nanomaterials and their impacts on the Earth system. Science 363:eaau8299. https://doi.org/10.1126/science.aau8299
Griffin S, Masood MI, Nasim MJ et al (2018) Natural nanoparticles: a particular matter inspired by nature. Antioxidants 7:3. https://doi.org/10.3390/antiox7010003
Gonzalez L, Lison D, Kirsch-Volders M (2008) Genotoxicity of engineered nanomaterials: a critical review. Nanotoxicology 2:252–273. https://doi.org/10.1080/17435390802464986
Vance ME, Kuiken T, Vejerano EP et al (2015) Nanotechnology in the real world: redeveloping the nanomaterial consumer products inventory. Beilstein J Nanotechnol 6:1769–1780. https://doi.org/10.3762/bjnano.6.181
Abrica-González P, Zamora-Justo JA, Sotelo-López A et al (2019) Gold nanoparticles with chitosan, N-acylated chitosan, and chitosan oligosaccharide as DNA carriers 14:258. Nanoscale Res Lett. https://doi.org/10.1186/s11671-019-3083-y
Zamora-Justo JA, Abrica-González P, Vázquez-Martínez GR et al (2019) Polyethylene glycol-coated gold nanoparticles as DNA and atorvastatin delivery systems and cytotoxicity evaluation. J Nanomater 2019:1–11. https://doi.org/10.1155/2019/5982047
Remant Bahadur KC, Thapa B, Bhattarai N (2014) Gold nanoparticle-based gene delivery: promises and challenges. Nanotechnol Rev 3:269–280. https://doi.org/10.1515/ntrev-2013-0026
Aied A, Greiser U, Pandit A, Wang W (2013) Polymer gene delivery: overcoming the obstacles. Drug Discovery Today 18:1090–1098. https://doi.org/10.1016/j.drudis.2013.06.014
Zou P, Yang X, Wang J et al (2016) Advances in characterisation and biological activities of chitosan and chitosan oligosaccharides. Food Chem 190:1174–1181. https://doi.org/10.1016/j.foodchem.2015.06.076
Robinson KJ, Corrie SR, Thurecht KJ et al (2016) Nanoparticle-based medicines: a review of FDA-approved materials and clinical trials to date. Pharm Res 33:2373–2387. https://doi.org/10.1007/s11095-016-1958-5
Ventola CL (2017) Progress in nanomedicine: approved and investigational nanodrugs. P& T: a peer-reviewed. J Formul Manag 42:742–755. https://doi.org/10.1016/j.psychres.2007.07.030
Hüffer T, Praetorius A, Wagner S et al (2017) Microplastic exposure assessment in aquatic environments: learning from similarities and differences to engineered nanoparticles. Environ Sci Technol 51:2499–2507. https://doi.org/10.1021/acs.est.6b04054
Hashmi ASK, Hutchings GJ (2006) Gold catalysis. Angew Chem Int Ed 45:7896–7936. https://doi.org/10.1002/anie.200602454
Hendrich CM, Sekine K, Koshikawa T et al (2021) Homogeneous and heterogeneous gold catalysis for materials science. Chem Rev 121:9113–9163. https://doi.org/10.1021/acs.chemrev.0c00824
Kim EY, Kumar D, Khang G, Lim D-K (2015) Recent advances in gold nanoparticle-based bioengineering applications. J Mater Chem B 3:8433–8444. https://doi.org/10.1039/C5TB01292A
Yang X, Yang M, Pang B et al (2015) Gold nanomaterials at work in biomedicine. Chem Rev 115:10410–10488. https://doi.org/10.1021/acs.chemrev.5b00193
Schmitz C, Gökce B, Jakobi J et al (2016) Integration of gold nanoparticles into NIR-radiation curable powder resin. Chem Select 1:5574–5578. https://doi.org/10.1002/slct.201601288
Bhagawati M, You C, Piehler J (2013) Quantitative real-time imaging of protein–protein interactions by LSPR detection with micropatterned gold nanoparticles. Anal Chem 85:9564–9571. https://doi.org/10.1021/ac401673e
Russo CJ, Passmore LA (2014) Ultrastable gold substrates for electron cryomicroscopy. Science 346:1377–1380. https://doi.org/10.1126/science.1259530
Pan D, Pramanik M, Senpan A et al (2011) Molecular photoacoustic imaging of angiogenesis with integrin-targeted gold nanobeacons. FASEB J 25:875–882. https://doi.org/10.1096/fj.10-171728
Perry HL, Botnar RM, Wilton-Ely JDET (2020) Gold nanomaterials functionalised with gadolinium chelates and their application in multimodal imaging and therapy. Chem Commun 56:4037–4046. https://doi.org/10.1039/D0CC00196A
Bansal SA, Kumar V, Karimi J et al (2020) Role of gold nanoparticles in advanced biomedical applications. Nanoscale Adv 2:3764–3787. https://doi.org/10.1039/D0NA00472C
Kauffman GB (1985) The role of gold in alchemy. Part II. Gold Bull 18:69–78. https://doi.org/10.1007/BF03214689
Pal D, Sahu CK, Haldar A (2014) Bhasma : the ancient Indian nanomedicine. J Adv Pharm Technol Res 5:4–12. https://doi.org/10.4103/2231-4040.126980
Cobley CM, Chen J, Cho EC et al (2011) Gold nanostructures: a class of multifunctional materials for biomedical applications. Chem Soc Rev 40:44–56. https://doi.org/10.1039/B821763G
Sasidharan A, Monteiro-Riviere NA (2015) Biomedical applications of gold nanomaterials: opportunities and challenges. Wiley Interdiscip Rev: Nanomed Nanobiotechnol 7:779–796. https://doi.org/10.1002/wnan.1341
Obaid G, Chambrier I, Cook MJ, Russell DA (2015) Cancer targeting with biomolecules: a comparative study of photodynamic therapy efficacy using antibody or lectin conjugated phthalocyanine-PEG gold nanoparticles. Photochem Photobiol Sci 14:737–747. https://doi.org/10.1039/c4pp00312h
Han G, Ghosh P, de Vincent Rotello MM (2007) Drug and gene delivery using gold nanoparticles. 3:40–45
Her S, Jaffray DA, Allen C (2017) gold nanoparticles for applications in cancer radiotherapy: mechanisms and recent advancements. Adv Drug Deliv Rev 109:84–101. https://doi.org/10.1016/j.addr.2015.12.012
Pissuwan D, Niidome T, Cortie MB (2011) The forthcoming applications of gold nanoparticles in drug and gene delivery systems. J Control Release 149:65–71. https://doi.org/10.1016/j.jconrel.2009.12.006
Kaul S, Gulati N, Verma D et al (2018) Role of nanotechnology in cosmeceuticals: a review of recent advances. J Pharm 2018:1–19. https://doi.org/10.1155/2018/3420204
Fytianos G, Rahdar A, Kyzas GZ (2020) Nanomaterials in cosmetics: recent updates. Nanomaterials 10:979. https://doi.org/10.3390/nano10050979
Bilal M, Iqbal HMN (2020) New insights on unique features and role of nanostructured materials in cosmetics. Cosmetics 7:24. https://doi.org/10.3390/cosmetics7020024
Dhawan S, Sharma P, Nanda S (2020) Cosmetic nanoformulations and their intended use. In: Nanocosmetics. Elsevier, pp 141–169
Sani A, Cao C, Cui D (2021) Toxicity of gold nanoparticles (AuNPs): a review. Biochem Biophys Rep 26:100991. https://doi.org/10.1016/j.bbrep.2021.100991
Ferin J, Oberdörster G, Soderholm SC, Gelein R (1991) Pulmonary tissue access of ultrafine particles. J Aerosol Med 4:57–68. https://doi.org/10.1089/jam.1991.4.57
Ferin J, Oberdörster G, Penney DP et al (1990) Increased pulmonary toxicity of ultrafine particles? I. Particle clearance, translocation, morphology. J Aerosol Sci 21:381–384. https://doi.org/10.1016/0021-8502(90)90064-5
Donaldson K (2004) Nanotoxicology. Occup Environ Med 61:727–728. https://doi.org/10.1136/oem.2004.013243
Stone V, Miller MR, Clift MJD et al (2017) Nanomaterials versus ambient ultrafine particles: an opportunity to exchange toxicology knowledge. Environ Health Perspect 125:1–18. https://doi.org/10.1289/EHP424
Perreault F, Oukarroum A, Gerson Matias W et al (2010) Evaluation of copper oxide nanoparticles toxicity using chlorophyll a fluorescence imaging in Lemna gibba. J Bot 2010:1–9. https://doi.org/10.1155/2010/763142
Song G, Gao Y, Wu H et al (2012) Physiological effect of anatase TiO2 nanoparticles on Lemna minor. Environ Toxicol Chem 31:2147–2152. https://doi.org/10.1002/etc.1933
Glenn JB, White SA, Klaine SJ (2012) Interactions of gold nanoparticles with freshwater aquatic macrophytes are size and species dependent. Environ Toxicol Chem 31:194–201. https://doi.org/10.1002/etc.728
Oukarroum A, Barhoumi L, Pirastru L, Dewez D (2013) Silver nanoparticle toxicity effect on growth and cellular viability of the aquatic plant Lemna gibba. Environ Toxicol Chem 32:902–907. https://doi.org/10.1002/etc.2131
Reis P, Pereira R, Carvalho FP et al (2018) Life history traits and genotoxic effects on Daphnia magna exposed to waterborne uranium and to a uranium mine effluent - a transgenerational study. Aquat Toxicol 202:16–25. https://doi.org/10.1016/j.aquatox.2018.06.009
Asghari S, Johari SA, Lee JH et al (2012) toxicity of various silver nanoparticles compared to silver ions in Daphnia magna. J Nanobiotechnol 10:1–11. https://doi.org/10.1186/1477-3155-10-14
Mantecca P, Guazzoni N, Santo N et al (2014) Toxic effects and ultrastructural damages to Daphnia magna of two differently sized ZnO nanoparticles: Does size matter? Water Res 53:339–350. https://doi.org/10.1016/j.watres.2014.01.036
Wiench K, Wohlleben W, Hisgen V et al (2009) Acute and chronic effects of nano- and non-nano-scale TiO2 and ZnO particles on mobility and reproduction of the freshwater invertebrate Daphnia magna. Chemosphere 76:1356–1365. https://doi.org/10.1016/j.chemosphere.2009.06.025
McClellan-Green P, Zhu S, Haasch ML et al (2005) Ecotoxicology of carbon-based engineered nanoparticles: effects of fullerene (C60) on aquatic organisms. Carbon 44:1112–1120. https://doi.org/10.1016/j.carbon.2005.11.008
Bacchetta R, Santo N, Marelli M et al (2017) Chronic toxicity effects of ZnSO4 and ZnO nanoparticles in Daphnia magna. Environ Res 152:128–140. https://doi.org/10.1016/j.envres.2016.10.006
Römer I, White TA, Baalousha M et al (2011) Aggregation and dispersion of silver nanoparticles in exposure media for aquatic toxicity tests. J Chromatogr A 1218:4226–4233. https://doi.org/10.1016/j.chroma.2011.03.034
Jensen LHS, Skjolding LM, Thit A et al (2017) Not all that glitters is gold—electron microscopy study on uptake of gold nanoparticles in Daphnia magna and related artifacts. Environ Toxicol Chem 36:1503–1509. https://doi.org/10.1002/etc.3697
Pontes MS, Graciano DE, Antunes DR et al (2020) In vitro and in vivo impact assessment of eco-designed CuO nanoparticles on non-target aquatic photoautotrophic organisms. J Hazard Mater 396:122484. https://doi.org/10.1016/j.jhazmat.2020.122484
Auclair J, Quinn B, Peyrot C et al (2020) Detection, biophysical effects, and toxicity of polystyrene nanoparticles to the cnidarian Hydra attenuata. Environ Sci Pollut Res 27:11772–11781. https://doi.org/10.1007/s11356-020-07728-1
Nasser F, Constantinou J, Lynch I (2020) Nanomaterials in the environment acquire an “eco-corona” impacting their toxicity to Daphnia magna—a call for updating toxicity testing policies. Proteomics 20:1–15. https://doi.org/10.1002/pmic.201800412
Nasser F, Davis A, Valsami-Jones E, Lynch I (2016) Shape and charge of gold nanomaterials influence survivorship, oxidative stress and moulting of Daphnia magna. Nanomaterials 6:222. https://doi.org/10.3390/nano6120222
Kimling J, Maier M, Okenve B et al (2006) Turkevich method for gold nanoparticle synthesis revisited. J Phys Chem B 110:15700–15707. https://doi.org/10.1021/jp061667w
Peter JHJT, Cooper, (1951) A study of the nucleation and growth process in the synthesis of colloidal gold. Discuss Faraday Soc 55:55–75. https://doi.org/10.1039/df9511100055
Zhou X, Zhang X, Yu X et al (2008) The effect of conjugation to gold nanoparticles on the ability of low molecular weight chitosan to transfer DNA vaccine. Biomaterials 29:111–117. https://doi.org/10.1016/j.biomaterials.2007.09.007
Thanou M, Verhoef JC, Junginger HE (2001) Oral drug absorption enhancement by chitosan and its derivatives. Adv Drug Deliv Rev 52:117–126. https://doi.org/10.1016/S0169-409X(01)00231-9
Aiba S (1991) Studies on chitosan: 3. Evidence for the presence of random and block copolymer structures in partially N-acetylated chitosans. Int J Biol Macromol 13:40–44. https://doi.org/10.1016/0141-8130(91)90008-I
Lim JW, Kang IJ (2013) Chitosan-gold nano composite for dopamine analysis using raman scattering. Bull Korean Chem Soc 34:237–242. https://doi.org/10.5012/bkcs.2013.34.1.237
Paquet-Mercier F, Babaei Aznaveh N, Safdar M, Greener J (2013) A microfluidic bioreactor with in situ SERS imaging for the study of controlled flow patterns of biofilm precursor materials. Sensors (Switzerland) 13:14714–14727. https://doi.org/10.3390/s131114714
OECD (2006) Test No. 221: Lemna sp. Growth Inhibition Test. OECD. https://doi.org/10.1787/9789264016194-en
OECD (2004) Test No. 202: Daphnia sp. Acute Immobilisation Test. OECD. https://doi.org/10.1787/9789264069947-en
Garner KL, Qin Y, Cucurachi S et al (2018) Linking exposure and kinetic bioaccumulation models for metallic engineered nanomaterials in freshwater ecosystems. ACS Sustain Chem Eng 6:12684–12694. https://doi.org/10.1021/acssuschemeng.8b01691
Inskeep WP, Bloom PR (1985) Extinction coefficients of chlorophyll a and b in N, N -dimethylformamide and 80% acetone. Plant Physiol 77:483–485. https://doi.org/10.1104/pp.77.2.483
Noguez C (2007) Surface plasmons on metal nanoparticles: the influence of shape and physical environment. J Phys Chem C 111:3606–3619. https://doi.org/10.1021/jp066539m
Roduner E (2006) Size matters: why nanomaterials are different. Chem Soc Rev 35:583–592. https://doi.org/10.1039/b502142c
Franconetti A, Carnerero JM, Prado-Gotor R et al (2019) Chitosan as a capping agent: insights on the stabilization of gold nanoparticles. Carbohyd Polym 207:806–814. https://doi.org/10.1016/j.carbpol.2018.12.046
Ma X, Geiser-Lee J, Deng Y, Kolmakov A (2010) Interactions between engineered nanoparticles (ENPs) and plants: phyto toxicity, uptake and accumulation. Sci Total Environ 408:3053–3061. https://doi.org/10.1016/j.scitotenv.2010.03.031
Seitz F, Rosenfeldt RR, Storm K et al (2015) Effects of silver nanoparticle properties, media pH and dissolved organic matter on toxicity to Daphnia magna. Ecotoxicol Environ Saf 111:263–270. https://doi.org/10.1016/j.ecoenv.2014.09.031
Taylor AF, Rylott EL, Anderson CWN, Bruce NC (2014) Investigating the toxicity, uptake, nanoparticle formation and genetic response of plants to gold. PLoS ONE 9:e93793. https://doi.org/10.1371/journal.pone.0093793
Khoshnamvand M, Ashtiani S, Liu J (2020) Acute Toxicity of gold nanoparticles synthesized from macroalga Saccharina japonica towards Daphnia magna. Environ Sci Pollut Res 27:22120–22126. https://doi.org/10.1007/s11356-020-08770-9
Botha TL, James TE, Wepener V (2015) Comparative aquatic Toxicity of gold nanoparticles and ionic gold using a species sensitivity distribution approach. J Nanomater 2015:1–16. https://doi.org/10.1155/2015/986902
Baumann J, Köser J, Arndt D, Filser J (2014) The coating makes the difference: acute effects of iron oxide nanoparticles on Daphnia magna. Sci Total Environ 484:176–184. https://doi.org/10.1016/j.scitotenv.2014.03.023
Hou J, Zhou Y, Wang C et al (2017) Toxic effects and molecular mechanism of different types of silver nanoparticles to the aquatic Crustacean Daphnia magna. Environ Sci Technol 51:12868–12878. https://doi.org/10.1021/acs.est.7b03918
Bozich JS, Lohse SE, Torelli MD et al (2014) Surface chemistry, charge and ligand type impact the toxicity of gold nanoparticles to Daphnia magna. Environ Sci Nano 1:260–270. https://doi.org/10.1039/c4en00006d
Acknowledgements
The authors thank the support of the Universidad Austral de Chile through the Instituto de Materiales y Procesos Termomecánicos (Facultad de Ciencias de la Ingeniería), the Instituto de Ciencias Marinas y Limnológicas (Facultad de Ciencias), and Instituto de Ciencias Químicas (Facultad de Ciencias); and the Instituto Politécnico Nacional through the Secretaría de Investigación y Posgrado, both for the resources and facilities granted to carry out this research. PAG acknowledges the Consejo Nacional de Ciencia y Tecnología (CONACYT) for the Ph.D. scholarship (430637). IMV thanks Fondecyt Regular 1181695 and INLARVI network of VIDCA-UACh, Chile.
Author information
Authors and Affiliations
Contributions
PAG, EZ, and JN conceived and designed the study. PAG and JN carried out the experiments and data collection. All authors analyzed the data and revised the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Abrica-González, P., Zumelzu, E., Nimptsch, J. et al. The effect of chitosan-modified gold nanoparticles in Lemna valdiviana and Daphnia pulex. Gold Bull 55, 77–91 (2022). https://doi.org/10.1007/s13404-021-00306-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13404-021-00306-4