Humic acid attenuation of silver nanoparticle toxicity by ion complexation and the formation of a Ag3+ coating
Graphical abstract
Introduction
The intensive use of silver nanoparticles (AgNPs) raises serious concerns about the environmental risks arising from exposure to this material. This concern has led to a number of studies focusing on the toxicological effects of Ag in different models, such as animal cell lines [1], microorganisms [2,3], algae [4], terrestrial plants[5], invertebrates (Daphnia magna [6,7] and Lumbriculus variegatus [7]), and vertebrates (Rana catesbeiana[8], Oryzias latipes [9,10] and Danio rerio [[11], [12], [13]]).
The toxicity of AgNPs is known to be mainly caused by the release of silver ions [3,14], but it can also be caused by the nanoparticles themselves [14,15]. The ion release results from the oxidation of AgNPs, and normally, Ag1+ ions are released [14,15]. It is known that AgNPs can increase the production of ROS, which in turn can disrupt the electron transport chain, inducing major structural damage and lower ATP production [16]. Likewise, silver ions can bond to the thiol groups in enzymes, such as NADH dehydrogenase, causing the effects mentioned above [16,17]. Other toxic effects caused by AgNP exposure may occur after endocytosis or AgNP adhesion in the cell membranes, due to the possibility of generating a flux of ions through the cell membranes and/or active transport of Ag+ to sensitive biological targets inside the cells [17]. Other mechanisms for AgNP toxicity are related to the direct contact with agglomerated or precipitated nanoparticles, nanoparticles released as colloids into the solution and by ions released from both agglomerates and nanoparticles [18]. Thus, AgNP toxicity may not be related solely to silver concentration but also to the identity of the silver species in the medium and other factors, such as the ionic strength, as well as the presence of H2O2 and organic matter in the media [19].
A typical colloidal dispersion of AgNPs could include metallic AgNPs, free silver ions (including any soluble complexes) and surface-adsorbed silver ions. These species can have a significant influence on the biodistribution and amount of bioavailable silver [19]. Free silver ions have a strong tendency to associate with negatively charged ions to reach a stable state. Five anionic inorganic binders, namely, fluoride (F−), chloride (Cl−), sulfate (SO42−), hydroxide (OH−) and carbonate ions (CO32−), can be found in natural water. AgNPs and/or released silver ions can also bind strongly to humic substances such as humic acid (HA), which are considered the dominant complexing agents in natural water [20,21]; therefore, HA plays an important role in the transport, stability, dissolution, bioavailability and deposition of xenobiotics in aquatic organisms [[22], [23], [24]].
Although some authors have already evaluated the toxicity of AgNPs (i.e., stabilized with citrate) and AgNPs in the presence of HA (i.e., Suwannee River Humic and Fulvic Acid Standards) [25,26], the environmental transformations, transport, and implications of the interaction between HA and AgNPs are still unclear, considering that the physico-chemical characteristics of each type of these materials and the experimental conditions can induce different biological responses in dissimilar aquatic environments. In this context, the aim of this work is to expand the current knowledge regarding the influence of commercial HA and salts (NaCl, KCl, CaCl2 and MgSO4) on the oxidation state of the AgNPs, Ag ion release (Ag° and Ag3+) and toxic effects in zebrafish embryos, using two kinds of fresh water.
Section snippets
Materials
Silver nanopowder (CAS Number 7440-22-4) and HA sodium salt (CAS Number 68131-04-4) were obtained from Sigma-Aldrich. According to the AgNPs Safety Data Sheet provided by Sigma-Aldrich, the particle size was ˂100 nm. Experiments were performed using different aqueous media such as ultrapure water (UPW) (NANOpure Diamond Barnstead, D11931 model), zebrafish growing media (ZGM) (a mixture of salts for simulating freshwater, containing 294.0 mg/L of CaCl2·2H2O, 123.3 mg/L of MgSO4·7H2O, 63.0 mg/L
Characterization
We observed AgNPs with irregular shape (Fig. S1), with the average diameter of 26 ± 16 nm and the mean crystalline size of ∼20 nm, as determined by TEM and XRD, respectively. Examination of the XRD results showed that the diffraction peaks’ positions correspond to the crystalline phase of metallic silver (Ag°), which was corroborated by the Ag3d5/2 peak position (Fig. S2A) of approximately 368.4 eV obtained in the XPS technique.
We also performed tests for HA characterization, which showed the
Conclusions
Our results indicated that the complexation of AgNPs with HA and the presence of salts can change the stability and oxidation state of the AgNPs surface and then affect their dissolution in the aqueous media tested. The Ag3+ formation on the AgNP surface was caused mainly by the presence of NaHCO3, MgSO4 and HA for which the biological effects in zebrafish embryos were not significant for acute exposure. HA coated on the AgNP surface reduced the amount of free Ag ions present in the media, the
Conflict of interest
There is no conflict of interest.
Acknowledgements
The authors are grateful to the Brazilian National Council for Scientific and Technological Development (CNPq), the Brazilian Coordination for the Improvement of Higher Education Personnel (CAPES) and the Brazilian National Institute of Science and Technology in Nanobiotechnology (INCT in Nanobiotechnology). P.R. Cáceres-Vélez, L. Yate and S.E. Moya thank the Marie Curie Projects FP7-PEOPLE-IRSES HIGRAPHEN grant number: 612704 and the FP7-PEOPLE-IRSES- BRASINOEU grant number: 318916 for
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