Fate and behaviour of silver nanoparticles in terrestrial ecosystems

Abstract

With the ongoing development of nanotechnology, silver nanoparticles (Ag-NPs) are used extensively in a wide range of products due to their strong and broad-spectrum antimicrobial activities. Most of this Ag eventually moves into wastewater treatment plants (WWTPs) where the majority of the Ag is transformed to Ag2S. Of particular concern is the subsequent land-application of these Ag-containing biosolids from WWTPs to agricultural soils, with this resulting in the accumulation of Ag in soils and potentially posing a threat to the health of terrestrial ecosystems and humans.The first experiment aimed to examine the effects of salinity on the transformation and availability of Ag2S-NPs given that a large area of land worldwide is considered saline. In this study, we used two soils with low (2.8 dS m−1 for the soil solution) and high salinity (27 dS m−1) and amended them with Ag2S-containning sludge. We also investigated the impacts of Ag on the microbially mediated N cycle. We found that Ag remained largely as Ag2S, with salinity causing no major change in the speciation of the Ag. Furthermore, the increased Ag availability in the high salinity soil (although overall still low) increased nitrification gene and denitrification gene levels, and increased relative abundance of halophilic denitrifiers (Salinimicrobium, and Zunongwangia), resulting in increased N2O emission. In summary, our findings indicate that applying Ag2S-containing sludge to saline soils can disrupt the N cycle in agricultural ecosystems.Next, we compared the effects of Ag (Ag2S-NPs or Ag2SO4) on the earthworm-mediated (Eisenia fetida and Pontoscolex corethruru) N cycle. We found that the presence of either earthworms or added Ag resulted in significant increases in denitrification and N2O emissions. However, when soils contained both Ag2S and earthworms, N2O emissions decreased by 14–33% compared to soils with earthworms without added Ag, due to a Ag-induced decrease in the abundance of gut denitrifiers, as well as a decrease in copy numbers of the nitrification gene (nxrB) and the denitrification genes (napA, nirS and nosZ) in the earthworm gut. In conclusion, our work shows that the application of Ag2S-containing sludge can disrupt the denitrification process of the earthworm gut.The third experiment examined the role of soil organic matter in altering the bioavailability of Ag2S-NPs. In this study, two soils (with low [7.9 g C kg-1 soil] and high [52 g C kg-1 soil] organic matter content) were amended with Ag2S-NPs-contained sludge to study the impacts of soil organic matter on Ag availability to soybean (Glycine max L.) and earthworms (Eisenia fetida). We found that Ag2S-NPs were more easily converted to Ag-NPs in the soil solution of the high organic soil, with this soil having a higher Ag bioavailability compared to the soil with low organic matter content. The interaction between earthworms and organic matter effectively increased the bioavailability of Ag. In addition, Ag2S-NPs eliminated the stimulative effects of earthworms on plant nutrient uptake. In soils amended with Ag2S-NPs, plant tissues had lower concentrations of Cu, Fe, and P when grown in high organic matter soils in the presence of earthworms than compared to the soils without earthworms. Importantly, in the presence of earthworm, Ag2S-NPs reduce the relative abundance of Chloroflexi associated with nutrient cycling, while they increase the relative abundance of resistant bacteria, belonging to the phylum Bacteroides. These results provide valuable information for understanding the biological and biochemical effects of Ag2S-NP exposure on the function of earthworms.Finally, given that we observed that Ag2S-NPs can potentially have adverse effects on soil microorganisms, we were also interested in the potential effect of Ag when consumed in drinking water. Despite the high effectiveness of the filter paper in killing E. coli in the water, the concentration of Ag in the filtrate subsequently exceeded the drinking water quality standard (0.1 mg L-1), with the release of Ag depending upon the chemical properties of water. For example, an increase in Cl concentration increased the release of Ag. Although 64% of the Ag in the filter paper was present as Ag-NPs, up to 36% of the Ag in the filter paper was present as AgNO3 – this AgNO3 may contribute to the high Ag concentrations found in the filtrate. Finally, we also examined the impacts of oral gavage of this Ag-containing filtrate on the mouse gut microbiome. It was found that Ag in the filtrate mainly accumulated in the liver and kidney. In female mice, Ag-containing filtrate increased the relative abundance of Bacteroides in the feceas, while reducing the relative abundance of Fimicutes. Thus, our data show that although Ag-NP-containing filtration products are suitable for their antibacterial properties, they may also have an effect on the gut microbiota.Together, these studies have demonstrated that soil properties affect the behaviour of Ag2S-NPs, the functions of earthworms, and the structure of microbial community.