Silver nanoparticles impact phototrophic biofilm communities to a considerably higher degree than ionic silver
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Due to the significant increase in nanoparticle production and especially that of silver nanoparticles over the past decade, the toxicity of silver in both ionic (Ag+) and nanoparticulate (AgNPs) form must be studied in detail in order to understand their impact on natural ecosystems. A comparative study of the effect of AgNPs and ionic silver on two independent phototrophic biofilms was conducted in a rotating annular bioreactor (RAB) operating under constant conditions. The concentration of dissolved silver in the inlet solution was progressively increased every 4 days of exposure, from 0.1 to 100 μg L−1. In the course of the 40-day experiment, biofilm samples were collected to determine the evolution of biomass, chlorophyll-a, as well as photosynthetic and heterotrophic enzymatic activities in response to silver addition. Analysis of both dissolved and particulate silver allowed quantification of the distribution coefficient and uptake rate constants. The presence of both AgNPs and Ag+ produced significant changes in the biofilm structure, decreasing the relative percentage of Diatomophyceae and Cyanophyceae and increasing the relative percentage of Chlorophyceae. The accumulation capacity of the phototrophic biofilm with respect to ionic silver and the corresponding distribution coefficients were an order of magnitude higher than those of the phototrophic biofilm with respect to AgNPs. Higher levels of AgNPs decreased the biomass from 8.6 ± 0.2 mg cm−2 for 0–10 μg L−1 AgNPs to 6.0 ± 0.1 mg cm−2 for 100 μg L−1 added AgNPs, whereas ionic silver did not have any toxic effect on the biofilm growth up to 100 μg L−1 of added Ag+. At the same time, AgNPs did not significantly affect the photosynthetic activity of the biofilm surface communities compared to Ag+. It can thus be hypothesized that negatively charged AgNPs may travel through the biofilm water channels, thereby affecting the whole biofilm structure. In contrast, positively charged Ag+ is bound at the cell surfaces and EPS, thus blocking its further flux within the biofilm layers. On the whole, the phototrophic biofilm demonstrated significant capacities to accumulate silver within the surface layers. The main mechanism to avoid the toxic effects is metal complexation with exopolysaccharides and accumulation within cell walls, especially pronounced under Ag+ stress. The significant AgNPs and Ag+ uptake capacities of phototrophic biofilm make it a highly resistant ecosystem in silver-polluted river waters.
KeywordsAgNPs Ionic silver Phototrophic biofilm Bioreactor
This research work has been supported by Midi-Pyrénées Regional Council (France) within the program Gagilau (NoDAER-R93 90173), funding the postdoctoral fellowship for Aridane G. González. Support from BIO-GEO-CLIM grant of Russian Ministry of Science and Education (No. 14.B25.31.0001) and ANR CITTOXIC Nano are equally acknowledged.
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