Mixed messages from benthic microbial communities exposed to nanoparticulate and ionic silver: 3D structure picks up nano-specific effects, while EPS and traditional endpoints indicate a concentration-dependent impact of silver ions.

Alexandra Kroll,Linn Sgier,Thomas Backhaus,Marcus Rybicki,Dirk Jungmann,Corinna Burkart,Marianne Matzke,Rudo Verweij,Kerstin Jurkschat,Claus Svendsen,Patrick Obert-Rauser

doi:10.1007/s11356-015-4887-7

Abstract

Silver nanoparticles (AgNP) are currently defined as emerging pollutants in surface water ecosystems. Whether the toxic effects of AgNP towards freshwater organisms are fully explainable by the release of ionic silver (Ag+) has not been conclusively elucidated. Long-term effects to benthic microbial communities (periphyton) that provide essential functions in stream ecosystems are unknown. The effects of exposure of periphyton to 2 and 20 μg/L Ag+ (AgNO3) and AgNP (polyvinylpyrrolidone stabilised) were investigated in artificial indoor streams. The extracellular polymeric substances (EPS) and 3D biofilm structure, biomass, algae species, Ag concentrations in the water phase and bioassociated Ag were analysed. A strong decrease in total Ag was observed within 4 days. Bioassociated Ag was proportional to dissolved Ag indicating a rate limitation by diffusion across the diffusive boundary layer. Two micrograms per liter of AgNO3 or AgNP did not induce significant effects despite detectable bioassociation of Ag. The 20-μg/L AgNO3 affected green algae and diatom communities, biomass and the ratio of polysaccharides to proteins in EPS. The 20-μg/L AgNO3 and AgNP decreased biofilm volume to about 50 %, while the decrease of biomass was lower in 20 μg/L AgNP samples than the 20-μg/L AgNO3 indicating a compaction of the NP-exposed biofilms. Roughness coefficients were lower in 20 μg/L AgNP-treated samples. The more traditional endpoints (biomass and diversity) indicated silver ion concentration-dependent effects, while the newly introduced parameters (3D structure and EPS) indicated both silver ion concentration-dependent effects and effects related to the silver species applied.Electronic supplementary materialThe online version of this article (doi:10.1007/s11356-015-4887-7) contains supplementary material, which is available to authorized users.

Highlights

Natural biofilms in the photic benthic zone are an essential element of stream ecosystems
Diatom and green algae communities, biomass and extracellular polymeric substances (EPS) composition were impacted by 20 μg/L AgNO3 indicating that the effective threshold was between 4.9 μg/L Ag+ (20 μg/L AgNP, no effect) and 13.7 μg/L Ag+ (20 μg/L AgNO3 significant changes) in this setup
Both 20 μg/L AgNO3 and AgNP significantly decreased biofilm volume to about 50 % compared to the controls; the decrease of the biomass was much lower in 20 μg/L AgNP-treated samples than in the 20-μg/L AgNO3 samples

Summary

Introduction

Natural biofilms in the photic benthic zone are an essential element of stream ecosystems. They are formed by phototrophic and heterotrophic microorganisms, i.e. eukaryotic algae, cyanobacteria, heterotrophic bacteria and fungi. The phototrophic fraction of these communities has initially been referred to as periphyton (Azim et al 2006). As the terms periphyton and biofilms are used more commonly to refer to the entire community, we will adopt this terminology in the following. Biofilm formation is influenced by environmental conditions, such as availability of nutrients, type and roughness of the substratum, as well as hydrodynamic shear force (Azim et al 2006; Harrison et al 2006; Labiod et al 2007; Larned 2010). The species composition of the diatoms inhabiting the biofilms is employed in various water quality indices to assess the impact of anthropogenic activities

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