Gut-microbial adaptation and transformation of silver nanoparticles mediated the detoxification of Daphnia magna and their offspring

Abstract

Despite extensive studies on the toxicity of antibacterial silver (either ionic Ag⁺ or nanoparticles – AgNPs) at the cellular or organism level, little is known about the differences in toxicity at the community level, especially regarding the gut microbiota. In the present study, we applied 16S rRNA sequencing, metatranscriptome sequencing and gut microbiota transplants (GMTs) to investigate the gut-microbial adaptation and transformation of different silver (Ag) forms over 4 generations of exposure of Daphnia magna to environmentally relevant concentrations of Ag⁺ and AgNPs. Our results demonstrated that the gut-accumulated Ag⁺ and AgNPs were transformed by gut microbial sulfidation, which subsequently affected the toxic symptoms of D. magna. Multi-generational exposure revealed that selection of the toxicity-adapted gut microbiota was both Ag form- and exposure time- dependent, resulting in a distinctive gut-microbial community between generations and treatments. Specifically, the expression of gut microbial genes for sulfide synthesis and organic matter degradation was simultaneously expressed when encountering Ag challenge and was positively correlated with the reduced toxic symptoms. The reciprocal GMTs further illustrated that the Ag⁺- and AgNP-adapted gut microbiota were unable to fully acclimate to the toxicity of other Ag forms, resulting in a dramatic community shift and aggravated toxic symptoms of recipient D. magna. Toxic differences between Ag⁺ and AgNPs were related to the enriched organic matter in the gut, which functioned as an electron donor for sulfidation-based detoxification of Ag⁺ through degradation and as an inhibitor of Ag⁺ release from AgNPs by surface adsorption. Our findings provided fundamental understanding about gut-microbial detoxification and transformation of Ag⁺ and AgNPs, which finally resulted in physiological changes of D. magna and their offspring.