Colonizing microbiota protect zebrafish larvae against silver nanoparticle toxicity

Abstract

Metal-based nanoparticles exhibiting antimicrobial activity are of emerging concern to human and environmental health. In addition to their direct adverse effects to plants and animals, indirect effects resulting from disruption of beneficial host–microbiota interactions may contribute to the toxicity of these particles. To explore this hypothesis, we compared the acute toxicity of silver and zinc oxide nanoparticles (nAg and nZnO) to zebrafish larvae that were either germ-free or colonized by microbiota. Over two days of exposure, germ-free zebrafish larvae were more sensitive to nAg than microbially colonized larvae, whereas silver ion toxicity did not differ between germ-free and colonized larvae. Using response addition modeling, we confirmed that the protective effect of colonizing microbiota against nAg toxicity was particle-specific. Nearly all mortality among germ-free larvae occurred within the first day of exposure. In contrast, mortality among colonized larvae increased gradually over both exposure days. Concurrent with this gradual increase in mortality was a marked reduction in the numbers of live host-associated microbes, suggesting that bactericidal effects of nAg on protective microbes resulted in increased mortality among colonized larvae over time. No difference in sensitivity between germ-free and colonized larvae was observed for nZnO, which dissolved rapidly in the exposure medium. At sublethal concentrations, these particles moreover did not exert detectable bactericidal effects on larvae-associated microbes. Altogether, our study shows the importance of taking host–microbe interactions into account in assessing toxic effects of nanoparticles to microbially colonized hosts, and provides a method to screen for microbiota interference with nanomaterial toxicity.