Microbially-mediated indirect effects of silver nanoparticles on aquatic invertebrates

Complex natural systems are affected by multiple anthropogenic stressors, and therefore indirect effects within food webs are increasingly investigated. In this context, dead organic matter (OM) or detritus provides a food source sustaining detrital food webs that recycle the retained energy through microbial decomposition and invertebrate consumption. In aquatic environments, poorly water-soluble contaminants, including nanoparticles (NPs), quickly adsorb onto OM potentially modifying OM-associated microbial communities. Since invertebrates often depend on microbial conditioning to enhance OM quality, adverse effects on OM-associated microbial communities could potentially affect invertebrate performances. Therefore, this study assessed the effect of environmentally relevant concentrations of the model emerging contaminant, silver nanoparticles (AgNPs), on OM-associated microorganisms and subsequent indirect effects on growth of the invertebrate Asellus aquaticus. At low concentrations (0.8 ug/L), AgNPs inhibited activity and altered metabolic diversity of the OM-associated microbial community. This was observed to coincide with a negative effect on the growth of A. aquaticus due to antimicrobial properties, as a decreased growth was observed when offered AgNP-contaminated OM. When A. aquaticus were offered sterile OM in the absence of AgNPs, invertebrate growth was observed to be strongly retarded, illustrating the importance of microorganisms in the diet of this aquatic invertebrate. This outcome thus hints that environmentally relevant concentrations of AgNPs can indirectly affect the growth of aquatic invertebrates by affecting OM-associated microbial communities, and hence that microorganisms are an essential link in understanding bottom-up directed effects of chemical stressors in food webs.