Microbially-mediated indirect effects of silver nanoparticles on aquatic invertebrates

Yujia Zhai,Eline Hin,Maarten Schrama,Ellard R Hunting,Nadja R Brun,Mirco Bundschuh,Martina G Vijver

doi:10.1007/s00027-018-0594-z

Abstract

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.

Highlights

Dead organic matter (OM) or detritus serves as a major food source fueling aquatic detritivorous food webs
The metabolic activity of the OM-associated microorganisms was negatively affected by AgNP at low and environmentally relevant concentrations with a decline in microbial activity and metabolic diversity with increasing AgNP concentration
Microorganisms are considered an important diet of macro-invertebrates (Graça et al 1993ab; Chung and Suberkropp 2009), supporting their growth (Findlay and Tenore 1982; Findlay et al 1984)

Summary

Introduction

Dead organic matter (OM) or detritus serves as a major food source fueling aquatic detritivorous food webs. OM-associated microbial communities can partly degrade OM through enzymatic activity (known as conditioning), and therewith form an essential trophic link by stimulating invertebrate feeding (Graça 2001; Danger et al 2012). OM-associated microorganisms positively affect growth and reproduction of many invertebrates relative to unconditioned food sources (Graça et al 1993a, b), a benefit that relies on the provisioning of essential nutrients such as nitrogen, some fatty acids, and vitamins Increasing evidence suggests that many such contaminants can have adverse effects on OM-associated microbial communities, with consequences for OM decomposition rates Tlili et al 2016; Du et al 2018; Pradhan et al 2012; Batista et al 2017a, b), bottom-up directed effects on detritivore growth remain unclear While NPs were observed to negatively affect growth and diversity of OM-associated microbial communities (e.g. Tlili et al 2016; Du et al 2018; Pradhan et al 2012; Batista et al 2017a, b), bottom-up directed effects on detritivore growth remain unclear

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Conclusion