Low Concentrations of Silver Nanoparticles in Biosolids Cause Adverse Ecosystem Responses under Realistic Field Scenario

Benjamin P Colman,Brian C Reinsch,Bojeong Kim,Sarah Anciaux,Gregory V Lowry,Bonnie M Mcgill,Claudia K Gunsch,Christina L Arnaout,Emily S Bernhardt,Liyan Yin,Justin P Wright,Curtis J Richardson,Jason M Unrine,Michael F Hochella,Stephen J Johnson

doi:10.1371/journal.pone.0057189

Abstract

A large fraction of engineered nanomaterials in consumer and commercial products will reach natural ecosystems. To date, research on the biological impacts of environmental nanomaterial exposures has largely focused on high-concentration exposures in mechanistic lab studies with single strains of model organisms. These results are difficult to extrapolate to ecosystems, where exposures will likely be at low-concentrations and which are inhabited by a diversity of organisms. Here we show adverse responses of plants and microorganisms in a replicated long-term terrestrial mesocosm field experiment following a single low dose of silver nanoparticles (0.14 mg Ag kg−1 soil) applied via a likely route of exposure, sewage biosolid application. While total aboveground plant biomass did not differ between treatments receiving biosolids, one plant species, Microstegium vimeneum, had 32 % less biomass in the Slurry+AgNP treatment relative to the Slurry only treatment. Microorganisms were also affected by AgNP treatment, which gave a significantly different community composition of bacteria in the Slurry+AgNPs as opposed to the Slurry treatment one day after addition as analyzed by T-RFLP analysis of 16S-rRNA genes. After eight days, N2O flux was 4.5 fold higher in the Slurry+AgNPs treatment than the Slurry treatment. After fifty days, community composition and N2O flux of the Slurry+AgNPs treatment converged with the Slurry. However, the soil microbial extracellular enzymes leucine amino peptidase and phosphatase had 52 and 27% lower activities, respectively, while microbial biomass was 35% lower than the Slurry. We also show that the magnitude of these responses was in all cases as large as or larger than the positive control, AgNO3, added at 4-fold the Ag concentration of the silver nanoparticles.

Highlights

Engineered silver nanoparticles (AgNPs) are an emerging environmental contaminant of concern for regulators and consumer advocates because of their antimicrobial properties
Given the low concentrations used in our experiment, direct observations of the physical and chemical properties of Ag recovered in our mesocosm soils and plants using techniques including transmission electron microscopy (TEM) and extended x-ray absorption fine structure (EXAFS) proved to be elusive
The EXAFS data showed that after just fifteen minutes of exposure at 22 uC, 25% of the Ag was transformed into Ag2S (Figure 3B).The second line of evidence comes from the detection of Ag intimately associated with TiO2NP aggregates[25] in our surface soils in the Slurry+AgNPs treatment (Figure S1), suggesting the potential for partial oxidation of Ag2S or AgNPs over the course of the experimental exposure, and that TiO2-NPs and other metal-oxide nanoparticles found in soils and biosolids may serve as a sink and/or carrier for Ag in the environment

Summary

Introduction

Engineered silver nanoparticles (AgNPs) are an emerging environmental contaminant of concern for regulators and consumer advocates because of their antimicrobial properties. Our knowledge of AgNP toxicity is largely drawn from controlled laboratory experiments with single strains of bacteria or fungi. These studies have shown that AgNP exposure leads to membrane damage, oxidative stress, and significant mortality [6,7,8,9,10]. The small number of laboratory AgNP exposure experiments conducted in environmental media (i.e., soil, streamwater, sediment) with diverse native microbial communities have shown that AgNPs had no effects[13,14], limited sublethal effects[15], or reduced effects in comparison to dissolved Ag[14,16]

Methods

Results

Conclusion