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

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.

[1]  Benjamin P Colman,et al.  Long-term transformation and fate of manufactured ag nanoparticles in a simulated large scale freshwater emergent wetland. , 2012, Environmental science & technology.

[2]  U. Epa Process Design Manual: Land Application of Sewage Sludge and Domestic Septage , 1995 .

[3]  W. Liesack,et al.  Use of the T-RFLP technique to assess spatial and temporal changes in the bacterial community structure within an agricultural soil planted with transgenic and non-transgenic potato plants. , 2000, FEMS microbiology ecology.

[4]  Enrique Navarro,et al.  Toxicity of silver nanoparticles to Chlamydomonas reinhardtii. , 2008, Environmental science & technology.

[5]  Dicksen Tanzil,et al.  Relative risk analysis of several manufactured nanomaterials: an insurance industry context. , 2005, Environmental science & technology.

[6]  F. Rohlf Paleontological Data Analysis , 2007 .

[7]  K. Hungerbühler,et al.  Estimation of cumulative aquatic exposure and risk due to silver: contribution of nano-functionalized plastics and textiles. , 2008, The Science of the total environment.

[8]  C. Richardson,et al.  Spatial Impacts of Stream and Wetland Restoration on Riparian Soil Properties in the North Carolina Piedmont , 2011 .

[9]  Aaron M.Ellison PC‐ORD: Multivariate Analysis of Ecological Data , 1998, The Bulletin of the Ecological Society of America.

[10]  Jamie R Lead,et al.  Silver nanoparticle impact on bacterial growth: effect of pH, concentration, and organic matter. , 2009, Environmental science & technology.

[11]  Benjamin P Colman,et al.  More than the ions: the effects of silver nanoparticles on Lolium multiflorum. , 2011, Environmental science & technology.

[12]  R. L. Sinsabaugha,et al.  The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil , 2002 .

[13]  Richard D Handy,et al.  Impact of silver nanoparticle contamination on the genetic diversity of natural bacterial assemblages in estuarine sediments. , 2009, Environmental science & technology.

[14]  R. Burns Enzyme activity in soil: Location and a possible role in microbial ecology , 1982 .

[15]  Zong-ci Zhao,et al.  Climate change 2001, the scientific basis, chap. 8: model evaluation. Contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change IPCC , 2001 .

[16]  J. Jung,et al.  Effects of Colloidal Silver Nanoparticles on Sclerotium-Forming Phytopathogenic Fungi , 2009 .

[17]  Chi-Ming Che,et al.  Proteomic analysis of the mode of antibacterial action of silver nanoparticles. , 2006, Journal of proteome research.

[18]  H. Gauch,et al.  Analysis of T-RFLP data using analysis of variance and ordination methods: a comparative study. , 2008, Journal of microbiological methods.

[19]  J. Houghton,et al.  Climate change 2001 : the scientific basis , 2001 .

[20]  M. Clarholm Interactions of bacteria, protozoa and plants leading to mineralization of soil nitrogen , 1985 .

[21]  Anna M. Wise,et al.  Sulfidation of silver nanoparticles decreases Escherichia coli growth inhibition. , 2012, Environmental science & technology.

[22]  Stella M. Marinakos,et al.  Intracellular uptake and associated toxicity of silver nanoparticles in Caenorhabditis elegans. , 2010, Aquatic Toxicology.

[23]  G. Lowry,et al.  Role of Particle Size and Soil Type in Toxicity of Silver Nanoparticles to Earthworms , 2011 .

[24]  Noah Fierer,et al.  Variations in microbial community composition through two soil depth profiles , 2003 .

[25]  Paul Westerhoff,et al.  Nanoparticle silver released into water from commercially available sock fabrics. , 2008, Environmental science & technology.

[26]  Jan Lepš,et al.  Multivariate Analysis of Ecological Data , 2006 .

[27]  Michael F. Hochella,et al.  Characterization and environmental implications of nano- and larger TiO(2) particles in sewage sludge, and soils amended with sewage sludge. , 2012, Journal of environmental monitoring : JEM.

[28]  P. Hamal,et al.  Antifungal activity of silver nanoparticles against Candida spp. , 2009, Biomaterials.

[29]  Hugh G. Gauch,et al.  T-REX: software for the processing and analysis of T-RFLP data , 2009, BMC Bioinformatics.

[30]  Hansruedi Siegrist,et al.  Behavior of metallic silver nanoparticles in a pilot wastewater treatment plant. , 2011, Environmental science & technology.

[31]  C. Emmerling,et al.  Effects of silver nanoparticles on the microbiota and enzyme activity in soil , 2010 .

[32]  Gregory V Lowry,et al.  Sulfidation processes of PVP-coated silver nanoparticles in aqueous solution: impact on dissolution rate. , 2011, Environmental science & technology.

[33]  Cláudia Pascoal,et al.  Can Metal Nanoparticles Be a Threat to Microbial Decomposers of Plant Litter in Streams? , 2011, Microbial Ecology.

[34]  P. Curtis,et al.  INTERACTIVE EFFECTS OF ATMOSPHERIC CO2 AND SOIL‐N AVAILABILITY ON FINE ROOTS OF POPULUS TREMULOIDES , 2000 .

[35]  Benjamin P Colman,et al.  Antimicrobial effects of commercial silver nanoparticles are attenuated in natural streamwater and sediment , 2012, Ecotoxicology.

[36]  M. Noguer,et al.  Climate change 2001: The scientific basis. Contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change , 2002 .

[37]  A. Ravishankara,et al.  Nitrous Oxide (N2O): The Dominant Ozone-Depleting Substance Emitted in the 21st Century , 2009, Science.

[38]  Byoung-In Sang,et al.  Analysis of the toxic mode of action of silver nanoparticles using stress-specific bioluminescent bacteria. , 2008, Small.

[39]  J E O N G K I M,et al.  Discovery and Characterization of Silver Sulfide Nanoparticles in Final Sewage Sludge Products , 2010 .

[40]  Jamie R Lead,et al.  Nanomaterials in the environment: Behavior, fate, bioavailability, and effects , 2008, Environmental toxicology and chemistry.

[41]  Benjamin P Colman,et al.  Effects of Silver Nanoparticle Exposure on Germination and Early Growth of Eleven Wetland Plants , 2012, PloS one.

[42]  K. R. Clarke,et al.  Non‐parametric multivariate analyses of changes in community structure , 1993 .

[43]  M. Yacamán,et al.  The bactericidal effect of silver nanoparticles , 2005, Nanotechnology.