Final Report: Transatlantic Initiative for Nanotechnology and the Environment

EPA Grant Number: R834574
Title: Transatlantic Initiative for Nanotechnology and the Environment
Investigators: Bertsch, Paul M. , Dorey, Robert A , Rocks, Sophie A , McNear, David H. , Unrine, Jason M. , Wiesner, Mark R. , Lowry, Gregory V. , Tsyusko, Olga V. , Neal, Andy , Jefferson, Bruce , Svendsen, Claus , Spurgeon, David , Casman, Elizabeth , Zhang, Hao , Harris, J. , Liu, Jie , Ritz, Karl , Kabengi, Nadine , McGrath, Steve , Lofts, Steve
Institution: University of Kentucky , Carnegie Mellon University , Lancaster University , Cranfield University , Centre for Ecology and Hydrology , Duke University , Rothamsted Research
Current Institution: University of Kentucky , Carnegie Mellon University , Centre for Ecology and Hydrology , Cranfield University , Duke University , Lancaster University , Rothamsted Research
EPA Project Officer: Klieforth, Barbara I
Project Period: August 1, 2010 through September 30, 2014 (Extended to June 30, 2016)
Project Amount: $2,000,000
RFA: Environmental Behavior, Bioavailability and Effects of Manufactured Nanomaterials - Joint US – UK Research Program (2009) RFA Text |  Recipients Lists
Research Category: Chemical Safety for Sustainability

Objective:

We have developed a life cycle perspective inspired conceptual model (CM) that suggests the importance of terrestrial ecosystems as a major repository of ZnO, TiO2, and Ag manufactured nanomaterials (MNMs) introduced via the land application of MNM-containing biosolids. In this project, we investigated the transport, fate, behavior, bioavailability, and effects of MNMs in(to) agroecosystems under environmentally realistic scenarios organized around three key hypotheses:

Hypothesis (H1)—Surface chemistry is the primary factor influencing the fate and transport of MNMs in the terrestrial environment as well as the bioavailability and effects to biological receptors;

Hypothesis (H2)—Once released to the environment, pristine MNM surfaces will be modified by interactions with organic and inorganic ligands (macromolecules) or via other biogeochemical transformations (aging effects forming a-MNMs); and

Hypothesis (H3)—Ecoreceptors will respond to interactions with pristine metal and metal oxide MNMs, a-MNMs, and/or dissolved constituent metal ions and bulk oxides by specific ecological and toxicogenomic responses that will reflect their combined effects.

The overall objectives are to:

Objective 1 (O1): Compare the transport, fate, behavior, bioavailability, and effects of MNMs, a-MNMs, and/or dissolved free metals/bulk oxides to organisms with key terrestrial ecosystem functions, as well as exposure pathways involving humans;

Objective 2 (O2): Determine MNM, surface modified MNM and a-MNM interactions with important biological targets relevant to the BLM and pBRM models and relate these interactions to physicochemical properties;

Objective 3 (O3): Validate models with information generated from experiments designed to address O1 for MNMs introduced through a pilot scale Waste Water Treatment Process (WWTP) to key terrestrial ecoreceptors, including effects of MNMs on the WWTP itself;

Objective 4 (O4): Determine realistic MNM emission scenarios for Tier 1 MNMs in wastewater from the WWT pilot plant data and develop first generation Life-Cycle-Analysis-inspired Risk Assessment (LCA-RA) model components for terrestrial effects of Tier 1 MNMs and a-MNMs based on data generated in experiments designed to address O1, O2, and O3; and

Objective 5 (O5): Provide tools for in situ detection, monitoring, and characterization of pristine MNMs and a-MNMs in environmental media and biota.

Summary/Accomplishments (Outputs/Outcomes):

We completed a series of major pot experiments investigating the toxicity of the nano-metal and bulk metal spiked sewage sludge biosolids to the model legume Medicago truncatula and Sinorhizobium melliloti. The sewage sludge biosolids were generated at a pilot wastewater treatment plant facility at Cranfield University. We published a paper detailing the speciation of metals in the biosolids as measured using synchrotron-based X-ray absorption spectroscopy (XAS) as received and after composting (Ma, et al., 2013). These results suggested no difference in the speciation of the nano and bulk metals as measured by XAS. The first experiments included exposures to fresh sewage sludge biosolids mixtures containing 50% sewage sludge (simulating 10 years of sludge application) mixed with a natural sandy loam soil from the United Kingdom. These mixtures had a very high salinity so that even the control soil/sludge mixtures did not support adequate plant growth. Subsequent experiments were performed on 25% sludge, 75% biosolids mixtures (simulating 5 years of application). Relatively minor effects on plant growth were noted in both the nano and bulk treatments; however, none of the plants nodulated. The next round of experiments focused on the 50% sludge/soil mixture after leaching in outdoor lysimiters at Rothamstead Research in the United Kingdom for 6 months. These mixtures appeared to have lower salinity, perhaps more reflective of actual field exposures, which would be subject to leaching. In this experiment we noted a complete inhibition of nodulation of Medicago in the nano treatment, but not in the control and bulk treatments. These differences were explained by increased uptake of Zn from the nano amended biosolids. The results from this study were published during the reporting period (Judy, et al., 2015)

We also have completed transcriptomic analysis of the plants from the leached sewage sludge biosolids mixtures where we observed differences in nodulation between the nano and bulk metal treatments. There were 1,032 differentially expressed genes in the nano treatment shoots that were not expressed in the bulk treatment and 2261 in the roots. Many of the differentially expressed genes in the nano treatment were involved in flavonoid biosynthesis, which controls signaling of rhizobia for nodulation as well as the nodulation genes themselves. The bulk treatment had more differentially expressed genes in common with the control treatment (Figure 1). These differences in toxicity and gene expression are correlated with greater uptake of Zn from the soil sludge mixtures into plant shoots. There were no differences in metal bioaccumulation observed for Ti or Ag. In addition, phospholipid fatty acid analyses conducted at the University of Kentucky indicate that the soil microbial communities were distinct among the treatments. Overall, the transcriptomic data reinforced the conclusion that increased Zn uptake in the nano treated plants was responsible for toxicity (Chen, et al., 2015).

We participated in similar experiments conducted with the earthworm E. fetida using the same leached sewage sludge biosolids mixtures at the Center for Ecology and Hydrology (CEH) in the United Kingdom. We concluded that the toxicity of the nano biosolids was greater than the bulk biosolids supporting the above findings (Lahive, et al., in review). 

The coherence of all of these observations is beginning to suggest that the U.S. biosolids application regulations (CFR 40 part 503) may not be protective for nanomaterials. The level of protection of these regulations for nanomaterials should be investigated further. To this end, we analyzed data from a pot experiment with M. truncatula where we diluted the metal dosed biosolids/soil mixtures with control biosolid/soil mixture. The results showed that there were no adverse effects on plant health at currently expected concentrations for the three studied nanomaterials, but there were shifts in microbial community composition. The results of this study currently are being peer reviewed.

Ongoing studies of pristine and aged (fully suflidized) Ag NPs in C. elegans are complete and the first manuscript describing these results are accepted for publication Starnes, et al., (2014); Starnes, et al., (2015). The results indicated that there are particle-specific effects and that the relative importance of Ag ions as a contributor to toxicity decreases with increasing Ag concentration. The results of imaging and toxicogenomic studies suggested that toxicity of pristine and aged Ag NPs differs from each other and from Ag ions. The mechanism of fully sulfidized Ag NP toxicity is likely related to damage to the cuticle. We now have completed whole genome gene expression profiling of pristine and sulfidized Ag NPs. Little overlap between differentially expressed genes in the pristine, sulfidized and Ag ion treatments suggested distinct modes of toxicity. The importance of several of the differentially expressed genes was investigated using RNA interference and knock out strains (Starnes, et al., 2015). 

Similar exposures were conducted with sulfide aged, phosphate aged and pristine ZnO nanomaterials. While differences in toxicity were observed, with the aged materials being about 10 times less toxic than the pristine materials, we found that Zn ions were the main driver of toxicity. Interestingly the dissolution did not occur in the exposure medium but rather within the C. elegans gut and cells.

We have developed a one-dimensional mass balance diagenetic model of the sulfide- and oxygen-dependent chemical transformations of AgNPs in sediments. Results show that the relative abundance of the toxic species Ag+ is extremely low (< 0.01 wt-%), and that environmental conditions play an important role in AgNP fate. The half-life of sulfidized AgNPs can vary from 6.6 years to more than a century depending on oxygen availability in the sediments (Dale, et al., 2014)

A watershed-scale model whose backbone is a hybrid of the EPA models HSPF and WASP7 is near completion. This model simulates watershed hydrology and agricultural practices, including biosolids application to crop lands and runoff to stream during storms, and has capabilities necessary to track point- and non-point nanoparticle sources, sinks, advection, and transformations in the environment. This model was the result of a collaboration with the EPA Chesapeake Bay Program.

A WWTP model was completed for Ag, ZnO, and TiO2 using transformation data gathered and experimental distribution data. In addition, work has been completed to investigate the transformations and distribution of CeO2 as a function of coating. These papers now have been published (Money, et al., 2014; Barton, et al., 2014a, 2014b).


Journal Articles on this Report : 38 Displayed | Download in RIS Format

Other project views: All 68 publications 38 publications in selected types All 38 journal articles
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Journal Article Barton LE, Auffan M, Bertrand M, Barakat M, Santaella C, Masion A, Borschneck D, Olivi L, Roche N, Wiesner MR, Bottero J-Y. Transformation of pristine and citrate-functionalized CeO2 nanoparticles in a laboratory-scale activated sludge reactor. Environmental Science & Technology 2014;48(13):7289-7296.
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  • Journal Article Barton LE, Therezien M, Auffan M, Bottero J-Y, Wiesner MR. Theory and methodology for determining nanoparticle affinity for heteroaggregation in environmental matrices using batch measurements. Environmental Engineering Science 2014;31(7):421-427.
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  • Journal Article Barton LE, Auffan M, Durenkamp M, McGrath S, Bottero J-Y, Wiesner MR. Monte Carlo simulations of the transformation and removal of Ag, TiO2, and ZnO nanoparticles in wastewater treatment and land application of biosolids. Science of the Total Environment 2015;511:535-543.
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  • Journal Article Barton LE, Auffan M, Olivi L, Bottero J-Y, Wiesner MR. Heteroaggregation, transformation and fate of CeO2 nanoparticles in wastewater treatment. Environmental Pollution 2015;203:122-129.
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  • Journal Article Chen C, Unrine JM, Judy JD, Lewis RW, Guo J, McNear Jr. DH, Tsyusko OV. Toxicogenomic responses of the model legume Medicago truncatula to aged biosolids containing a mixture of nanomaterials (TiO2, Ag, and ZnO) from a pilot wastewater treatment plant. Environmental Science & Technology 2015;49(14):8759-8768.
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  • Journal Article Choi J, Tsyusko OV, Unrine JM, Chatterjee N, Ahn J-M, Yang X, Thornton BL, Ryde IT, Starnes D, Meyer JN. A micro-sized model for the in vivo study of nanoparticle toxicity: what has Caenorhabditis elegans taught us? Environmental Chemistry 2014;11(3):227-246.
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  • Journal Article Dale AL, Lowry GV, Casman EA. Modeling nanosilver transformations in freshwater sediments. Environmental Science & Technology 2013;47(22):12920-12928.
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  • Journal Article Dale AL, Lowry GV, Casman EA. Much ado about α: reframing the debate over appropriate fate descriptors in nanoparticle environmental risk modeling. Environmental Science: Nano 2015;2(1):27-32.
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  • Journal Article Dale AL, Lowry GV, Casman EA. Stream dynamics and chemical transformations control the environmental fate of silver and zinc oxide nanoparticles in a watershed-scale model. Environmental Science & Technology 2015;49(12):7285-7293.
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  • Journal Article Dale AL, Casman EA, Lowry GV, Lead JR, Viparelli E, Baalousha M. Modeling nanomaterial environmental fate in aquatic systems. Environmental Science & Technology 2015;49(5):2587-2593.
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  • Journal Article Eduok S, Martin B, Villa R, Nocker A, Jefferson B, Coulon F. Evaluation of engineered nanoparticle toxic effect on wastewater microorganisms: current status and challenges. Ecotoxicology and Environmental Safety 2013;95:1-9.
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  • Journal Article Handy RD, Cornelis G, Fernandes T, Tsyusko O, Decho A, Sabo-Attwood T, Metcalffe C, Steevens JA, Klaine SJ, Koelmans AA, Horne N. Ecotoxicity test methods for engineered nanomaterials: practical experiences and recommendations from the bench. Environmental Toxicology and Chemistry 2012;31(1):15-31.
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  • Journal Article Hendren CO, Badireddy AR, Casman E, Wiesner MR. Modeling nanomaterial fate in wastewater treatment: Monte Carlo simulation of silver nanoparticles (nano-Ag). Science of the Total Environment 2013;449:418-425.
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  • Journal Article Hendren CO, Lowry GV, Unrine JM, Wiesner MR. A functional assay-based strategy for nanomaterial risk forecasting. Science of the Total Environment 2015;536:1029-1037.
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  • Journal Article Judy JD, Unrine JM, Bertsch PM. Evidence for biomagnification of gold nanoparticles within a terrestrial food chain. Environmental Science & Technology 2011;45(2):776-781.
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  • Journal Article Judy JD, Unrine JM, Rao W, Wirick S, Bertsch PM. Bioavailability of gold nanomaterials to plants: importance of particle size and surface coating. Environmental Science & Technology 2012;46(15):8467-8474.
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  • Journal Article Judy JD, Unrine JM, Rao W, Bertsch PM. Bioaccumulation of gold nanomaterials by Manduca sexta through dietary uptake of surface contaminated plant tissue. Environmental Science & Technology 2012;46(22):12672-12678.
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  • Journal Article Judy JD, Tollamadugu NVKVP, Bertsch PM. Pin oak (Quercus palustris) leaf extract mediated synthesis of triangular, polyhedral and spherical gold nanoparticles. Advances in Nanoparticles 2012;1(3):79-85.
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  • Journal Article Judy JD, McNear Jr. DH, Chen C, Lewis RW, Tsyusko OV, Bertsch PM, Rao W, Stegemeier J, Lowry GV, McGrath SP, Durenkamp M, Unrine JM. Nanomaterials in biosolids inhibit nodulation, shift microbial community composition, and result in increased metal uptake relative to bulk/dissolved metals. Environmental Science & Technology 2015;49(14):8751-8758.
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  • Journal Article Levard C, Hotze EM, Colman BP, Dale AL, Truong L, Yang XY, Bone AJ, Brown Jr. GE, Tanguay RL, Di Giulio RT, Bernhardt ES, Meyer JN, Wiesner MR, Lowry GV. Sulfidation of silver nanoparticles: natural antidote to their toxicity. Environmental Science & Technology 2013;47(23):13440-13448.
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  • Journal Article Lombi E, Nowack B, Baun A, McGrath SP. Evidence for effects of manufactured nanomaterials on crops is inconclusive. Proceedings of the National Academy of Sciences of the United States of America 2012;109(49):E3336.
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  • Journal Article Lowry GV, Espinasse BP, Badireddy AR, Richardson CJ, Reinsch BC, Bryant LD, Bone AJ, Deonarine A, Chae S, Therezien M, Colman BP, Hsu-Kim H, Bernhardt ES, Matson CW, Wiesner MR. Long-term transformation and fate of manufactured Ag nanoparticles in a simulated large scale freshwater emergent wetland. Environmental Science & Technology 2012;46(13):7027-7036.
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  • Journal Article Ma R, Levard C, Michel FM, Brown Jr GE, Lowry GV. Sulfidation mechanism for zinc oxide nanoparticles and the effect of sulfidation on their solubility. Environmental Science & Technology 2013;47(6):2527-2534.
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  • Journal Article Ma R, Stegemeier J, Levard C, Dale JG, Noack CW, Yang T, Brown Jr. GE, Lowry GV. Sulfidation of copper oxide nanoparticles and properties of resulting copper sulphide. Environmental Science: Nano 2014;1(4):347-357.
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  • Journal Article Ma R, Levard C, Judy JD, Unrine JM, Durenkamp M, Martin B, Jefferson B, Lowry GV. Fate of zinc oxide and silver nanoparticles in a pilot wastewater treatment plant and in processed biosolids. Environmental Science & Technology 2014;48(1):104-112.
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  • Journal Article Money ES, Reckhow KH, Wiesner MR. The use of Bayesian networks for nanoparticle risk forecasting: model formulation and baseline evaluation. Science of the Total Environment 2012;426:436-445.
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  • Journal Article Money ES, Barton LE, Dawson J, Reckhow KH, Wiesner MR. Validation and sensitivity of the FINE Bayesian network for forecasting aquatic exposure to nano-silver. Science of The Total Environment 2014;473-474:685-691.
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  • Journal Article Neal AL, Kabengi N, Grider A, Bertsch PM. Can the soil bacterium Cupriavidus necator sense ZnO nanomaterials and aqueous Zn2+ differentially? Nanotoxicology 2012;6(4):371-380.
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  • Journal Article Rathnayake S, Unrine JM, Judy J, Miller A-F, Rao W, Bertsch PM. A multitechnique investigation of the pH dependence of phosphate induced transformations of ZnO nanoparticles. Environmental Science & Technology 2014;48(9):4757-4764.
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  • Journal Article Schultz CL, Wamucho A, Tsyusko OV, Unrine JM, Crossley A, Svendsen C, Spurgeon DJ. Multigenerational exposure to silver ions and silver nanoparticles reveals heightened sensitivity and epigenetic memory in Caenorhabditis elegans. Proceedings of the Royal Society B: Biological Sciences 2016;283(1832):20152911.
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  • Journal Article Starnes DL, Unrine JM, Starnes CP, Collin BE, Oostveen EK, Ma R, Lowry GV, Bertsch PM, Tsyusko OV. Impact of sulfidation on the bioavailability and toxicity of silver nanoparticles to Caenorhabditis elegans. Environmental Pollution 2015;196:239-246.
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  • Journal Article Starnes DL, Lichtenberg SS, Unrine JM, Starnes CP, Oostveen EK, Lowry GV, Bertsch PM, Tsyusko OV. Distinct transcriptomic responses of Caenorhabditis elegans to pristine and sulfidized silver nanoparticles. Environmental Pollution 2016;213:314-321.
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  • Journal Article Stegemeier JP, Schwab F, Colman BP, Webb SM, Newville M, Lanzirotti A, Winkler C, Wiesner MR, Lowry GV. Speciation matters: bioavailability of silver and silver sulfide nanoparticles to alfalfa (Medicago sativa). Environmental Science & Technology 2015;49(14):8451-8460.
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  • Journal Article Tsyusko OV, Unrine JM, Spurgeon D, Blalock E, Starnes D, Tseng M, Joice G, Bertsch PM. Toxicogenomic responses of the model organism Caenorhabditis elegans to gold nanoparticles. Environmental Science & Technology 2012;46(7):4115-4124.
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  • Journal Article Tsyusko OV, Hardas SS, Shoults-Wilson WA, Starnes CP, Joice G, Butterfield DA, Unrine JM. Short-term molecular-level effects of silver nanoparticle exposure on the earthworm, Eisenia fetida. Environmental Pollution 2012;171:249-255.
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  • Journal Article Unrine JM, Shoults-Wilson WA, Zhurbich O, Bertsch PM, Tsyusko OV. Trophic transfer of Au nanoparticles from soil along a simulated terrestrial food chain. Environmental Science & Technology 2012;46(17):9753-9760.
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  • Journal Article von der Kammer F, Ferguson PL, Holden PA, Masion A, Rogers KR, Klaine SJ, Koelmans AA, Horne N, Unrine JM. Analysis of engineered nanomaterials in complex matrices (environment and biota): general considerations and conceptual case studies. Environmental Toxicology and Chemistry 2012;31(1):32-49.
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  • Journal Article Whitley AR, Levard C, Oostveen E, Bertsch PM, Matocha CJ, von der Kammer F, Unrine JM. Behavior of Ag nanoparticles in soil: effects of particle surface coating, aging and sewage sludge amendment. Environmental Pollution 2013;182:141-149.
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