Bioaccumulation of nanoparticle CuO within a terrestrial food chain increases by weathering in soil

04-07-2017

Engineered nanoparticles are additives in commercial products that we consume, apply to our skins, and disperse in agriculture as fertiliser and pesticides. This study examines the bioaccumulation in lettuce and possible trophic transfer to crickets, using µ-XRF and µ-XANES to map the distribution and Cu speciation for lettuce exposed to weathered and unweathered CuO nanoparticles.

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Engineered nanoparticles have been of great interest in the agricultural sector, with the most common applications being nanofertiliser and nanopesticide products for improved crop productivity [1]. However, the fate of these materials in the environment remains poorly understood.  Nanoparticles released to soil may aggregate significantly, thereby changing their size, shape and surface chemistry over time. The aging and transformation of  nanoparticles in soil during weathering processes could increase or decrease particle mobility and bioavailability within terrestrial food chains. In the present study, the impact of these transformations during CuO weathering was evaluated by means of micro X-ray fluorescence (µ-XRF) and micro X-ray absorption near-edge structure (µ-XANES) spectroscopy at beamline ID21.  Lettuce roots were exposed to weathered and unweathered CuO nanoparticles at 400 mg/kg for 70 days, following which 30 µm cross sections were analysed. Additionally, crickets fed for 15 days with lettuce exposed to weathered CuO nanoparticles were depurated for 5 days and then analysed by µ-XRF.

The µ-XRF analysis results demonstrate that Cu was localised primarily in the main and secondary roots (Figures 1a and 2a) of the exposed lettuce plants, regardless of weathering conditions. However, the distribution of Ca (green colour, Figure 1a) was altered due to weathering in soil, showing greater distribution within the main root in the weathered treatment when compared to the unweathered treatment (Figure 2a). Additionally, a more localised and heterogeneous Cu distribution was observed in the unweathered treatment (Figure 2b) as compared to the weathered exposure, where the element was homogenously distributed within root tissue (Figure 1b).

Images of lettuce root cross section exposed to weathered CuO nanoparticles at 400 mg/kg for 70 days

Figure 1. Images of lettuce root cross section exposed to weathered CuO nanoparticles at 400 mg/kg for 70 days. a) Tricolour micro-XRF maps of root cross sections, red colour stands for Cu, blue for K, and green for Ca. The µ-XRF map was acquired at 9.2 keV, 100 ms dwell time, 3–0.8 µm2 pixel size. b) Cu temperature map, colour scale units are raw intensity; areas where µ-XANES was acquired from ASR: aggregate sec. root; SR: secondary root; E: epidermis; MR: main root and C: cortex are indicated. c–e) Cu temperature map of main and secondary roots, colour scale units are raw intensity. f–h) µ-XRF maps from main and secondary roots.

µ-XANES analysis of roots from weathered nanoparticles exposure demonstrated a significant Cu (II) reduction to Cu (I) compounds, including sulfidation, in all selected root areas (main, secondary, epidermis and cortex). For example, aggregates from the secondary root in weathered treatments were mostly present as Cu2O (94.2%) and Cu2S (5.7%). Additionally, Cu localised in the epidermis was reduced and present as Cu2O (45.9%) and Cu2S (43.5%). Conversely, roots from unweathered nanoparticles treatments contained Cu mostly as the original CuO in multiple tissues; for example, in the secondary and main roots, CuO was present largely as CuO. As such, µ-XANES analysis of the Cu K edge suggest that the reduction of CuO to Cu (I) complexes occurred in the soil during the weathering processes. Importantly, this reductive transformation of weathered nanoparticles correlated well with increased Cu in lettuce root tissues as measured by ICP-MS.

Images of lettuce root cross section exposed to unweathered CuO nanoparticles at 400 mg/kg for 70 days

Figure 2. Images of lettuce root cross section exposed to unweathered CuO nanoparticles at 400 mg/kg for 70 days. a) Tricolour micro-XRF maps of root cross sections, red colour stands for Cu, blue for K, and green for Ca. The µ-XRF map was acquired at 9.2 keV, 100 ms dwell time, 3–0.8 µm2 pixel size. b) Cu temperature map, colour scale units are raw intensity. c, d) µ-XRF maps from main and secondary roots e, f) Cu temperature map of main and secondary roots from (c, d) µ-XRF maps, colour scale units are raw intensity. Areas where µ-XANES was acquired from ASR: aggregate secondary root; SR: secondary root; EMR: epidermis main root and AMR: aggregate main root are indicated.

µ-XRF analysis from the trophic transfer study was used to localise Cu in the abdominal region of primary consumer (cricket; A. domestica) after feeding for 15 days with lettuce exposed to weathered CuO nanoparticle treatments (data not shown). µ-XRF results showed the homogenous distribution of P and S within the cricket’s digestive system, but Cu was not associated with the cricket’s digestive system, suggesting either absorption or elimination during the 5-day depuration period. Importantly, this study demonstrated the impact of transformation processes in soil that may result in an increased availability of chemically-altered nanoparticles within terrestrial food chains. Moreover, µ-XRF analysis also demonstrated altered Ca and Cu distribution within lettuce upon weathering processes, suggesting a potential influence on the overall nutritional quality of crop plants.

 

Principal publication and authors
Weathering in soil increases nanoparticle CuO bioaccumulation within a terrestrial food chain, A.D. Servin (a), L. Pagano (a,b,c), H. Castillo-Michel (d), R. De la Torre-Roche (a), J. Hawthorne (a), J.A. Hernandez-Viezcas (a), R. Loredo-Portales (f,g), S. Majumdar (a), J. Gardea-Torresdey (e,h), O. Parkash Dhankher (b), J.C. White (a), Nanotoxicology 11, 98-111 (2017); doi: 10.1080/17435390.2016.1277274.
(a) Department of Analytical Chemistry, Connecticut Agricultural Experiment Station, New Haven (USA)
(b) Stockbridge School of Agriculture, University of Massachusetts, Amherst (USA)
(c) Department of Life Sciences, University of Parma (Italy)
(d) ESRF
(e) Chemistry Department, University of Texas at El Paso (USA)
(f) Universidad de Guanajuato Noria Alta (Mexico)
(g) Elettra Sincrotorone Trieste, Basovizza (Italy)
(h) University of California Center for Environmental Implications of Nanotechnology (UC CEIN), El Paso (USA)

 

References
[1] A.D. Servin and J.C. White, NanoImpact 1, 9 (2016).