Trophic Transfer, Transformation, and Impact of Engineered

Feb 5, 2014 - Engineered nanomaterials (ENMs) are released into the environment with unknown implications in the food chain. Recent findings ...
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Critical Review pubs.acs.org/est

Trophic Transfer, Transformation, and Impact of Engineered Nanomaterials in Terrestrial Environments Jorge L. Gardea-Torresdey,*,†,‡,§ Cyren M. Rico,†,§ and Jason C. White∥ †

Department of Chemistry, The University of Texas at El Paso, 500 W. University Avenue, El Paso Texas 79968, United States Environmental Science and Engineering PhD Program, The University of Texas at El Paso, 500 W. University Avenue, El Paso Texas 79968, United States § University of California Center for Environmental Implications of Nanotechnology (UC CEIN), The University of Texas at El Paso, El Paso Texas 79968, United States ∥ Department of Analytical Chemistry, The Connecticut Agricultural Experiment Station, 123 Huntington Street, New Haven, Connecticut 06504, United States ‡

ABSTRACT: Engineered nanomaterials (ENMs) are released into the environment with unknown implications in the food chain. Recent findings demonstrate that ENMs may accumulate and/or increase concentrations of the component metal or carbon nanomaterials in the fruits/grains of agricultural crops, have detrimental or beneficial effects on the agronomic traits, yield, and productivity of plants, induce modifications in the nutritional value of food crops, and transfer within trophic levels. Given this information, important questions needed to be resolved include a determination of actual or predicted concentrations of ENMs through the development of new and perhaps hybridized analytical tools, assessment of the nutritional content modifications and/or accumulation of ENMs, component metal, and cocontaminants in edible plants and their implications on human diet, nutrition, and health, assessment of the consequences of ENM-induced changes in soil health, physiological process, and yield on agricultural production and food security, and transfer of ENMs in trophic levels. Given the significant implications of ENMs exposure and the rather large knowledge gaps that exist, it will be prudent to observe judicious and targeted use of ENMs so as to minimize environmental release until a comprehensive environmental fate and effects assessment can be undertaken.



INTRODUCTION The contamination of food supply with engineered nanomaterials (ENMs) via the addition of biosolids to agricultural fields1−5 or through the application of nanoenabled agricultural1,6,7 and soil remediation8,9 technologies for crop production is not far from reality. This practice repeated overtime could result in soil accumulation of ENMs, which opens an important route of ENMs entry into the food chain. While plants are most certainly exposed to naturally produced nanomaterials (nonengineered), the apparent lack of significant nanophytotoxicity from natural nanomaterials deserves further study so as to understand ENMs toxicity in plants.8,10,11 However, the imminent contamination of agricultural soils from novel ENMs poses new concerns and challenges to crop production and possible compromising of the food chain. Therefore, understanding the consequences of plants and food crops exposure to ENMs is of utmost importance. A considerable number of publications have been reported in an effort to understand the interaction between ENMs and plants. In fact, several reviews have already examined the implications of ENMs absorption, translocation, accumulation, and biotransformation in food crops,12−15 and have found sufficient evidence that ENMs can yield both beneficial and harmful effects in plant systems at the physiological, biochemical and genetic level.13−16 A cursory evaluation of literature reveals that © 2014 American Chemical Society

in the past two years, the majority of these studies measured ENMs impacts on the photosynthetic processes, oxidative stress, antioxidative enzyme activity, radical scavenging ability, gene expression, and macromolecular (DNA, protein, carbohydrates, fatty acid, lignin) modification within edible plants. However, most of these studies were conducted at the germination phase or early growth stages and under short exposure times; thus, there is a lack of understanding of the long-term risks and benefits of ENMs to plants and plant systems.13 To date, only 30 studies on fully mature fruit/grain producing plants have been performed since an initial life cycle study in rice (Oryza sativa L.) exposed to MWCNTs17 was first reported in 2009. Therefore, important questions on the long-term effects of ENMs in plants remain unanswered. Herein we examined important data from long-term (≥4 weeks exposure) or full life cycle studies published in the last two years to comment on ENM accumulation and biotransformation in plants, on the productivity and nutritional value of food crops, and on the transfer and biomagnification within trophic levels. Despite nearly 200 publications reported on Received: Revised: Accepted: Published: 2526

November 21, 2013 January 28, 2014 February 5, 2014 February 5, 2014 dx.doi.org/10.1021/es4050665 | Environ. Sci. Technol. 2014, 48, 2526−2540

Environmental Science & Technology

Critical Review

A third exposure pathway for plants exposure to ENMs is through the application of soil remediation nanotechnologies.7,8 For example, nanozero-valent iron (nZVI) was effective for soil remediation of organic and inorganic pollutants such as chlorinated hydrocarbons and organochlorine pesticides,34,35 whereas nFe2O3 improved soil remediation of persulfate and arsenic.36,37 Similarly, hydroxyapatite ENMs were used for soil remediation and removal of heavy metals (Cu2+, Zn2+, Pb2+, Cd2+) in wastewater.38,39 The interactions of these nanotechnologies with plant and crop species are unknown but will likely be highly site and product specific. Additional routes of ENMs exposure to plants may include atmospheric deposition, spillage, discharge, surface runoff, and wastewater reuse for food production.3,23,24 Exposure Condition. Exposure condition is an important issue in ENMs-plant interaction studies, and factors that influence the behavior and toxicity of ENMs in soil have been examined in other reviews.3,7−9,24 Table 1 summarizes the mode, time, and length of exposure and control treatment used in the experimental procedure of long-term studies analyzed in this review. The bulk of this review analyzed long-term studies performed in soil and hydroponics since they provide better understanding of how ENMs could impact the whole life cycle of plants under realistic cultivation scenarios. As seen in Table 1, 17 studies exposed the plants to ENMs in soil and six from foliar treatments, while four others exposed plants through hydroponic and three studies treated the plants/ seeds for a short period of time prior to soil cultivation. ENMs exposure via roots either through soil or hydroponic culture usually starts from sowing or transplanting a few days after germination until harvest stage, whereas exposure via leaves was done by spraying several times during the course of plant growth. The use of appropriate dissolved component metal ions as control treatments is also needed to distinguish the effects of ENMs from those of released ions. This is especially true for nZnO, which readily undergoes dissolution in various media.26,40 Unfortunately, only seven studies specifically addressed/included appropriate dissolved component metal ions as control treatments, which raises serious concerns over whether the observed results were due to ENMs or the dissolved metal ions. Exposure concentration is a common issue of concern raised in ENMs-plant interaction studies, and a separate critical review of the literature with a focus on this issue is indeed needed. However, the current review only examines available reports on the long-term impacts of ENMs on plants. Biotransformation and Speciation of ENMs. Knowledge on the speciation and biotransformation of ENMs in soil and plant tissues is critical to understanding the physiological, biochemical, molecular and genetic modifications in exposed plants.41 This knowledge may also be important to understanding the potential risk of ENM trophic transfer, since the implications of ENMs for human health via this exposure pathway are still largely unknown. Table 1 represents a comprehensive assessment of the current literature focused on ENM biotransformation in plants during long-term (full life cycle up to grain/fruit production) exposure. Figure 1 also illustrates the speciation of these ENMs in soil, as well as the proposed pathways of ENM biotransformation in plants. A review of select studies on metal-based (nCeO2, nTiO2, nZnO, nCuO, nYb2O3, nAg, and nAu) and carbon-based (MWCNTs and C60/fullerol) ENMs follows below. Speciation in Soil. The speciation and dissolution of ENMs in soil have been assessed in several reviews.2,8,24,41 Cornelis et al.42 was among the first to examine the solubility of nCeO2

ENM-plant interaction in the last two years, we found that long-term studies were limited to nCeO2, nTiO2, nZnO, nCuO, nAg, nAu, MWCNTs, and C60/fullerol ENMs with a few shortterm studies (≤15 days exposure) on the biotransformation and speciation of nCeO2, nTiO2, nZnO, nCuO, nAg, and nYbO3 in plants. We also use this venue to highlight major knowledge gaps in the existing literature and to offer suggestions for eliminating these shortcomings so as to enable appropriate and accurate risk assessment of ENMs in the food chain. Exposure Pathways of Plants to ENMs. The most likely pathway for ENMs exposure to plants is through the application of biosolids to agricultural lands.1−3,18,19 Biosolids are rich in organic matter and nutrients such as N and P; as such, they are used as cheaper alternatives to synthetic fertilizers for improving the soil fertility of agricultural soils.1,20 In the U.S., more than 60% of biosolids produced each year are applied to agricultural lands,21 which amounts to approximately 3.36 million tons of material applied to more than 70 million acres of agricultural fields.5 These biosolids are known to contain ENMs; a review by Gottschalk et al.22 estimated the amount of ENMs in biosolids to be in the range of 10−6−104 ppm depending on types of ENMS, whereas Keller et al.23 found that biosolids from San Francisco Bay wastewater treatment plant could contain ENMs anywhere between 0.01 and 1000 ppm. A recent estimate showed that of the ENMs that enter wastewater treatment plants, 44−47% ENMs may end up in soils via biosolids.23 While current estimates of predicted environmental concentrations are much smaller than the predicted no effects concentrations in toxicity estimates,24 the regular application of biosolids would likely result in the accumulation of ENMs in agricultural fields.1,24 A second pathway of exposure involves nanoenabled agricultural products including pesticides, fertilizers, plant protectives, soil additives, and growth regulators; all offer promising approaches for improving crop protection and production at reduced cost.1,6,7 Nanofertilizers can be used to deliver nutrients in plants by directly applying the nanoformulation onto or into the plant or by coating slow release fertilizers with ENMs.25 For example, nZnO could be used as substitute to bulk ZnO to improve the efficacy of Zn fertilizers.26 Slow release fertilizers coated with chitosan nanoparticles, carbon nanotubes, or nanoporous materials have also been used in agriculture.25,27 DeRosa28 has documented dozens of patents incorporating ENMs in novel nanoenabled fertilizers while Gruere et al.29 reported that by 2015, developing countries would start commercialization of nanoenabled fertilizers. Nanoenabled agriculture is particularly attractive to developing countries because of its potential to enhance soil fertility, achieve yield targets,30,31 as well as for benefits in combatting hunger, malnutrition, and child mortality.32 Although still in its infancy, the industry is growing so fast that the number of scientific publications and patents increased exponentially since the start of the millennium.6 As such, it is highly possible that edible plants could be exposed to high levels of ENMs from direct purposeful application of nanoenabled agricultural inputs, and that accumulation of ENMs in soil through time could occur from the repeated inputs. One group predicted that the beneficial impacts of ENMs application in agriculture may exceed those of farm mechanization and the green revolution;33 however, it is clear that the extent of ENM environmental implications are not yet fully understood. As such, nanophytotoxicity studies of ENMs or nanoenabled agricultural inputs specifically developed for agricultural production are needed. 2527

dx.doi.org/10.1021/es4050665 | Environ. Sci. Technol. 2014, 48, 2526−2540

Ag

NP

2528

1, 10, 100

38.6

100, 1000

10−12

0.14

20, 40, 60

25

21

500, 1000, 1500, 2000, 2500, 3000

leaves

root

root

leaves

leaves

fertilized compost soil

surface mineral soil, biosolid

tomato hydroponic grown in (Lycopersiculture suspension con from 6week old to esculentum) maturity

speciation

•reduced chlorophyll content •enhanced superoxide dismutase activity •total antioxidant capacity was not affected •only Microstegium vimineum was affected with 32% less biomass relative to biosolid treatment •plants had more roots at the top 1 cm of the soil

•improved growth indices (except fruit pH) at increased concentration of the treatment •highest chlorophyll content at AgNO3 (100 ppm) •nAg did not affect the chlorophyll content •inhibited ethylene action

physiological/ biochemical effects nutritional content

amount in the edible portion

•no significant •AgNO3 difference in (100 polyphenol and ppm) tannin contents obtained between the treatments highest seed yield •16−45% increase in seed yield in nAg treatment compared to control •35−60% decrease in fruit yield

ref

5

83

78

77

73 •hundred-folds higher Ag content in treated compared to the controls