Lead Et Al 2012 Transformations of Nanomaterials in The Environment
Lead Et Al 2012 Transformations of Nanomaterials in The Environment
pubs.acs.org/est
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posed by these materials. transport, and toxic properties. For example, metallic silver NPs
will oxidize and may become sulfidized in the environment.9
INTRODUCTION Sulfidation of the particles changes their aggregation state,
The nanotechnology field continues to grow rapidly and surface chemistry, and charge, as well as their ability to release
the increasing use of engineered nanomaterials (NMs) in toxic Ag+ ions10 and therefore their persistence and toxicity.
commercial products translates into an increasing presence in Similarly, the interaction between NMs and humic substances
the biosphere. Engineered NMs are manufactured materials (HS) including natural organic matter (NOM) results in a
having at least one dimension in the nanoscale (ca. 1−100 nm) nanoscale coating of the NMs,11 analogous to protein coronas
dimension. Naturally occurring NMs are also ubiquitous in the in mammalian systems,12 that dramatically changes their aggregation,
environment, resulting from both natural processes and from deposition, and toxic properties.13,14
anthropogenic impacts (e.g., flocculation of nanometer-scale Because environmental systems are dynamic and stochastic,
metal oxides in acid mine drainage). The extremely small sizes the physicochemical changes that accompany engineered and
of both naturally occurring and engineered NMs results in a incidental coatings, as well as subsequent reactions in the
high percentage of surface atoms which can result in novel environment, greatly complicate the understanding of risks
properties and reactivity compared to a larger size material with associated with the release of NMs in the environment. We
the same chemical composition.1,2 Examples of such engineered currently lack sufficient knowledge of the types, rates, and
NMs include semiconductors like quantum dots which have extent of transformations expected for NMs in environmental
different optical and electrical properties depending on their and biological systems. By extension, we also fail to understand
size,3 and gold nanoparticles (NPs) that are typically inert but
become catalytic as their size is decreased to a few nanometers.4
Special Issue: Transformations of Nanoparticles in the Environment
NMs are becoming increasingly complex and include those
5
with coatings that target specific cells in the body or that Published: May 14, 2012
© 2012 American Chemical Society 6893 dx.doi.org/10.1021/es300839e | Environ. Sci. Technol. 2012, 46, 6893−6899
Environmental Science & Technology Feature
the impact of those transformations on the fate, transport, and Nanomaterials are commonly produced with an organic
toxicity of NMs. To correctly forecast the environmental and capping agent or stabilizer, often a small anion or polymer
human health risks associated with these materials, we must (Table 1). Transformations of the material can therefore affect
endeavor to broaden our knowledge of the transformations the core material, the capping agent, or both. For example,
of NMs. the simple coordination of ZnS nanoparticles (NPs) with water
The U.S. National Research Council has recently proposed a molecules can alter their crystalline phase and properties.19 The
new framework for nano EHS research.8 This committee recom- capping agent may be bioavailable and removed by bacteria.20
mended that research should focus on understanding “critical Indeed, the rate, extent, and type of transformations possible
elements of nanomaterial interactions”, needed for assessing expo- will depend on the properties of the initial NM, its coating, and
sure, hazards, and hence risks posed by engineered nanomaterials its surrounding chemical and biological environment. Impor-
(Figure 1). These critical elements include physical, chemical, and tantly, many transformations are slow or effectively irreversible
and cannot necessarily be predicted using thermodynamics.
Here, we briefly review what is known about chemical, physical,
and biologically mediated transformations of NMs in natural
systems and their effects on the resulting NM behavior. We
also discuss state-of-the-science knowledge and instrumentation
gaps preventing us from quantifying and predicting these
transformations in biological and environmental media.
Figure 2. (a) Representative chemical transformations of metal nanomaterials and the potential impacts on their behavior and effects in the
environment. AgNPs are used to exemplify the types of transformations that may occur. The magnitude of arrows approximately correlates with
potential for these processes to occur as determined from the limited data available on these processes. (b) Effects of physical transformations
including aggregation and heteroaggregation on the reactivity and transport of nanomaterials. The magnitude of arrows approximately correlates
with potential for these processes to occur as determined from the limited data available on these processes. (c) Biologically mediated
transformations of nanomaterials and their coatings, and the subsequent impact on fate, transport, and effects. Arrows do not indicate the relative
potential for these processes to occur due to the limited data currently available for that assessment. (d) Effects of nanomaterial interactions with
macromolecules such as proteins and natural organic matter. Adsorbed macromolecules can affect aggregation, nanoparticle-biointeractions,
biouptake, and fate, transport, and effects in the environment. Arrows do not indicate the relative potential for these processes to occur due to the
limited data currently available for that assessment.
processes affecting NM coatings, oxidation state, generation of highly reactive with sulfur-containing biomacromolecules and
reactive oxygen species (ROS), and persistence. The oxidation inorganic sulfur in sediments, soils, and air. Formation of a
and mineralization of fullerenes dispersed in water by natural relatively insoluble metal-sulfide shell on the particle surface
sunlight may attenuate carbon-based nanomaterials.26 Sunlight can alter the surface charge and induce aggregation.10 Deter-
exposure caused the degradation of gum arabic coatings on Ag mining the particle properties (e.g., particle size, capping agent,
NPs and induced aggregation and sedimentation from solution.27 etc.) and environmental conditions (redox state and availability
Many NMs will be innately photoactive (e.g., TiO2 and CNTs), of free sulfide) that affect their dissolution and/or sulfidation
potentially producing ROS when exposed to sunlight.28 Others rates are important for assessing their potential to release toxic
may be oxidized or reduced by sunlight, changing their redox metal cations, and their ultimate toxicity29 and persistence in
state, charge, and therefore potential for toxicity. the environment.30
Dissolution and sulfidation are important processes affecting Adsorption of macromolecules or organic and inorganic
NP surface properties, toxicity, and persistence. This is especi- ligands on NM surfaces can significantly affect their surface
ally true for NMs made from Class B soft metal cations (e.g., chemistry and resulting behavior in biological and environ-
Ag, Zn, and Cu) because they form partially soluble metal- mental systems. For example, adsorption of polymer coatings
oxides, and because they have a strong affinity for inorganic and on NPs generally decreases their attachment to silica surfaces,
organic sulfide ligands. Class B metal NMs commonly express suggesting greater mobility in the environment and potentially
toxicity through dissolution and release of toxic cations, such less effective removal in drinking water treatment.31 Adsorption
that persistence is reduced but toxicity is increased. Complete of biomacromolecules is a particularly important transformation
dissolution may allow prediction of their impact using existing and is treated separately below. Adsorption of organic ligands
models for metal speciation and effects. However, Class B or metal cations or oxo-anions can occur on either the surface
metals’ affinities for electron-dense sulfur molecules make them of the core NM or within the organic macromolecular coating
6895 dx.doi.org/10.1021/es300839e | Environ. Sci. Technol. 2012, 46, 6893−6899
Environmental Science & Technology Feature
of the particle. Organic ligands, such as those containing thiol Biologically mediated transformations of both the underlying
groups may affect NM dissolution, charge, and stability against NM core and the coatings are possible, and these trans-
aggregation.32,33 Organics present in the atmosphere can also formations can affect the behavior of the NMs including surface
condense onto airborne NMs, altering their surface chemistry.34 charge, aggregation state, and reactivity, which ultimately can
Understanding the effects of organic ligands and adsorbed affect transport, bioavailability, and toxicity. The oxidation and
cocontaminants on NM toxicity is needed to fully assess the carboxylation of CNTs by OH radicals produced from the
potential for harm. horseradish peroxidase enzyme has been demonstrated.40 This
Physical Transformations (Figure 2b). Aggregation of oxidation increases the surface charge of the CNTs and stability
NPs reduces the surface area to volume effects on NM against aggregation while decreasing hydrophobicity. Moreover,
reactivity. This increase in aggregate size in turn affects their this biological oxidation and surface functionalization may affect
transport in porous media, sedimentation, reactivity, uptake by the toxic potential of CNTs.41
organisms, and toxicity. Over time, aggregation of NPs into Biotransformation of polymer coatings used on many NMs
clusters is inevitable without engineered or incidental coatings for biomedical applications is also feasible. Covalently bound
to decrease aggregation. Aggregation may take on two forms: poly(ethylene glycol) (PEG) coatings on engineered NMs, for
homoaggregation between the same NMs, or heteroaggregation instance, were shown to be bioavailable to microorganisms
between a NM and another particle in the environment. In isolated from an urban stream.20 Moreover, the biotransforma-
most cases, the greater concentration of environmental particles tion of the PEG coating caused the NMs to aggregate.
compared to NMs will result in heteroaggregation. Where Biological transformations of NMs, especially carbon-based
aggregation occurs, the number concentration of NMs in the ones, and their organic coatings may ultimately act to attenuate
suspension decreases, with a concomitant increase in their their concentrations in the environment or to affect transport,
effective (aggregate) size. For example, 30−70 nm diameter but it remains to be seen if these processes occur at rates that
Fe(0) NPs rapidly aggregate in water to form micrometer- are high enough to be important. Perhaps the most critical
sized aggregates,35 greatly decreasing their mobility in the sub- biotransformation of NMs is adsorption of biomacromolecules
surface and likely pathways of exposure to sensitive receptors. on their surfaces as discussed next.
Heteroaggregation between NMs and comparatively larger Macromolecule NM Interactions (Figure 2d). There
particles (e.g., clay) could change NM behavior if the NM−clay are an endless number of biomacromolecules in living cells
heteroaggregates ultimately move more like a clay particle that (e.g., proteins) and in the environment (e.g., NOM, poly-
the NM.36 saccharides). Adsorption of these macromolecules can occur in
Aggregation can also decrease the “available” surface area of
all environments. On uptake by biological organisms, NMs may
the materials, thereby decreasing reactivity. However, the
be transformed through their interaction with biomacromolecules
decrease in specific surface area will depend on particle number,
which can coat and thereby transform their outer surfaces.42
size distribution, and the fractal dimensions of the aggregate.37
Adsorbed protein coatings, also known as protein coronas, form
Aggregation can therefore decrease toxicity when the toxic
in biological fluids for several classes of NMs.12,43,44 The
response is a result of a surface area-mediated reaction such as
coronas result from the adsorption of a wide range of proteins
ROS generation or dissolution. Aggregation may also serve to
increase the persistence of the NM if aggregation decreases the and are dynamic in nature, with the proteins capable of exchang-
rate of dissolution or degradation, albeit in a different location ing between free and bound forms. However, many proteins and
compared to the dispersed NPs. The size of a NP may also other macromolecules are effectively irreversibly adsorbed over
affect its bioavailability to organisms. When aggregates or relevant time scales,45,46 and therefore in part determine the
heteroaggregates become too large for direct transport across “identity” of the NM (e.g., size, electrophoretic mobility, and
the cell wall and/or membrane, uptake may be prevented. surface composition) and subsequent environmental behavior
Phagocytosis and similar mechanisms may also be affected. and biological response. The adsorbed proteins may also offer a
Conversely, heteroaggregation with soft biogenic particles way of entry for NMs into cells through the process of receptor-
might increase NM bioavailability (e.g., uptake by filter feeders mediated endocytosis.44 The presence of biomacromolecules can
who preferentially remove larger particles). Delineating the affect their dissolution rate, ROS production, and may determine
effects of aggregation on uptake and any subsequent toxicity the fate of the material in the organism (e.g., excretion vs accu-
will be challenging since it is a dynamic process, uptake will be mulation in specific organs). Therefore, the types of biomacro-
highly dependent on both the species examined and its aqueous molecules present on the surface can affect important processes
chemical environment and metabolic state, and because such as bioaccumulation and toxicity.
instruments for tracking NMs in situ or in vivo are lacking. Once discharged into the environment, uncoated or coated
Biologically Mediated Transformations (Figure 2c). NMs will be subjected to alterations through interactions with
Biological transformations of NMs are inevitable in living naturally occurring biomacromolecules or geomacromolecules
tissues (both intracellular and extracellular) and environmental including proteins, polysaccharides, and humic substances
media (e.g., soils). Redox reactions are fundamental to growth (HS). NOM concentrations are typically orders of magnitude
in all biological systems. These reactions take place in the higher in concentration than manufactured NMs and so are
cytoplasm, cell wall, cell membrane, and extracellularly via likely to substantially modify the properties and behaviors of
redox-labile enzymes and cytochromes or through ancillary the manufactured NMs. The observed interactions are
intracellular ROS production such as hydroxyl radicals or H2O2. analogous to the interactions with proteins and the formation
The redox reactions between bacteria and naturally occurring, of “protein coronas” in biological systems, which have been the
nanoscale iron oxide are well understood.38 Moreover, bacteria subject of more intensive research reaching similar conclusions;
such as Geobacter and Shewanella spp. were recently the behavior and impacts of NMs depends highly on the types
demonstrated to produce nanoscale silver particles by reduction and amounts of these biological and environmental compo-
of Ag+ from solution.39 nents attached to their surfaces.
6896 dx.doi.org/10.1021/es300839e | Environ. Sci. Technol. 2012, 46, 6893−6899
Environmental Science & Technology Feature
Most work to date on NM−NOM interactions has been because the arrangement on the surface to reach the final
performed using extracted humic substances (HS), which will conformation is slow. Third, NMs will likely undergo multiple
displace weakly bound synthetic capping agents on the particle transformations simultaneously (e.g., interaction with NOM
surface to form nanoscale coatings which can be either coherent and oxidation or reduction), or successive irreversible transfor-
(i.e., fully coating the NM surface) or noncoherent. They mations (e.g., irreversible adsorption of different proteins upon
can form relatively “flat” monolayers or more extended (thick) successive exposures to plasma and intercellular materials).53
monolayers or multilayers. The coherence and thickness Therefore, answering the question of how a specific NM will
depend on the particle properties and the conditions (e.g., behave in the environment requires information about the
pH and ionic strength) during interaction. NOM provides both environment properties and the history of the NM over time
charge and steric stabilization of NMs,11,47 although they may scales of interest. We will have to address this using a well-
also result in bridging flocculation,24 so their effects are com- planned (and likely multidimensional) matrix of representative
plex and can be difficult to predict. In addition, deagglomera- materials and media, as opposed to a case by case basis, because
tion may occur in the presence of NOM.48 For larger MW the large number of permutations of NMs and environmental
polymeric coatings that are strongly bound mixed polymer− systems makes the latter impossible in practice. Simplification
NOM layers may form on NMs, however, in some cases may be possible by measuring transformations in specific
interactions with NOM may be minimal.49,50 The conditions representative environments, i.e. environmental and biological
under which mixed layers form and the influence of those layers matrices, at both short times and long times to capture the end
on NM behavior has yet to be explored. member behaviors expected.
NOM coatings on NMs will affect the attachment to surfaces, There are many instruments available to measure the pro-
and therefore both homoaggregation and heteroaggregation perties of NMs such as chemical composition, size, and charge.
described previously. However, determining the interaction However, most of these techniques are generally not capable
between NMs and every type of environmental surface (various of measuring these properties in situ and in vivo or in
clay surfaces, iron oxides, quartz, etc.) is not feasible. The environmentally relevant concentrations and conditions.
problem may be simplified, however, if the NOM coatings on Equally importantly, methods are needed to better track the
the NM (and on the environmental surfaces) are relatively rate and extent of transformations of NMs under realistic
coherent. Then all surfaces would be expected to behave conditions, especially for those where multiple transformations
similarly and complex heteroaggregation phenomena may be occur. Method validation and development are required to take
treated as simpler homoaggregation processes, at least to a first this forward and greater collaboration between metrological
approximation. The influence of the underlying NM properties and analytical researchers with environmental scientists and
and the NOM−NM interactions on the resulting forces affect- environmental chemists is needed. In some cases, trans-
ing attachment must be determined to test this hypothesis. formations of NMs will occur over time scales of months or
In addition to changes in aggregation and disaggregation, years. Understanding these transformations completely will
interaction with NOM has been shown to reduce short-term require an ability to recover the NMs from environmental and
bacterial toxicity for fullerenes,14 Ag(0),13 and Fe(0),51 while biological matrices and measure the properties of these partially
increasing bioaccumulation in biofilms. 17 In all cases, transformed NMs, or to measure them in vivo/in situ. A
presumably the NOM had the effect of “masking” the NP recent NRC report provides more specific suggestions for tools
effect, either by directly coating the surface or by minimizing and instrumentation that are needed to advance nano EHS
dissolution. NOM have also been known to alter surface research.8
chemistry, for instance altering ceria NM oxidation state.24
Changing the redox state of the NM can affect its toxicity and
mechanisms of action as described above.
■ IMPLICATIONS OF NM TRANSFORMATIONS ON
NANO EHS RESEARCH
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difficult. However, it is also possible that transformations may Reinsch, B. C.; Bryant, L. D.; Bone, A.; Deonarine, A.; Chae, S.;
decrease heterogeneity if ubiquitous transformations (e.g., Therezien, M.; Colman, B. P.; Hsu-Kim, H.; Bernhardt, E.; Matson, C.
coating with humic acids, NOM, or proteins, or sulfidation) W.; Wiesner, M. W. Long-term transformation and fate of
lead to NMs with behaviors that are less influenced by the NM manufactured Ag nanoparticles in a simulated large scale freshwater
core than by the coating. Transformations and the properties of emergent wetland. Environ. Sci. Technol. 2012, No. 10.1021/
the transformed NM will ultimately depend on the environ- es204608d.
ment that they enter, and on the order of the environments in (10) Levard, C.; Reinsch, B. C.; Michel, F. M.; Oumahi, C.; Lowry,
which they are exposed. This fact, and the uncertainty regarding G. V.; Brown, G. E. Sulfidation processes of PVP-coated silver
use and release scenarios, makes the determination of risk nanoparticles in aqueous solution: Impact on dissolution rate. Environ.
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challenging.
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(11) Diegoli, S.; Manciulea, A. L.; Begum, S.; Jones, I. P.; Lead, J. R.;
Preece, J. A. Interaction between manufactured gold nanoparticles and
AUTHOR INFORMATION naturally occurring organic macromolecules. Sci. Total Environ. 2008,
Corresponding Author 402, 51−61.
*E-mail: [email protected]. (12) Cedervall, T.; Lynch, I.; Lindman, S.; Berggard, T.; Thulin, E.;
Nilsson, H.; Dawson, K. A.; Linse, S. Understanding the nanoparticle-
Notes protein corona using methods to quantify exchange rates and affinities
The authors declare no competing financial interest. of proteins for nanoparticles. Proc. Natl. Acad. Sci. U.S.A. 2007, 104,
2050−2055.
Biography (13) Fabrega, J.; Fawcett, S. R.; Renshaw, J. C.; Lead, J. R. Silver
nanoparticle impact on bacterial growth: Effect of pH, concentration,
Greg Lowry is a Professor of Environmental Engineering at Carnegie
and organic matter. Environ. Sci. Technol. 2009, 43, 7285−7290.
Mellon University in Pittsburgh, PA and Deputy Director of the Center
(14) Li, D.; Lyon, D. Y.; Li, Q.; Alvarez, P. J. J. Effect of soil sorption
for Environmental Implications of Nanotechnology (CEINT). Kelvin and aquatic natural organic matter on the antibacterial activity of a
Gregory is an Associate Professor of Environmental Engineering at fullerene water suspension. Environ. Toxicol. Chem. 2008, 27, 1888−
Carnegie Mellon University. Simon Apte leads the Contaminant 1894.
Chemistry and Ecotoxicology Program at CSIRO Land and Water, (15) Mahendra, S.; Zhu, H. G.; Colvin, V. L.; Alvarez, P. J. Quantum
Sydney Australia. Jamie Lead is Professor of Environmental Nanoscience dot weathering results in microbial toxicity. Environ. Sci. Technol. 2008,
at the University of Birmingham, UK, and Professor of Environmental 42, 9424−9430.
Nanoscience and Risk at the University of South Carolina, USA. (16) Tong, Z. H.; Bischoff, M.; Nies, L.; Applegate, B.; Turco, R. F.
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Impact of fullerene (c-60) on a soil microbial community. Environ. Sci.
Technol. 2007, 41, 2985−2991.
ACKNOWLEDGMENTS (17) Fabrega, J.; Renshaw, J. C.; Lead, J. R. Interactions of silver
G.V.L. and K.B.G. were supported by the Center for nanoparticles with Pseudomonas putida biofilms. Environ. Sci. Technol.
Environmental Implications of Nanotechnology (funded by 2009, 43, 9004−9009.
the National Science Foundation and the U.S. Environmental (18) Bian, S. W.; Mudunkotuwa, I. A.; Rupasinghe, T.; Grassian, V.
Protection Agency under grant EF-0830093. J.R.L. acknowl- H. Aggregation and dissolution of 4 nm ZnO nanoparticles in aqueous
edges financial support from the Natural Environment Research environments: Influence of ph, ionic strength, size, and adsorption of
humic acid. Langmuir 2011, 27, 6059−6068.
Council (NERC FENAC and NE/H013148/1).
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(19) Zhang, H. Z.; Gilbert, B.; Huang, F.; Banfield, J. F. Water-driven
structure transformation in nanoparticles at room temperature. Nature
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