Particle size, surface charge and concentration dependent ecotoxicity of three organo-coated silver nanoparticles: Comparison between general linear model-predicted and observed toxicity
Graphical abstract
Introduction
Envisioned as a promising technology touted to offer greater benefits to mankind, nanotechnology has emerged as a cross-disciplinary science of the twenty first century encouraging collaboration among interdisciplinary scientists in a way never witnessed before (Pokhrel and Dubey, 2012). Progress in tuning engineered nanomaterial (ENM) functionality for desired applications has extended ENMs' fields of applications (Costanza et al., 2011), and therefore, a rapid commercialization of nano-enabled products is taking place (www.nanotechproject.org; Tolaymat et al., 2010, National Academy of Sciences, 2012). As nano-enabled products can release chemical(s) in ‘nano’ and/or ionic form into the environment (Impellitteri et al., 2009, Benn et al., 2010, Tolaymat et al., 2010), concerns over environmental contamination and subsequent hazard to the receptor organisms have often been raised (Klaine et al., 2008, Vecitis et al., 2010, Yamashita et al., 2011, Pokhrel et al., 2012, Pokhrel and Dubey, 2012, Pokhrel and Dubey, 2013a, Rahaman et al., 2012). Because aquatic systems can be regarded a major sink for environmental contaminants, systematic investigation of the potential aquatic toxicity of the most common nanomaterial types, such as silver nanoparticles (AgNP), may provide insights into if and how nanoparticles would cause toxicity should the exposure occur.
The mechanistic basis of AgNP toxicity to the biotic receptors—both prokaryotic and eukaryotic organisms—has remained less clear as has been the case for other (in)organic nanomaterials (Vecitis et al., 2010, El Badawy et al., 2011, Yamashita et al., 2011, Pokhrel et al., 2012, Barceló et al., 2013). Nonetheless, recent evidence of oxidative stress via generation of reactive oxygen species (Choi and Hu, 2008), direct physical contact leading to membrane perturbation or cell-pitting (Choi and Hu, 2008, Fabrega et al., 2009, El Badawy et al., 2011), and DNA damage (Ahamed et al., 2008) have been documented in the literature following exposure to AgNPs. Less well understood is whether nanoparticles or the associated ionic form is more toxic than the other (Xiu et al., 2012, Pokhrel and Dubey, 2013a), and whether there is any combined effects of the two forms (Pokhrel et al., 2012). Identifying factors enabling our understanding of nanoparticle toxicity has long remained challenging (Xiu et al., 2012, Pokhrel et al., 2013, Pokhrel et al., in review, Pokhrel and Dubey, 2013b). Unclear is how nanoparticle characteristics would interact with the biologic receptor characteristics at the nano-bio interface, as such interaction can potentially influence the toxicity (Vecitis et al., 2010, El Badawy et al., 2011).
Amongst the factors identified to mediate nanoparticle toxicity, primary particle size has generally remained central (Choi and Hu, 2008, Jiang et al., 2008, Park et al., 2011); however, it is beginning to be understood that particle dissolution into toxic ions, particle state of aggregation, other transformations that could potentially occur once nanoparticles enter different environments, and surface charge/coating agent could also influence the toxicity and therefore studies suggest considering them during toxicity assessment (Liu and Hurt, 2010, El Badawy et al., 2011, Lowry et al., 2012, Pokhrel et al., 2012, Pokhrel et al., in review, Tejamaya et al., 2012, Xiu et al., 2012).
Citrate, polyvinylpyrrolidone (PVP), and branched polyethyleneimine (BPEI) represent, in part, the most commonly employed coating/stabilizing agents (Tolaymat et al., 2010) as they enable effective nanoparticle dispersion (El Badawy et al., 2012); whilst citrate has been widely used as a reductant for nanoparticle synthesis (El Badawy et al., 2012, Pokhrel et al., 2012). In this study, not only that these coating materials differentially charge AgNPs surface, they also confer stability via distinctly different mechanisms, namely, electrostatic (for citrate-coated AgNPs), steric (for PVP-coated AgNPs), and electrosteric (for BPEI-coated AgNPs). Different primary particle sizes are obtained employing different methods of synthesis (El Badawy et al., 2012). We systematically evaluate AgNP toxicity using the three different types of organo-coated AgNPs: Citrate-AgNP, PVP-AgNP, and BPEI-AgNP, and characterize for hydrodynamic diameters (HDD), particle morphology (i.e., diameter and shape using transmission electron microscopy (TEM)), state of aggregation, ion release rate, solution pH, and zeta (ζ) potential including that of the biologic receptor surfaces. Our results demonstrate particle size, surface charge, and concentration dependent toxicity of the three different organo-coated AgNPs against both the prokaryotic (Escherichia coli) and eukaryotic (Daphnia magna) organisms. Using the regression method of general linear model (GLM), herein we demonstrate for the first time a significant interactive effect of primary particle size (TEM diameter) and surface charge to satisfactorily explain acute toxicity of the three different organo-coated AgNPs against both the test organisms. Notably, our GLM shows an association between a minimum set of AgNP properties and the biologic responses in E. coli and D. magna.
Section snippets
Organo-coated silver nanoparticle synthesis and characterization
This study considers three different organo-coated silver nanoparticles (AgNPs): citrate-coated AgNP (Citrate-AgNP), polyvinylpyrrolidone-coated AgNP (PVP-AgNP), and branched polyethyleneimine-coated AgNP (BPEI-AgNP), presenting different surface charge scenarios and particle sizes which enabled us to study the potential main effects of the particle size and surface charge, including their interactions, on AgNP toxicity. These AgNPs were synthesized as described previously by El Badawy et al.
Results and discussion
The physico-chemical characteristics of the TFF-purified three different organo-coated AgNP samples used in this study are summarized in Table 1. These NPs had primary particle size (TEMdia) within the 100 nm size range, with variable average TEM diameter enabling us for size-dependent toxicity to be evaluated (Table 1). Not only that the three different, yet commonly used, organo-coatings imparted stability to AgNPs by three distinct stabilization mechanisms as previously stated, they also
Acknowledgments
This study was supported in part by the East Tennessee State University (ETSU) Research Development Council Grant# 82064 and the ETSU Office of Research and Sponsored Programs Grant# 83003. The authors thank TEM Analysis Services Lab, TX for support with TEM characterization of NPs. This study has not been subjected to the US EPA internal review, and the opinions expressed are those of the authors and do not reflect that of the associated institutions. Any mention of the trade names does not
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These first co-authors contributed equally to this work.
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Current address: US Environmental Protection Agency, National Health and Environmental Effects Research Laboratory, 200 SW 35th St., Corvallis, OR 97333, United States.