Anaerobic toxicity of cationic silver nanoparticles
Graphical abstract
Introduction
Nanotechnology has seen a dramatic increase in utilization in environmental, medical, chemical and pharmaceutical industries (Nel et al., 2006). Engineered nanoparticles (ENPs) possess unique characteristics, compared to their bulk counterparts, such as the large surface area to volume ratio, high chemical reactivity, unique antimicrobial/fungicidal activity, and biocompatible surface properties (Khaydarov et al., 2009). Most of these properties are directly attributed to the small particle size of nanomaterials and only manifest within a particular size regime (Maynard and Michelson, 2006). These unique properties of materials at the nanoscale raise the need to examine the behavior of these particles in diverse environmental scenarios. Fundamental research on the fate, transport and toxicity of NPs is essential within an effort to determine their impact on natural and engineered environmental systems such as groundwater, soils and sediments, wastewater treatment and municipal solid waste management systems.
In particular, silver which has been well known for its antibacterial properties for centuries has become among the most commercially used nanoparticles (Tolaymat et al., 2010). Currently silver nanoparticles are employed in many consumer products such as textiles, biomedical products, plastics, socks, food storage containers and various cleaning products (Dobias and Bernier-Latmani, 2013). These particles are synthesized using various techniques to produce particles with different chemical and physical characteristics (Iravani et al., 2014). Most of the AgNPs incorporated into consumer products are coated, surface modified and or functionalized to achieve certain properties (Reinhart et al., 2010, Nowack, 2009). Different surface functionalization, obtained by applying different capping agents, was shown to influence the toxicity, aggregation and dissolution of AgNPs (Kvitek et al., 2008, Unrine et al., 2012).
A considerable amount of silver may be released from silver nanoparticle-containing consumer products within just a few washing cycles (Benn and Westerhoff, 2008, Geranio et al., 2009). Once released, depending on the circumstances, AgNPs can end up in a variety of environmental scenarios. It is highly likely that AgNPs travel through municipal sewer lines and reach wastewater treatment plants (WWTPs) and potentially accumulate in the biosolids (Kiser et al., 2012, Shafer et al., 1998, Marambio-Jones and Hoek, 2010).
One of the primary methods of biosolids treatment utilized is anaerobic digestion which relies on active anaerobic bacterial communities to degrade the organics (Donoso-Bravo et al., 2011). Therefore, it is vital to assess the potential impacts AgNPs may have on these bacterial species under anaerobic conditions and also the possible transformations of these particles within these systems. In addition to aggregation, AgNPs may undergo surface changes that influence their behavior. For example, in a system with elevated chlorides and sulfides levels (e.g., wastewater, composter leachate and landfill leachate), the released AgNPs may transform to silver chlorides (AgCl) and silver sulfides (Ag2S) which are less toxic relative to ionic Ag and metallic AgNPs (Levard et al., 2012, Kim et al., 2010, Gitipour et al., 2013).
It is worthy to mention that the antibacterial properties of AgNPs on microorganisms under aerobic conditions have been significantly studied (Choi et al., 2008). The antibacterial mechanism of silver nanoparticles is linked to a combination of release of Ag+ by AgNPs oxidative dissolution or specific nanoparticle properties such as Trojan-horse type mechanism and generation of reactive oxygen species (ROS) leading to cell membrane damage (Marambio-Jones and Hoek, 2010, Sotiriou and Pratsinis, 2010). Comparatively, the antibacterial activity of AgNPs under anaerobic conditions has been less studied and understood. According to Kim et al., municipal wastewater treatment plants control the flows of silver between anthropogenic and environmental compartments (Kim et al., 2010). Therefore, the current study aims at investigating the effect of AgNPs on the anaerobic degradation process in simulated environmental systems. The antibacterial impacts of different AgNPs on the digestion process of anaerobic biosolids were studied at various concentrations and compared to that of Ag+. Based on the observed surface charge dependent impacts, the nanoparticles exhibiting toxicity were further investigated by performing real-time speciation analysis and taxonomical analysis.
Section snippets
Nanoparticles synthesis, purification, and characterization
Three types of AgNPs with different capping agents were utilized, citrate coated AgNPs (citrate-AgNPs), Polyvinylpyrrolidone coated AgNPs (PVP-AgNPs), and branched polyethyleneimine-coated AgNPs (BPEI-AgNPs). The nanomaterials were prepared and purified as described by El Badawy et al. (2010). The hydrodynamic diameter (HDD) and zeta potential (ζ) of the AgNPs were measured using a Zetasizer Nanoseries (Malvern Instruments). Transmission electron microscopy (TEM) was used to verify
AgNPs characterization
Silver nanoparticles with three different capping agents were characterized. The fundamental characteristics that may contribute to the toxicological behavior of these AgNPs (e.g., the (HDD) and the (ζ)) are summarized in Table S2 of SI (Silva et al., 2014). The AgNPs synthesized for this experiment were spherical and in the size range between 10 and 15 nm, well below the size at which nanoparticles exhibit unique properties (Auffan et al., 2009). The AgNPs size distributions obtained from the
Implications
At low concentrations, AgNPs seem not to drastically impact anaerobic degradation which is the result of the functional redundancy built within the microbial community and not the lack of toxicity of AgNPs. At relatively high concentrations the cationic BPEI-AgNPs demonstrate elevated toxicity as compared with PVP-AgNPs and the anionic citrate-AgNPs. Because of the lack of oxidative dissolution in anaerobic environments, the results further support previous research that suggests a different
Acknowledgements
This research was funded by the USEPA's Office of Research and Development Chemical Safety for Sustainability Program and has gone through the internal review process. Any mention of products or trade names does not constitute a recommendation for use by the USEPA. MRCAT operations are supported by the Department of Energy and the MRCAT member institutions. This research used resources of the Advanced Photon Source, a U.S. Department of Energy (DOE) Office of Science User Facility operated for
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