Silver nanoparticles in soil–plant systems

1 downloads 0 Views 608KB Size Report
Jul 22, 2013 - nanowires, nanoplates, or nanobelts (Sun et al. 2003;. Pal et al. ... medical products, such as surgical gowns and dressing bandages (Boxall et ...
J Nanopart Res (2013) 15:1896 DOI 10.1007/s11051-013-1896-7

REVIEW

Silver nanoparticles in soil–plant systems Naser A. Anjum • Sarvajeet S. Gill • Armando C. Duarte • Eduarda Pereira Iqbal Ahmad



Received: 8 June 2013 / Accepted: 22 July 2013 Ó Springer Science+Business Media Dordrecht 2013

Abstract Silver nanoparticles (AgNPs) have broad spectrum antimicrobial/biocidal properties against all classes of microorganisms and possess numerous distinctive physico-chemical properties compared to bulk Ag. Hence, AgNPs are among the most widely used engineered NPs in a wide range of consumer products and are expected to enter natural ecosystems including soil via diverse pathways. However, despite: (i) soil has been considered as a critical pathway for NPs environmental fate, (ii) plants (essential base component of all ecosystems) have been strongly recommended to be included for the development of a comprehensive toxicity profile for rapidly mounting NPs in varied environmental compartments, and (iii) the occurrence of an intricate relationship between ‘‘soil–plant systems’’ where any change in soil

N. A. Anjum (&)  A. C. Duarte  E. Pereira  I. Ahmad CESAM-Centre for Environmental and Marine Studies, Department of Chemistry, University of Aveiro, 3810-193 Aveiro, Portugal e-mail: [email protected] S. S. Gill Stress Physiology and Molecular Biology Lab, Centre for Biotechnology, Faculty of Life Sciences, MD University, Rohtak 124001, India I. Ahmad (&) CESAM-Centre for Environmental and Marine Studies, Department of Biology, University of Aveiro, 3810-193 Aveiro, Portugal e-mail: [email protected]

chemical/biological properties is bound to have impact on plant system, the knowledge about AgNPs in soils and investigations on AgNPs–plants interaction is still rare and in its rudimentary stage. To this end, the current paper: (a) overviews sources, status, fate, and chemistry of AgNPs in soils, AgNPs-impact on soil biota, (b) critically discusses terrestrial plant responses to AgNPs exposure, and (c) illustrates the knowledge-gaps in the current perspective. Based on the available literature critically appraised herein, a multidisciplinary integrated approach is strongly recommended for future research in the current direction aimed at unveiling the rapidly mounting AgNPs-fate, transformation, accumulation, and toxicity potential in ‘‘soil–plant systems,’’ and their cumulative impact on environmental and human health. Keywords Silver  Nanoparticle  Soil–plant systems  Phytotoxicity  Tolerance

Introduction Engineered nanoparticles (NPs)-based technologies have fascinated almost every walk of life. However, a credible number of recent studies have demonstrated that not all engineered NPs are inherently benign and also their indiscriminate multidisciplinary applications can be fatal for both environmental and human

123

Page 2 of 26

health. Owing to the growing markets for engineered NPs-based products, the annual production of engineered NPs is increasing at war level. Nevertheless, this trend has been expected to lead to the appearance of varied NPs in air, water, soils, and organisms (Blaser et al. 2008; Mueller and Nowack 2008; Navarro et al. 2008; Ma et al. 2010). According to a recent estimate, 63–91 % of over 260,000–309,000 metric ton of global engineered NP-production in the year 2010 ended up in landfills, with the balance released into soils (8–28 %), water bodies (0.4–7 %), and atmosphere (0.1–1.5 %) (Keller et al. 2013). Among a credible number of NPs, metallic NPs have a high specific surface area and a high surface-tovolume ratio besides exhibiting unique electrical, chemical, optical, and photo-electrochemical properties, and can be easily synthesized and modified chemically. Hence, metallic NPs have enchanted researchers from multiple disciplines including physics, chemistry, electronics, and biology (Lanje et al. 2010). Nevertheless, the Woodrow Wilson International Centre for Scholars product inventory of nanomaterials, indicated that 1,015 different nanocontaining products were on the market in 2009, and these products mostly involved metal-based NPs (http://www.nanotechproject.org/inventories/consumer/ analysis_draft). Thus, as a result of multidisciplinary applications (such as electronics, optics, textiles, medical applications, cosmetics, food packaging, water-treatment technology, fuel cells, catalysts, biosensors and agents for environmental remediation), exposure of varied metallic NPs to the environment and humans is becoming increasingly widespread which needs an urgent and exhaustive evaluation (Handy et al. 2008; Thakkar et al. 2010; Gerloff et al. 2012; Luque-Garcia et al. 2013). Additionally, NPs are extensively used or tried for environmental (soil, water) remediation (Zhang et al. 2013; Ngomsik et al. 2005; Uheida et al. 2006), where information on their fate and impact is largely limited. Varied NPs, thus released to the atmosphere, may be deposited in the soil where they can persist for a long time or be taken up by biological organisms; hence, can act as ecotoxicological hazard, undergo biodegradation or bio-accumulate in the food chain (SCENIHR 2006; Bystrzejewska-Piotrowska et al. 2009). Since there always exist difficulties in the evaluation of potential toxic effects of majority of NPs, their multidisciplinary uses represent important toxicological risks to both environmental and human health. Nevertheless,

123

J Nanopart Res (2013) 15:1896

biotic communities interaction with varied environmental compartments contaminated potentially with NPs may cause bioaccumulation where subsequent exposure of higher level organisms to NPs through food chain cannot be ignored (Blaser et al. 2008; Navarro et al. 2008; Ma et al. 2010; Priester et al. 2012; Rico et al. 2011, 2013). Silver nanoparticles (AgNPs) AgNPs have a size range from 1 to 100 nm and consist of about 20–15,000 Ag atoms. Compared to bulk Ag, a number distinctive physico-chemical properties such as a high electrical and thermal conductivity, surfaceenhanced Raman scattering, chemical stability, catalytic activity and nonlinear optical behavior make AgNPs unique (Frattini et al. 2005; Warheit et al. 2007; Chen and Schluesener 2008; Wijnhoven et al. 2009; Fabrega et al. 2011). In addition, AgNPs possess large surface area-to-volume ratio, exhibit a better contact with the microorganism and are known potent and broad spectrum antibacterial agents with activity against diverse species within both Gram-positive and Gram-negative bacteria (Morones et al. 2005; Kim et al. 2007; Lee et al. 2007; Vigneshwaran et al. 2007; Marambio-Jones and Hoek 2010). AgNPs can form different nanoshapes, like nanocylinders, nanorods, nanowires, nanoplates, or nanobelts (Sun et al. 2003; Pal et al. 2007; Wiley et al. 2007; Jana et al. 2012; Kim et al. 2012; reviewed by Schluesener and Schluesener 2013). Nevertheless, AgNPs can be nanoscale in zero dimension (atomic clusters, filaments and cluster assemblies), one dimension (surface films, multilayers), two dimensions (strands, ultrafine-grained overlayers or buried layers and fibers), or three dimensions (particles, nanophase materials consisting of equiaxed nanometer sized grains) (Golovina and Kustov 2013). Since several pathogenic bacteria have developed resistance against various antibiotics, metallic Ag in the form of AgNPs has made a remarkable comeback as a potential antimicrobial agent. Hence, AgNPs have emerged up with diverse medical applications ranging from Ag-based dressings, Ag-coated medicinal devices, such as nanogels, nanolotions, etc. (Rai et al. 2009). Nevertheless, AgNP-products have been claimed earlier to ‘‘eliminate 99 % of bacteria’’ render material ‘‘permanently antimicrobial and antifungal’’ ‘‘kill approximately 650 kinds of harmful germs and viruses’’ and ‘‘kill bacteria in a short time as 30 min and can be

J Nanopart Res (2013) 15:1896

effective 2–5 times faster than other forms of Ag (Shahrokh and Emtiazi 2009). Moreover, since Ag ions attack various proteins in cells, these ions have widely been used as antifungal and antimicrobial agents (Pana´cˇek et al. 2009) and also to increase the efficacy of antiseptics (Golubeva et al. 2010). Hence due mainly to remarkable antimicrobial properties, AgNPs are one of the most widely used engineered NPs in over 250 consumer products including antimicrobial agent in domestic appliances (e.g., fridges, vacuum cleaners, air conditioning), paints, textiles/fabrics, plastics, varnish, clothes, socks and laboratory gowns, as well as in medical products, such as surgical gowns and dressing bandages (Boxall et al. 2007; Kim et al. 2007; Blaser et al. 2008; Klaine et al. 2008; Ma et al. 2010). However, US-EPA (2008) has classified all products containing nanoscale Ag as pesticides and also recommended the analysis of their potential risks to human and environmental health. Nevertheless, Ag? and/or AgNPs composites are also widely applicable in various agricultural activities including for the control of various phytopathogens and for plant disease management (Liu et al. 2002; Park et al. 2006; Jo et al. 2009). It was reported that about 25 % of the [1,300 NPs-containing consumer products contain AgNPs (Yu et al. 2013). Recently, Nowack et al. (2011) have reported the current production and industrial use of about 320 ton AgNPs per year. Nevertheless, the number of the AgNPcontaining products has already been increased from 30 in 2006 to over 300 at the beginning of 2011; whereas the use of 1,120 ton of AgNP has been estimated until 2015 (Stensberg et al. 2011). It has also been reported that the number of consumer products with AgNPs surpassed threefold that of the succeeding component as of March 2011 (http://www.nanotechproject.org/ inventories/consumer/analysis_draft). In the United States only, a production of AgNPs between 2.8 and 20 ton year-1 has been estimated (Hendren et al. 2011). Moreover, though, the National Institute for Occupational Safety and Health has considered 0.01 mg-1 m-3 as permitted exposure limit for all forms of Ag (NIOSH 1992) but severe damages were reported in mammalian models at levels lower than the permissible one (Kim et al. 2008; Sung et al. 2009). In this context, a separate review has been strongly advocated for AgNP-exposure (Kulthong et al. 2010). Owing to a wide use in a vast number of AgNPbased consumer products, the entry of AgNPs into

Page 3 of 26

varied environmental compartments including soil– plant systems and subsequently to human food chain may increase manifolds. Unfortunately, due to their nanoscale size, high reactivity and ill-defined dissolution properties, AgNPs’ environmental risks were considered very difficult to determine (Benoit et al. 2013). Of particular concern is whether there are new risks that are a direct consequence of their nanoscale size. In addition, the identification of AgNPs potential risks associated with their nanoscale structure has been difficult due to the fundamental challenge of detecting and monitoring nanoparticles in products or the environment (Glover et al. 2011). To this end, based on the Woodrow Wilson Database (2010) and the review by Fabrega et al. (2011), Fig. 1 summarizes AgNP-containing major products available in the market. Soil–plant systems Soil has always been vital to humans and fundamental to human health since it is the main resource for food production and is the major source of trace elements

Creams and Cosmetics Items 32.4 % Textiles and Clothing 18.0 % Household Items 16.4 % Air and Water Filters 12.3 % Others 8.6 % Detergents 8.2 % Health Supplements 4.1 %

AgNPs-Containing Products Fig. 1 Major products in the market containing silver nanoparticles (AgNPs). [Woodrow Wilson Database (March 2010); modified from Fabrega et al. (2011)]

123

Page 4 of 26

entering the food chain. The ‘‘soil–plant systems’’ are intricately linked where any change in soil chemical and biological properties are bound to have impact on plant growth, development and productivity. Environmental buildup of engineered NPs could profoundly alter soil-based food crop quality and yield. In particular, majority of AgNPs released from consumer products are expected to enter terrestrial ecosystems through land-application of biosolids (Blaser et al. 2008). Where AgNPs have widely been reported to threaten soil system-inhabitants including free-living nitrogen-fixing bacteria and symbiotic relationships involving fungi, bacteria, which cumulatively may affect soil’s physico-chemical characteristics. Hence, AgNPs may potentially alter ecosystem productivity and biogeochemistry by negatively impacting ‘‘soil– plant systems’’-lead vital ecosystem services (Klaine et al. 2008; Navarro et al. 2008). Moreover, the incorporation of wastewater-released AgNPs into sewage sludge released and their subsequent spread further on agricultural fields has been evidenced (Blaser et al. 2008). To the other, being essential base components of all ecosystems and having sessile nature plants expose huge interfaces to the air and soil environment, thus, have greater chance to interact with rapidly mounting varied NPs; where their possible toxicological impacts and underlying basic mechanisms are speculative and unsubstantiated (Navarro et al. 2008; Ma et al. 2010; Dietz and Herth 2011). Moreover, earlier, information on mode of interaction, uptake, accumulation and impact on the bio-systems at various levels of NPs in plants have been considered essential to device and implement proper mitigation or control measures to avoid nano-pollution hence to turn-out to be a serious ecological deterioration (Navarro et al. 2008; Ma et al. 2010). In addition, extensive research on ‘‘soil–plant systems’’-NPs interaction has also been strongly advocated (Dietz and Herth 2011). However, much less attention has been paid to soils, despite the importance of this pathway; and also data on terrestrial plants and other photosynthetic organisms are also lacking (Navarro et al. 2008; Monica and Cremonini 2009; Benoit et al. 2013). Based on modeling approaches and the use of probabilistic methods, the ‘‘predicted environmental concentrations’’ status values for soil and sludge-treated soils for Europe and the United States (Gottschalk et al. 2009; Fabrega et al. 2011) have been summarized in Fig. 2a.

123

J Nanopart Res (2013) 15:1896

However, despite the fact that: (a) soil system is the ultimate sink of directly or indirectly released varied NPs and may wide-open the most significant exposure avenues for assessing potential environmental risk by opening-up more chances for NPs-entry into food webs and human access to contaminated agriculture (Unrine et al. 2010; Pan and Xing 2012; Reme´dios et al. 2012), (b) soil microbial consortia and plant growth are closely related, and any perturbation in the former can have significant consequences for ecosystems and also influence by/also affect plant growth (Davidson and Janssens 2006), (c) AgNP-interaction with soil environment may yield changes in the chemistry of AgNPs and/or that of soils which may, in turn may control AgNP-stability, and consequently their transport through the environment and availability and subsequent toxicity to organisms (Benn and Westerhoff 2008; Geranio et al. 2009; Kim et al. 2010; Nowack 2010; Stone et al. 2010; Levard et al. 2012), and (d) plants—being a critical component of ecosystems, may significantly interact with NPs including AgNPs and control their fate and transport in the environment by accumulating them into their biomass (Navarro et al. 2008; Ma et al. 2010; Dietz and Herth 2011; Rico et al. 2011, 2013) by serving a potential pathway for AgNP-transport and bioaccumulation into food chains (Rico et al. 2011, 2013; Priester et al. 2012), there exists a dearth of literature on AgNPs chemistry modulation in a range of soil types and subsequent AgNP-impact on terrestrial plants and soil microbial communities (Navarro et al. 2008; Ma et al. 2010; Kumar et al. 2011; Cornelis et al. 2012; Coutris et al. 2012a; Tourinho et al. 2012; Benoit et al. 2013). Hence given the information paucity particularly on AgNPs in ‘‘soil–plant systems,’’ considering recent breakthroughs on AgNPs, the current paper: (a) overviews sources, status, fate, and chemistry of AgNPs in soils, AgNPs-impact on soil biota, (b) critically discusses terrestrial plant responses to AgNPs exposure, and (c) illustrates the knowledge-gaps in the current perspective.

Silver nanoparticles in soils Sources and status Though AgNPs can be generated spontaneously from manmade objects but because of a multidisciplinary

J Nanopart Res (2013) 15:1896

Page 5 of 26

A Europe

Sludge treated soil: 662

Soil: 8.3

Soil: 22

United States

Sludge treated soil: 1581

AgNPs-Predicted Environmental concentrations (PECs)

B Soil Chemistry

Particle Size

Major Factors Affecting AgNPs-Toxicity

Particle Shape

Particle Stability

Fig. 2 a Status of the values for predicted environmental concentrations (PECs; shown as mode, i.e., most frequent value) for Europe and the United States for soil and sludge-treated soils. [Base year 2008; modified from Gottschalk et al. (2009)

and Fabrega et al. (2011)], and b the summary of major factors affecting silver nanoparticle (AgNP) toxicity. See text for discussion

use, AgNPs may come to soils from the wet or dry deposition of AgNPs suspended in air, or from point sources such as production facilities, application of organic wastes in agriculture, application of a plant growth-promoting spray, sewage sludge recycling as a fertilizer to agricultural soils, waste incineration plants and landfill, or from nonpoint sources such as AgNPscontaining consumer products (Mueller and Nowack 2008; Navarro et al. 2008; Benn et al. 2010; Bernhardt et al. 2010; Glover et al. 2011; Coutris et al. 2012a, b; VandeVoort et al. 2012). Nevertheless, on-site wastewater management systems, biosolids application, improper disposal, accidental spills, as well as the application of AgNPs as an ‘‘organic’’ fertilizer/ pesticide may also significantly contaminate different soils (Blaser et al. 2008; Walters 2011; Calder et al. 2012). However, as it can happen with other NPs, accidental release during AgNP-production or AgNPtransport is also possible. In addition, intentional release of AgNP into soil system is also possible. Despite our knowledge of potential environmental release pathways of AgNPs, information on the

current budget for AgNPs in the soil system is lacking. Moreover, despite AgNPs are credibly synthesized following eco-friendly and cost-effective procedures (Poliakoff et al. 2002; Sharma et al. 2009; Ahmed et al. 2013; Bhaduri et al. 2013; Khan et al. 2013; Rao and Paria 2013), a huge amount of AgNPs are added globally to varied environmental compartments including soils. The current global production of AgNPs has been estimated at about 500 ton per annum (Mueller and Nowack 2008), and a steady increase on the volume manufactured was predicted for the next few years (Boxall et al. 2008). A higher extent of partition of AgNPs has been expected into sewage sludge contingent to advanced waste treatments (Blaser et al. 2008). In this perspective, with the use of sewage sludge, Mueller and Nowack (2008) projected input of 1 lg kg-3 of AgNPs to agricultural land per year. According to the Federal Environmental Agency of Germany (Umweltbundesamt 2008), AgNPs-utilization in Germany can be approximately estimated to 1,100 kg year-1. In the United States only, amounts in the order of 2,500 ton year-1 have been reported, out

123

Page 6 of 26

of which 150 ton ended up in sewage sludge and 80 ton have been released into surface waters (Khaydarov et al. 2009; El-Temsah and Joner 2012). Based on the use of environmental exposure models and the application of simple algorithms, Boxall et al. (2008) estimated 0.43 lg Ag kg-1 of soil arising from consumer products. Though incineration of annually produced sewage sludge is performed (Gottschalk et al. 2009) but in countries such as the United Kingdom and United States, a large proportion of such wastes is used as a fertilizer in agricultural soil (Nicholson et al. 2003) which in turn may act as major sources of AgNPs in agricultural soil system. Moreover, since natural background levels of Ag can be considered very low, the quantity of AgNPs produced has been considered as the main factor determining the concentrations found in all environmental compartments (Gottschalk et al. 2009; Johnson et al. 2011; Tourinho et al. 2012). Hence, the exact disposal route may strongly affect the amount of AgNPs that each environmental compartment receives (Fabrega et al. 2011). However, despite soils are known to be exposed to most manufactured NPs there is a paucity of information on the availability of the methodology for the assessment of their retention in soils, which in fact, determines potential mobility and bioavailability (Cornelis et al. 2010). Silver nanoparticle chemistry versus soil properties Soil environment can act as a major sink for AgNPs contributed by diverse pathways including on-site wastewater management systems, biosolids application, improper disposal, accidental spills, and the application of AgNPs-constituted organic fertilizers/ pesticides (Blaser et al. 2008; Walters 2011; Calder et al. 2012). Nevertheless, soils represent a solid matrix and a relatively complex medium with which NPs may interact and provide a good opportunity for the understanding manufactured NP-physico-chemical behavior (Pan and Xing 2012; Tourinho et al. 2012). AgNP-properties (such as dispersibility, agglomeration/aggregation, dissolution rate, aging, size, surface area, transformation and charge, and surface chemistry) can be modified by their interaction with soil environments which in turn may control AgNP-stability, and consequently their transport through the environment and availability, and

123

J Nanopart Res (2013) 15:1896

subsequent toxicity to organisms (Benn and Westerhoff 2008; Geranio et al. 2009; Kim et al. 2010; Nowack 2010; Stone et al. 2010; Cornelis et al. 2012; Coutris et al. 2012a; Levard et al. 2012; Tourinho et al. 2012; Benoit et al. 2013). To this end, however, a comprehensive understanding of the distribution, transformation, toxicity of AgNPs, and the significance of soil system-physico-chemical variables in the current context has been strongly considered important to correctly forecast and/or understand their benefits and risks to environmental and human health (Calder et al. 2012; Yin et al. 2012; Yu et al. 2013). Nevertheless, despite: (a) the importance of the soil as the major pathway of terrestrial AgNP contamination, and (b) the consideration of physico-chemical interactions between soils and NPs has been strongly advocated while studying the chemistry and behavior of NPs including AgNPs hence to scientifically extrapolate the effects of pure culture research to realistic field scenarios (Yin et al. 2012), much less attention has been paid to this end and also AgNP’s fate, behavior and bioavailability particularly in soil environment are largely unexplored and unsubstantiated (Cornelis et al. 2012; Benoit et al. 2013; Wang et al. 2013). Rather to date, most studies available in the literature in the current context have examined the AgNPs-fate and behavior in aquatic systems (Benn and Westerhoff 2008; Mueller and Nowack 2008; Geranio et al. 2009; Gottschalk et al. 2009; Kulthong et al. 2010; Liu and Hurt 2010). Hence given the above, a critical appraisal of the available recent literature on the AgNPs chemistry modulation only under soil environment is presented hereunder. A number of variables, such as the particle size, surface charge of AgNPs and the soil physicochemical traits largely govern the chemistry, fate, and transport of AgNPs in soil system, and hence their bioavailability and subsequent toxicity to biota (Tolaymat et al. 2010; Oromieh 2011; Shoults-Wilson et al. 2011; Cornelis et al. 2012; Sagee et al. 2012; VandeVoort et al. 2012; Benoit et al. 2013). A differential AgNP retention has been evidenced in suspensions of natural soils which was correlated mainly with the clay content of the soil (Cornelis et al. 2012). The authors advocated the role of heterocoagulation of AgNP with naturally occurring colloids to explain this correlation. Various stabilizing agents have been reported to modify AgNPs where their mobility may be altered by the electrostatic interaction

J Nanopart Res (2013) 15:1896

with different soil types (Tolaymat et al. 2010). For example, a positive charged soil may prevent the long distance mobility of negative charge-bearing citratecapped AgNPs. On the contrary, a negative charged soil may cause AgNPs to be more mobile in such soils (Tolaymat et al. 2010; reviewed by Yu et al. 2013). The strong adsorption capability of AgNPs onto soils has also been documented (Jacobson et al. 2005; Oromieh 2011; VandeVoort et al. 2012). Oromieh (2011) reviewed the possible fate of both Ag and AgNPs in soils; where a high soil pH value and cation exchange capacity (CEC) were reported to enhance Ag-sorption to the soil due to higher negatively charged sites and more cation exchange reactions, respectively. In addition, soils with fine texture were reported to exhibit higher surface areas which also facilitate Ag-sorption (Jacobson et al. 2005). Agsorption and mobility are also controlled by soil organic matters (Jones and Peterson 1986). Soils with high organic matter concentration sorb Ag more strongly than to mineral soils; where the sorption of Ag to soil was advocated due either to cation exchanges or complexation reactions (Jacobson et al. 2005). Moreover, higher binding affinity of Ag to reduced sulfur groups (thiol) on soil organic matter in order to form S–Ag–S bonds has been reported (Bell and Kramer 1999). Enhanced mobility of AgNPs was reported in the presence of organic matter such as surfactants or humic acid (Tian et al. 2010; Lin et al. 2012; Thio et al. 2012); whereas the promotion of AgNP-aggregation and retention was widely evidenced due to higher ionic strength and divalent cations (Lin et al. 2011; Thio et al. 2012). In addition to organic matter, pH has also been evidenced important soil property controlling the occurrence and the transformation of AgNP amendments to soils (Benoit et al. 2013). AgNP-aggregation and soil adsorption behavior have been reported to be closely associated with environmental factors such as ionic strength and natural organic matter (Bae et al. 2013). The authors observed increased aggregation rate of AgNPs with increasing ionic strength and decreasing natural organic matter concentration. Additionally, at higher ionic strength, the AgNPs were found unstable, where AgNPs tended to be adsorbed to the soil, while increased natural organic matter concentration hindered soil adsorption. Hence, a thorough understanding of particle–particle interaction mechanisms assessment has been suggested in order to correctly

Page 7 of 26

assess AgNP-environmental fate and transport (Bae et al. 2013). The authors also reported more availability of free Ag ions in acidic soils, while in the presence of organic matter, Ag ions were reported to be tightly bound in complexes. Information is still sparse on the mobility of AgNP in natural soils under dynamic flow conditions, and the effect of soil properties on AgNPtransport in soils (Cornelis et al. 2012). Negative f potential of most natural soil minerals results in a highenergy barrier for the attachment of AgNPs (Christian et al. 2008; Theng and Yuan 2008; Lin et al. 2011) and the demonstration of relatively high mobility of AgNPs was expected (Sagee et al. 2012). In context with the retention and dissolution of AgNPs in natural soils: (a) free Ag? was expected to preferentially bind to thiol groups and natural organic matter (VandeVoort et al. 2012), (b) Ag ions exhibit strong binding capacities of the humic and fulvic acids; resulting into less than 5 % of the total dissolved Ag to be biologically available (Jacobson et al. 2005), (c) much of the Ag in soils has been evidenced to be bound either to colloidal particles (size 10–200 nm) or adsorbed to the soils (Coutris et al. 2012a, and (d) the most of the Ag? are highly retained by the soil (Cornelis et al. 2012). The modulation of soil denitrification kinetics by AgNPs (35–60 nm, uncoated and coated with 0.3 % polyvinylpyrrolidone; 1, 10, or 100 mg L-1) was correlated with AgNP affinity for soil surfaces (Kd), as determined through the isotherm study (VandeVoort et al. 2012). Soil-harbored environmental pollutant’s aging, as physical or chemical transformations over time, is a well-known phenomenon that describes temporal aspects of their bio-accessibility (Coutris et al. 2012b). In context also with AgNPs, the aging has been considered essential for understanding their fate in the environment (Scheckel et al. 2010; ShoultsWilson et al. 2011; Coutris et al. 2012b). Moreover, since AgNPs are susceptible to environmental transformations (changes in aggregation state, oxidation state, precipitation of secondary phases, sorption of (in)organic species), the assessment of the toxicity of the transformed NPs as well as the ‘‘fresh’’ ones has been recommended (Levard et al. 2012). Since AgNPs have small particle size, the kinetics of AgNPs was expected to be faster than for bulk Ag which in fact is the reason behind the significantly reduced lifetime of the metallic state of Ag in nature. AgNPs may also readily transform in the environment, which can

123

Page 8 of 26

modify their properties and alter their transport, fate, and toxicity. Hence, the consideration of such transformations has been strongly recommended when assessing the potential environmental impact of AgNPs in realistic complex natural systems (Levard et al. 2012; Lowry et al. 2012). Additionally because of availability of Ag-corrosion agents in nature, AgNPenvironmental transformations have been envisaged to strongly affect their surface properties (Liu et al. 2010) and consequently their transport, reactivity, and toxicity in soils and aqueous systems (Levard et al. 2012). However, despite the previous facts, most of the information available on potential environmental transformations of AgNPs are restricted to aqueous systems (Elzey and Grassian 2010; Levard et al. 2011, 2012; Zhang et al. 2011; Gondikas et al. 2012); and only a few studies are available in this context with AgNP-potential transformations in soil system (Scheckel et al. 2010; Shoults-Wilson et al. 2011). Using X-ray absorption spectroscopy, the time-dependent evolution of AgNPs in kaolin (Scheckel et al. 2010) and soil (Shoults-Wilson et al. 2011) has been evidenced. No change was revealed in uncoated AgNPs (mean particle diameter 100 nm) over 18 months, even in the presence of NaCl; whereas organically coated AgNPs (mean particle diameter 148 nm) became coated with chloride when NaCl was present. Additionally, no destabilization/dissolution of these particles was observed during 18 months (Scheckel et al. 2010). In another similar study, Shoults-Wilson et al. (2011) studied the speciation of PVP-coated AgNPs (mean particle diameter 10 and 30–50 nm) aged 28 days in soil. Most silver remained as Ag0, while 10–17 % was present as Ag2O, indicating that AgNPs had undergone partial oxidation in soil. The changes in colloidal stability and their interaction with different environmental surfaces can significantly control the fate of engineered NPs in environmental systems (Abraham et al. 2013). In this perspective, the studies on the sorption of engineered AgNPs from stable and unstable suspensions to model (sorbents with specific chemical functional groups) and environmental (plant leaves and sand) surfaces have revealed the role of classical sorption isotherms to this end (Abraham et al. 2013). In addition, the nonlinear nature of sorption of AgNPs from stable suspensions was revealed. AgNPs have also been evidenced to largely irreversibly interact in a primary

123

J Nanopart Res (2013) 15:1896

minimum associated with microscopic heterogeneity (Liang et al. 2013). Colloidally stable AgNP suspensions exhibited greater toxicity to bacterium Pseudomonas fluorescens (ATCC 13525) biofilms than corresponding particle-free supernatants containing only dissolved Ag released from the particles; whereas this distinct NP-specific toxicity was not observed for less stable, highly aggregated particles, suggesting that biofilms were protected against NP-aggregate toxicity (Wirth et al. 2012). It is important to underline here that to date no information on the influence of NPs on soil is available in the possibly vulnerable ecosystems of polar-regions. In this context, however, AgNPs (0.066 %) were evidenced highly toxic to arctic consortia (on a high latitude, [78°N) (Kumar et al. 2011); hence, the authors advocated more studies need on NP’s potential toxicity, particularly in high latitude soils. Because ion release is an important environmental behavior of AgNP and estimation and/or characterization of Ag? release in soil environment is critical for understanding the environmental fate, transport, bioavailability and bio-accessibility, and subsequent biological impacts of AgNPs (Coutris et al. 2012a; Benoit et al. 2013). Given their ability to oxidize in soil environment (Shoults-Wilson et al. 2011; Cornelis et al. 2012), it is not clear whether the AgNPs, Ag? or Ag complexes are the most bioavailable species (Benoit et al. 2013). To this end, the AgNP-bioavailability (Fortin and Campbell 2001) or AgNP-toxicity may be modulated by both Ag? (Ratte 1999) and some of their complexes. Radniecki et al. (2011) found that NP-specific toxicity to ammonia oxidizing bacteria— Nitrosomonas europaea was reported negligible for AgNPs and that dissolved Ag was responsible for the observed AgNP-toxicity. Other studies on Ag behavior in sewage sludge suggested that Ag2S was the dominant species originating either from Ag? or AgNPs, and that the very low solubility of Ag2S would limit the bioavailability and adverse effects of silver in the environment (Kim et al. 2010; Nowack 2010). Hence, the studies aimed at evaluating the risk of the AgNPs, and at distinguishing these particles from that of the released free Ag and Ag-complexes should perform speciation studies. However, very few data are available in the literature on the partitioning of AgNPs in soils or on the determination of the speciation of Ag? in soils following the AgNPamendment (Benoit et al. 2013). Furthermore,

J Nanopart Res (2013) 15:1896

AgNPs-toxicity to microbes has been reported to be significantly modulated by culture conditions/types (pure culture, natural sediments), where environmental physico-chemical interactions significance in damping NPs toxicity was reflected (Bradford et al. 2009; Colman et al. 2012). Thus, it is clear from the above discussion that part or all of the toxicity attributed to AgNPs may be due to the release of Ag?. Therefore, in order to determine the relative toxicity of Ag? with respect to AgNPs, it is essential to precisely quantify AgNPs dissolution under the conditions that are most relevant to the biological or environmental media of interest (e.g., complex matrices, low AgNP-concentrations, etc.) (Hadioui et al. 2013). Silver nanoparticles impact on soil microbial communities Soil bacteria play a key role in nitrogen fixation and the breakdown of organic matter. In addition, soil bacteria also form symbiotic relationships with legumes which provide a major source of fixed nitrogen for both of them and other plants. Nevertheless, significant consequences for ecosystems can be influenced by any perturbations of soil microbial consortia which in turn could affect soil fertility, water quality and ecosystem, and plant growth and productivity (Davidson and Janssens 2006; Throba¨ck et al. 2007; Yang et al. 2013). However, to date, the majority of the toxicity studies on AgNPs have considered mammals or aquatic species, and comparatively few studies have considered soil microorganisms (US-EPA 2007; Christian et al. 2008; Klaine et al. 2008; El-Temsah and Joner 2012). Moreover, the available reports on AgNP-toxicity to bacteria have been largely performed in laboratory settings and have not been conducted within environmental media (VandeVoort et al. 2012; VandeVoort and Arai 2012). In soils with low organic matter, AgNPs exposure may cause a dramatic collapse in metabolic abilities and the diversity of soil microbial populations (i.e., bacteria, archaea, or eukarya); whereas in higher organic matter soils the response may be of lesser extent where detectable and significant implications to diversity of the soil system can be envisaged. The implications of this collapse were expected to be tremendous as the soil biology is critical in controlling the environmental fate of many other

Page 9 of 26

chemicals (http://water.usgs.gov/wrri/08grants/2008 IN251B.html). Furthermore, soil exo-enzyme activities can be negatively impacted by AgNPs where higher sensitivity of urease activity towards AgNPs was noted (Shin et al. 2012). Hence, the potential of AgNPs to adversely affect beneficial bacteria in the environment, especially in soil system has become a particular concern (http://nano.foe.org.au/node/190). The toxic effect of AgNPs on bacteria has been widely evidenced to disrupt denitrification processes, with the potential to cause ecosystem-level disruption (SenJen 2007; Throba¨ck et al. 2007; Panyala et al. 2008; VandeVoort and Arai 2012). Soil bacteria exposure to 100–1,000 mg L-1 of various types of AgNPs has been evidenced to significantly inhibit nitrification (Choi and Hu 2008, 2009; Radniecki et al. 2011; Arnaout and Gunsch 2012). In this context, the AgNP-toxicity to nitrification bacteria has been reported to be highly dependent on their size; where AgNPs with less than 5 nm diameter were reported to significantly inhibit the activity of nitrification bacteria (Choi and Hu 2008). Rootcolonization by beneficial soil bacterium (Pseudomonas chlororaphis O6) has been evidenced to promote plant growth and tolerance to abiotic and pathogen stresses (Ryu et al. 2007; Cho et al. 2008). However, the toxicity of AgNPs (10 nm spherical; 1 and 3 mg Ag L-1) to PcO6 has been reported (Calder et al. 2012). The authors observed 1 and 3 mg Ag L-1 mediated loss in bacterial cultureability in sand whereas no cell death was observed in a loam soil. In another study, Fabrega et al. (2009a, b) evidenced partial disaggregation and stabilization of AgNPs due to humic acids which can also reduce AgNPs antimicrobial effects against P. fluorescens. Moreover, the properties of solution such as pH, ionic strength, and background electrolytes were reported to alter the surface charge and aggregation of AgNPs (El-Badawy et al. 2010) which in turn can lead to altered toxicity (Jin et al. 2010; Yang et al. 2012). Despite the clearly known AgNP-impact on beneficial soil bacteria, little research has been conducted on how nitrogen-cycling bacteria respond to AgNPs at the molecular level and the resulting impact on the associated metabolic pathways. Hence, the studies on the relative sensitivity and transcriptomic response of ecologically important microorganisms to both AgNPs and Ag? would help significantly to get more insights in the current context (Yang et al. 2013).

123

Page 10 of 26

Silver nanoparticles in plants Accumulation Studies have shown that NPs may undergo accumulation in plants. Since plants possess a large size and high leaf area, and are of stationary in nature they have a greater chance of exposure to a wide range of NPs available in their surrounding environment (Dietz and Herth 2011). Thus, plants may significantly control varied NP’s fate and transport in the environment by accumulating them into their biomass (Navarro et al. 2008; Ma et al. 2010). The major pathways of terrestrial plant’s exposure to NPs through soil were earlier reported to include potential leaching from nano-enabled products, intentional sub-surface release for environmental remediation, land applications of contaminated biosolids, or wastewater effluent discharge (Pokhrel and Dubey 2013; Zhang et al. 2013). Plant roots have been considered as the main route of plant’s exposure to NPs which may harbor a major part of accumulated NPs which subsequently may lead to physical or chemical toxicity in plants. Proper hydraulic conductivity has been considered essential for the mobility and encounter of AgNPs to plant roots and rhizobacteria (Bystrzejewska-Piotrowska et al. 2009; Fabrega et al. 2011). Cucurbita pepo shoots contained 4.7 greater Ag-concentration under AgNPs (10–1,000 mg L-1) exposure than did the plants from the corresponding bulk solutions at similar concentrations (Stampoulis et al. 2009). The authors considered a greater ion release from AgNPs as the major reason leading to a greater Ag-concentration in C. pepo shoots. Uptake of AgNPs as large as 40 nm has been evidenced in Arabidopsis thaliana roots, where though the majority of AgNPs adhere to the root cap their transport to the shoots was also observed (Ma et al. 2010). A differential Ag-accumulation capability of Populus deltoides 9 nigra and A. thaliana was revealed under hydroponic exposure to AgNPs (PEGcoated 5 and 10 nm AgNPs, and carbon-coated 25 nm AgNPs) concentrations (0.01–100 mg L-1) (Wang et al. 2013). In this study, Ag-distribution in shoot organs varied between plant species, where A. thaliana accumulated Ag primarily in leaves (at tenfold higher concentrations than in the stem or flower tissues), whereas poplars accumulated Ag at similar concentrations in leaves and stems. Moreover, within the particle sub-inhibitory concentration range,

123

J Nanopart Res (2013) 15:1896

Ag-accumulation in P. deltoides 9 nigra tissues increased with exposure concentration and with smaller AgNP size. However, compared to larger AgNPs, the authors observed the faster uptake of smaller AgNPs which impacted evapotranspiration at lower concentrations (e.g., 1 mg L-1 of 5 nm AgNPs) in P. deltoides 9 nigra. Sabo-Attwood et al. (2012) reported the uptake of AgNPs by Nicotiana xanthi seedlings as size selective, with further translocation to cells and tissues and resulting biotoxicity. No accumulation of Ag in any form was noted in AgNPexposed Brassica juncea plants (Haverkamp and Marshall 2009); where the authors also evidenced the bioaccumulation of the AgNPs in the B. juncea cells as a function of the reduction potential in the system. In context with AgNPs-cellular uptake, the uptake mechanisms and distribution of AgNPs in cells are still insufficiently explored, and very few studies have addressed this question (Kokina et al. 2013). In AgNPs-exposed Linum usitatissimum, Kokina et al. (2013) demonstrated the uptake of AgNPs by calli cells and regenerants where AgNPs were localized mainly in the cytoplasm, and they did not affect regenerant viability and also influenced the type and frequency of flax calli regeneration. The authors envisaged that this effect of AgNPs could be used for the delivery of metal NPs to plant cells. Deposition of AgNPs has been evidenced inside the root cells in Oryza sativa (Mazumdar and Ahmed 2011). Where the authors concluded that AgNPs can enter through small pores of cell walls and causes damages in cell wall and vacuoles as well. In Zea mays, the bio-uptake concentration was 1.8 ng Ag mg-1 dry weight of seedlings for citrate-AgNP treatments (Pokhrel and Dubey 2013). To the other, A. thaliana exposed to AgNP suspensions bioaccumulated higher Ag content than plants exposed to AgNO3 solutions (Ag? representative) (Geisler-Lee et al. 2013). Moreover, AgNPs accumulated progressively in this sequence: border cells, root cap, columella, and columella initials. AgNPs were apoplastically transported in the cell wall and found aggregated at plasmodesmata. The bioavailability of NPs to plant-uptake can be influenced by any difference in media with AgNPs-concentrations. In this context, the bioavailability and effect of Ag? dissolved from AgNPs were observed less in soil than agar (Lee et al. 2012). Nevertheless, the amounts of Ag? release from AgNPs in soil and agar media significantly differed; where the authors noted the

J Nanopart Res (2013) 15:1896

maximum concentration of Ag? released from AgNPs in the agar and soil samples used as: 1.3 mg L-1 and 2.7 mg kg-1, respectively. The AgNPs accumulated in Phaseolus radiatus and Sorghum bicolor in agar medium increased in an exposure concentrationdependent manner where the bioaccumulation factors of P. radiatus and S. bicolor were calculated to be 0.14 and 0.08 L kg-1, respectively. Moreover, the authors noted AgNPs-concentration-dependent increase in AgNP-bioaccumulation only in the roots but not in the shoots. The bioaccumulation factors of the root of P. radiatus and S. bicolor were 0.008 and 0.006 kg-1, respectively; whereas the bioaccumulation factors of the shoot of P. radiatus and S. bicolor were calculated as 0.001 and 0.001 kg-1, respectively. As reported also by Coutris et al. (2012a), the low bioavailability of AgNPs may attribute to their binding to organic substances and the low mobility. The soil media may change the properties and dissolution of NPs hence may affect their bioavailability. The lower AgNPsbioavailability was suggested to be due to a greater aggregation in pore water and AgNP sorption onto soil particles contributed to lower bioavailability of AgNPs in soil (Lee et al. 2012). In common metallophytes namely B. juncea and Medicago sativa, Ag was stored as discrete NP, with a mean size of approximately 50 nm (Harris and Bali 2008). In Glycine max and C. pepo exposed to 500 or 2,000 mg L-1 of bulk or AgNP, De La Torre-Roche et al. (2013) reported Ag-mediated significant impact on overall element uptake, where in G. max, AgNP-exposure resulted in 1.8–6.6 times more tissue Ag than did the corresponding bulk material exposure; whereas in C. pepo, this pattern of greater NP uptake held at 500 mg L-1 but disappeared at the higher exposure level. Ag-mediated significant alteration in the accumulation and translocation of co-contaminants in agricultural systems has been reported where the co-contaminant interactions varied both with Ag-particle size (NP versus bulk) and plant species (De La Torre-Roche et al. 2013). Nevertheless, especially in agro-ecosystems, in addition to direct toxicity to and accumulation by crop plants, the interaction of NPs with co-contaminants and other chemical constituents (such as pesticides, fertilizers) have been evidenced to impact food safety (De La TorreRoche et al. 2013). In G. max and C. pepo exposed to 500 or 2,000 mg L-1 of bulk or AgNP, De La Torre-Roche et al. (2013) reported a suppressed uptake and translocation of (dichlorodiphenyldichloroethylene, p,p0 -

Page 11 of 26

DDE–DDT metabolite), a widespread persistent and estrogenic pollutant upon co-exposure to Ag; where the authors envisaged the role of element interactions with membrane transport proteins. Toxicity and tolerance In consideration of the vast use of AgNPs and their various possible routes of entry into the environment (Som et al. 2011; Speranza et al. 2013), there is an urgent need to critically discuss available literature on potential mechanisms underlying AgNP’s phytotoxicity and tolerance. Nevertheless, though toxicity of the Ag ionic form is well-understood comprehension the toxicological impact of AgNPs is more complicated due largely to uncertainties in the amounts of aggregation or exposure (Mirzajani et al. 2013). In comparison with the bacteria, there are limited toxicology studies on the effects and mechanisms of NPs on higher plants. Also, there is a dearth of information in the literature on AgNP-impacts on terrestrial plant species; where AgNPs–plant interaction-study results have yielded both positive and negative or inconsequential effects where merely more speculation and un-substantiation are perceptible. Though, a number of factors related with plants (species types, seeds, seedlings, cell suspensions), AgNPs (concentration, size, aggregation, functionalization), and environmental/experimental conditions (temperature and time, and method of exposure) may control AgNP-phytotoxicity extent Navarro et al. (2008) (Table 1; Fig. 2b) but only a few studies have considered these aspects during AgNPs–plant interaction experiments. Figure 3 schematically illustrates major sources of AgNPs to the soil, role of soil physico-chemical characteristics in the control of AgNPs mobility/bioavailability modulation and their subsequent influence on the extent of plant AgNPs-uptake/accumulation and toxicity. In the following sub-sections, recent information available on AgNPs-mediated toxicity to plant growth and physiology/general biochemistry and cells will be critically discussed. In addition, information pertaining to AgNPs-accrued oxidative stress and its metabolism will also be appraised. Toxicity to plant growth and physiology/biochemistry A higher toxicity has been credited to very small size of NPs in a number of studies in NPs-exposed plants

123

Page 12 of 26

(reviewed by Rico et al. 2011). To this end, El-Temsah and Joner (2012) evidenced a greater toxicity in L. usitatissimum, Hordium vulgare, and Lolium perenne due to Ag-colloid (0.6–2 nm) when compared to AgNPs of 5 and 20 nm. In L. usitatissimum, H. vulgare, and L. perenne exposed to 0–100 mg L-1 Ag, El-Temsah and Joner (2012) evidenced inhibitory effects in aqueous suspensions at 10 mg AgNP L-1 where the authors did not achieve a complete inhibition of germination; hence, considered reduction in shoot growth as a more sensitive endpoint than germination percentage. Moreover, the authors showed no clear size dependency of the AgNP-effects. Though AgNP (size 29 nm) may exert visible reduction effects on the germination of C. pepo and Lactuca sativa seeds but no toxicity effect was observed (Barrena et al. 2009). Growth in terms of fresh weight, root and shoot length, and vigor index of seedlings has been reported positively affected by AgNPs concentrations (0, 25, 50, 100, 200, and 400 ppm) in B. juncea (Sharma et al. 2012). The authors noted AgNPsmediated increase of 326 % in root length and 133 % in vigor index. In sand matrix culture, there is a report of AgNPs-dose-dependent inhibition of Triticum aestivum growth where the authors noted a dose-dependent reduction in shoot and especially the root lengths with amendments with AgNPs (Dimkpa et al. 2013). In another study by Mahna et al. (2013), the lower concentrations of AgNP (100, 250, 500, 1,000, and 2,000 ppm; exposed for 5, 10, 20, 30, and 60 min) acted as an antimicrobial agent with no side effect on the explant viability, and consequently, all decontaminated seeds germinated, and leaf and cotyledon explants survived in Lycopersicon esculentum cv. Micro-Tom, A. thaliana and Solanum tuberosum. In a recent study, a stimulatory effect was observed on root elongation, fresh weight, and evapotranspiration of both plants at a narrow range of sub-lethal concentrations (e.g., 1 mg L-1 of 25 nm carbon-coated AgNPs for P. deltoides 9 nigra) (Wang et al. 2013). These authors also observed some toxicity at higher AgNPconcentrations (e.g., 100 mg L-1 of 25 nm carboncoated AgNPs for P. deltoides 9 nigra, 1 mg L-1 of 5 nm AgNPs for A. thaliana) where plant susceptibility to AgNPs increased with decreasing AgNP size. No significant effects on seedling growth were reported in AgNPs-exposed Ricinus communis plants even at higher concentration of 4,000 mg L-1 (Yasur and Rani 2013), while the authors noted a decreased seed

123

J Nanopart Res (2013) 15:1896

germination under the exposure of Ag in bulk form as AgNO3. A size- and concentration-dependent citratestabilized AgNPs (sizes 20, 40, and 80 nm)-toxicity (in terms of physiological phytotoxicity, cellular accumulation, and subcellular transport) in A. thaliana (Geisler-Lee et al. 2013). In addition, the authors noted inhibition in the seedling root elongation where a linear dose–response relationship was perceptible within the tested concentration range. The available literature on seed germination, root elongation, and root growth under biologically synthesized AgNPs exposure have showed both insignificant effect (at 10 ppb and 100 ppb AgNP; Krishnaraj et al. 2012) and significant negative impact at very low engineered AgNPs concentration (Ma et al. 2010; Yin et al. 2011). In P. vulgaris and Z. mays exposed to varying AgNP-concentrations (20, 40, 60, 80, and 100 ppm), Salama (2012) reported a AgNPdose-dependent effect on plant growth. Where the authors noted increase in the lengths and weights of shoot and root and the area of leaf surface of the studied plants with increase in AgNPs concentration up to 60 ppm; thereafter, declines in the studied parameters were noted. The authors have given the credit of increased plant growth up to 60 ppm AgNPs to increased chlorophyll, carbohydrate, and protein contents. In Z. mays, root hair density appeared unaffected with citrate-coated AgNPs; where also little to no effect on root growth was noted (Pokhrel and Dubey 2013). The authors observed some potential of citrate-coated AgNPs to inhibit germination in Z. mays; this inhibition was, however, always less than 35 % even at the highest concentration tested (73.4 lg mL-1; compared to the control). The biologically synthesized AgNPs resulted in an insignificant decrease in the root and shoot length along with disappearance of air chamber in root cortex, alteration of shape, size, and distribution of xylem elements in the stems of Bacopa monnieri (Krishnaraj et al. 2012). AgNP-penetration into the O. sativa cell wall and subsequent destruction of the cell morphology and the structural features has been evidenced up to 60 lg mL-1 of AgNPs (Mirzajani et al. 2013). The authors also noted a linear and significant decline in the dry matter accumulation under AgNPs exposure. In contrast, O. sativa plant-incubation for 7, 14, and 21 days with the treated growth media diminished the observed AgNPs inhibitory impact on the plants dry weight. In this context, the authors expected the role of AgNPs size which might have increased during the incubation period which in turn

Plant species and endpoints

Solution culture

Agar culture media (20 mL of 0.5 % agar and 10 mL of 0.25 % agar); incubated for 2 days

C. pepo

Phaseolus radiatus; seedling growth

Concentration: 250 and 750 mg L-1

Citrate-coated; particle size range: 5–25 nm (average 10 nm); concentrations: 0, 0.5, 1, 5, and 10 mg L-1

Size: 2 nm; concentrations: 62, 100, and 116 mg L-1

NOAEC: \100; LOAEC: \100; EC50: [2,000 NOAEC: 100; LOAEC: 300; EC50: [2,000 Low to zero toxicity

S. bicolor: shoot growth S. bicolor: root growth Cucumis sativus; Lactuca sativa seed germination

NOAEC: [2,000; LOAEC: [2,000; EC50: [2,000

NOAEC: \5; LOAEC: 5; EC50: 26

NOAEC: [2,000; LOAEC: [2,000; EC50: [2,000

Solvent solution and concentration: sodium borohydride (2.64 mM)

Hawthorne et al. (2012)

Musante and White (2012) Dimkpa et al. (2013)

References

Barrena et al. (2009)

No-observed-adverse-effect concentration (NOAEC): Lee et al. \5; the lowest-observed-adverse-effect (2012) concentration (LOAEC): 5; median effective concentration (EC50): 13

Plant biomass and transpiration decreased by 49–91 % compared to equivalent bulk Ag

Dose-dependent elevation in the accumulation of oxidized glutathione (GSSG) and induction in the expression of a gene encoding a metallothionein

Dose-dependent reduction in shoot and especially the root lengths with amendments with AgNPs

Reduced biomass and transpiration by 66–84 % when compared with bulk Ag

Effect

P. radiatus; root growth

Soil adjusted with moisture content of 40 %); controlled temperature of 25 ± 1° C; incubated for 5 days

Sand matrix

T. aestivum

Size: 10 nm; concentration: 0–5 mg kg-1

Citrate-coated; particle size range: 5–25 nm (average 10 nm); concentrations: 0, 100, 200, 300, 400, 500, 600, and 800 mg kg-1 dry soil

Sand matrix

Triticum aestivum

Size: 10 nm; concentration: 0–5 mg kg-1

Sorghum bicolor; seedling growth P. radiatus; shoot growth

25 % Hoagland’s solution

Curcubita pepo

Exposure condition and incubation period

Size: \100 nm; concentration: 500 mg L-1

Plant germination, growth, and physiology/biochemistry

Particle size/range and concentration(s)

Table 1 Summary of some representative recent studies on silver nanoparticles (AgNPs)-impacts in plants

J Nanopart Res (2013) 15:1896 Page 13 of 26

123

123 P. deltoides 9 nigra

Size: 25 nm; concentration: 1 mg L-1

1/4 strength Hoagland solution; 11 days

Increased poplar evapotranspiration by 42 % compared to unexposed controls; Root and stem biomass were increased by 63 and 46 %, respectively

Significantly decreased evapotranspiration by 87 %; reduced the fresh weights of roots, stems, and leaves by 87, 42, and 81 %, respectively

Populus deltoides 9 nigra

Size: 25 nm; concentration: 100 mg L-1

1/4 strength Hoagland solution; 11 days

Toxicity increased with increased AgNPconcentration; seedlings failed to develop root hairs, had highly vacuolated and collapsed cortical cells and broken epidermis and rootcap; root biomass decreased from 18.6 to 4.7 mg; root length decreased from 7 to 0.7; roots AgNP sensitivity [ shoots

Seeds were soaked in 5 mL test solutions; incubation period: 7 days

Reduced transpiration (41–79 %)

Lolium multiflorum

25 % Hoagland solution

Gum arabic-coated AgNPs; size: 6 nm; concentrations: 1–40 mg L-1

C. pepo

Ag; size: 100 nm; AgNP-concentrations: 100, 500, and 1,000 mg L-1

Reduced shoot length

Reduced germination and shoot length

Reduced biomass (57–71 %)

H. vulgare; L. perenne

Ag; size: 20 nm; AgNP-concentration: 20 mg L-1

Reduced germination Reduced shoot length

Ag; size: 100 nm; AgNP-concentrations: 500 and 1,000 mg L-1

H. vulgare

Ag; size: 20 nm; AgNP-concentration: 10 mg L-1

L. usitatissimum; H. vulgare

Hordeum vulgare; L. perenne; L. usitatissimum H. vulgare

Ag (colloid); size: 0.6–2 nm; AgNPconcentration: 20 mg L-1

Ag; size: 5 nm; AgNP-concentration: 10 mg L-1

Reduced shoot length

L. perenne; L. usitatissimum

Reduced germination (20 %)

Ag (colloid); size: 0.6–2 nm; AgNPconcentration: 10 mg L-1

Aqueous suspension (0.1 % v/v Tween 20)

No effect on the germination

Effect

Reduced germination (50 %)

Lolium perenne

Ag (colloid); size: 0.6–2 nm; AgNPconcentration: 10 mg L-1

Exposure condition and incubation period

Ag (colloid); size: 0.6–2 nm; AgNPconcentration: 20 mg L-1

Linum usitatissimum

Plant species and endpoints

Size: 20 nm; concentrations: 20, 40, 60, 80, and 100 mg L-1

Particle size/range and concentration(s)

Table 1 continued

Wang et al. (2013)

Yin et al. (2011)

Stampoulis et al. (2009)

El-Temsah and Joner (2012)

References

Page 14 of 26 J Nanopart Res (2013) 15:1896

1/4 strength Hoagland solution; 11 days

Arabidopsis thaliana A. thaliana A. thaliana A. thaliana

Sizes: 5 and 10 nm; concentration: 0.05 mg L-1

Sizes: 5 and 10 nm; concentration: 1 mg L-1

Size: 5 nm; concentrations: 0.01–0.05 mg L-1

Size: 10 nm; concentrations: 0.01–0.02 mg L-1

Biologically synthesized; (biogenically male inflorescence of screw pine, Pandanus odorifer); 2 h

A. cepa 5,000 cells

Allium cepa

Vicia faba root tips

Size: 24–55 nm; concentrations: 0–80 lg L-1

Size: \100 nm; concentration: 100 mg L-1

Size: 60 nm; concentrations: 12.5, 25, 50, and 100 mg L-1

Modified after Rico et al. (2011)

Solution culture; commercial, Sigma; 2h

Allium cepa 5,000 cells

Size: 70 nm; concentrations: 0–80 mg L-1

AgNPs were suspended directly in deionized water

Aqueous suspension; 4 h

Hoagland solution; 12 days; temperature: 25 ± 5 °C; to prevent aggregations it was stirred with glass rod after every 12 h.

Oryza sativa

1/4 strength Hoagland solution; 11 days

1/4 strength Hoagland solution; 11 days

Concentrations: 50, 500, and 1,000 lg mL-1

Cellular-/geno-toxicity

1/4 strength Hoagland solution; 11 days

P. deltoides 9 nigra

PEG-coated 10 nm AgNPs; concentration: 0.1 mg L-1

1/4 strength Hoagland solution; 11 days

Exposure condition and incubation period

Plant species and endpoints

Particle size/range and concentration(s)

Table 1 continued

Dose-dependent decrease in the mitotic index but increase in the frequencies of chromosomal abnormalities and micronuclei

Decreased mitosis; disturbed metaphase; sticky chromosome; cell wall disintegration and breaks

Patlolla et al. (2012)

Kumari et al. (2009)

Panda et al. (2011)

Panda et al. (2011)

Cytotoxicity LC50: up to 10 lg mL-1 no effects on genotoxicity; Comet assay 20–40 lg mL-1; DNA damage doses 10 lg mL-1 ROS-induced cell death and DNA damage doses 20 lg mL-1; up to 10 lg mL-1 no genotoxic; concentrations \ 5 lg mL-1 were noncytotoxic, and concentrations [80 lg L-1 were cytotoxic, which was evident from cell death as well as mitotic index

Mazumdar and Ahmed (2011)

References

1,000 lg mL-1 reflected the highest toxicity where: breakage of cell wall and vacuoles in root cells of test species described the toxicity of particles; depositions of silver nanoparticles inside the root cell by smaller particles

Increased root growth by 20 %

Increased root growth by 38 %

Root growth rate was completely inhibited; smaller rosette size

Moderate increases in overall rosette size and coloration

Significantly enhanced poplar evapotranspiration by 43 %; the final fresh weight of roots, stems, and leaves was also increased relative to the control poplars by 48, 50, and 39 %, respectively

Effect

J Nanopart Res (2013) 15:1896 Page 15 of 26

123

Page 16 of 26

J Nanopart Res (2013) 15:1896

AgNP-Laden Plant-Entry to Food Chain

AgNPs-ShootBiological Compounds Interaction

AgNPsPhytotoxicity Extent Modulation

AgNPs-Plant Uptake/Accu mulationModulation AgNPs-Rhizosphere Microbes Interaction AgNPs Mobility/Bioa vailability Modulation AIR

AIR Soil Physico-Chemical Characteristics-Mediated Control of AgNPs Agglomeration and/or Transformation NON-POINT SOURCES

POINT SOURCES Environmental Factors Influence During the AgNPs Transport to Soil Intentional Release

Accidental Release

Fig. 3 Schematic illustration of silver nanoparticles (AgNPs)interaction with ‘‘soil–plant systems’’ highlighting the major pathways of AgNP-entry to the soil system, role of soil physicochemical characteristics in the control of AgNPs mobility/ bioavailability modulation, and their subsequent influence on

the extent of plant AgNPs-uptake/accumulation and toxicity. In addition, AgNP-laden plant-mediated potential food chaincontamination has also been highlighted. (Based on the available literature including Nowack and Bucheli 2007). See text for details

caused aggregation and agglomeration of AgNPs. O. sativa shoots exhibited their higher susceptibility towards AgNPs when compared to roots. Though AgNPs treatment up to 30 lg mL-1 accelerated root growth AgNPs at 60 lg mL-1 was able to restrict a root’s ability to grow. Moreover, AgNPs treatment led to an alteration of root branching systems, where the branched root systems were enhanced through the treatment of 60 lg mL-1 of AgNPs. The authors considered this phenotype of a root system as a consequence of a direct or indirect effect of AgNPs. Between the photosynthetic pigments studied namely chlorophyll b and carotenoids, the former was evidenced most susceptible to the highest concentration of AgNPs. It was concluded that under AgNPs exposure, O. sativa might have shifted the allocation of resources (carbohydrate, starch) from shoot to root growth. An

improved seed yield has also been reported with increasing concentration of AgNP from 20 to 60 ppm in Borago officinalis (Seif et al. 2011). It has been demonstrated that Ag? or particles phytotoxicity could differ when soil and agar were used as growth media. In this context, an inhibition of the growth rates of P. radiatus and S. bicolor by 34 and 55 %, respectively, has been reported in agar media; where the majority of adverse effects on S. bicolor were attributed to Ag? (Lee et al. (2012). To the other, the influence of Ag? (2.7 mg Ag? kg-1) was negligible for both plants in soil medium. This study implies that ion can be responsible for the apparent toxicity in agar, while, the apparent toxicity observed in soil can be attributed to particle toxicity. Considering both AgNPs and corresponding bulk counterpart (1,000 mg L-1) in a hydroponic culture experiment

123

J Nanopart Res (2013) 15:1896

with C. pepo, Stampoulis et al. (2009) reported no impact on seed germination. However, during a 15-day hydroponic trial, the biomass of AgNPsexposed C. pepo plants reduced by 75 %, respectively, as compared to control plants and corresponding bulk Ag powder solution. AgNPs concentrations namely 500 and 100 mg L-1 resulted in 57 and 41 % decreases in plant biomass and transpiration, respectively, as compared to controls or to plants exposed to bulk Ag. The authors concluded that half the observed phytotoxicity is from the elemental NPs themselves and that germination and root elongation may not be sensitive enough or appropriate when evaluating nanoparticle toxicity to terrestrial plant species. AgNPs of varying size rage (20–80 nm) were reported to be toxic to A. thaliana seedlings where stunted growth even at very low concentration (340 lg L-1) was evidenced (Ma et al. 2010). In addition, the authors observed a continuous decrease in the root biomass and root length with increasing AgNP-concentrations. A completely vacuolated and collapsed the cortical cells have been evidenced in L. multiforum at 40 ppm concentration of 6 nm AgNPs when compared to 25 nm size particles-effect (Yin et al. 2011). Additionally, broken epidermis and root cap were also noted by these authors in L. multiforum. Though Ag is known to be one of the most toxic trace metals (Ratte 1999) the mechanism involved in Ag- and AgNPtoxicity may differ. In this context, various experiments carried out with AgNPs and AgNO3 demonstrated that the results obtained were contradictory as nano-form had no impact on plant/seedling growth, whereas the bulk form treatment had retarded the growth of the R. communis exposed to different concentrations of AgNP and AgNO3 (0, 500, 1,000, 2,000, and 4,000 mg L-1) (Yasur and Rani 2013). In contrast, AgNPs at 250 mg L-1 decreased C. pepo plant growth by 49 and 59 % relative to bulk Ag and control treatments, respectively; at 750 mg L-1, the reductions in plant mass were 55 and 64 %, respectively. The presence of 100 mg L-1 humic acid minimized AgNP-phytotoxicity at 250 mg L-1 but at 750 mg L-1, AgNP reduced plant biomass by 70 % (Hawthorne et al. 2012). Moreover, 500 mg L-1 AgNPs reduced C. pepo biomass and transpiration by 66–84 % when compared with bulk Ag (Musante and White 2012). AgNPs were reported to retard root elongation in C. pepo seeds higher than the

Page 17 of 26

corresponding bulk form at 1,000 mg L-1 (Stampoulis et al. 2009). AgNP-concentrations depended elevated toxicity (measured in terms of root length and germination) has been reported in L. esculentum and Z. mays which was found higher than the toxicity caused by its equivalent Ag? concentration (Ravindran et al. 2012). However, the root elongation values in L. esculentum and Z. mays treated with 1 % bovine serum albumin, BSA ? AgNP (20 mg L-1) were reported similar those seedlings in control. The coating of BSA on the surface of the AgNP may result in a controlled release of the ions, thereby modulating the toxic effects of the AgNP (Ravindran et al. 2010, 2012). Using pollen culture as a model system for AgNP-toxicity assessment in Actinidia deliciosa var. deliciosa [(A. Chev) C.F. Liang et A.R. Ferguson], Speranza et al. (2013) for the first time demonstrated that AgNPs were more potent at disrupting pollen tube elongation, while Ag? damaged pollen membranes and inhibited pollen germination to a larger extent. There exists also inconsistency in the toxicity extent in different plant species caused by different AgNPs concentrations. In this context, at one hand, Yasur and Rani (2013) observed no significant toxicity was observed in R. communis up to the highest concentration (4,000 mg AgNP L-1) to the other a reduction in biomass and transpiration by 66–84 % by 500 mg L-1 AgNPs was noted in C. pepo (Musante and White 2012). In this perspective, the significance of the seed coat-thickness was expected to modulate the NPs-penetration into the seedlings (Yasur and Rani 2013). A lack of information on AgNPs potential impact on photosynthesis and its related variables is perceptible in the literature. To this end, growth in terms of fresh weight, root and shoot length, and vigor index of seedlings has been reported positively affected by AgNPs concentrations (0, 25, 50, 100, 200, and 400 ppm) in B. juncea (Sharma et al. 2012). The authors noted AgNPs-mediated increase of 326 % in root length and 133 % in vigor index. Since biochemical responses of organisms to environmental stresses are regarded as early warning signs of pollution in the environment (Anjum et al. 2010, 2012a, b, 2013; Gill and Tuteja 2010; Hu et al. 2012; Gill et al. 2013), the following sections deal with the recent information available on the AgNPs-mediated cellular-genotoxicity and also oxidative stress and its metabolism.

123

Page 18 of 26

Cellular- and geno-toxicity Since plants systems have a variety of well-defined genetic endpoints including alterations in ploidy, chromosomal aberrations, and sister chromatid exchanges, they have been used as indicator organisms, in a wide range of studies including on mutagenesis in higher eukaryotes (Kumari et al. 2009). In the current context, varied NPs owing to their size can enter freely into the cells and can interfere in cell’s normal function. Though there are a significant number of studies on the genotoxicity and cytotoxicity of AgNPs on mammalian and human cell lines (Ghosh et al. 2012) only a few reports on AgNPsaccrued cyto-genotoxicity in plant systems are available in the literature (Babu et al. 2008; Kumari et al. 2009; Ghosh et al. 2012; Patlolla et al. 2012). Nevertheless, a paucity of knowledge pertaining to the genotoxicity or DNA-damaging potential of AgNP in terrestrial plants still exists in the available literature. In Allium cepa root meristems exposed to AgNPs concentrations (10, 20, 40, and 50 ppm; for 0.5, 1, 2, and 4 h), Babu et al. (2008) reported AgNPs concentrations and time intervals dependent increase in the frequency of chromosomal aberrations and decrease in mitotic index. In addition, the authors noted various types of chromosomal and mitotic abnormalities such as fragments, C-metaphase, stickiness, laggard, anaphasic bridge, and disturbed anaphase. In Vicia faba root tip cells, AgNPs exposure significantly increased the number of chromosomal aberrations, micronuclei, and decreased the mitotic index (Patlolla et al. 2012). The induction of chromosomal breaks and micronuclei by AgNPs has also been earlier reported in V. faba root tips (Raun and Lilum 1992). A sharp decrease in mitotic index (from 60.30 to 27.62 %) has been evidenced in A. cepa root tip cells exposed to AgNPconcentrations (25, 20, 75, and 100 ppm) (below 100 nm size) (Kumari et al. 2009). The authors inferred that AgNPs penetration into plant system lead to cell division arrest at metaphase and caused chromatin-bridge, stickiness, disturbed metaphase, multiple chromosomal breaks, and cell disintegration. AgNPs also impaired cell division and caused cell disintegration in A. cepa root tips (Kumari et al. 2009; Stampoulis et al. 2009; Nair et al. 2010). Using A. cepa and N. tabacum as model plant systems, Ghosh et al. (2012) employed a genotoxic and cytotoxic approach to elucidate the activity of AgNPs (0, 25, 50, and

123

J Nanopart Res (2013) 15:1896

75 lg mL-1; for 24 h) in vitro and in vivo where the authors observed a more pronounced AgNP-genotoxic effect in root than shoot/leaf of the plants and also a good correlation between the in vitro and in vivo AgNPs’ effects. Kuriyama and Sakai (1974) reported the ineffective mitotic spindle function as a result of AgNPs interaction with tubulin-SH group. AgNPs possess mitodepressive, mitoclassic, and clastogenic properties (Tanti et al. 2012). To this end, an increase in the frequency of chromosomal abnormalities such as fragments, C-metaphase, stickiness, laggard, anaphasic bridge, chromosome divergence, spiral chromosome, micronuclei, nuclear disintegration, polyploidy, distortion of pole and unequal nuclear distribution and decrease in mitotic index with increase in AgNP-concentrations (25, 50, 75, and 100 ppm; for 6, 12, 18, and 24 h) were observed in A. sativum (Tanti et al. 2012). Oxidative stress and its metabolism An imbalance between the generation of reactive oxygen species (ROS) and its antioxidant defense components-mediated scavenging causes oxidative  stress. ROS such as O2 , OH , and H2O2 are strong oxidizing agents and cause oxidative damage to biomolecules such as proteins and lipids that weakens membrane integrity and elevate electrolyte leakage, and eventually cause cell death. Hence, equilibrium between the production and elimination of ROS must be maintained in cells if metabolic disorder or oxidative burst is to be avoided (Gill and Tuteja 2010; Anjum et al. 2012a, b; Gill et al. 2013). However, despite the clearly known significance of ascorbate–glutathione pathway for the alleviation of oxidative stress in different plant species under metal– metalloids (Anjum et al. 2010, 2012a, b; Gill and Tuteja 2010; Gill et al. 2013), other NPs such as graphene oxide (Anjum et al. 2013), cerium oxide (Rico et al. 2013), and copper oxide (Shaw and Hossain 2013), the current literature search reflects a clear paucity of information on this aspect in AgNPsexposed plant species. Nevertheless, alterations in antioxidant defense components have recently been considered as useful biomarkers in ecotoxicological tests with AgNPs. Moreover, such data can be valuable in providing information for monitoring and forecasting early effects of exposure to AgNPs in different scenarios (Yasur and Rani 2013). However,

J Nanopart Res (2013) 15:1896

AgNPs-toxicity studies in plants in context with oxidative stress and its metabolism have been least explored. Elevated generation of ROS has been reported in O. sativa plant species under AgNPs exposure (Mirzajani et al. 2013). However, there is no or little information available on the adaptation of strategies by NPs and/or AgNPs-exposed plant for the metabolism of ROS and its reaction products. As reported also by Mirzajani et al. (2013) in AgNPsexposed O. sativa plants, the induction of antioxidant activity by elevated carotenoids levels has earlier been confirmed to potentially reduce the toxic effects of ROS and its reaction products (Chew and Park 2004; He et al. 2011). Compared to AgNPs, a higher degree of induced oxidative stress due to higher generation of O2 and H2O2 was reported in A. cepa root tips under AgNP-exposure (Panda et al. 2011). The significance of some other factors was expected in the modulation of ROS-mediated AgNP-toxicity in nitrifying bacteria (Choi and Hu 2008). In contrast, in an effort to test the phytotoxicity potential of the biologically synthesized AgNPs in B. monnieri, Krishnaraj et al. (2012) reported a mild stress where lower elevations in CAT and POX activities reflected the better B. monnieri growth with reduced toxicity compared to the AgNO3-treated plants. Since AgNPs application is widely used to control several plant diseases (Park et al. 2006), Krishnaraj et al. (2012) speculated that the mild stress due to biologically synthesized AgNPs may be beneficial to plants in protecting them against pathogen attacks and disease control and mandates further study in the future. An elevated activities of superoxide dismutase (SOD) and peroxidase have been reported in R. communis exposed to AgNP and AgNO3 (0, 500, 1,000, 2,000, and 4,000 mg L-1) (Yasur and Rani 2013). The authors concluded that the enhanced peroxidase and SOD activities are indicative of the AgNPs-accrued increased oxidative stress where AgNPs might have interacted with cellular components and have caused the elevation in ROS formation. The significance of phenols and phenolic acids in the protection of Ag? and AgNPs-mediated oxidative stress has been evidenced (Winkel-Shirley 2002; Krishnaraj et al. 2012; Yasur and Rani 2013). Ag (both micro and macro forms)-mediated enhanced accumulation of the phenolics (aromatic benzene ring compounds with one or more hydroxyl groups) was reported in R. communis where AgNP treatments recorded lesser phenol content than the plants treated

Page 19 of 26

with AgNO3. The occurrence of oxidative stress in the AgNPs-varying concentrations (0–5 mg kg-1 sand)exposed T. aestivum roots was assessed by measuring levels of oxidized glutathione (GSSG) (Dimkpa et al. 2013), where AgNPs exposure caused enhanced GSSG accumulation and also induced expression of a gene encoding a metallothionein involved in detoxification by metal ion sequestration. On the brighter side of AgNPs, since: (a) AgNPs exhibit their ability to support electron exchange with Fe2? and Co? 3 (the two elements that participate in several biological redox reactions) (Mukherjee and Mahapatra 2009) and AgNP clusters show efficient catalytic activity in redox reactions by acting as electron relay centers, behaving alternatively as an acceptor and donor of electrons (Mallick et al. 2006), AgNPs have been considered among most potential candidates for modulating the redox status of plants (Sharma et al. 2012). However, a little attention has been paid to the possibility that AgNPs can possibly help improve plant’s redox status and growth. To this end, using B. juncea, Sharma et al. (2012) attempted to elucidate the role of AgNP-concentrations (0, 25, 50, 100, 200, and 400 ppm) in plant growth promotion under specified conditions. The authors noted significantly decreased levels of the two widely used oxidative stress biomarkers namely malondialdehyde (membrane lipid peroxidation) and hydrogen peroxide at 25, 50, and 400 ppm AgNPs when compared to the controls. These responses were accompanied by significant and parallel increase in the activity of guaiacol peroxidase (GPX; a known H2O2 metabolizing enzyme; Anjum et al. 2010, 2012a, b, 2013; Gill and Tuteja 2010; Gill et al. 2013) and the drastic decrease in the level of free proline (an excellent index of the existing stress experienced by the plant; Szabados and Savoure 2010) which the authors considered to be responsible for improving the antioxidant status and subsequently the growth of AgNPsexposed B. juncea.

Conclusions and perspectives A clear imbalance between the rapid application of AgNPs in multiple disciplines and the safety/toxicity aspects of AgNPs in biotic systems is perceptible in the available literature. Since metal-based NPs have dual-toxicity of metal and NPs, their bi-toxicity and

123

Page 20 of 26

ecological risk are the hotspots in the studies of nanotoxicology. In particular, due to their bactericidal and viricidal properties, AgNPs have been synthesized and widely applied and get accumulated in soil–plant systems; hence, warrants a detail toxicological investigation to justify its safety. The effects of engineered AgNPs on soil–plant systems are of great concern because of their crucial interface with the environment. However, it is clearly perceptible from the literature surveyed in the current paper that the knowledge on the AgNP-chemistry modulation in soils and its significance in AgNPs and Ag/Ag? bioavailability and bio-accessibility to and subsequent impact on soil biota in general and to plants in particular is still in its infancy. The majority of reports available on AgNPs interaction with soil (and/or soil microbial community) and plants evidenced AgNP’s negative effects. Additionally, there is still a dearth information on: the potential mechanisms underlying AgNP-uptake and AgNP-phytotoxicity remain largely unknown, potential transmission of seed-harbored AgNPs to next plant generation and their subsequent fate within food chains is available. Because plants are essential base component of ecosystem; as it is true with metals–metalloids, plants may acts as a potential pathway for AgNPs bioaccumulation and entering into food chain. However, limited phytotoxicity studies reported both positive and negative effects of AgNPs on higher plants. The available AgNP-phytotoxicity studies have revealed that AgNPs may enter the plant system and disturb the growth and physiology/biochemistry of plants by impairing mitosis causing chromosomal abnormalities and micronuclei. The question/concern pertaining to the AgNPs biotransformation in food crops—in particular—possible AgNPs-transmission to the next generation of AgNPs-exposed plants remains wide-open unanswered. The uptake mechanisms and distribution of AgNPs in cells are still insufficiently explored, and very few studies have addressed this question. In particular, future plant toxicological research should intensify the inclusion of different plant types while evaluating the overall toxicological impact of the rapidly mounting AgNPs in the environment. As it has widely been established in different plants under metal–metalloids exposure, the significance of ascorbate–glutathione pathway components in the protection of plants under AgNPs exposure against AgNP-accrued oxidative stress, however, are so far

123

J Nanopart Res (2013) 15:1896

scarcely investigated. Molecular-genetic mechanisms underlying AgNP-uptake across the plant cell membrane, generation of reactive oxygen species, the activation of redox-sensitive signaling cascades, and the major cell organelle-specific responses to AgNPs should be explored. Hence, a multi-level standard biomarkers approach must be considered in order to get better insights into the AgNPs potential to cause toxicity at cytological, genetic physiological/biochemical levels. It would also be imperative to determine a relatively inexpensive and commonly used short-term plant assay for in situ evaluation of the potential bio-hazards of AgNPs in the environment. Together, this approach would help understanding the underlying AgNP-toxicity mechanisms, interpreting molecular-genetic, and/or physiological/biochemical data; which subsequently will complement current toxicological screening strategies with a mechanismbased approach. The interaction of AgNPs with other persistent pollutants occurring at the same time should be considered because these pollutants can both amplify as well as alleviate the AgNP-toxicity. The determination of AgNP’s potential transformation in complex matrices of varied environmental compartments including soil and also in biotic systems should be worked out. Specific information on AgNP’s aging, redox chemistry, and their light-driven transformations, including the creation of reactive sites by photochemical pathways may yield important clues on AgNP-environment interaction. Hence, in addition to performing studies in laboratory settings, the consideration of the ‘‘environmental AgNPs exposure’’ will of great interest in order to further our understanding of AgNP-fate and AgNP-impact in terrestrial environments. Most importantly, the most of the reports discussed herein have considered germination and/or seedlings stage as the AgNPpotential toxicity test system; which may not be sensitive enough or appropriate for deciphering the full picture of the ‘‘AgNP and/or its bulk counterpart (Ag)-plants interaction’’ outcome. In contrast, toxicity indicators based on biological markers, plant defense mechanism, changes in plant integrity at cellular, or genetic levels tested periodically during the plant’s life cycle should be considered which were confirmed earlier more appropriate in the current context. The inclusion of a multidisciplinary integrated approach is strongly recommended for future research in the current direction aimed at unveiling quantitatively

J Nanopart Res (2013) 15:1896

and qualitatively the fate, transformation, accumulation and toxicity potential of rapidly mounting AgNPs-in ‘‘soil–plant systems,’’ and their cumulative impact on environmental and human health. Acknowledgments NAA (SFRH/BPD/84671/2012), ACD, EP, and IA are grateful to the Portuguese Foundation for Science and Technology (FCT) and the Aveiro University Research Institute/Centre for Environmental and Marine Studies (CESAM) for partial financial supports. SSG would like to acknowledge the receipt of funds from CSIR and UGC, Govt. of India, New Delhi. Authors apologize if some references related to the main theme of the current review could not be cited due to space constraint.

References Abraham PM, Barnikol S, Baumann T, Kuehn M, Ivleva NP, Schaumann GE (2013) Sorption of silver nanoparticles to environmental and model surfaces. Environ Sci Technol 47:5083–5091 Ahmed F, Arshi N, Kumar S, Gill SS, Gill R, Tuteja N, Koo BH (2013) Nanobiotechnology: scope and potential for crop improvement. In: Tuteja N, Gill SS (eds) Crop improvement under adverse conditions. Springer, New York, pp 245–269 Anjum NA, Umar S, Chan MT (eds) (2010) Ascorbate-glutathione pathway and stress tolerance in plants. Springer, Dordrecht Anjum NA, Ahmad I, Mohmood I, Pacheco M, Duarte AC, Pereira E, Umar S, Ahmad A, Khan NA, Iqbal M, Prasad MNV (2012a) Modulation of glutathione and its related enzymes in plants’ responses to toxic metals and metalloids—a review. Environ Exp Bot 75:307–324 Anjum NA, Umar S, Ahmad A (2012b) Oxidative stress in plants: causes, consequences and tolerance. IK International Publishing House, New Delhi Anjum NA, Singh N, Singh MK, Shah ZA, Duarte AC, Pereira E, Ahmad I (2013) Single-bilayer graphene oxide sheet tolerance and glutathione redox system significance assessment in faba bean (Vicia faba L.). J Nanopart Res 15:1770 Arnaout CL, Gunsch CK (2012) Impacts of silver nanoparticle coating on the nitrification potential of Nitrosomonas europaea. Environ Sci Technol 46:5387–5395 Babu K, Deepa M, Shankar S, Rai S (2008) Effect of nano-silver on cell division and mitotic chromosomes: a prefatory siren. Internet J Nanotechnol 2:2 Bae S, Hwang YS, Lee Y-J, Lee S-K (2013) Effects of water chemistry on aggregation and soil adsorption of silver nanoparticles. Environ Health Toxicol 28:1–7 Barrena R, Casals E, Colo´n J, Font X, Sa´nchez A, Puntes V (2009) Evaluation of the ecotoxicity of model nanoparticles. Chemosphere 75:850–857 Bell RA, Kramer JR (1999) Structural chemistry and geochemistry of silver–sulfur compounds: critical review. Environ Toxicol Chem 18:9–22

Page 21 of 26 Benn TM, Westerhoff P (2008) Nanoparticle silver released into water from commercially available sock fabrics. Environ Sci Technol 42:4133–4139 Benn T, Cavanagh B, Hristovski K, Posner JD, Westerhoff P (2010) The release of nanosilver from consumer products used in the home. J Environ Qual 39:1875–1882 Benoit R, Wilkinson KJ, Sauve´ S (2013) Partitioning of silver and chemical speciation of free Ag in soils amended with nanoparticles. Chem Cent J 7:75 Bernhardt ES, Colman BP, Hochella MF, Cardinale BJ, Nisbet RM, Richardson CJ, Yin LY (2010) An ecological perspective on nanomaterial impacts in the environment. J Environ Qual 39:1954–1965 Bhaduri GA, Little R, Khomane RB, Lokhande SU, Kulkarni BD, Mendis BG, Sˇiller L (2013) Green synthesis of silver nanoparticles using sunlight. J Photochem Photobiol A Chem 258:1–9 Blaser SA, Scheringer M, MacLeod M, Hungerbuhler K (2008) Estimation of cumulative aquatic exposure and risk due to silver: contribution of nanofunctionalized plastics and textiles. Sci Total Environ 390:396–409 Boxall AB, Tiede K, Chaudhry Q (2007) Engineered nanomaterials in soils and water: how do they behave and could they pose a risk to human health? Nanomedicine 2:919–927 Boxall ABA, Chaudhry Q, Jones A, Jefferson B, Watts CD (2008) Current and future predicted environmental exposure to engineered nanoparticles. Central Science Laboratory, Sand Hutton Bradford A, Handy RD, Readman JW, Atfield A, Muhling M (2009) Impact of silver nanoparticle contamination on the genetic diversity of natural bacterial assemblages in estuarine sediments. Environ Sci Technol 43:4530–4536 Bystrzejewska-Piotrowska G, Golimowski J, Urban PL (2009) Nanoparticles: their potential toxicity, waste and environmental management. Waste Manag 29:2587–2595 Calder AJ, Dimkpa CO, McLean JE, Britt DW, Johnson W, Anderson AJ (2012) Soil components mitigate the antimicrobial effects of silver nanoparticles towards a beneficial soil bacterium, Pseudomonas chlororaphis O6. Sci Total Environ 429:215–222 Chen X, Schluesener HJ (2008) Nanosilver: a nanoproduct in medical applications. Toxicol Lett 176:1–12 Chew BP, Park JS (2004) Carotenoid action on the immune response. J Nutr 134:257S–261S Cho SM, Kang BR, Han SH, Anderson AJ, Park J-Y, Lee Y-H, Cho BH, Yang K-Y, Ryu C-M, Kim YC (2008) 2R, 3Rbutanediol, a bacterial volatile produced by Pseudomonas chlororaphis O6, is involved in induction of systemic tolerance to drought in Arabidopsis thaliana. Mol Plant Microbe Interact 21:1067–1075 Choi O, Hu Z (2008) Size dependent and reactive oxygen species related nanosilver toxicity to nitrifying bacteria. Environ Sci Technol 42:4583–4588 Choi OK, Hu ZQ (2009) Nitrification inhibition by silver nanoparticles. Water Sci Technol 59:1699–1702 Christian P, Von der Kammer F, Baalousha M, Hofmann T (2008) Nanoparticles: structure, properties, preparation and behaviour in environmental media. Ecotoxicology 17:326–343

123

Page 22 of 26 Colman BP, Wang SY, Auffan M, Wiesner MR, Bernhardt ES (2012) Antimicrobial effects of commercial silver nanoparticles are attenuated in natural stream water and sediment. Ecotoxicology 21:1867–1877 Cornelis G, Kirby JK, Beak D, Chittleborough D, McLaughlin MJ (2010) A method for determination of retention of silver and cerium oxide manufactured nanoparticles in soils. Environ Chem 7:298–308 Cornelis G, Doolette C, Thomas M, McLaughlin MJ, Kirby JK, Beak DG, Chittleborough D (2012) Retention and dissolution of engineered silver nanoparticles in natural soils. Soil Sci Soc Am J 76:891–902 Coutris C, Hertel-Aas T, Lapied E, Joner EJ, Oughton DH (2012a) Bioavailability of cobalt and silver nanoparticles to the earthworm Eisenia fetida. Nanotoxicology 6:186–195 Coutris C, Joner EJ, Oughton DH (2012b) Aging and soil organic matter content affect the fate of silver nanoparticles in soil. Sci Total Environ 420:327–333 Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–173 De La Torre-Roche R, Hawthorne J, Musante C, Xing B, Newman LA, Ma X, White JC (2013) Impact of Ag nanoparticle exposure on p,p0 -DDE bioaccumulation by Cucurbita pepo (Zucchini) and Glycine max (Soybean). Environ Sci Technol 47:718–725 Dietz JK, Herth S (2011) Plant nanotoxicology. Trends Plant Sci 16:582–589 Dimkpa CO, McLean JE, Martineau N, Britt DW, Haverkamp R, Anderson AJ (2013) Silver nanoparticles disrupt wheat (Triticum aestivum L.) growth in a sand matrix. Environ Sci Technol 47:1082–1090 El-Badawy AME, Luxton TP, Silva RG, Scheckel KG, Suidan MT, Tolaymat TM (2010) Impact of environmental conditions (pH, ionic strength, and electrolyte type) on the surface charge and aggregation of silver nanoparticles suspensions. Environ Sci Technol 44:1260–1266 El-Temsah YS, Joner EJ (2012) Impact of Fe and Ag nanoparticles on seed germination and differences in bioavailability during exposure in aqueous suspension and soil. Environ Toxicol 27:42–49 Elzey S, Grassian VH (2010) Agglomeration, isolation and dissolution of commercially manufactured silver nanoparticles in aqueous environments. J Nanopart Res 12:1945–1958 Fabrega J, Fawcett SR, Renshaw JC, Lead JR (2009a) Silver nanoparticle impact on bacterial growth: effect of pH, concentration, and organic matter. Environ Sci Technol 43:7285–7290 Fabrega J, Renshaw JC, Lead JR (2009b) Interactions of silver nanoparticles with Pseudomonas putida biofilms. Environ Sci Technol 43:9004–9009 Fabrega J, Luoma SN, Tyler CR, Galloway TS, Lead JR (2011) Silver nanoparticles: behaviour and effects in the aquatic environment. Environ Int 37:517–531 Fortin C, Campbell PGC (2001) Thiosulfate enhances silver uptake by a green alga: role of anion transporters in metal uptake. Environ Sci Technol 35:2214–2218 Frattini A, Pellegri N, Nicastro D, Sanctis OD (2005) Effect of amine groups in the synthesis of Ag nanoparticles using aminosilanes. Mater Chem Phys 94:148–152

123

J Nanopart Res (2013) 15:1896 Geisler-Lee J, Wang Q, Yao Y, Zhang W, Geisler M, Li K, Huang Y, Chen Y, Kolmakov A, Ma X (2013) Phytotoxicity, accumulation and transport of silver nanoparticles by Arabidopsis thaliana. Nanotoxicology 3:323–337 Geranio L, Heuberger M, Nowack B (2009) The behavior of silver nanotextiles during washing. Environ Sci Technol 43:8113–8118 Gerloff K, Fenoglio I, Carella E, Kolling J, Albrecht C, Boots AW, Fo¨rster I, Schins RP (2012) Distinctive toxicity of TiO2 rutile/anatase mixed phase nanoparticles on Caco-2 cells. Chem Res Toxicol 25:646–655 Ghosh JM, Sinha S, Chakraborty A, Mallick SK, Bandyopadhyay M, Mukherjee A (2012) In vitro and in vivo genotoxicity of silver nanoparticles. Mutation Res 749:60–69 Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930 Gill SS, Anjum NA, Hasanuzzaman M, Gill R, Trivedi DK, Ahmad I, Pereira E, Tuteja N (2013) Glutathione and glutathione reductase: a boon in disguise for plant abiotic stress defense operations. Plant Physiol Biochem 70:204–212 Glover RD, Miller JM, Hutchison JE (2011) Generation of metal nanoparticles from silver and copper objects: nanoparticle dynamics on surfaces and potential sources of nanoparticles in the environment. ACS Nano 5:8950–8957 Golovina NB, Kustov LM (2013) Toxicity of metal nanoparticles with a focus on silver. Mendeleev Commun 23:59–65 Golubeva O, Shamova O, Orlov D, Pazina T, Boldina A, Kokryakov V (2010) Study of antimicrobial and hemolytic activities of silver nanoparticles prepared by chemical reduction. Glass Phys Chem 36:628–634 Gondikas AP, Morris A, Reinsch BC, Marinakos SM, Lowry GV, Hsu-Kim H (2012) Cysteine-induced modifications of zero-valent silver nanomaterials: implications for particle surface chemistry, aggregation, dissolution, and silver speciation. Environ Sci Technol 46:7037–7045 Gottschalk F, Sonderer T, Scholz RW, Nowack B (2009) Modeled environmental concentrations of engineered nanomaterials (TiO2, ZnO, Ag, CNT, fullerenes) for different regions. Environ Sci Technol 43:9216–9222 Hadioui M, Leclerc S, Wilkinson K (2013) Multimethod quantification of Ag? release from nanosilver. Talanta 105:15–19 Handy RD, Owen R, Valsami-Jones E (2008) The ecotoxicology of nanoparticles and nanomaterials: current status, knowledge gaps, challenges, and future needs. Ecotoxicology 17:315–325 Harris A, Bali R (2008) On the formation and extent of uptake of silver nanoparticles by live plants. J Nanopart Res 10:691–695 Haverkamp RG, Marshall AT (2009) The mechanism of metal nanoparticle formation in plants: limits on accumulation. J Nanopart Res 11:1453–1463 Hawthorne J, Musante C, Sinha SK, White JC (2012) Accumulation and phytotoxicity of engineered nanoparticles to Cucurbita pepo. Int J Phytoremediation 14:429–442 He D, Jones AM, Garg S, Pham AN, Waite TD (2011) Silver nanoparticle–reactive oxygen species interactions: application of a charging–discharging model. J Phys Chem C 115:5461–5468

J Nanopart Res (2013) 15:1896 Hendren CO, Mesnard X, Dro¨ge J, Wiesner MR (2011) Estimating production data for five engineered nanomaterials as a basis for exposure assessment. Environ Sci Technol 45:2562–2569 http://nano.foe.org.au/node/190. Accessed 02 July 2013 http://water.usgs.gov/wrri/08grants/2008IN251B.html. Accessed 02 July 2013 http://www.nanotechproject.org/inventories/consumer/analysis_ draft. Accessed 02 July 2013 Hu C, Li M, Wang W, Cui Y, Chen J, Yang L (2012) Ecotoxicity of silver nanoparticles on earthworm Eisenia fetida: responses of the antioxidant system, acid phosphatase and ATPase. Toxicol Environ Chem 94:732–741 Jacobson AR, McBride MB, Baveye P, Steenhuis TS (2005) Environmental factors determining the trace-level sorption of silver and thallium to soils. Sci Total Environ 345: 191–205 Jana D, Mandal A, De G (2012) High Raman enhancing shapetunable Ag nanoplates in alumina: a reliable and efficient SERS technique. ACS Appl Mater Interfaces 4:3330–3334 Jin X, Li M, Wang J, Marambio-Jones C, Peng F, Huang X, Damoiseaux R, Hoek EMV (2010) High-throughput screening of silver nanoparticle stability and bacterial inactivation in aquatic media: influence of specific ions. Environ Sci Technol 44:7321–7328 Jo YK, Kim BH, Jung G (2009) Antifungal activity of silver ions and nanoparticles on phytopathogenic fungi. Plant Dis 93:1037–1043 Johnson AC, Bowes MJ, Crossley A, Jarvie HP, Jurkschat K, Ju¨rgens MD, Lawlor AJ, Park B, Rowland P, Spurgeon D, Svendsen C, Thompson IP, Barnes RJ, Williams RJ, Xu N (2011) An assessment of the fate, behaviour and environmental risk associated with sunscreen TiO2 nanoparticles in UK field scenarios. Sci Total Environ 409:2503–2510 Jones KC, Peterson PJ (1986) The influence of humic and fulvicacids on silver uptake by perennial ryegrass, and its relevance to the cycling of silver in soils. Plant Soil 95:3–8 Keller A, McFerran S, Lazareva A, Suh S (2013) Global life cycle releases of engineered nanomaterials. J Nanopart Res 15:1–17 Khan M, Khan M, Adil SF, Tahir MN, Tremel W, Alkhathlan HZ, Al-Warthan A, Siddiqui MRH (2013) Green synthesis of silver nanoparticles mediated by Pulicaria glutinosa extract. Int J Nanomed 8:1507–1516 Khaydarov RA, Estrin Y, Evgrafova S, Scheper T, Endres C, Cho SY (2009) Silver nanoparticles: environmental and human health impacts. In: Linkov I, Steevens J (eds) Nanomaterials: risks and benefits. Springer, Dordrecht, pp 287–297 Kim JS, Kuk E, Yu KN, Kim J-H, Park SJ, Lee HJ, Kim SH, Park YK, Park YH, Hwang C-Y (2007) Antimicrobial effects of silver nanoparticles. Nanomed Nanotechnol Biol Med 3:95–101 Kim YS, Kim JS, Cho HS, Rha DS, Kim JM, Park JD, Choi BS, Lim R, Chang HK, Chung YH, Kwon IH, Jeong J, Han HS, Yu IJ (2008) Twenty-eight day oral toxicity, genotoxicity, and gender-related tissue distribution of silver nanoparticles in Spraque–Dawley rats. Inhal Toxicol 20:575–583 Kim B, Park C-S, Murayama M, Hochella MF (2010) Discovery and characterization of silver sulfide nanoparticles in final

Page 23 of 26 sewage sludge products. Environ Sci Technol 44:7 509–7514 Kim RS, Zhu J, Park JH, Li L, Yu Z, Shen H, Xue M, Wang KL, Park G, Anderson TJ (2012) E-beam deposited Ag-nanoparticles plasmonic organic solar cell and its absorption enhancement analysis using FDTD-based cylindrical nanoparticle optical model. Opt Express 20:12649–12657 Klaine SJ, Alvarez PJJ, Batley GE, Fernandes TF, Handy RD, Lyon DY, Mahendra S, McLaughlin MJ, Lead JR (2008) Nanomaterials in the environment: behavior, fate, bioavailability and effects. Environ Toxicol Chem 27: 1825–1851 Kokina I, Gerbreders V, Sledevskis E, Bulanovs A (2013) Penetration of nanoparticles in flax (Linum usitatissimum L.) calli and regenerants. J Biotechnol 165:127–132 Krishnaraj C, Jagan G, Ramachandran R, Abirami SM, Mohan N, Kalaichelvan PT (2012) Effect of biologically synthesized silver nanoparticles on Bacopa monnieri L. Wettst. plant growth metabolism. Process Biochem 47:651–658 Kulthong K, Srisung S, Boonpavanitchakul K, Kangwansupamonkon W, Maniratanachote R (2010) Determination of silver nanoparticle release from antibacterial fabrics into artificial sweat. Part Fibre Toxicol 7:8 Kumar N, Shah V, Walker VK (2011) Perturbation of an arctic soil microbial community by metal nanoparticles. J Hazard Mater 190:816–822 Kumari M, Mukherjee A, Chandrasekaran N (2009) Genotoxicity of silver nanoparticles in Allium cepa. Sci Total Environ 407:5243–5246 Kuriyama R, Sakai H (1974) Role of tubulin-SH group in polymerization to microtubules. J Biochem 76:651–654 Lanje AS, Sharma SJ, Pode RB (2010) Synthesis of silver nanoparticles: a safer alternative to conventional antimicrobial and antibacterial agents. J Chem Pharm Res 2: 478–483 Lee HY, Park HK, Lee YM, Kim K, Park SB (2007) A practical procedure for producing silver nanocoated fabric and its antibacterial evaluation for biomedical applications. Chem Commun (Camb) 28:2959–2961 Lee W-M, Kwak JI, An Y-J (2012) Effect of silver nanoparticles in crop plants Phaseolus radiatus and Sorghum bicolor: media effect on phytotoxicity. Chemosphere 86:491–499 Levard C, Reinsch BC, Michel FM, Oumahi C, Lowry GV, Brown GEJ (2011) Sulfidation processes of PVP-coated silver nanoparticles in aqueous solution: impact on dissolution rate. Environ Sci Technol 45:5260–5266 Levard C, Hotze EM, Lowry GV, Brown GE (2012) Environmental transformations of silver nanoparticles: impact on stability and toxicity. Environ Sci Technol 46:6900–6914 Liang Y, Bradford SA, Simunek J, Vereecken H, Klumpp E (2013) Sensitivity of the transport and retention of stabilized silver nanoparticles to physicochemical factors. Water Res 47:2572–2582 Lin S, Cheng Y, Bobcombe Y, Jones KL, Liu J, Wiesner MR (2011) Deposition of silver nanoparticles in geochemically heterogeneous porous media: predicting affinity from surface composition analysis. Environ Sci Technol 45: 5209–5215 Lin S, Cheng Y, Liu J, Wiesner MR (2012) Polymeric coatings on silver nanoparticles hinder autoaggregation but enhance attachment to uncoated surfaces. Langmuir 28:4178–4186

123

Page 24 of 26 Liu JY, Hurt RH (2010) Ion release kinetics and particle persistence in aqueous nano-silver colloids. Environ Sci Technol 44:2169–2175 Liu Y, Laks P, Heiden P (2002) Controlled release of biocides in solid wood. III. Preparation and characterization of surfactant-free nanoparticles. J Appl Polym Sci 86:615–621 Liu JY, Sonshine DA, Shervani S, Hurt RH (2010) Controlled release of biologically active silver from nanosilver surfaces. ACS Nano 4:6903–6913 Lowry GV, Espinasse BP, Badireddy AR, Richardson CJ, Reinsch BC, Bryant LD, Bone AJ, Deonarine A, Chae S, Therezien M (2012) Long-term transformation and fate of manufactured Ag nanoparticles in a simulated large scale freshwater emergent wetland. Environ Sci Technol 46:7027–7036 Luque-Garcia JL, Sanchez-Dı´az R, Lopez-Heras I, Camara C, Martin P (2013) Bioanalytical strategies for in vitro and in vivo evaluation of the toxicity induced by metallic nanoparticles. Trends Anal Chem 43:254–268 Ma X, Geiser-Lee J, Deng Y, Kolmakov A (2010) Interactions between engineered nanoparticles (ENPs) and plants: phytotoxicity, uptake and accumulation. Sci Total Environ 408:3053–3061 Mahna N, Vahed SZ, Khani S (2013) Plant in vitro culture goes nano: nanosilver-mediated decontamination of ex vitro explants. J Nanomed Nanotechnol 4:161 Mallick K, Witcomb M, Scurrell M (2006) Silver nanoparticle catalysed redox reaction: an electron relay effect. Mater Chem Phys 97:283–287 Marambio-Jones C, Hoek EV (2010) A review of the antibacterial effects of silver nanomaterials and potential implications for human health and the environment. J Nanopart Res 12:1531–1551 Mazumdar H, Ahmed G (2011) Phytotoxicity effect of silver nanoparticles on Oryza sativa. Int J ChemTech Res 3:1494–1500 Mirzajani F, Askari H, Hamzelou S, Farzaneh M, Ghassempour A (2013) Effect of silver nanoparticles on Oryza sativa L. and its rhizosphere bacteria. Ecotoxicol Environ Saf 88:48–54 Monica RC, Cremonini R (2009) Nanoparticles and higher plants. Caryologia 62:161–165 Morones JR, Elechiguerra JL, Camacho A, Holt K, Kouri JB, Ramirez JT, Yacaman MJ (2005) The bactericidal effect of silver nanoparticles. Nanotechnology 16:2346–2353 Mueller NC, Nowack B (2008) Exposure modeling of engineered nanoparticles in the environment. Environ Sci Technol 42:4447–4453 Mukherjee M, Mahapatra A (2009) Catalytic effect of silver nanoparticle on electron transfer reaction: reduction of [Co(NH3)5Cl](NO3)2 by iron(II). Colloid Surf A 350:1–7 Musante C, White JC (2012) Toxicity of silver and copper to Cucurbita pepo: differential effects of nano and bulk-size particles. Environ Toxicol 27:510–517 Nair R, Varghese SH, Nair BG, Maekawa T, Yoshiba Y, Kumar DS (2010) Nanoparticulate material delivery to plants. Plant Sci 179:154–163 Navarro E, Baun A, Behra R, Hartmann NB, Filser J, Miao AJ, Quigg A, Santschi PH, Sigg L (2008) Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi. Ecotoxicology 17:372–386

123

J Nanopart Res (2013) 15:1896 Ngomsik AF, Bee A, Draye M, Cote G, Cabuil V (2005) Magnetic nano- and microparticles for metal removal and environmental applications: a review. CR Chim 8:963–970 Nicholson FA, Smith SR, Alloway BJ, Carlton-Smith C, Chambers BJ (2003) An inventory of heavy metals inputs to agricultural soils in England and Wales. Sci Total Environ 311:205–219 NIOSH (1992) Reports and memoranda. NIOSH publication no. 92-100. U.S. Department of Health, Education, and Welfare, Washington, DC Nowack B (2010) Nanosilver revisited downstream. Science 330:1054–1055 Nowack B, Bucheli TD (2007) Occurence, behavior and effects of nanoparticles in the environment. Environ Pollut 150:5–22 Nowack B, Krug HF, Height MJ (2011) 120 years of nanosilver history: implications for policy makers. Environ Sci Technol 45:1177–1183 Oromieh AG (2011) Evaluating solubility, aggregation and sorption of nanosilver particles and silver ions in soils. Master’s Thesis in Environmental Science, Swedish University of Agricultural Sciences, Department of Soil and Environment, Sweden Pal S, Tak YK, Song JM (2007) Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the gram-negative bacterium Escherichia coli. Appl Environ Microbiol 73:1712–1720 Pan B, Xing B (2012) Applications and implications of manufactured nanoparticles in soils: a review. Eur J Soil Sci 63:437–456 Pana´cˇek A, Kola´rˇ M, Vecˇerˇova´ R, Prucek R, Soukupova´ J, Krysˇtof V, Hamal P, Zborˇil R, Kvı´tek L (2009) Antifungal activity of silver nanoparticles against Candida spp. Biomaterials 30:6333–6340 Panda KK, Achary VMM, Krishnaveni R, Padhi BK, Sarangi SN, Sahu SN, Panda BB (2011) In vitro biosynthesis and genotoxicity bioassay of silver nanoparticles using plants. Toxicol In Vitro 25:1097–1105 Panyala NR, Pena-Mendez EM, Havel J (2008) Silver or silver nanoparticles: a hazardous threat to the environment and human health? J Appl Biomed 6:117–129 Park HJ, Kim SH, Kim SJ, Choi SH (2006) A new composition of nanosized silica-silver for control of various plant diseases. Plant Pathol J 22:295–302 Patlolla AK, Berry A, May LB, Tchounwou PB (2012) Genotoxicity of silver nanoparticles in Vicia faba: a pilot study on the environmental monitoring of nanoparticles. Int J Environ Res Public Health 9:1649–1662 Pokhrel LR, Dubey B (2013) Evaluation of developmental responses of two crop plants exposed to silver and zinc oxide nanoparticles. Sci Total Environ 452–453:321–332 Poliakoff M, Fitzpatrick JM, Farren TR, Anastas PT et al (2002) Green chemistry: science and politics of change. Science 297:807 Priester JH, Ge Y, Mielke RE, Horst AM, Moritz SC, Espinosa K, Gelb J, Walker SL, Nisbet RM, An Y-J, Schimel JP, Palmer RG, Hernandez-Viezcas JA, Zhao L, Gardea-Torresdey JL, Holden PA (2012) Soybean susceptibility to manufactured nanomaterials with evidence for food quality and soil fertility interruption. Proc Natl Acad Sci 109:E2451–E2456

J Nanopart Res (2013) 15:1896 Radniecki TS, Stankus DP, Neigh A, Nason JA, Semprini L (2011) Influence of liberated silver from silver nanoparticles on nitrification inhibition of Nitrosomonas europaea. Chemosphere 85:43–49 Rai M, Yadav A, Gade A (2009) Silver nanoparticles as a new generation of antimicrobials. Biotechnol Adv 27:76–83 Rao KJ, Paria S (2013) Green synthesis of silver nanoparticles from aqueous Aegle marmelos leaf extract. Mater Res Bull 48:628–634 Ratte HT (1999) Bioaccumulation and toxicity of silver compounds: a review. Environ Toxicol Chem 18:89–108 Raun C, Lilum J (1992) Application of micronucleus test in Vicia faba root tips in the rapid detection of mutagenic environmental pollutants. Chin J Environ Sci 4:56–58 Ravindran A, Singh A, Raichur AM, Chandrasekaran N, Mukherjee A (2010) Studies on interaction of colloidal Ag nanoparticles with bovine serum albumin (BSA). Colloids Surf B 76:32–37 Ravindran A, Prathna T, Verma VK, Chandrasekaran N, Mukherjee A (2012) Bovine serum albumin mediated decrease in silver nanoparticle phytotoxicity: root elongation and seed germination assay. Toxicol Environ Chem 94:91–98 Reme´dios C, Rosa´rio F, Bastos V (2012) Environmental nanoparticles interactions with plants: morphological, physiological, and genotoxic aspects. J Bot. doi:10.1155/2012/ 751686 Rico CM, Majumdar S, Duarte-Gardea M, Peralta-Videa JR, Gardea-Torresdey JL (2011) Interaction of nanoparticles with edible plants and their possible implications in the food chain. J Agric Food Chem 59:3485–3498 Rico C, Hong J, Morales MI, Zhao L, Barrios AC, Zhang J-Y, Peralta-Videa JR, Gardea-Torresdey JL (2013) Effect of cerium oxide nanoparticles on rice: a study involving the antioxidant defense system and in vivo fluorescence imaging. Environ Sci Technol 47:5635–5642 Ryu C-M, Kang BR, Han SH, Cho SM, Kloepper JW, Anderson AJ, Kim YC (2007) Tobacco cultivars vary in induction of systemic resistance against Cucumber mosaic virus and growth promotion by Pseudomonas chlororaphis O6 and its gacS mutant. Eur J Plant Pathol 119:383–390 Sabo-Attwood T, Unrine JM, Stone JW, Murphy CJ, Ghoshroy S, Blom D, Bertsch PM, Newman LA (2012) Uptake, distribution and toxicity of gold nanoparticles in tobacco (Nicotiana xanthi) seedlings. Nanotoxicology 6:353–360 Sagee O, Dror I, Berkowitz B (2012) Transport of silver nanoparticles (AgNPs) in soil. Chemosphere 88:670–675 Salama HMH (2012) Effects of silver nanoparticles in some crop plants, common bean (Phaseolus vulgaris L.) and corn (Zea mays L.). Int Res J Biotechnol 3:190–197 SCENIHR (2006) The appropriateness of existing methodologies to assess the potential risks associated with engineered and adventitious products of nanotechnologies. Scientific Committee on Emerging and Newly Identified Health Risks (SCENIHR) European Commission, Washington, DC Scheckel KG, Luxton TP, El Badawy AM, Impellitteri CA, Tolaymat TM (2010) Synchrotron speciation of silver and zinc oxide nanoparticles aged in a kaolin suspension. Environ Sci Technol 44:1307–1312 Schluesener JK, Schluesener HJ (2013) Nanosilver: application and novel aspects of toxicology. Arch Toxicol 87:569–576

Page 25 of 26 Seif SM, Sorooshzadeh A, Rezazadehs H, Naghdibadi HA (2011) Effect of nanosilver and silver nitrate on seed yield of borage. J Med Plant Res 5:171–175 SenJen R (2007) Nano silver—a threat to soil, water and human health?. Friends of the Earth Australia, Fitzroy Shahrokh S, Emtiazi G (2009) Toxicity and unusual biological behavior of nanosilver on gram positive and negative bacteria assayed by microtiter-plate. Eur J Biol Sci 1:28–31 Sharma VK, Yngard RA, Lin Y (2009) Silver nanoparticles: green synthesis and their antimicrobial activities. Adv Colloid Interface Sci 145:83–96 Sharma P, Bhatt D, Zaidi M, Saradhi PP, Khanna P, Arora S (2012) Silver nanoparticle-mediated enhancement in growth and antioxidant status of Brassica juncea. Appl Biochem Biotechnol 167:2225–2233 Shaw AK, Hossain Z (2013) Impact of nano-CuO stress on rice (Oryza sativa L.) seedlings. Chemosphere. doi:10.1016/j. chemosphere.2013.05.044 Shin Y-J, Kwak JI, An Y-J (2012) Evidence for the inhibitory effects of silver nanoparticles on the activities of soil exoenzymes. Chemosphere 88:524–529 Shoults-Wilson WA, Reinsch BC, Tsyusko OV, Bertsch PM, Lowry GV, Unrine JM (2011) Role of particle size and soil type in toxicity of silver nanoparticles to earthworms. Soil Sci Soc Am J 75:365–377 Som C, Wick P, Krug H, Nowack B (2011) Environmental and health effects of nanomaterials in nanotextiles and fac¸ade coatings. Environ Int 37:1131–1142 Speranza A, Crinelli R, Scoccianti V, Taddei AR, Iacobucci M, Bhattacharya P, Ke PC (2013) In vitro toxicity of silver nanoparticles to kiwifruit pollen exhibits peculiar traits beyond the cause of silver ion release. Environ Pollut 179:258–267 Stampoulis D, Sinha SK, White JC (2009) Assay-dependent phytotoxicity of nanoparticles to plants. Environ Sci Technol 43:9473–9479 Stensberg MC, Wei QS, McLamore ES, Porterfield DM, Wei A, Sepu´lveda MS (2011) Toxicological studies on silver nanoparticles: challenges and opportunities in assessment, monitoring and imaging. Nanomedicine 6:879–889 Stone V, Nowack B, Baun A, van den Brink N, von der Kammer F, Dusinska M, Handy R, Hankin S, Hassello¨v M, Joner E, Fernandes TF (2010) Nanomaterials for environmental studies: classification, reference material issues, and strategies for physico-chemical characterisation. Sci Total Environ 408:1745–1754 Sun Y, Mayers B, Xia Y (2003) Transformation of silver nanospheres into nanobelts and triangular nanoplates through a thermal process. Nano Lett 3:675–679 Sung JH, Ji JH, Park JD, Yoon JU, Kim DS, Jeon KS, Song MY, Jeong J, Han BS, Han JH, Chung YH, Chang HK, Lee JH, Cho MH, Kelman BJ, Yu IJ (2009) Subchronic inhalation toxicity of silver nanoparticles. Toxicol Sci 108:452–461 Szabados L, Savoure A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97 Tanti B, Das AK, Kakati H, Chowdhury D (2012) Cytotoxic effect of silver-nanoparticles on root meristem of Allium sativum L. J Res Nanobiotechnol 1:1–8 Thakkar KN, Mhatre SS, Parikh RY (2010) Biological synthesis of metallic nanoparticles. Nanomed Nanotechnol Biol Med 6:257–262

123

Page 26 of 26 Theng BKG, Yuan G (2008) Nanoparticles in the soil environment. Elements 4:395–399 Thio BJR, Montes MO, Mahmoud MA, Lee DW, Zhou D, Keller AA (2012) Mobility of capped silver nanoparticles under environmentally relevant conditions. Environ Sci Technol 46:6985–6991 Throba¨ck IN, Johansson M, Rosenquist M, Pell M, Hansson M, Hallin S (2007) Silver (Ag?) reduces denitrification and induces enrichment of novel nirK genotypes in soil. FEMS Microbiol Lett 270:189–194 Tian YA, Gao B, Silvera-Batista C, Ziegler KJ (2010) Transport of engineered nanoparticles in saturated porous media. J Nanopart Res 12:2371–2380 Tolaymat TM, El Badawy AM, Genaidy A, Scheckel KG, Luxton TP, Suidan M (2010) An evidence-based environmental perspective of manufactured silver nanoparticle in syntheses and applications: a systematic review and critical appraisal of peer-reviewed scientific papers. Sci Total Environ 408:999–1006 Tourinho PS, Van Gestel CA, Lofts S, Svendsen C, Soares AM, Loureiro S (2012) Metal-based nanoparticles in soil: fate, behavior, and effects on soil invertebrates. Environ Toxicol Chem 31:1679–1692 Uheida A, Iglesias M, Fonta`s C, Hidalgo M, Salvado´ V, Zhang Y, Muhammed M (2006) Sorption of palladium(II), rhodium(III), and platinum(IV) on Fe3O4 nanoparticles. J Colloid Interface Sci 301:402–408 Umweltbundesamt (2008) Beurteilung der Gesamtumweltexposition von Silberionen aus Biozid-Produkten. UBATexte 43/08, ISSN 1862-4804 Unrine JM, Hunyadi SE, Tsyusko OV, Rao W, Shoults WA, Bertsch PM (2010) Evidence for bioavailability of Au nanoparticles from soil and biodistribution within earthworms (Eisenia fetida). Environ Sci Technol 44: 8308–8313 US-Environmental Protection Agency (2007) Nanotechnology white paper. US Environmental Protection Agency, Washington, DC, p 132 US-Environmental Protection Agency (2008) Petition for rulemaking requesting EPA regulate nanoscale silver products as pesticides; notice of availability. Fed Regist 73: 69644–69646 VandeVoort AR, Arai Y (2012) Effect of silver nanoparticles on soil denitrification kinetics. Ind Biotechnol 8:358–364 VandeVoort AR, Arai Y, Sparks DL (2012) Environmental chemistry of silver in soils: current and historic persective. In: Advances in agronomy, vol 114. Elsevier Academic Press Inc., San Diego, pp 59–90 Vigneshwaran N, Kathe AA, Varadarajan PV, Nachane RP, Balasubramanya RH (2007) Functional finishing of cotton fabrics using silver nanoparticles. J Nanosci Nanotechnol 7:1893–1897 Walters C (2011) Plant growth and colloidal silver. http://www. ehow.com/info_12004814. Accessed 2 July 2013

123

J Nanopart Res (2013) 15:1896 Wang J, Koo Y, Alexander A, Yang Y, Westerhof S, Zhang Q, Schnoor JL, Colvin VL, Braam J, Alvarez PJ (2013) Phytostimulation of poplars and Arabidopsis exposed to silver nanoparticles and Ag? at sublethal concentrations. Environ Sci Technol 47:5442–5449 Warheit DB, Borm PJA, Hennes C, Lademann J (2007) Testing strategies to establish the safety of nanomaterials: conclusions of an ECETOC workshop. Inhal Toxicol 19:631–643 Wijnhoven SW, Peijnenburg WJ, Herberts CA, Hagens WI, Oomen AG, Heugens EH, Roszek B, Bisschops J, Gosens I, Van De Meent D (2009) Nano-silver-a review of available data and knowledge gaps in human and environmental risk assessment. Nanotoxicology 3:109–138 Wiley B, Sun Y, Xia Y (2007) Synthesis of silver nanostructures with controlled shapes and properties. Acc Chem Res 40:1067–1076 Winkel-Shirley B (2002) Biosynthesis of flavonoids and effects of stress. Curr Opin Plant Biol 5:218–222 Wirth SM, Lowry GV, Tilton RD (2012) Natural organic matter alters biofilm tolerance to silver nanoparticles and dissolved silver. Environ Sci Technol 46:12687–12696 Woodrow Wilson Database (2010) (http://www.nanotechproject. org). Accessed 02 July 2013 Yang X, Gondikas AP, Marinakos SM, Auffan M, Liu J, HsuKim H, Meyer JN (2012) Mechanism of silver nanoparticle toxicity is dependent on dissolved silver and surface coating in Caenorhabditis elegans. Environ Sci Technol 46:1119–1127 Yang Y, Wang J, Xiu Z, Alvarez PJ (2013) Impacts of silver nanoparticles on cellular and transcriptional activity of nitrogen-cycling bacteria. Environ Toxicol Chem 32: 1488–1494 Yasur J, Rani P (2013) Environmental effects of nanosilver: impact on castor seed germination, seedling growth, and plant physiology. Environ Sci Pollut Res. doi:10.1007/ s11356-013-1798-3 Yin L, Cheng Y, Espinasse B, Colman BP, Auffan M, Wiesner M, Rose J, Liu J, Bernhardt ES (2011) More than the ions: the effects of silver nanoparticles on Lolium multiflorum. Environ Sci Technol 45:2360–2367 Yin L, Colman BP, McGill BM, Wright JP, Bernhardt ES (2012) Effects of silver nanoparticle exposure on germination and early growth of eleven wetland plants. PLoS ONE 7:e47674 Yu S-J, Yin Y-G, Liu J-F (2013) Silver nanoparticles in the environment. Environ Sci Process Impacts 15:78–92 Zhang W, Yao Y, Sullivan N, Chen Y (2011) Modeling the primary size effects of citrate-coated silver nanoparticles on their ion release kinetics. Environ Sci Technol 45: 4422–4428 Zhang H, Peng C, Yang JJ, Shi JY (2013) Eco-toxicological effect of metal-based nanoparticles on plants: research progress. Chin J Appl Ecol 24:885–892