Biosynthesized silver nanoparticles as a nanoweapon ...

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Appl Microbiol Biotechnol DOI 10.1007/s00253-014-6296-0

MINI-REVIEW

Biosynthesized silver nanoparticles as a nanoweapon against phytopathogens: exploring their scope and potential in agriculture Sandhya Mishra & H. B. Singh

Received: 21 October 2014 / Revised: 2 December 2014 / Accepted: 4 December 2014 # Springer-Verlag Berlin Heidelberg 2014

Abstract The beneficial use of silver nanoparticles (AgNPs) in agroecosystems is not fully explored with partial information available, of which most of the studies are limited to laboratory conditions and only few involve natural ecosystems. AgNPs, being the most popular metallic nanoparticles exhibiting antimicrobial property, are predominantly used for plant disease management. Owing to the ill hazards of chemically synthesized AgNPs, their biosynthesis using environment-friendly biomolecules is gaining noteworthy attention. In addition, considering the advantages of nanoformulations over biopesticides, there is no doubt that biosynthesized AgNP-based biopesticides could revolutionize the agricultural sector in the future. Though enhanced commercial use of AgNPs has generated biosafety issues in modern scenario but expecting their significant contribution towards agricultural sector, it is too early to predict the risk factor associated with their usage. To unveil the toxicity factor of AgNPs, we need to focus and understand the major interactions of AgNPs in agroecosytems. Hence, the present review highlights (i) the potential application of AgNPs in the agricultural sector particularly for plant disease management, (ii) significance of biosynthesized AgNPs using microbes and plants over their chemical synthesis, (iii) major interactions of AgNPs in agroecosystems (with soil, soil biota, and plants) with emphasis to deal with toxicity-determining factors, and (iv) identifying future research work holding promising applications of biosynthesized AgNPs in agroecosystems.

Keywords Silver nanoparticles . Biosynthesis . Soil . Soil biota . Plants . Agriculture S. Mishra : H. B. Singh (*) Department of Mycology and Plant Pathology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi 221005, India e-mail: [email protected]

Introduction The silver metal has long been used in Ayurvedic therapeutics since ancient times due to its efficient antimicrobial properties. The popularity of silver out of all metals with antimicrobial property is mainly due to efficient antimicrobial action and least toxicity (Guggenbichler et al. 1999). However, in modern scenario, the use of silver is not limited to medical applications only; it is also used for non-medical purposes such as in electronic appliances and cosmetics (Klasen 2000; Jung et al. 2008). Being an antimicrobial agent, silver has a long ancient history since Greek and Roman civilizations, where silver was used as a disinfectant for food and water. Moreover, considering the importance of silver as an antimicrobial agent, the US Food and Drug Administration approved silver solution in 1920 for its usage in the food and drug industry. The different forms of silver, viz. silver salt, silver acetate, silver nitrate, and silver sulfadiazine, are being used for microbial inhibition (Jung et al. 2008), but currently, in the era of nanotechnology, the nanoform of silver, i.e., silver nanoparticles (AgNPs), is gaining noteworthy considerations due to its unique properties. Compared to bulk silver, AgNPs due to their miniscule size possess a large surface-area-to-volume ratio and thus exhibit a high reaction rate that helps in establishing a better contact with microorganisms and hence enhances their antimicrobial property, making them a potent broad-spectrum antimicrobial agent (Morones et al. 2005; Kim et al. 2007; Marambio-Jones and Hoek 2010). The AgNPs emerged as a potential antimicrobial agent to combat the problem of generation of antibiotic-resistant pathogenic bacteria and hence were incorporated in medical applications in the form of nanogels, nanolotions, silver-based dressings, and silver-coated medicinal devices (Rai et al. 2009). The effectiveness of AgNPs could be estimated by the fact that they kill approximately 650 types of pathogenic microbes such as bacteria, fungi, viruses, yeasts etc. and kill

Appl Microbiol Biotechnol

pathogenic bacteria in a very short time, i.e., 30 min (Shahrokh and Emtiazi 2009). It is interesting to note that AgNPs are largely used as an antimicrobial agent in a variety of approximately 250 consumer products ranging from domestic appliances, textiles, and paints to medical products such as surgical products and dressing bandages (Kim et al. 2007; Blaser et al. 2008; Klaine et al. 2008; Ma et al. 2010). Owing to the growing market of AgNP-based products in multifarious sectors, this mini-review summarizes and discusses the potential applications and advantages of AgNPs in agroecosystems with a strong emphasis on employing biosynthesized AgNPs for plant disease management. We also attempted to update the contemporary knowledge of toxicity of AgNPs towards major agroecosystem components, viz. soil, soil biota, and plants, by underlining the fact that before making any final remarks, we need to study the interactions and toxicity level of biosynthesized AgNPs with agroecosystem components as earlier reports have assessed the toxicity of AgNPs which are from non-biological sources.

AgNPs in agriculture for plant disease management After witnessing the adverse effects of the “first green revolution” during the 1970s, there is an urgent need of the “second green revolution” with an ecofriendly and more sustainable approach. Therefore, to cope with various kinds of biotic and abiotic stresses, the modern agriculture is adopting innovative technology of which nanotechnology is carrying robust application in the agricultural field (Nair et al. 2010; Ghormade et al. 2011; Wang et al. 2013a; NAAS 2013). In general, the agricultural production is largely affected by various kinds of plant diseases leading to huge economic losses. To combat this major challenge, the concept of biopesticides emerged after the first green revolution, mainly to minimize the indiscriminate use and ill effects of chemical pesticides. Though the idea of using biopesticides helped in modernization of the agricultural sector owing to their ecofriendly and sustainable approach, it is worth mentioning here that the major drawbacks associated with their usage recently gave birth to the innovative approach of harnessing nanotechnology in agriculture (Ghormade et al. 2011) (Fig. 1). As stated above, AgNPs, being the most popular metallic nanoparticles, have left no field untouched due to their unique properties; the agricultural sector is no exception. Therefore, considering the antimicrobial property of AgNPs, it is interesting to note that AgNPs are predominantly used for plant disease management (Park et al. 2006; Jo et al. 2009; Kim et al. 2012; Mishra et al. 2014). Many workers have advocated the antimicrobial activity of AgNPs against a diverse and broad range of plant pathogens (Table 1). Initially, Park et al. (2006) effectively developed a nanosized silica-silver particle formulation demonstrating antimicrobial activity against

Fig. 1 Multifarious factors determining relative advantages of using nanoformulations in agriculture in comparison to biopesticides

various phytopathogens, viz. Pythium sp., Colletotrichum sp., Pseudomonas syringae, Xanthomonas compestris, etc. In addition, this formulation was also found to be efficient in controlling powdery mildew of pumpkin at a very low concentration of 0.3 ppm under field and greenhouse conditions. In this perspective, many earlier reports gave experimental evidences to verify the suitability of AgNPs in generating novel pesticidal formulations to control various plant diseases. Intriguingly, Kim et al. (2009) investigated the inhibitory effect of AgNP suspension on the fungal growth and conidial germination of ascomycetous phytopathogen Raffaelea sp. causing oak wilt disease. Furthermore, comprehensive studies made by many researchers provided evidence of a wider applicability of AgNPs for controlling a variety of plant pathogens such as Bipolaris sorokiniana, Magnaporthe grisea (Jo et al. 2009), Fusarium culmorum (Kasprowicz et al. 2010), Colletotrichum sp. (Lamsal et al. 2011a), sclerotium-forming fungi (Min et al. 2009), powdery mildew on cucumber and pumpkin (Lamsal et al. 2011b), Pseudomonas syringae pv. tomato (Chu et al. 2012), and gray mold in strawberry (Moussa et al. 2013). Here, it is very important to recognize the fact that these studies have included silver nanoparticles obtained either from different sources (excluding biological sources) or synthesized using physical or chemical methods.

Biological synthesis of silver nanoparticles: a more ecofriendly approach As evident from previous studies, a variety of physical and chemical methods including high-energy ball milling, arc discharge, laser pyrolysis or ablation, electrochemical and

Appl Microbiol Biotechnol Table 1

List of examples showing antimicrobial activity of AgNPs against various plant pathogens

Source/mode of synthesis of silver nanoparticles used in the study

Target pathogen

References

Nanosized silver–chitosan composite prepared using chitosan extracted from Aspergillus niger and silver nanoparticles (Sigma-Aldrich, St. Louis, MO, USA) according to the method described by Rhim et al. (2006) Colloidal solution of AgNPs provided by BioPlus Co. Ltd. (Pohang, Korea)

Gray mold in strawberry

Moussa et al. (2013)

Various plant pathogenic fungi

Kim et al. (2012)

Nanosized Ag–silica hybrid complex prepared by γ-irradiation

Pseudomonas syringae pv. tomato

Chu et al. (2012)

Colloidal solution of AgNPs provided by BioPlus Co. (Pohang, Korea)

Colletotrichum sp.

Lamsal et al. (2011a)

AgNPs provided by BioPlus Co. Ltd. (Pohang, Korea)

Powdery mildews on cucumber and pumpkins Fusarium culmorum

Lamsal et al. (2011b)

Silver nanoparticles synthesized using high-voltage arc discharge method AgNPs provided by Quantum Sphere Inc., Santa Ana, CA

Kasprowicz et al. (2010) Jo et al. (2009)

AgNPs provided by BioPlus Co., Ltd.

Bipolaris sorokiniana and Magnaporthe grisea Sclerotium-forming phytopathogenic fungi Oak wilt pathogen Raffaelea sp.

Nanosilver (Shanghai Huzheng Nano Technology Co. Ltd., China)

Stem-end bacteria on cut gerbera

Liu et al. (2009)

The nanosized silica–silver prepared by combining nanosilver with silica molecules and water-soluble polymer and exposing a solution including silver salt, silicate, and water-soluble polymer to radioactive rays

Powdery mildews of pumpkin

Park et al. (2006)

Colloidal solution of AgNPs provided by BioPlus Co. Ltd. (Pohang, Korea)

chemical vapor deposition, micro-emulsion sol-gel, and reverse precipitation have been adopted for synthesis of metallic nanoparticles (Sastry et al. 2003, 2004; Daniel et al. 2013). Moreover, it is important to mention that these methods are harmful to the environment due to involvement of a myriad of toxic chemicals. In addition, such methods are expensive and unstable (Dubey et al. 2010). Therefore, nowadays, the biosynthesis of nanoparticles using plant extracts and microbes such as bacteria, fungi, algae, and yeasts is gaining noteworthy attention and becoming successful. In the biosynthetic process, the biomolecules involved are non-toxic, of low cost, and most importantly environment friendly and the obtained nanoparticles are more biocompatible (Mandal et al. 2006; Gericke and Pinches 2006). In this regard, owing to the promising application of AgNPs for plant disease management, researchers have started using biological agents for AgNP synthesis (Table 2). Table 2 List of examples showing antimicrobial activity of biosynthesized AgNPs against phytopathogens

Biological sources for synthesis of AgNPs

Applications

Min et al. (2009) Kim et al. (2009)

Involvement of agriculturally important microbes for AgNP synthesis could lead to more environment-friendly and biocompatible nanoparticles for their efficient application in agroecosystems. In this context, most recently, a wellknown plant growth-promoting Serratia sp. has been used to synthesize AgNPs with antifungal activity against B. sorokiniana, the spot blotch pathogen of wheat (Mishra et al. 2014). Likewise, beneficial microbes such as Bacillus sp., Trichoderma sp., and Spirulina platensis have also been employed for biosynthesis of AgNPs holding antimicrobial property against a broad range of phytopathogens (Fayaz et al. 2009; Gopinath and Velusamy 2013). Apart from microbes, plant sources such as Acalypha indica, Piper nigrum, and pine cone-mediated biosynthesized AgNPs have also shown strong inhibition of phytopathogens (Krishnaraj et al. 2012a; Velmurugan et al. 2013; Paulkumar et al. 2014). Additionally, innovative biological sources such as milk have been used for

References

Serratia sp. BHU-S4

Antifungal activity against Bipolaris sorokiniana

Mishra et al. (2014)

Piper nigrum

Antifungal activity against phytopathogens

Paulkumar et al. (2014)

Bacillus sp. GP-23 Milk

Antifungal activity against Fusarium oxysporum Antifungal activity against phytopathogens

Gopinath and Velusamy (2013) Lee et al. (2013)

Pine cone

Velmurugan et al. (2013)

Spirulina platensis

Antibacterial activity against Bacillus megaterium, Pseudomonas syringae, Burkholderia glumae, Xanthomonas oryzae, and Bacillus thuringiensis Bactericidal activity against phytopathogens

Acalypha indica

Antifungal activity against plant pathogen

Krishnaraj et al. (2012a)

Trichoderma viride

Vegetable and fruit preservation

Fayaz et al. (2009)

Mala et al. (2012)

Appl Microbiol Biotechnol

AgNP synthesis exhibiting antifungal activity against phytopathogens (Lee et al. 2013). As evident from these studies, until now, very limited focus has been directed towards the biological synthesis of AgNPs holding efficient application especially for plant disease management. Hence, the use of beneficial microbes and plant extracts for AgNP synthesis could minimize the risk factor and biosafety concerns associated with their application in agroecosystems. However, besides their biological synthesis, we also need to consider other factors, which will be dealt later on in this article.

Potential impact of AgNPs on agroecosystems: exploring major interactions The past and current researches in the booming field of nanotechnology have generated great interest in important research topics, i.e., the probable interactions of nanoparticles in an environmental system involving plants, macro-microorganisms, soil, humans, etc. (Abhilash et al. 2012; Bakshi et al. 2014; Mohanty et al. 2014). It is important to identify the fact that about 500 tons per annum production of AgNPs is reported globally (Mueller and Nowack 2008). Therefore, there is obvious and unintentional release of AgNPs into the environment, and in general, AgNPs enter the soil through various routes, viz., waste incineration plants, landfill, air, water, sewage sludge, AgNPs comprising fertilizers or pesticides, various AgNP-containing consumer products, etc. (Benn et al. 2010; Lin et al. 2011; Glover et al. 2011; VandeVoort et al. 2012). Once AgNPs enter the soil, they are likely to contaminate the environment, but considering the importance of agroecosystems, here, we will focus mainly on the three Fig. 2 A proposed model displaying the interactions of AgNPs with three major agroecosystem components, viz. soil, soil biota, and plants

major kinds of interactions involving AgNPs with special reference to their impact on soil, microbial population, and most importantly plants (Fig. 2).

AgNP-soil interaction Once AgNPs find their way into the soil environment, their fate, transport, bioavailability, and consequent toxicity are largely affected by the soil physico-chemical properties (Shoults-Wilson et al. 2011; Cornelis et al. 2012; Benoit et al. 2013). The factors such as soil texture, pH, cation exchange capacity, and soil organic matter mostly govern the transport, mobility, and sorption of AgNPs in the soil (Oromieh 2011; Benoit et al. 2013). Few reports have significantly evaluated the substantial interactions between AgNPs and soil, and their comprehensive understanding could actually build a baseline for recognizing the benefits and risks of AgNPs to the environment (Jacobson et al. 2005; Shoults-Wilson et al. 2011; Oromieh 2011; Benoit et al. 2013) (Table 3). Based on studies reported by these researchers, there are three important soil parameters, viz., pH, cation exchange capacity, and organic matter content, affecting toxicity behavior of AgNPs (Fig. 3). Soil pH and cation exchange capacity both significantly affect the bioavailability of AgNPs and Ag in soil (Oromieh 2011; Benoit et al. 2013). It has been observed that a high pH of the soil directly elevates cation exchange capacity due to which Ag ions are sorbed onto the soil surface, and consequently, their bioavailability would be drastically reduced. Likewise, organic matter content also govern sorption and mobility of Ag as high organic matter present in soil would facilitate the strong binding of Ag to the soil, hence reducing

Appl Microbiol Biotechnol Table 3 Effect of soil physicochemical properties on fate and behavior of AgNPs

Soil properties

Interaction and subsequent impact on AgNPs

References

Soil texture

Fine-textured soils facilitate Ag sorption

Jacobson et al. 2005

pH

Organic matter Cation exchange capacity

Sandy soils show greater toxicity of AgNPs

Shoults-Wilson et al. 2011

High soil pH enhances Ag sorption to the soil

Oromieh 2011; Benoit et al. 2013

Acidic soil shows greater toxicity of AgNPs as Ag ions are more available for biological uptake High organic matter in soil helps in strong binding of Ag and thus making its less bioavailability

Shoults-Wilson et al. 2011

High cation exchange capacity facilitates Ag sorption to the soil

Oromieh 2011; Benoit et al. 2013

their mobility, availability for biological uptake, and subsequent toxicity (Shoults-Wilson et al. 2011). Furthermore, physico-chemical properties of soil and nanoparticles (size, shape, and surface charge) are believed to exert important control on dissolution, agglomeration, and aggregation of nanoparticles. Aggregation tends to increase particle size, leading to their sedimentation and further adsorption onto the soil matrix ultimately affecting the toxicity behavior of nanoparticles (El Badawy et al. 2010; Tourinho et al. 2012). Interestingly, enhanced ionic strength and divalent cations were found to promote AgNP aggregation and retention in soil (Lin et al. 2011; Thio et al. 2012). In accordance to this, results obtained by Bae et al. (2013) clearly indicated the close association of ionic strength and organic matter with soil adsorption and aggregation behavior of citrate-coated AgNPs. The aggregation rate of AgNPs enhanced with increased ionic strength and decreased organic matter content. This finding was consistent with the result achieved by El Badawy et al. (2010) for uncoated AgNPs and citrate- and sodium borohydride-coated AgNPs. Conversely, agglomeration of polyvinylpyrrolidone (PVP)-AgNPs was not influenced by increasing ionic strength reflecting the importance of stabilizing agents. Reproductive toxicity of AgNPs was noticed towards Eisenia fetida in soil due to negative zeta potential causing decreased aggregation that finally enhanced its bioavailability (Heckmann et al. 2011). Similarly, Wirth et al. (2012) noted no toxicity of highly aggregated AgNPs on Fig. 3 Soil factors playing an important role in determining the fate, behavior, and bioavailability of AgNPs in soil

Shoults-Wilson et al. 2011; Benoit et al. 2013

Pseudomonas fluorescens biofilms. As discussed above that the fate and toxicity of AgNPs vary with soil properties (Shoults-Wilson et al. 2011), in this perspective, Cornelis et al. (2013) suggested that heteroaggregation of AgNPs with natural soil colloids significantly reduced their mobility and their further potential risk by studying transport behavior of AgNPs in saturated columns of natural soils with different physico-chemical properties. Thus, it is clear from the above discussions that studies aimed at appraising soil conditions favoring aggregation of AgNPs into large agglomerates with reduced toxicity could be of great concern for verifying their robust application in agriculture. Additionally, future research in this direction involving biosynthesized AgNPs is strongly recommended. AgNP-soil biota interaction Although the broad-spectrum antimicrobial property of AgNPs against human and plant pathogens is a well-known and accepted fact worldwide, their impact on soil biota is still not well executed and hence attracted noteworthy attention from the scientific community. Therefore, when talking about the application of AgNPs in agroecosystems, their major interaction with residing soil biota cannot be ignored. The adverse effect of AgNPs is found to be more pronounced on denitrifying bacteria, disrupting the process of denitrification in soil (VandeVoort and Arai 2012). As a result,

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the denitrifying bacterial community being highly vulnerable to AgNPs in soil has been used as a model system to evaluate the dose-dependent effects of silver (Johansson et al. 1998; Throbäck et al. 2007). In this viewpoint, Yang et al. (2013) studied the interaction of AgNPs (carbon coated, size 35 nm) and Ag+ (provided as AgNO3) with Pseudomonas stutzeri (denitrifier), Azotobacter vinelandii (nitrogen fixer), and Nitrosomonas europaea (nitrifier). They concluded lower toxicity of AgNPs towards these bacteria in comparison to 20–48 times higher toxicity exerted by Ag+. Conversely, low and sublethal concentrations of Ag+ and AgNPs (20–25 μg/L) yielded no significant impact on the expression pattern of denitrifying genes and nitrogen-fixing genes but showed 2.1- to 3.3-fold upregulation in nitrifying genes, indicating the sensitivity of the nitrification process towards silver. Another study representing the impact of nanosilver on aerobic denitrification process by Shahrokh et al. (2014) advocated that a low dose of AgNPs had no adverse effect on nitrate reductase activity of Rhizobium and Azotobacter. Interestingly, 0.2 ppm of AgNP treatment enhanced the process of nitrate reduction in Azotobacter. Taken together, these findings clearly indicate a dose-dependent effect of AgNPs on the microbial process of nitrogen cycle, giving us clue that entering an optimum concentration of AgNPs into the environment could be favorable for microbial processes with no hindrance in beneficial plant-microbe interactions in agroecosystems. However, size-dependent toxicity of AgNPs has also been evidenced by Choi and Hu (2008), where they found that AgNPs of size less than 5 nm were more toxic to nitrification bacteria. Being an integral part of the natural ecosystem and contributing towards soil fertility and plant growth, it becomes necessary to study the microbial community and its interaction with AgNPs for a comprehensive understanding of the level of ecotoxicity possessed by AgNPs. For this reason, this aspect has been discussed and summarized in recent research articles (Chunjaturas et al. 2014; Yang et al. 2014; Zhang et al. 2014; Shah et al. 2014; Mohanty et al. 2014). The more pronounced effect of AgNP exposure was reported in activated sludge system causing about 50 % reduction in Chloroflexi population and significant decline in total species richness. Moreover, there was a notable shift in microbial community structure leading to recruitment of silver-tolerant species of Acidobacteria and Bacteroidetes (Yang et al. 2014). On the contrary, Zhang et al. (2014) reported no significant impact of even long-term exposure of nanosilver at sub-parts per million concentration (0.10 mg Ag/L) on microbial community structure and abundance of nitrifying bacterial community in activated sludge system. Interestingly, a noticeable augmentation in the copy number of the silver-resistant gene silE was also reported indicating changes in population dynamics. On the same note, enhancement in diversity of nirK denitrifiers (nirK encodes the copper nitrite reductase) was observed in response

to increasing concentration of silver (provided as AgNO3) in soil though the gene copy number and denitrification activity was found to decrease (Throbäck et al. 2007). Additionally, silver-mediated enrichment of “novel nirK denitrifiers” was also observed that actually suggests the establishment of unknown silver-tolerant denitrifier populations in soil that carry novel nirK sequences displaying no matches with previously reported nirK sequences. Most importantly, these results evidently indicate the intrinsic capability of microbial diversity to resist and recover from the disturbances imposed by silver. Besides microbial diversity, microbial community functions are also getting influenced simultaneously by AgNP exposure, and varying degrees of response have been recorded. Apart from the nitrification process as discussed above, other microbial processes are also found to be affected by AgNP treatment. In this context, observation made by Hänsch and Emmerling (2010) suggested a dose-reliant effect of AgNPs on soil microbial biomass and enzyme activities, where they found diminution in soil microbial biomass with increasing application rate of AgNPs. In addition, no effect of the treatments was reported for microbial biomass nitrogen and enzymatic activities playing a key role in C, N, and P cycling in soil. While, on other side, Shin et al. (2012) evaluated the negative impact of AgNPs (1, 10, 100, and 1000 μg/ g) on common soil exoenzyme activities linked to important nutrient cycles such as carbon, nitrogen, phosphorus, and sulfur. Urease activity was observed to be more sensitive to AgNPs showing inhibition at a very low concentration of 1 μg/g. The interesting study by Chunjaturas et al. (2014) highlighted the impact of different AgNP concentrations (0, 100, 250, and 500 μg/g soil) and incubation periods (0, 2, 4, 8 weeks) on soil properties, bacterial community structure, and soil microbial activity. Overall, their findings revealed a marked decline in bacterial community structure and soil respiration with increasing concentration and incubation of AgNPs. However, no significant impact on N mineralization and soil properties (such as pH, electrical conductivity, cation exchange capacity, and organic matter) was recorded. Most recently, Colman et al. (2013) also throw light on the concentration-dependent ecotoxicity of AgNPs and advocated that a very low dose of AgNPs (0.14 mg Ag/kg soil) altered bacterial community composition and lowered microbial biomass and enzyme activities of leucine amino peptidase and phosphatase in slurry. However, N2O flux was found to be unaffected by the treatment. It is interesting to note that the degree of response caused by AgNP treatment was much higher in comparison to AgNO3 added at a fourfold higher concentration. With reference to agricultural soil, few reports certainly provide baseline for comprehensive understanding of the interaction of AgNPs with soil properties, underlining the risk factors and the ways to circumvent them (Calder et al. 2010; Chunjaturas et al. 2014; Shah et al. 2014). A higher toxicity

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level of AgNPs (size 10 nm; concen. 1 and 3 mg Ag/L) towards beneficial soil bacterium Pseudomonas chlororaphis O6 was noticed in sandy soil as compared to loamy soil. Sandy soil when mixed with soil pore water or humic acid was able to protect the bacterium from toxicity of AgNPs. Here, the protective routes involved precipitation and removal of Ag ions by chloride, drop in negative charge by interaction with Ca in pore water, and reduced bioreactivity of AgNPs due to generation of inactive soluble Ag complexes by association with dissolved organic carbon (Calder et al. 2012). Similarly, the toxicity of AgNPs on soil microbial community was found to be largely dependent on soil types along with concentration and exposure time of AgNP treatment (Chunjaturas et al. 2014). Moreover, the impact of various engineered nanoparticles (silver, cobalt, iron, and nickel nanoparticles) on soil bacterial diversity is also attributed to environmental parameters and the transportation behavior in soil matrix beyond soil properties (Shah et al. 2014). A fast migration of AgNPs through the soil matrix appeared to cause a bimodal distribution of silver mostly present in the top and bottom layers of soil. Interestingly, 16 % increase in species richness was observed in the top horizon of soil (acting as a major source for Ag+ ions). On the whole, no significant impact of engineered nanoparticles on richness of soil bacterial community was reported through pyrosequencing analysis (Shah et al. 2014). Here, attention should be given to the fact that we are still unable to assume the impact of biologically synthesized AgNPs on soil microbiota due to scarcity of literatures. Hence, this concern highlights the need for more future researches concentrating on studying the probable interaction of biosynthesized AgNPs with soil environment with quantitative assessment of mobility, precipitation, aggregation, and sorption of AgNPs in soil to circumvent their negative effect on soil microbial population and functions. AgNP-plant interaction The toxicity of AgNPs towards prokaryotic microorganisms and mammalian cell lines has been studied in detail however, owing to the progressive usage of AgNPs in agriculture; nowadays, its phytotoxicity towards higher plants is gaining more importance. As plants are the governing bodies of our environment, therefore, it is important to study and understand the possible risk of AgNP application to plants. Earlier reports focusing on this aspect have yielded both positive and negative effects and are also very limited (Navarro et al. 2008). Phytotoxicity of AgNPs is basically controlled by three factors: plants (seeds, species type, growth stage), AgNPs (size, concentration, mode of application), and experimental conditions (time and method of AgNP exposure). Here, one thing is important to understand whether the toxicity is attributed to AgNPs itself or to Ag+ ions (dissolved form of Ag). As stated by Stampoulis et al. (2009), Ag+ ions released from AgNPs

caused accumulation of Ag in Cucurbita pepo shoot. Interestingly, accumulation of NPs in plant biomass actually leads to phytotoxicity and mainly depends on the concentration and size of AgNPs (Wang et al. 2013b). The faster uptake of smallsized AgNPs at a low concentration was observed in Populus deltoides x nigra (Wang et al. 2013b). Mazumdar and Ahmed (2011) reported AgNP accumulation in root cells in Oryza sativa, while on other hand, Haverkamp and Marshall (2009) evidenced no accumulation of Ag in Brassica juncea. The availability of AgNPs for plant uptake could also be affected by the media used for plant growth, for example, soil or agar. In this context, Lee et al. (2012) elucidated less bioavailability of Ag+ (released from AgNPs) in soil as compared to agar. Moreover, their study highlights the concentration-dependent toxicity of citrate-coated AgNPs (5–25 nm) on seedling growth of Phaseolus radiatus and Sorghum bicolor, where they analyzed no-observed-adverse-effect concentration (NOAEC) and lowest-observed-adverse-effect-concentration (LOAEC) of AgNPs at 2000 mg/kg soil, whereas values for S. bicolor root growth were estimated as NOAEC 100 mg/kg soil and LOAEC 300 mg/kg soil, and for shoot growth as NOAEC

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