Surface Coating-Modulated Phytotoxic Responses of Silver Nanoparticles: History
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Subjects: Plant Sciences
Contributor:
Biljana Balen

Silver nanoparticles (AgNPs) have been implemented in a wide range of commercial products, resulting in their unregulated release into aquatic as well as terrestrial systems.Once released into the environment, they are prone to various transformation processes that modify their reactivity. In order to increase AgNP stability, different stabilizing coatings are applied during their synthesis. However, coating agents determine particle size and shape and influence their solubility, reactivity, and overall stability as well as their behavior and transformations in the biological medium. The employment of different stabilizing coatings can modulate AgNP-induced phytotoxicity with respect to growth, physiology, and gene and protein expression in terrestrial and aquatic plants and freshwater algae.

  • silver nanoparticles
  • plants
  • green algae
  • growth
  • photosynthesis

1. Introduction

Among a variety of applied nanomaterials, silver nanoparticles (AgNPs) attract a lot of attention due to their prominent antimicrobial effects. Therefore, they have been implemented in a wide range of commercial products [1][2]. Unceasing production and utilization of AgNPs consequently results in their unregulated release into aquatic as well as terrestrial systems through numerous pathways, which raises concerns over their impending environmental effects [3][4].
AgNP stability and susceptibility to transformation upon synthesis are directly related to their surface chemistry [5]. The most important processes that impact bioavailability and biological effects of AgNPs are agglomeration and aggregation, oxidation of elemental silver (Ag0) to silver ion (Ag+), and subsequent dissolution to dissolved Ag+ species, which all modify the AgNP reactivity [6]. In order to prevent that, different stabilizing coatings, such as carboxylic acids (citrate), polymers (polyvinylpyrrolidone, PVP), polysaccharides (gum arabic, GA), and surfactants (cetyltrimethylammonium bromide, CTAB, and sodium dodecyl sulphate, SDS) are applied during their synthesis. However, coating agents can change AgNP surfaces and thus affect their behavior and transformations in the medium [7].
Plants, being sessile organisms, are prone to accumulation of many environmentally released substances, including AgNPs, and are, in this respect, particularly affected. So far, mostly negative impact of AgNP exposure on growth, morphology, and physiology of vascular plants has been reported, although some positive effects have also been found (reviewed in Tkalec et al. [1]). On the other hand, AgNP toxic effects on the growth and physiology of freshwater algae are far less documented, although they are an important component of water environment and ecosystem.
In studies dealing with phytotoxicity of AgNPs, different types of coating agents were used. AgNP stabilization is usually obtained by either steric stabilization [8] or electrostatic stabilization [9]. Among nonionic polymer coatings, the most frequently used is polyvinylpyrrolidone (PVP) as well as polyethylene glycol (PEG) and polyvinyl alcohol (PVA).  Considering the electrostatic stabilization of AgNPs, citrate is the most commonly applied coating that provides a negative charge (Figure 1).
Nanomaterials 12 00024 g001 550Figure 1. Proportional representation of coatings used for AgNP stabilization in plant (A) and algal (B) research.

2. AgNP Stability in Various Exposure Media

Different exposure conditions may affect AgNP size, shape, and surface electric charge [10][11][12] and, consequently, alter their uptake, toxicokinetics, toxicodynamics, and biological fate [11][13]. Biological media have a high chemical complexity and interactions of AgNPs and the medium can lead to their agglomeration/aggregation and dissolution [14][15][16]. On top of that, chemical or photo-induced reduction of Ag+ ions released from the AgNP surface can lead to formation of secondary particles with different characteristics compared to the original ones [12][17][18].
Colloidal stability of AgNPs in different media used for plant and algal toxicological studies is greatly determined by the composition of the medium itself and the exposure period of the treatment [1][19]. Moreover, intrinsic properties of AgNPs (size, shape, and surface charge) also direct their behavior in the environment [20]. Generally, rate of dissolution is higher for smaller uncoated AgNPs in media rich in molecules that tend to complex released Ag+ ions [21]. Plant and algal experiments  revealed significantly higher agglomeration and dissolution rates of uncoated AgNPs compared to the coated ones. Application of coatings lowers AgNP surface energy, prevent interactions with the environment, and diminish aggregation rates [22][23], although not all coatings behave in the same way. This becomes even more complicated when plants or algae are added to the media. Interaction of AgNPs with the biomolecules present in biological environment (nucleic acids, proteins, lipids, etc.) can lead to the formation of the surface corona [12][24] that can reverse AgNP surface charge [25]. These processes can either stabilize AgNPs or result in their increased aggregation and dissolution rates, depending on the AgNP intrinsic characteristics [14][26].

3. Silver Uptake and Effects on Growth and Morphology

Seed germination represents the first and the most crucial step for plant growth and the overall crop yield [27] and it is  heavily susceptible to various environmental factors [28]. Studies performed to assess AgNP effects on seed germination and early growth, revealed both positive and negative effects, depending on the plant species, exposure method, and characteristics of AgNPs (reviewed in Tkalec et al. [1]). Another important factor determining AgNP phytotoxic effects is their uptake. The main route of AgNPs entry into the plant cell occurs through the pores in the cell wall [15][29]. Their further translocation occurs by endocytosis and through plasmodesmata [30][31]. AgNP movement and effects are highly dependent on the plant growth stage. If taken up by roots of seedlings or adult plants, AgNPs can penetrate the vascular tissue and reach the stems and leaves (Figure 2), where they can cause further damage [32]. If AgNPs enter the seeds during imbibition period, they can move to embryonic cells and in that way cause long-term effects for the plant [33].
Algal accumulation of AgNPs is an important process of AgNP transport through the aquatic ecosystem. AgNPs can be adsorbed onto the algae surface and/or internalized in the cell due to the porous structure of the cell wall. In normal conditions, only particles smaller than 20 nm can enter the algal cell, but during cell division and stress induction cell wall permeability increases, allowing entry of even bigger sized particles (Figure 2), causing detrimental effects on their growth and morphology. 
Nanomaterials 12 00024 g002 550
Figure 2. Uptake of differently coated and uncoated AgNPs in plants and freshwater algae and their effects on growth and morphology. EPS - extracellular polymeric substances. Figure was created with BioRender.com. Accessed on 24 November 2021.

4. Oxidative Stress Induction and Mobilization of Antioxidant Machinery

Studies have shown that AgNPs are contributing to production of reactive oxygen species (ROS) [1][19], which induce oxidative stress in plant and algal cells by combined effects of direct surface oxidation and ability of ROS species to react with important biomolecules (Figure 3), which under severe oxidative stress can even lead to the cell death. Indirectly, release of Ag+ ions from AgNPs  and properties of their coatings  affect AgNP toxicity and additionally contribute to ROS production in promotion of oxidative stress.

Although oxidative stress plays an important role in the toxicity mechanism of AgNPs, it is still not clear whether production of ROS is a direct or indirect effect through release of Ag+ ions, as in most of the studies evaluated in this review detailed analysis of AgNPs stability is missing. Differentially coated AgNPs show different extents of ROS production as well as altered activity of antioxidant enzymes. The overall results suggest that coating-stabilized AgNPs influence plant and green algae response to stressful conditions in time- and concentration-dependent manner, although plant developmental stage can also interfere with the extent of AgNP-induced oxidative stress.

Figure 3. Effect of differently coated AgNPs on plant and algal cells by direct interaction or through ROS formation. ROS - reactive oxygen species, ER - endoplasmic reticulum, CAT - catalase, SOD - superoxide dismutase, POD - peroxidase. Adapted from “Structural Overview of a Plant Cell” by BioRender.com (2021). Retrieved from https://app.biorender.com/biorender-templates. Accessed December 17th, 2021.

5. Impact on Photosynthesis

Most research to date shows that photosynthesis, the most important biochemical process on Earth for providing energy and oxygen, is particularly sensitive to AgNPs (Figure 4). Several studies have reported a decrease in chlorophyll and carotenoid content upon exposure to uncoated AgNPs in freshwater algae  as well as vascular plants [1].

Although the exact mechanism of AgNP phytotoxicity is still not fully understood, AgNPs in the cell may dissociate to the toxic Ag+ ions [1][19]. They can competitively replace Cu+ ions in plastocyanin, an electron carrier in the photosynthetic electron-transfer chain, resulting in the disturbance of the photosynthetic electron transport and ROS generation. Furthermore, Ag+ can interact with the thiol group of enzymes of chlorophyll biosynthesis, thus interfering with this process. Another possible explanation for impaired photosynthesis could be diminished transpiration rate and stomatal conductance, resulting in lower rate of gas exchange and reduced CO2 assimilation.

Exposure of plants and freshwater algae to AgNPs with different surface coatings can cause both structural changes of the photosynthetic apparatus and functional ones that manifest as a decrease in the content of photosynthetic pigments, as well as an inhibition of photochemical reactions and CO2 assimilation. The divergence of the AgNP-induced effects on photosynthesis can be partly attributed to differences in physicochemical characteristics of AgNPs and their bioavailability imposed by different surface coatings. However, the effect of other factors such as plant species, developmental phase, type, and time of exposure should be also considered.

Figure 4. Structural and functional changes of the photosynthetic apparatus in plants and freshwater algae upon exposure to AgNPs with different surface coatings. RuBP - ribulose 1,5-bisphosphate, 3-PGA - 3-phosphoglyceric acid, G3P -glyceraldehyde 3-phosphate, PS - photosystem, PQ - plastoquinone, Cyt b6f - cytochrome b6f, PC - plastocyanin, Fd - ferredoxins. Figure was adapted from “Light Dependent Reactions of Photosynthesis” by BioRender.com (2021). Retrieved from https://app.biorender.com/biorender-templates. Accessed November 24th, 2021.

6. Changes in Gene and Protein Expression

The application of AgNPs modulates morphophysiological, biochemical, and molecular status of plants and freshwater green algae [1][19]. In spite of the attention that nanomaterial phytotoxicity attracted in recent years, only limited investigations have been conducted on the molecular level effects of AgNPs in plants, while for studies on green algae, even less information in the literature can be found. To examine the molecular bases of AgNP phytotoxicity, gene and protein expression analyses have been performed in model as well as in different crop plants and only a few species of freshwater green algae.

Studies have shown that differently coated AgNPs have impact on gene and protein expression in various plant and algae species. Information obtained from these studies increase our understanding of the mechanisms involved in plant and green algae responses to AgNPs, which is relevant for environmental assessments. However, it is difficult to draw unambiguous conclusions since these studies have been investigated in different species, applied different concentrations of AgNPs with different coatings, and employed different exposure times. Therefore, in order to investigate the role of stabilizing coatings in AgNP-induced phytotoxicity on molecular level and to be able to compare different coatings, it would be useful to conduct a research that implemented differently coated AgNPs in the same experimental setup.

7. Conclusion

AgNP behavior in plant and algal exposure systems is dependent on surface coatings. On one hand, they stabilize nanoparticles, but on the other hand, are responsible for their physiochemical modifications, such as changes in aggregation and agglomeration, oxidation states, and dissolution rate of Ag+ ions. Surface coating-determined AgNP properties play an important role in AgNP uptake and modulate their effects on germination and development in plants. In algae, EPS plays an important role in AgNP bioaccumulation, which is why effects of differently coated AgNPs on EPS should be further investigated. Oxidative stress is proved to be the one of the major mechanisms of the AgNP-induced phytotoxicity in both plants and algae, although application of certain surface coatings seems to alleviate AgNP-induced ROS formation. The process of photosynthesis, in all its complexity, has been particularly affected by AgNPs, although algae, being unicellular organisms, seem to be more susceptible compared to plants. At the molecular level, gene and protein expression analyses confirmed AgNP-generated induction of oxidative stress and photosynthesis as the most sensitive target of AgNP toxic action, regardless of which coating is applied. However, in order to investigate the role of stabilizing coatings in AgNP-induced phytotoxicity on molecular level and to be able to compare different coatings, it would be useful to conduct a more studies which will implement differently coated AgNPs in the same experimental setup.

This entry is adapted from the peer-reviewed paper 10.3390/nano12010024

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