2022 Volume 10 Pages 186-205
The purpose of the review was to analyze soil pollution with various chemical compounds of silver (oxides, sulfides, nitrates, nanoparticles) and the ecotoxic effect on the response of microbiological indicators, enzymatic activity, initial growth, and development of plants to soil pollution. The objectives of the study were to analyze modern literature sources, versus to data on chemical compounds, silver concentrations, and duration of exposure. The analytical review is devoted to the presentation and analysis of the ecotoxicity of chemical compounds of silver (Ag) for animals, plants, and soil. It has been established that the main anthropogenic sources of Ag pollution of the environment, including soils, are emissions from thermal power plants when burning coal, the operation of non-ferrous and ferrous metallurgy enterprises, cement plants, waste storage at solid waste landfills, the production of photographic and electrical materials, the use of pesticides, and the use of sewage sludge as fertilizer. The published values for the Ag content in contaminated soil range from 8 to 35 mg/kg, and in soils of ore deposits up to 7000 mg/kg. The negative effect of Ag is manifested in a decrease in the length of roots and biomass of plants, suppression of the growth and reproduction of earthworms, a decrease in the number of soil bacteria, and inhibition of the activity of soil enzymes. It is concluded that it is necessary to conduct experiments aimed at assessing the consequences of the entry of various chemical compounds of Ag into soils and ecosystems. The duration of experiments is from days to a year, when using concentrations of oxide, sulfide, nitrate, and nanoparticles of Ag more than 0.5 mg/kg. It is advisable to develop maximum permissible concentrations (MPCs) and approximate permissible concentrations (APCs) for Ag chemical compounds in the soil.
The antibacterial properties of silver (Ag) have been known since ancient times, so the study of its ecotoxic effects on the components of terrestrial ecosystems deserves special attention. It is because every year its emission increases into the environment in various chemical types and compounds. Due to the intense growth and development of nanotechnology, the emission of Ag nanoparticles into the environment has significantly increased and it has continued to increase in recent years [1, 2, 3].
As a result of technogenic activity, silver particles of various sizes, including nanoparticles (from 20 to 500 nm) enter the soil and other environmental objects [4, 5, 6]. However, in terms of toxicity, various forms of silver for environmental objects reflect diametrically opposed points of view. When comparing Ag compounds, silver nitrate was recognized as the most toxic inorganic compound, since it is highly soluble in water [7, 8, 9, 10]. The range of values of soil contamination by this element with silver in lead-zinc deposits varies from 10 to 1000 mg/kg and more, in pyrite-polymetallic deposits - from 100 to 350 mg/kg, in porphyry copper - from 0.5 to 85 mg/kg, cuprous sandstones and shales - from 1 to 250 mg/kg, an increased content of silver is associated with freibergite ores (from 1800 mg/kg and more) and galena (from 500 to 7000 mg/kg) [11]. In contaminated soils, the silver content according to various sources reaches from 9 to 34 mg/kg [12, 13, 14]. The widespread use of silver nanoparticles in the industry has a pronounced toxic effect on human health. Silver can interact with various proteins, like other metalloids and heavy metals: inhibition of enzymes and a decrease in the permeability of biological membranes, DNA damage, disruption of ATP production and causes cell necrosis [15, 16, 17, 18, 19, 20].
The novelty of this literary review lies in the collection of information and literary sources on the problem of soil pollution with silver, and the impact on the vital activity of plants, animals, and ultimately humans. Previously, such survey works have not been found. Exploring the issue of Ag contamination of soil and ecosystems, the following objectives were formulated: 1) to study the Ag emission sources in ecosystems; 2) to identify the main chemical forms of Ag emission and presence in soil; 3) to assess the Ag content in contaminated and uncontaminated soils; 4) to research the Ag effect on animals, plants, microorganisms, and the activity of soil enzymes.
The purpose of the literature review is to evaluate the influence of various chemical compounds of silver (oxides, sulfides, nitrates, nanoparticles) and the ecotoxic effect on the response of microbiological indicators, enzymatic activity, initial growth, and development of plants to soil pollution.
There are both essential and anthropogenic sources of Ag entering the environment. These include volcanic activity, and hydrothermal-sedimentary deposits [11, 21]. The natural sources of Ag in the soil include volcanic activity [22, 23]. Gold-silver mineralization of the continental Pacific margin of Northeast Asia is controlled by volcanogenic belts of different ages [24, 25]. A significant number of small-scale veined silver mine deposits associated with Cenozoic volcanism are known in Peru (Western Cordillera of the Peruvian Andes) [11]. Hydrothermal-sedimentary silver deposits were found in the bottom sediments of the Red and Azov Seas [21]. Over the past decades, new areas of distribution of metal-bearing sediments in the Pacific, Indian and Atlantic oceans, as well as metal-bearing sediments of the Red Sea, have been identified. In 1964, in its central depression at a depth of 2190 m, hot brines were discovered with a temperature of 44 °C and a salinity of 261‰, enriched in dissolved metals. Silver concentrations during mining from bottom sediments and during volcanic activity are negligible and do not pose a threat to human life and health. There are both natural and anthropogenic sources of Ag emission in soils [26]. The natural source of Ag is volcanic activity [27]. Anthropogenic sources of environmental Ag pollution, including soil pollution, include emissions of coal-fired power plants [28, 29, 30, 31], operation of enterprises of non-ferrous and ferrous metallurgy [33], emissions of cement plants [34], solid domestic waste landfills [35], use of sludge fertilizers [16, 36], and combustion of materials with silver nanoparticles [37]. The anthropogenic sources of environmental Ag pollution were shown in Figure 1. It is known that when coal is burned, 50% of the total mass of Ag contained in it emits into the atmosphere [30].
Figure 1: The main anthropogenic sources of environmental Ag pollution
Over a half-century, China has produced about 3,864 tons of Ag by burning coal [31]. When products with silver nanoparticles are burned, about 80% of the silver they contain is emitted into the environment [37]. Germany produces 2 million tons of dried sludge annually from municipal sewage disposal plants. About 30% of silt is used as fertilizer for agricultural land [38]. According to Schlich et al. application of the sludge strictly followed the German sewage sludge ordinance according to which 5 tons of dry sludge per hectare over 3 years can be applied to agricultural areas [38]. Considering a soil depth of 20 cm, a soil density of 1.5 g/m3, and incorporation of the maximum amount of sludge in a single application, a maximum of 1.67 g of dry sludge could be applied per kilogram of dry soil. Ag concentrations in fertilizers across China range from 0.64 to 7.47 mg/kg, which averages 3.58 mg/kg [39]. The element level in crops depends mainly on the soil water regime and plant species. Thus, when using silt as fertilizer, Ag concentrations in wheat shoots ranged from 4.87 to 20.8 µg/kg and were more than in rice.
In addition, because of the nanotechnology development in manufacturing medical and consumer products, the sources of environmental pollution increasingly are Ag nanoparticles [4, 5, 6, 40, 41]. Silver nanoparticles emit into the environment during the synthesis, processing, or disposal of products based on them [42, 43, 44]. Global consumption of Ag nanoparticles ranges from 360 to 450 tons per year [45, 46]. By 2025, the global production of Ag nanoparticles will increase to 800 tons per year, which poses enormous risks of environmental and soil pollution [3, 36, 47, 48, 49, 50].
2.2 The silver content in the soilIn uncontaminated soil, Ag content as revealed by different authors is 0.01–1 mg/kg [4, 51], from 0.07 to 0.1 mg/kg [52]. In contaminated soils, Ag content as revealed by various sources ranges from 8 mg/kg [53], 9 mg/kg [14], 19.5 mg/kg [12], 23 mg/kg [54], 35.9 mg/kg [13], to 7000 mg/kg in soils of ore deposits [11]. Despite the low Ag clarke in soil, its technophilic properties have been growing exponentially over the last half-century and according to modern forecasts will increase in the coming years [55].
In uncontaminated soils, Ag occurs mainly in the form of sulfides (Ag2S) or argentite and in association with sulfides of other heavy metals such as iron, lead, and tellurium, which are practically insoluble [56]. Through its wide use, Ag can enter the environment in various chemical types or compounds. It is important to understand the impact of various Ag forms, and it is necessary to regulate the element emission into the environment. When contaminated on the soil surface, Ag is more often emitted as oxides [28, 29, 30, 31, 32], nanoparticles [4, 5, 57], and sulfide nanoparticles [58].
2.3 Rating silver content in the soilRussia is the leader in the total number of standards for gross and active forms of soil chemical elements, but among them, there are also under-researched, which is one reason for the small number of developed not only maximum permissible concentrations (MPCs) but also approximate permissible concentration (APCs). In Russia, Ag in soil is not rationed [59]. The U.S. National Institute for Occupational Safety and Health (NIOSH) has proposed a maximum silver exposure limit in the air environment, and it is 0.9 µg/m3 for silver nanoparticles and 10 µg/m3 for other forms of silver [60]. According to other literature, the thresholds are 0.1 mg/m3 for metallic silver and 0.01 mg/m3 for soluble forms of silver [61]. The regulation of silver nanoparticles in the environment, in particular soil, is quite challenging. The main reason lies in the lack of effective methods for assessing the impact of silver nanoparticles on the environment [62].
According to literature data, no MPCs and APCs of Ag in soils have been established in any country in the world. Kolesnikov et al. [63] first developed regional MPCs of Ag in haplic chernozems, arenosols, and cambisols – 4.4, 0.9 and 0.8 mg/kg. Normalization of the silver content in the soil of different types has not been previously studied.
The impact of Ag on plants, animals, and microorganisms, consequently, leads to ecosystem imbalance. In recent years, the number of studies examining the Ag ecotoxicity and bioavailability for living organisms in the soil environment has increased. However, studies of this kind remain rare compared to ecotoxicological studies of this element in the aquatic environment.
3.1 Assessment of silver ecotoxicity to terrestrial and soil animalsAg ions are known to be very toxic to living organisms [64]. The Ag effect on terrestrial animals has been studied mainly in laboratory models. According to Sun et al. [20], Ag nanoparticles increase the activity of intracellular reactive oxygen species (ROS) and caspase generation in rat brain astrocytes, leading to programmed cell death, while Ag ions disrupt cell membrane integrity and mainly cause cell necrosis. Ag nanoparticles cause neuroinflammation by causing secretion of multiple cytokines. In a study of neurotoxicity in rat brain astrocytes, Ag ions were significantly more toxic than nanoparticles. Increased Ag was also found in the liver of birds eating Ag-contaminated food [64]. It is known that soil organisms are indicators of changes in the soil because of anthropogenic influence and soil quality characteristics.
Silver had a toxic effect on the survival, growth, and reproduction of the earthworm (Lumbricus rubellus) [65, 66, 67, 68, 69]. Earthworms exposed to Ag nitrate accumulate significantly higher Ag concentrations than those exposed to Ag nanoparticles [70]. In a study by [71], Lumbricus rubellus was exposed to Ag sulfide (2000 mg/kg) soil for 14 days, and no side effects were observed. It is known that Ag nanoparticles in soil inhibited the growth and reproduction of nematodes (Caenorhabditis elegans) [72].
3.2 Assessment of silver ecotoxicity to plantsPlants are also susceptible to Ag contamination and can accumulate this element in high concentrations (Table 1). Silver is the second most toxic substance after mercury.
As for mutagenic properties, this reactivity series is somewhat different from the toxicity series Cr6+ >> Ag > Hg > Cd, > Mo6+, Pb > W6+ > Cu. In mutagenicity, Ag is second only to Cr. Since plants are a vital part of the ecosystem and the primary trophic level in ecosystems, representing the base of the food chain [73, 74], a good understanding of the Ag effects on plants is paramount to assessing its toxicity [75]. Researchers’ observations show potential risks of Ag nanoparticles to plant ecosystems [76, 77]. Ag nanoparticles have a significant phytotoxic effect on plants, which can be observed by analyzing various physical, physiological, biochemical, and structural features [78]. To assess the Ag phytotoxicity, the most used characteristics are growth potential, seed germination, biomass, and leaf surface area of plants [8, 79, 80].
| Biological indicators | Chemical compounds of Ag, mg/kg | Physicochemical properties of soil | T | Reference | |||||
|---|---|---|---|---|---|---|---|---|---|
| Ag2O | AgNO3 | Ag2S | AgNP | рН | SOC | PSD | |||
| Multidirectional influence (both decrease and increase) on the rate of seed germination, growth of leaves and roots of Phytolacca Americana, Lolium multiflorum, Carex spp. and Eupatorium fistulosum. | 1, 10, 40 | 1, 10, 40 | LL | 20 | [81] | ||||
| Decreased biomass and transpiration rate of zucchini (Cucurbita pepo L.) | 100, 500 | LL | [82] | ||||||
| Decreased root and aerial growth of corn (Zea mays L.), cucumber (Cucumis sativus L.) and tomato (Lycopersicum esculentum L.) seedlings. | 500 | [83] | |||||||
| Decreased root length of tomatoes (Lycopersicon esculentum L.) | 50 | [84] | |||||||
| Decreased germination of garden radish (Raphanus sativus L.) at a dose of 50 mg/kg silver oxide and sulfide | 0.5, 1, 5, 10, 50, 100 | 0.5, 1, 5, 10, 50, 100 | 7.80 | 2.30 | HL | 30 | [85] | ||
| Concentrations up to 30 mg/kg had a stimulating effect on the root length of rice (Oryza sativa L.), while a concentration of 60 mg/kg inhibited root length | 30, 60 | 7, 14, 21 | [86] | ||||||
| Reduction of root length of garden radish (Raphanus sativus L.) at 100 mg/kg. | 1, 10, 100 | 7.80 | 2.30 | HL | 10, 30, 90 | [63] | |||
| Decrease in root length of radish (Raphanus sativus L.) depending on the dose. | 1, 10, 100 | 6.80 | 2.30 | LL | 10 | ||||
| Decrease in root length of radish (Raphanus sativus L.) depending on the dose. | 1, 10, 100 | 5.60 | 1.80 | HL | 10 | ||||
| Reduced root length of garden radish (Raphanus sativus L.) at 1 mg/kg. | 0.5, 1, 5, 10, 50, 100 | 7.80 | 2.30 | HL | 10 | [87] | |||
SOC - soil organic carbon content, %; T - exposure period, days; PSD - particle size distribution: HL - hard loam; ML - middle loam; LL - light loam.
According to Table 1, the ecotoxicity of AgNP can be observed from the seed germination stage to the fully developed plant [81]. The multidirectional influence due to the 1, 10, and 40 mg/kg contamination of Ag in the soil on the rate of seed germination, growth of leaves and roots of Phytolacca Americana, Lolium multiflorum, Carex spp., and Eupatorium fistulosum. This effect is associated with the morphological features of different plant species and the dependence on the dose of silver. Ag nanoparticles harm the root growth of germinating seeds, thereby reducing the fresh biomass of the plant by reducing the root elongation and weight [78]. The main reason for the toxicity of Ag nanoparticles in plants is the effect on their biochemical properties and induction of free radical formation [88]. Silver affects plant metabolism and homeostasis [89]. The main mechanism underlying the Ag phytotoxicity is the formation of excess ROS, which subsequently leads to oxidative stress in plant cells [8, 88]. Ag nanoparticles also affect the reproductive structure of plants, leading to the destruction of DNA, including disruption of metaphase and multiple chromosomal breaks [90, 91, 92], modifying the expression of several proteins of the primary metabolism and cell defense system [74]. The increased generation of ROS in plant cells is an important toxic effect that affects plant growth and development and leads to cell death [78, 93, 94]. Ag nanoparticles cause morphological changes not only in the root sections but also in the stem and leaves [78], can interfere with chlorophyll synthesis [93], and thus influence the photosynthetic system [80]. Plants exposed to Ag nanoparticles and ions demonstrated a decrease in biomass and significantly reduced mycorrhizal colonization [96]. In a study of the effects of Ag nitrate and nanoparticles on the phytotoxicity of different soil types, a decrease in radish root length was noted [87, 97]. The high concentration of Ag nanoparticles (800 µg/kg) led to intracellular damage of cytoplasmic components through autophagy and bacteroid decay. It was proved that Ag nanoparticles significantly inhibited nitrogenase activity and mycorrhizal response, resulting in the early aging of root nodules [98]. Environmental factors such as temperature, timing, and the method of exposure can inhibit the phytotoxicity of Ag nanoparticles [99, 100]. Silver nanoparticles accumulated in the roots of marsh plants (Phragmites australis) and affected the rhizosphere microbial community [101].
It is known that heavy metal contamination of agricultural soils can seriously affect the functioning and food security of the soil ecosystem [102]. Silver accumulates in crops and easily enters the food chain [74], which not only affects food production and quality but also poses a risk to human health [9, 103, 104, 105]. However, Kranjc et al. [106] argue that there is currently no risk of contamination of agricultural products with silver nanoparticles. The toxic effect of Ag is more prominent in roots than in shoots because roots are the main site of interaction, while the self-protection mechanism of plants involves translocation of Ag nanoparticles from roots to shoots and thus fully or partially limits accumulation in the aboveground parts [81, 107]. The toxic effects of Ag nitrate solutions on barley, wheat, pea, and cruciferous seeds are known [64]. In a study of the effects of various Ag types on oats (Avena sativa L), the most toxic was nitrate, sulfide followed further. All Ag types were well absorbed by the roots, indicating bioavailability. Exposure to the element on the shoots was less, indicating that Ag is accumulated to a greater extent by plant roots [10]. In areas located near the silver deposits, the average value of silver in the soil is 35.93 mg/kg, in the roots of plants – 10.19 mg/kg, in the shoots – 11.51 mg/kg. Plants such as glaucium, silene, verbascum can be used as phytoremediants to clean or remediate soils contaminated with this element [54]. Although sulfide Ag is considered poorly soluble and bioavailable, a study by Schlich et al. [10] still noted its acute toxic effects on plants and soil microorganisms.
3.3 Assessment of silver ecotoxicity to soil microorganismsSoil microbiological indicators after Ag pollution was shown on Table 2. After 7 days, an increase in microbial biomass was established, regardless of the dose of AgNPs. After 60 days, a decrease in the biomass of Gram+ and actinobacteria was noted at all concentrations of AgNPs [108]. The negative effects found in them could be attributed to the exchange and/or the adhesion to the citrate anion by the humic acids, which are more abundant in the due to the compost addition. Among metal ions, Ag has the greatest ecotoxicity to microorganisms and the least to animal cells [109]. Ag+ bactericidal concentrations are 0.01 to 1.0 mg/L, well below dangerous thresholds for humans. It is known that in the toxicity level to bacteria, heavy metals create the following series: Ag+≫ Cu2+, Ni2+> Ba2+, Cr3+, Hg2+> Zn2+, Pb2+, Na+, Cd2+, As2O [64]. When Ag ions react with the SH-functional group of proteins, they cause inactivation in the bacterial cell [110]. Ag ions at the micromolar level were found to inhibit the process of microbial respiration and thus disrupt membrane permeability. Ag nanoparticles can interact with nucleic acid and disrupt DNA replication in bacteria [111].
After the disintegration of Ag nanoparticles, the released Ag ions interact with cytoplasmic proteins of the bacterial cell wall, resulting in impaired functionality [15, 17], and affect the thiol group, leading to bacterial cell malfunction or inhibition. Absorption and accumulation of Ag ions in bacterial cells destroy DNA molecules and can lead to undesirable changes in genes [111]. At a dose of silver nanoparticles100 mg/kg, an increase in the number of bacteria of the genus Bacteroidetes and Proteobacteria and a significant decrease in the number of bacteria of the genus Actinobacteria, Chloroflexi, Planctomycetes, and Verrucomicrobia were noted [112]. Silver-associated changes in bacterial community composition were affected by soil chloride content, with more acute responses to silver being observed in more saline soils.
Despite the antibacterial properties of Ag, its effect on the ecological condition of the soil is poorly known. Microbial communities are responsible for the main processes associated with soil fertility. By accumulating in soil ecosystems, Ag can alter microbial biomass and biodiversity [7, 10, 113, 114, 115, 116], as well as microbiocenos structure [117]. Under the Ag impact, the rate of microbiological processes and the activity of soil enzymes decrease [4, 118, 119]. Given the important role of microbial communities in the cycle of matter, the impact of Ag nanoparticles on the environment can change the productivity and biogeochemistry of the ecosystem [120]. These studies provide important information for characterizing the risk of environmental pollution with Ag.
| Biological indicators | Chemical compounds of Ag, mg/kg | Physicochemical properties of soil | T | Reference | |||||
|---|---|---|---|---|---|---|---|---|---|
| Ag2O | AgNO3 | Ag2S | AgNP | рН | SOC | PSD | |||
| After 7 days, an increase in microbial biomass was established, regardless of the dose of AgNPs. After 60 days, a decrease in the biomass of Gram+ and actinobacteria was noted at all concentrations of AgNPs. | 1.5-5, 0.00015, 0.0015 | LL | 7, 30, 60 | [108] | |||||
| Changes in the structure of the bacterial community with a pronounced toxic effect depending on the dose. | 60, 145, 347, 833, 2000 | LL | 63 | [121] | |||||
| Inhibition of soil nitrification at 0.01 and 0.1 mg/kg | 0.001; 0.01; 0.1 | 7.13 | 12.50 | 1, 16, 37 | [122] | ||||
| Toxic effect on the activity and diversity of soil bacteria | 49, 124, 287, 723, 1815 | LL | 7, 14, 28, 49, 63 | [115] | |||||
| At a dose of 100 mg/kg, an increase in the number of bacteria of the genus Bacteroidetes and Proteobacteria and a significant decrease in the number of bacteria of the genus Actinobacteria, Chloroflexi, Planctomycetes, and Verrucomicrobia were noted. | 1, 10, 100 | 7.13 | 12.50 | ML | 1, 4, 9, 16, 23, 30, 37 | [112] |
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| Decrease in the number of soil bacteria at a concentration of 5 mg/kg of silver oxide and sulfide | 0.5, 1, 5, 10, 50, 100 | 0.5, 1, 5, 10, 50, 100 | 7.80 | 2.30 | HL | 30 | [85] | ||
| Decrease in the number of nitrogen-fixing bacteria. | 0,01; 0,1; 1 | 7.20 | HL | 1, 7, 14, 28, 90, 180, 365 | [123] | ||||
| Decrease in the total number of bacteria. The toxicity was dose and exposure dependent. | 1, 10, 100 | 6.80 | 2.30 | LL | 10, 30, 90 | [63] | |||
| Decrease in the total number of bacteria. The toxicity was dose and exposure dependent. | 1, 10, 100 | 5.60 | 1.80 | HL | 10 | ||||
| Decrease in the of Azotobacter sp. abundance | 0.5, 1, 5, 10, 50, 100 | 7.80 | 2.30 | HL | 10 | [87] | |||
Note: SOC: soil organic carbon content, %; T: exposure period, days; PSD: particle size distribution: HL: hard loam; ML: middle loam; LL: light loam.
It is known that microorganisms are widely used as indicators and play a key role in nutrient turnover, as well as in energy flow. Soil bacteria are involved in major soil processes such as humification, recycling, mineralization of organic matter, and stabilization of soil structure. Their diversity and abundance affect functions such as organic matter decomposition, plant development, heavy metal detoxification, and others [124]. Silver emitting into the soil will inevitably interact with soil microorganisms that are responsible for the biogeochemical cycle (e.g., the carbon, nitrogen, phosphorus, and sulfur cycle) and waste biodegradation. In the literature, there is information about the negative impact of Ag on the forest soil microbial community [117]. Significant effects of Ag nanoparticles on the soil microbial community were observed at concentrations ranging from 11 to 706 mg/kg [125]. A study by Huang et al. [122] demonstrated the toxic effect of Ag nanoparticles on ammonia-oxidizing bacteria. In their study, Samarajeewa et al. [115] observed a negative effect of Ag nanoparticles on the microorganism count and their soil activity, the appearance of tolerant bacteria (Rhodanobacter sp.) was observed only at Ag concentrations of 49 to 287 mg/kg after 14-28 days of incubation. There was a decrease in the total bacterial count when soils were contaminated with nanoparticles at 1, 5, 10, 50, and 100 mg/kg [87]. Studies confirm the higher toxicity for soil bacteria of Ag nitrate vs metal nanoparticles [126]. In a study by Grün et al. [123], a dose of Ag nanoparticles of 1 mg/kg caused reductions in microbial biomass with nitrogen-fixing bacteria being the most affected. It was also reported that Ag nanoparticles (less than 5 nm) inhibited the growth of nitrifying bacteria [17, 109]. Silver ions inhibit enzymes acting in the phosphorus, sulphur, and nitrogen cycles of nitrifying bacteria. Silver ions can enter from the environment or originate from sustained dissolution of silver nanoparticles taken up by bacteria. Soil microorganisms are major contributors to the nutrient turnover in soil systems, and it was shown that the structure of soil microbial communities was influenced by both abiotic and biotic factors.
3.4 Assessment of silver ecotoxicity by soil enzyme activitySoils are constantly exposed to large amounts of engineered nanoparticles, especially Ag nanoparticles, which can affect the activity, stability, and specificity of soil enzymes (Table 3). Therefore, the measurement of enzyme activity can be used to identify major changes in the soil environment under their influence [4]. It is known that 10 and 50 nm-sized Ag particles can have an inhibitory effect on the activity of soil acid phosphatase, β-glucosaminidase, β-glucosidase, and arylsulfatase, and the decrease in enzymatic activity was independent of particle size [4].
| Biological indicators | Chemical compounds of Ag, mg/kg | Physicochemical properties of soil | T | Reference | |||||
|---|---|---|---|---|---|---|---|---|---|
| Ag2O | AgNO3 | Ag2S | AgNP | рН | SOC | PSD | |||
| Inhibition of arylamidase and phenoloxidase at 100 mg/kg, while arylamidase is more sensitive. Toxicity depended on dose and duration of exposure | 1, 10, 100 | HL | 0.125, 3, 30 | [127] |
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| Stimulation of enzyme activity after 3 hours. Inhibition of arylamidase and phenoloxidase at 100 mg/kg, while arylamidase is more sensitive. Toxicity depended on dose and exposure time, and the size of nanoparticles (30, 80 and 200 nm) had no effect | 1, 10, 100 | HL | 0.125, 3, 30 | ||||||
| Inhibition of phosphomonoesterase, arylsulfatase, β-D-glucosidase, leucine aminopeptidase | 0.00125, 0.0125, 0.125, 1.25, 6, 25, 31 | [119] | |||||||
| Inhibition of urease, acid phosphatase, arylsulfatase, β-glucosidase | 1, 10, 100, 1000 | 7.00 | 3.54 | LL | 0.041, 1, 7 | [118] | |||
| The greatest inhibition of acid phosphatase, β-glucosaminidase, β-glucosidase, arylsulfatase activity after 1 hour and after 7 days | 1.6, 3.2 | 7 | [4] | ||||||
| Inhibition of catalase and dehydrogenase activity under contamination with silver oxide and silver sulfide | 0.5, 1, 5, 10, 50, 100 | 0.5, 1, 5, 10, 50, 100 | 7.80 | 2.30 | HL | 30 | [85] | ||
| Activity of β-glucosidase, urease, phosphatase did not change | 1,5-5, 0.00015, 0.0015 | LL | 7, 3, 60 | [128] | |||||
| Inhibition of urease activity | 0.001; 0.01; 0.1 | 7.13 | 12.50 | 1, 16, 37 | [122] | ||||
| Inhibition of aminopeptidase activity | 0.01; 0.1; 1 | 7.20 | 28.80 | HL | 1, 7, 14, 28, 90, 180, 365 | [123] | |||
| Inhibition of urease and dehydrogenases activity | 1, 10, 100 | 7.13 | 12.50 | ML | 1, 4, 9, 16, 23, 30, 37 | [112] | |||
| Inhibition of catalase and dehydrogenase activity. The toxicity was dose and exposure dependent. | 1, 10, 100 | 5.60 | 1.80 | HL | 10, 30, 90 | [63] | |||
| Inhibition of catalase and dehydrogenases activity. The toxicity was dose and exposure dependent. | 1, 10, 100 | 6,80 | 2,30 | LL | 10 | ||||
| Inhibition of catalase and dehydrogenases activity. The toxicity was dose and exposure dependent. | 1, 10, 100 | 5,60 | 1,80 | HL | 10 | ||||
| Inhibition of catalase and dehydrogenases activity by more than 18–38% at a dose of 0.5 mg/kg | 0.5, 1, 5, 10, 50, 100 | 7.80 | 2.30 | HL | 10 | [87] | |||
Note: SOC: soil organic carbon content, %; T: exposure period, days; PSD: particle size distribution, HL: hard loam; ML: middle loam; LL: light loam.
Ag nanoparticles are oxidized, and the release of metal ions into the soil contributes to the toxic effect [129]. Stability depends on soil conditions [130]. Soil properties such as structure, pH, and organic matter content are known to influence the configuration of microbial communities [131], soil enzyme activity [132], as well as on the processes of Ag dissolution, agglomeration, and adsorption [133] and, consequently, its bioavailability [134, 135]. The results of Schlich and Hund-Rinke [136] found that soil pH affected the availability of Ag ions, with acidic soils (pH=4.59) experiencing the strong toxic effect vs alkaline soils (pH6.57). Organic matter content affects the ecotoxicity of Ag nanoparticles for soil bacteria (Pseudomonas chlororaphis) [7] because Ag can form a complex with soil organic matter [137]. Soils with a light granulometric composition are more susceptible to the toxic effects of nanoparticles and Ag nitrate than heavy loam soils [136, 138]. The temperature of the soil environment affects the ecotoxicity of Ag nanoparticles to ammonia-oxidizing bacteria and the soil urease activity. Ecotoxicity decreases as temperature decreases [122]. In addition, recent data indicate that Ag bioavailability is affected by the soil chloride content. In saline soils, a more acute reaction of soil bacterial and fungal communities to Ag was noted, which manifested itself in a decrease in their count and diversity [112].
It is known that Ag nanoparticles harmed the enzymatic activity of the soil, inhibiting the activity of soil enzymes such as urease, acid phosphatase, arylsulfatase, β-glucosidase, dehydrogenases, and fluorescein diacetate hydrolase. Urease activity was the most sensitive [118]. Yan et al. [127] obtained opposite results in which the dehydrogenase activity was more susceptible to Ag nanoparticles than the urease activity. A study by Rahmatpour et al. [138] demonstrated that a 1 mg/kg Ag dose inhibited urease activity, while the 1 mg/kg Ag concentration in the study by Yan et al. [127] did not affect urease activity. High concentrations of Ag nanoparticles (100 mg/kg) inhibited arylamidase and phenoloxidase activity [139]. Kolesnikov et al. [87] found that 5, 10, 50, and 100 mg/kg doses of Ag nanoparticles inhibited catalase and dehydrogenase activity. A decrease in the catalase and dehydrogenases activity in soils of different degrees of resistance to contamination with Ag nitrate has been observed [140, 141]. Previously, studies have noted a dose-dependent inhibitory effect of Ag nanoparticles on the germination of rice seeds and their subsequent growth and development [128], on microbial and enzymatic activities of soil [138]. The activity of urease, β-glucosidase, alkaline phosphatase, and the composition of the microbial community was practically unaffected by Ag nanoparticles [108].
A study by Peyrot et al. [119] noted the negative effect of Ag on the activity of soil enzymes: phosphomonoesterase, arylsulfatase, β-D-glucosidase, and leucine aminopeptidase. Ag nanoparticles inhibited the activity of soil exoenzymes, such as dehydrogenases, urease, acid phosphatase, neutral phosphatase, and alkaline phosphatase, in the rhizosphere of wetland plants such as iris (Iris wilsonii), bulrush (Typha orientalis), and giant reed (Arundo donax) [142]. There is a need to study the Ag effects on microorganisms and enzymatic activity in complex environmental systems such as soils.
In recent years, due to anthropogenic activity, both the amount of Ag emission into the environment and the soil contaminated with this element have increased. Most often, Ag emits into the environment, including the soil, in the form of oxides, oxide nanoparticles, and sulfides. The data obtained on the Ag toxicity to living organisms are based on model experiments. Soil bacteria are the most sensitive to Ag. Among heavy metals, Ag ranks first in terms of ecotoxicity to bacteria and second to plants. The toxicity of Ag to various ecosystem components is affected by the chemical form of the compound, concentration, and duration of contamination. The main way to assess the effects of various chemical types of Ag compounds emission in soils and terrestrial ecosystems is to conduct experiments with different exposure times using concentrations of Ag oxide, sulfide, nitrate, and nanoparticles more than 0.5 mg/kg. It would be useful to develop MPCs and APCs for chemical types of Ag compounds in soil.
Funding: The study was supported by a grant from the Russian Science Foundation No. 22-24-01041 at the Southern Federal University.
