Phytoaccumulation of Heavy Metals in South Kazakhstan Soils (Almaty and Turkestan Regions): An Evaluation of Plant-Based Remediation Potential

The unrelenting progress of industry and urbanization has resulted in significant damage to the environment, including pervasive pollution of soil, water, and atmosphere with dangerous materials. Heavy metals are particularly problematic among these pollutants because of their toxicity, persistence, and tendency to bioaccumulate. Heavy metal buildup in soils not only reduces fertility but also seriously jeopardizes ecosystem integrity and human health. This problem has sparked a concentrated effort to create and improve remediation techniques, with phytoremediation emerging as a viable, economical, and environmentally beneficial solution. Chaoua et al. [1] and Sandeep et al. [2] claim that because of heavy metals’ extreme toxicity, they are among the most important environmental issues facing the world today. Numerous human activities, including the use of fertilizers and pesticides, wastewater discharge, the dumping of industrial waste, mining operations, and fuel burning, cause these hazardous materials to build up in soils [3, 4].

Conforming to Nurzhanova et al. [5], in the soils of the South Kazakhstan region, the content of lead exceeds the standard by 1.8 times, while copper, vanadium, and nickel exceed it by 1.4 times, and zinc by 1.2 times. The contamination by these HMs is mainly attributed to gasoline combustion (60%), non-ferrous metal production (22%), and iron, steel, and ferroalloy production (11%). Keeping with the research by Yapiyev et al. [6], grey soils are formed on loess and consist of yellow-brown loam with a clay particle content of 35-40%. They contain carbonates but lack easily soluble salts. The A horizon has a thickness of 15-18 cm and is completely unstructured. Compared to soils in other zones, they exhibit a more homogeneous particle size distribution. Humus content is 1-2%, content of carbonates is 7-8%. The humus content ranges from 1-2%, carbonate content are 7-8%, gross nitrogen content is 0.05-0.1%, phosphorus content is 0.1-0.12%, and the carbon-to-gross nitrogen ratio is approximately 6-6.5%. The sum of absorbed bases (calcium and a small amount of magnesium) – 8-10 to 15 mg eq.

According to Harindintwali et al. [7], soil remediation technologies for HM-contaminated soils include physical methods such as surface covering, encapsulation, and burial; chemical – soil cleaning, solidification, and immobilization; electrical – electrokinetic extraction and vitrification; and biological – phytoremediation and bioremediation. Nnaji et al. [8] in their work reported that in order to extract HM from the soil by remediate plants, the following factors must be taken into account: the choice of species that are not toxic to humans and animals that effectively accumulate HM – sunflower, corn and peas; determination of pollution zones; soil quality control. Bioaccumulation of HM has a certain trend of variability in the properties of the plant in terms of metal absorption: intensive – Cd, Cs, Rb; medium degree – Zn, Mo, Cu, Ni, Pb, As; weak absorption – Mn, Cr, Co; hard-to-reach – Se, Fe, Ba, Te. According to the data of Jia et al. [9], distribution of HM in plants can vary with considerable heterogeneity, because minimum and maximal value of concentrations of gross forms of pollutants differ to 100 times in a range 1-40 mg/kg, connections of Cr – 2-30 mg/kg, Cu – 4-100 mg/kg, Ni – 1-50 mg/kg, Pb – 2-25 mg/kg; B – 2-3000 mg/kg.

Daurov et al. [10] emphasize that phytoremediation, which uses the combined metabolic potential of microorganisms and plants, plays a special role in the release of the arable soil layer from HM. The use of biological methods for soil restoration and purification ensures both environmental safety and economic benefits [11]. According to Atabayeva et al. [12], bacteria such as Agrobacterium, Alkaligenes, Arthrobacter, Azotobacter, Azospirillum, Bacillus, Burkholderia, Brevibacterium, Caulobacter, Chromobacterium, Enterobacter, Flavobacterium, Gluconacetobacter, Klebsiella, Micrococcus, and Pseudomonas are widely used as biofertilizers due to their ability to bind iron, thereby protecting the environment from HM accumulation in the soil, suppressing the development of plant pathogens, and promoting plant growth.

Although many pieces of literature have been written about the harmful effects of heavy metal pollution and the potential for phytoremediation as a sustainable solution, there are still few studies that are specifically focused on a particular region and are adapted to the distinct edaphic and climatic conditions of arid and semi-arid regions like South Kazakhstan. With a focus on the dynamics of copper, nickel, and cobalt accumulation, this study attempts to close this gap by offering a thorough assessment of the phytoremediation capability of seeding peas (Pisum sativum) in the grey soils of South Kazakhstan. Through the clarification of these heavy metals’ migration patterns within the soil profile, their modes of binding, and the mechanisms underlying their absorption by pea plants, this research provides crucial information that will direct the application of phytoremediation techniques in areas with comparable environmental limitations. The study aims to accomplish the following objectives:

(1) Experimentally identify the gross concentrations of various forms of copper, nickel, and cobalt in the initial and remediated soils.

(2) Examine the main forms of metals in the initial and remediated soils.

(3) Calculate the degree of extraction of metals from contaminated soils by sowing peas and determine the main forms of metals absorbed by the plant.

(4) Evaluate the phytoremediation ability of peas on the studied soils.

As an object of the study, two territories of the impact of heavy metals were considered, which differ in multifactorial conditions, including weather-climatic and physicochemical, located in South Kazakhstan, in Almaty and Turkestan regions. For the first territory, soil samples were taken from areas of irrigated agriculture belonging to Budan LLP in the Enbekshikazakh district, located 30 km north of Yesik city. Two sampling sites were chosen: one along the highway and the other at a distance of 1000 m from the first site. The second territory was situated in the zone influenced by the production activities and waste of Yuzhpolimetal JSC in the Abay district of Shymkent megalopolis. The total volume of dumps containing Pb²⁺ and Cd²⁺ ions is 1.8 million tons. The migration dynamics of heavy metals through the soil profile were analyzed based on chemical analyses of soil samples taken at depths of 10, 20, 30, and 40 cm. Reference territories located 8000 m away from the analyzed areas were also selected.

The selection of soils was conducted using the grid sampling method. Site selection criteria included geography, land usage, and potential sources of contamination. It was made possible to identify potential hotspots or regions of concern within the study area and to guarantee representative sampling thanks to these factors. 10 squares size 10*10 m were measured. Approximately 2 kg of soil material were taken from each square. The selection was held from a depth of more than 30 cm. The collected material was placed in a container and delivered to the laboratory. The pH of the soil was measured in two conditions: in salt and water extracts. A standard pH m with a hydrogen electrode was used to determine the pH of soils. The pH of the salt extract was determined as follows. Around 10 grams of prepared soil were placed in plastic cups, and 100 ml of a 1 mol/l KCl solution was added. Solution was stirred on a magnetic stirrer for 2 hours at a speed of 40 rpm. The solution was passed through a filter and the first part of the filtrate was removed and the pH value was measured. To determine the pH of the water extract, approximately 10 grams of soil were placed in plastic cups, and 100 ml of distilled water was added. The contents were stirred on a magnetic stirrer for 1 hour at a speed of 40 rpm, and in the same way, passed through a filter and the pH was measured. A neutral adsorption capacity filter, like a cellulose filter, was used for this study. Since cellulose filters are inert and do not react with the ions in the solution, the pH measurement reliably captures the chemical characteristics of the soil. For the analysis of the main forms and concentrations of heavy metals in the soil, a chemical phase analysis method was used, which involves sequential elution of heavy metals and their subsequent determination using atomic absorption spectrometry. The study utilized a sequential elution scheme for heavy metals established by W. Miller in 1983, as outlined in Table 2.

Table 2. W. Miller’s sequential elution scheme

The soil samples were exposed to the designated extractant solution for a specific period of time under carefully monitored circumstances for each extraction phase. After 16 hours of stirring the soil with deionized water, the water-soluble fraction was removed. The residue from the preceding stage was shaken with a 0.1 M calcium nitrate solution for five hours in order to remove the exchange fraction. Next, the residue was processed with a 0.1 M sodium hydroxide solution at 80℃ for 6 hours, sometimes stirring, in order to remove the metals associated to organic matter. After that, the residue was shaken for an hour at pH 7 with a 0.1 M EDTA solution to extract any metals that had co-precipitated with magnesium and calcium carbonates. By stirring the residue in 0.1 M hydroxylamine hydrochloride in 0.01 M nitric acid at 50℃ for 30 minutes, metals related to manganese oxides were removed. Lastly, to recover metals bound to iron and aluminum oxides, the residue was digested for five hours at 80℃ with occasional shaking using a 0.3 M sodium citrate/1 M sodium bicarbonate solution.

The samples were centrifuged in between each extraction, and the liquid supernatant containing the extracted metals was carefully taken for examination. Prior to the subsequent extraction stage, the residue was cleaned using deionized water. In order to achieve a more thorough removal of the targeted metal fractions, agitation or shaking of the soil during the extraction phases increased contact between the soil and extractant solution.

A sample preparation system was used to decompose soil and plant samples. The principle of operation of the installation is based on the use of thermal energy for rapid volumetric heating of samples in sealed containers with the addition of oxidants. Thus, the samples were processed at elevated temperatures (>100℃). The mineralization was held in the mode according to pre-compiled standard. During the entire mineralization process, the pressure and temperature inside the containers were monitored in real-time. When processing the pea seeds and soil in the system, they were introduced into solutions of concentrated nitric and sulphuric acids and hydrogen peroxide. The composition of the reagents and processing conditions were carefully chosen to achieve complete mineralization and decomposition of the solid phase into the liquid phase. After splitting, the solution was brought to the desired volume with distilled water. Processing time is 3 hours. Further, the soil was mechanically processed, cleaned of large stones, dead parts of plants, and crushed. Then, it was dried for 2-3 days. The dried soil was placed in containers for planting pea beans in a volume of ~400 grams per container. A small portion was further dried in an oven to conduct necessary procedures and analyses. Beans of seed peas were planted in the container. A hole was made at a depth of 5-7 cm, and the bean was placed inside and covered with soil material. The seeds underwent pre-sowing preparation, being soaked in water with a small addition of growth activators for a day. The beans were planted on August 27, 2022, and the first watering took place on August 29, 2022 (Monday), followed by regular watering every Monday and Thursday for 2.5 months. Each watering involved 50 ml of distilled water.

The planted beans were cultivated in a greenhouse with added illumination and carefully regulated moisture levels through the regular watering regime. Containers with planted beans were placed in a well-moistened, illuminated place to accelerate the processes of growth and development. Beans were also planted in soils that were selected for the study. The corresponding literature was used to determine the species composition of plants. Plant samples were collected following the route examination method and subsequently processed in laboratory conditions. In mid-November 2022, the leaves and stems were collected, washed with distilled water, and dried. Afterward, the leaves and stems were crushed and analyzed for their gross metal content together. The roots were analyzed separately. To calculate the biological accumulation and translocation factors of metals, the gross content of metals in stems, leaves, and roots of plants were determined. To analyze the heavy metal content in toxicotolerant plant species, X-ray analysis and X-ray electron microscopy JEOL-200 (Japan) were utilized. The obtained results were analyzed by calculating the mean and standard deviation in the range of 0.95>P>0.8. Each measurement was conducted in three replicates, and for improved accuracy, in five replicates. Data processing was performed using a personal computer and Excel software package.

The impact of human activities on the natural environment is increasing day by day and has reached a critical level, leading to fundamental and often irreversible changes in all components of the biosphere. This disruption affects the material and energy cycles, which are the foundation of the dynamic equilibrium and stability of the biosphere. Today, environmental problems pose such vital issues for humanity as the quality of air, water, soil, and food. Soil, being the main medium for the accumulation of heavy metals, receives pollutants from surface runoff, groundwater, rocks, and the atmosphere [38, 39]. Major factors negatively affecting the physicochemical properties of soil are the overall toxicity of hydrocarbons, pesticides, and HM salts [40]. In polluted soils, the availability of nutrients necessary for plant growth decreases, affecting the germination and yield of plants [41]. Utilization of HM in soils is a very laborious process since they are not decomposed but simply redistributed between various components of the natural environment.

The mobility and migration of heavy metals in the soil are influenced by several soil-ecological factors, such as humus content, presence of organic and inorganic ligands, soil colloids, soil pH acidity, granulometric and mineral composition, soil density, and the prevailing acidic, alkaline, or redox conditions in the soil environment. The distribution of macro- and microelements and the forms of HM occurrence vary with the depth of the soil cover. The main factors influencing this process are the mechanical composition of the soil, acidity, phosphorus and organic matter content. Neutral soils tend to retain metals better than acidic ones, yet metal sorption mainly occurs in alkaline conditions. The soils of Southern Kazakhstan are primarily grey or light chestnut soils, characterized by moderate alkalinity. The increased content of HM in soils is a favorable factor for their transition to plant organisms. According to Boluspayeva et al. [42], in soils little affected by economic activity, the content of heavy metals is insignificant, the approximate amount of cadmium is 0.13 mg/kg, mercury – 0.08 mg/kg, lead – 16 mg/kg, copper – 20 mg/kg, nickel – 40 mg/kg, cobalt – 8 mg/kg, chromium – 100 mg/kg, iron – 8000 mg/kg.

Increased concentrations of heavy metals are concerning in areas that are only mildly impacted, but things get much worse in places where there is a lot of industrial activity, mining, and uncontrolled waste disposal. Comparing such severely contaminated soils to baseline values seen in pure environments, studies have shown startling increases in heavy metal contents. According to Han et al. [43], studies carried out in the area of abandoned mining sites have revealed lead concentrations that are up to 50 times higher than the allowable limits. Additionally, levels of zinc and cadmium have been found to exceed regulations by factors of 25 and 15, respectively. In some extreme cases, such as the areas surrounding the Aznalcollar mine spill in Spain, mercury concentrations in affected soils have been recorded at levels a staggering 1,000 times higher than in uncontaminated soils [44]. These concerning numbers demonstrate the catastrophic effects of unchecked industrial activity on soil quality and the pressing need for efficient remediation techniques to reduce the hazards to ecological systems and public health.

Elevated concentrations of HM are found in landscapes as a result of various human activities, such as the use of fertilizers, discharge of wastewater from industrialized cities, and the application of metallurgical slag for soil liming [45]. According to Bian et al. [46], soil enrichment with zinc can occur through systematic use of organic fertilizers. Uranium, thorium, and radium can enter plants through phosphorus mineral fertilizers and from the atmosphere in areas with significant coal combustion. Stable strontium enters the landscape with simple superphosphate and phosphogypsum [47, 48]. Noticeable environmental contamination with copper is observed in regions with intensive vineyard cultivation, where this element is widely used to combat diseases affecting these crops. The study provides data on phytoremediation of heavy metals using field peas, a fast-growing annual legume that can produce 2-3 crops in a single growing season. According to Popek et al. [49], there are many herbaceous species capable of thriving in conditions of high anthropogenic pollution during the natural establishment of organic reservoirs. Some of these species include Melilotus officinalis (L.) Pall., Trifolium hybridum L., Trifolium repens L., Trifolium pratense L., Vicia cracca L., Medicago sativa L., Sonchus arvensis L., and Chamerion angustifolium (L.). These plants possess specific properties that make them suitable candidates for use as phytoremediation extractors on polluted soils.

The growing environment of the remediating plants has a major impact on the phytoremediation processes’ efficiency. The bioavailability and mobility of heavy metals are significantly influenced by the pH of the soil, with slightly acidic to neutral pH ranges often favoring enhanced metal uptake by plants. Certain species, such as Medicago sativa and Melilotus officinalis, have been shown to accumulate heavy metals optimally in soils that have a pH of 6 to 7.5. Another important consideration is the moisture condition of the soil, since water stress can hinder plant development and nutrient uptake. The majority of the herbaceous plants listed are able to flourish in soils that have good drainage and moderate moisture content, usually between 60% and 80% of field capacity [50]. Additionally, temperature affects the rates at which heavy metals are absorbed by plants and their metabolic activities; in general, warmer temperatures promote these processes. On the other hand, too much heat can cause physiological stress and stunt plant growth, indicating that there may be temperature optimalities unique to certain species.

In the arid conditions of Turkestan and Almaty regions, toxic substances tend to accumulate in the upper layers of the soil, where the processes of movement are much slower than in a temperate climate. As a result, the high toxicity of the processed soil layer hinders the growth and development of the root systems of annual plants and significantly reduces the reproductive capacity of seeds. Phytoremediation, using mechanisms of phytoextraction and phytostabilization, is a promising method for extracting heavy metal ions from contaminated soils. According to Khan [51], the hyperaccumulating properties of certain plants, which allow them to accumulate heavy metals in their vegetative parts and transport ions from the soil to various plant parts, represent one of the most prospective phytoremediation technologies. It was established that in the arid climatic conditions of the subtropical climate of Southern Kazakhstan, the highest concentration of heavy metal ions is in the upper layer of soil up to 40 cm deep.

As noted by Yan et al. [27], many plants with hyperaccumulation of heavy metals grow slowly and have low biomass, which limits their use for the phytoremediation of heavy metal-contaminated soils. During the process of plant stabilization, heavy metal ions are absorbed and retained in the roots and rhizosphere, thereby suppressing the mobility of these ions, limiting their leaching into groundwater, and reducing their bioavailability for transfer into the food chain. This helps lower dietary exposure and lessen the health dangers that come with it. This is especially crucial for communities living in areas impacted by mining or industrial activity that depend on locally grown vegetables and subsistence farming. By using phytoremediation to reduce the number of heavy metals that enter the food chain, we can protect sensitive populations like pregnant women and children, as well as improve the quality of food and provide a safer environment for farming and human consumption. Methods of soil purification from toxic components using phytoextraction are based on growing plants in a polluted environment. The phytoextraction process is most effective when cleaning soils from the accumulation of nickel, zinc, and copper [52]. Heavy metals accumulate in the root system and above-ground parts of plants until reaching maximum concentrations of toxic substances over several cycles of growing crops in contaminated soil. Subsequently, the plants are incinerated, and the ash is stored in hazardous waste disposal sites. Some plants accumulate significant amounts of metals in their root systems and soil masses: cobalt, copper, chromium, lead, and nickel are present in quantities exceeding 1000 mg/kg, and manganese and zinc are present in quantities exceeding 10 g/kg on an absolutely dry basis, making them suitable for metal-producing ores [53].

The results of the study on the content of different forms of nickel, cobalt, and copper in the initial and post-remediation soil samples indicate the process of soil reclamation, as the proportion of heavy metals has decreased. The addition of chelating organic preparations and co-precipitation with manganese carbonates and hydroxides reduced the overall percentage of heavy metals in the reclaimed soil due to decreased water solubility and exchange capacity of the metals. According to Kowalik et al. [54], plants assimilate mobile and water-soluble forms of HM. Organic components of soil, such as humic compounds like humic acids, fulvic acids, tannins, and flavonoids, play a crucial role in the uptake of heavy metals by plants. Nickel enters plants in the form of nickel humates and its biological role involves incorporation into the structural organization and functioning of nucleic acids DNA and RNA, and protein molecules. Nickel is also part of the urease enzyme, which aids in urea decomposition. Copper is absorbed by plants in the form of exchangeable and water-soluble compounds and serves as a regulator of metabolic processes, participating in the synthesis of growth inhibitors, water exchange, and the redistribution of substances, it is also involved in enzymes that enhance the ability of plants to withstand frost, heat, and drought. As per Alrawiq et al. [55], cobalt in plants is contained in ionic and complex form. Its main function is to participate in atmospheric nitrogen fixation, stimulate the development of plant tissues, increase the number of ribosomes, and enhance the mobility of bacteroids in the root nodules of leguminous plants. Cobalt also stimulates cell proliferation in leaves by increasing mesophyll tissue.