ISSN 2308-4057 (Печать),
ISSN 2310-9599 (Онлайн)

The microorganism-plant system for remediation of soil exposed to coal mining

Introduction. Coal mining causes a radical transformation of the soil cover. Research is required into modern methods and complementary technologies for monitoring technogenic landscapes and their remediation. Our study aimed to assess soil and rhizosphere microorganisms and their potential uses for the remediation of technogenic soils in Russian coal regions.
Study objects and methods. We reviewed scientific articles published over the past five years, as well as those cited in Scopus and Web of Science.
Results and discussion. Areas lying in the vicinity of coal mines and coal transportation lines are exposed to heavy metal contamination. We studied the application of soil remediation technologies that use sorbents from environmentally friendly natural materials as immobilizers of toxic elements and compounds. Mycorrhizal symbionts are used for soil decontamination, such as arbuscular mycorrhiza with characteristic morphological structures in root cortex cells and some mycotallia in the form of arbuscules or vesicles. Highly important are Gram-negative proteobacteria (Agrobacterium, Azospirillum, Azotobacter, Burkholderia, Bradyrizobium, Enterobacter, Pseudomonas, Klebsiella, Rizobium), Gram-positive bacteria (Bacillus, Brevibacillus, Paenibacillus), and Grampositive actinomycetes (Rhodococcus, Streptomyces, Arhtrobacter). They produce phytohormones, vitamins, and bioactive substances, stimulating plant growth. Also, they reduce the phytopathogenicity of dangerous diseases and harmfulness of insects. Finally, they increase the soil’s tolerance to salinity, drought, and oxidative stress. Mycorrhizal chains enable the transport and exchange of various substances, including mineral forms of nitrogen, phosphorus, and organic forms of C3 and C4 plants. Microorganisms contribute to the removal of toxic elements by absorbing, precipitating or accumulating them both inside the cells and in the extracellular space.
Conclusion. Our review of scientific literature identified the sources of pollution of natural, agrogenic, and technogenic landscapes. We revealed the effects of toxic pollutants on the state and functioning of living systems: plants, animals, and microorganisms. Finally, we gave examples of modern methods used to remediate degraded landscapes and reclaim disturbed lands, including the latest technologies based on the integration of plants and microorganisms.
Ключевые слова
Technogenic landscapes, heavy metals, pollutants, phytoremediation, remediation, mycorrhizal fungi, rhizogenic microorganisms

Areas of anthropogenically transformed soils continue to expand throughout the world. Soil transformation is caused by degradation or complete destruction of topsoil as a result of deforestation, wind and water erosion, pesticide pollution, mining, industrial and civil construction, and growing urbanization [1–6].

Russia accounts for 15% of coal production and export in the world [7]. One of its regions, Kemerovo Oblast-Kuzbass, has about 100 coal mines, of which half are open-pit mines. In the first half of 2021, it produced 116.84 million tons of high-quality coal, up 8% from the previous year.

Extraction of coal and other minerals transforms topsoil drastically, especially in case of opencast mining. Drilling and blasting are accompanied by enormous dust emissions that contain toxic pollutants, including heavy metals and carcinogenic gas (benzo(a)pyrene) [8–15]. Large amounts of methane and carbon dioxide released into the atmosphere have a greenhouse effect and change the thermal regime, vegetation, and topsoil of the area. All this exacerbates health problems, such as a growth in oncological and cardiovascular diseases, as well as congenital malformations [16].

Active mining causes a serious ecological imbalance. In particular, it transforms or destroys natural landscapes and creates new anthropogenic forms with different physical, chemical, and biological properties. According to Rosprirodnadzor (Russia’s environmental watchdog), the country had 194 225 hectares of disturbed lands by 2019. Back in 2015, the Center for Hygiene and Epidemiology in Kemerovo Oblast and the Kemerovo Center for Hydrometeorology and Environmental Monitoring confirmed a strong correlation between increased coal mining, industrial production, and total emission of pollutants into the air. They identified eight ecologically vulnerable districts: Yaysky, Topkinsky, Tisulsky, Leninsk-Kuznetsky, Guryevsky, Prokopyevsky, Novokuznetsky, and Mezhdurechensky.

The above factors call for research that applies modern methods to monitor technogenic landscapes and introduce the latest complementary technologies for their remediation [17–21]. This can be done by using living systems: plants and soil animals and microorganisms. Of great importance are plant-microbial complexes: arbuscular ecto- and endomycorrhizae, symbiotic associations of plants and nitrogen-fixing prokaryotes, as well as rhizobial and cyanobacterial symbioses.

Our aim was to assess the use of soil and rhizosphere microorganisms for remediating technogenic soils in Russia’s coal-mining regions.

We studied the scientific articles published over the past five years, as well as those cited in Scopus and Web of Science.

The Institute of Soil Science and Agrochemistry (Siberian Branch of the Russian Academy of Sciences) has developed theoretical and practical foundations for improving the methods of recultivating technogenic soils [3]. Unfortunately, the geobotanical approach to disturbed territories still prevails, with reclamation of dumps by pine trees or perennial grasses [22]. Along with that, it is important to scientifically substantiate the latest reclamation technologies, taking into account the biosystems of undisturbed soils in a particular geographical zone.

Until 2000, external dumps had been selectively formed during the exploitation of coal deposits. Overburden was selectively placed into the body of the dump. This method of reclamation was used to ensure the rational use of the area’s land and develop a harmonious anthropogenic landscape that met the ecological, socioeconomic, and sanitary requirements by using the fertile soil layer and potentially fertile species. Today, this method is not as common. The biological stage of forest and agricultural reclamation is not effective due to the water regime and, consequently, insufficient moisture supply to the biota. Low moisture in the root layer and the presence of highly toxic heavy metals and other pollutants result in poor survival among trees and poor germination of perennial grass seeds.

Irreversible soil degradation caused by technogenesis may have severe consequences for living systems. Of great concern is chemical pollution of landscapes, especially with heavy metals that are deposited and adsorbed in soil [23–27]. When the contents of metals exceed the ecological capacity or change the redox potential (pH), pollutants are released. The human body contains 81 out of 92 elements found in nature, of which 15 are vital (Fe, I, Cu, Zn, Co, Cr, Mo, Ni, V, Se, Mn, As, F, Si, and Li) and four are conditionally essential (Cd, Pb, Sn, and Rb). They were found in low concentrations in plant and animal tissues, but they are highly dangerous for human health even in the smallest amounts [28]. Almost all regions of the world have a chemically “aggressive” environment. However, biochemical anomalies are more common in the zones of industrial development of natural landscapes, during mineral extraction, and in urban industrial agglomerations. Agrogenic lands are polluted through excessive use of pesticides [29].

According to Li et al., mining operations in China resulted in increased copper and cadmium contents in the soil used to grow rice. The environmental load changed in decreasing order from lead to chromium: Pb > Cd > Ni > As > Zn > Cu > Cr [30]. Moreover, lead, chromium, and cadmium exceeded the maximum permissible concentrations in crop production 2–8 times [31, 32]. Lead has the longest period of clearance from the soil-plant system. Plants receive its excessive quantities from soil. As a result, lead inhibits their respiration, suppresses photosynthesis, and sometimes increases the amount cadmium, while decreasing the intake of zinc, calcium, phosphorus, and sulfur.

It has also been found that during coal transportation, many pollutants are deposited on the transport routes along with dust. Heavy metals accumulate in soils for a long time. Their excessive amounts affect plant growth, metabolism, physiology, and aging. Plants have stress control mechanisms responsible for maintaining homeostasis of the basic metals that they require. These mechanisms make plants tolerant to metal contamination by forming less toxic metal complexes with active metabolites excreted through the root system. Other mechanisms are triggered by specific stress [31].

Arsenic is the most dangerous inorganic substance. It does not immediately cause symptoms of poisoning in animals, but its concentrations in their blood, hair, hooves, and urine remain high in contaminated areas. It belongs to a special group of conditionally essential elements since it acts at the ionic level or as part of nonspecific molecules or ions that penetrate the organism of living systems.

Heavy metals in soil have a detrimental effect on living organisms as a result of bioaccumulation and biomagnification [33]. Due to their impact on physiological and biochemical processes, most pollutants are toxic to plants [34]. The extent of toxicity depends on their content in soil, which can vary from 1 to 100 000 mg/kg [35, 36]. Heavy metals are also dangerous because they can replace the ions of the main metals that living systems and humans need [37, 38]. This disturbs metabolic processes and biochemical reactions during food consumption and removes metabolites from the body. Excessive accumulation of heavy metals causes protein compounds to break down at the molecular level, ruptures peptide bonds, increases free radicals, and severely damages vulnerable organs (brain, kidneys, liver, and blood vessels).

Phytoremediation is a well-known method of cleaning contaminated soil by extracting pollutants through the roots of trees, shrubs, and herbaceous plants [17, 39]. The results depend on the plants’ tolerance to pollutants, the volume of biomass, and the efficiency of pollutant transportation from roots to shoots. Absorbed by the root system of plants, toxic elements accumulate in their tissues and are subsequently decomposed or converted into safer forms [40].

Russian and foreign researchers have recently developed efficient technologies to improve soil by physical and chemical methods [10–14]. For example, scientists in Kemerovo Oblast have proposed combining a bioorganic remediation agent from industrial waste with a technical agent to improve soil physicochemically and obtain a pollutant-free biomass of perennial grasses [41]. In another study, Altunina et al. developed a land reclamation method based on biocryogels. They have high porosity, good mechanical strength, stability in any biotechnological environment, and thermal resistance. Plants in cryostructured soil develop a good root system and do not inhibit soil microflora (www.ipc.

Soil can also be remediated by sorbents produced from environmentally friendly materials, such as humic acids from naturally oxidized coals [25]. The cleaning mechanism is based on the introduction of reaction centers into the composition of humic acids to bind with metal ions.

A mixture of dry lime and sapropel (5:1) can be used as an active natural sorbent. It is applied evenly to the surface of soil contaminated with heavy metals in an amount of 0.5–1.5 t/ha in early spring. The sorbent improves the redox potential (pH) and the soil’s absorbing capacity. Increased amounts of mineral and organomineral colloids contributes to active accumulation and long-term immobilization (3–5 years) of toxicants in the humus horizon, preventing the migration of heavy metals to other ecosystem components (patent RU 2655215C1).

Many studies report using groups of microorganisms with different biological functions to remove heavy metals, radionuclides, and organic compounds from soils. Microbiota used to clean soils, wastewater, bottom sediments, and overburden from pollution are able to extract elements and compounds from adjacent environments, convert them into less hazardous waste products or transport them to plant tissues as nutrition. The most efficient groups of microorganisms are those with high symbiotic activity in relation to plants of different classes, families, genera, and species.

Structurally largest is a group of arbuscular mycorrhiza with characteristic morphological structures in the cells of the root cortex and some mycotallia in the form of arbuscules or vesicles [12]. It has been established that by interacting with arbuscular mycorrhiza, host plants are often actively nourished with nitrogen and phosphorus [11, 13]. Just as important are groups of proteobacteria from the genera Agrobacterium, Azospirillum, Azotobacter, Burkholderia, Bradyrizobium, Enterobacter, Pseudomonas, Klebsiella, Rizobium (Gram-negative), Bacillus, Brevibacillus, Paenibacillus (Gram-positive), as well as Gram-positive actinomycetes (Rhodococcus, Streptomyces, Arhtrobacter).

Mycorrhizal chains can form in soil to transport and exchange various substances, including mineral forms of nitrogen, phosphorus, and organic forms of C3 and C4 plants. Many representatives of the above genera produce phytohormones, vitamins, and bioactive substances that stimulate plant growth, inhibit phytopathogenic diseases and harm from insects, and increase the tolerance to soil salinity, air and soil drought, and oxidative stress [12–16, 22–26]. Mycorrhizal chains are also involved in the removal of toxic elements by precipitating or accumulating them both inside cells and in the extracellular space. The activity of mycorrhizal networks is strongly influenced by soil animals: mites, amoeba, collembola, lumbricids, and others [42, 43].

Mycorrhiza can be identified in plant groups and communities in any ecological zone of the world. Their development depends on abiotic and biotic factors, such as moisture and heat supply of the soil and atmosphere, altitudes above sea level, atmospheric pressure, variety of vegetation, and the presence of phytopathogenic infection or harmful animals (invertebrates and vertebrates). These factors are interdependent and can exert varying degrees of environmental pressure on the development of mycorrhizal networks in the rhizoplane of plants. Mycorrhiza has been identified in 44% of bryophytes, 52% of ferns, 100% of gymnosperms, and 85% of flowering plants. However, it has not been found in the families Caryophyllaceae, Cyperaceae, Brassicaceae, Chenopodiaceae, and others.

Well studied is the interaction of plants and nitrogenfixing prokaryotes at the level of symbiotic, associative, and non-symbiotic nitrogen fixation. Lack of nitrogen in the soil limits the bioproductivity of many plant species. Plants absorb nitrogen from the soil in the form of nitrates, ammonium, and amino acids that are available to them as a result of the microbiological destruction of organic litter (leaves, branches, fruits, etc.) or nitrogen fixation. Symbiotic nitrogen fixation occurs in specialized structures of plants. Associative nitrogen fixation takes place in the rhizoplane or rhizosphere of roots and on the surface of leaves. Non-symbiotic nitrogen fixation occurs through external sources of organic matter or photosynthesis in cyanobacteria.

The type of rhizobial symbiosis is associated with prokaryotes of the order Rhizobiales and plants from the Fabaceae family and Ulmaceae family (Parasponia ssp.). Thanks to the short-lived nitrogen-fixing nodules on the plant roots, they are able to collect up to 450–550 kg/ha of nitrogen per year. These bacteria are active in wide pH ranges (5.0–8.5). In Siberia, active nitrogen-fixing nodules can be found on many species of clover, astragalus and other plants.

Actinorhizas of the order Frankia come into symbiosis with over 200 species of dicotyledonous plants, including woody ones. These long-lived root nodules collect up to 225 kg/ha of nitrogen per year. They can grow on pioneer substrates and easily function even in acidic boggy soils.

Cyanobacteria are mainly of the Nostoc genus and sometimes of the Anabaena genus. They are localized in the Azolla L. cavity, in intercellular spaces of cycad bark, on plant stems, and leaf petioles. Moisture and heat are the main conditions for their activation. Maximum nitrogen fixation is up to 720 kg/ha in Australia and much less in the boreal zone.

Actinorhizal plants are of the families Betulaceae, Elaefgnaceae, Rozaceae, Datiscaceae, Ramnaceae and other species. Flowering plants that come into symbiosis with cyanobacteria belong to the Gunneraceae genus and are common for the southern hemisphere. Cyanobacteria function mainly under aerobic conditions and can use their own photosynthesis or sources of organic matter.

Any type of symbiosis between plants and microorganisms can be used to clean the soil from pollutants. Figure 1 shows the main soil phytoremediation processes using microorganisms as plant symbionts.

Table 1 shows the main stages and processes in the plant during the transformation of toxicants [35, 44–49].

Plants and microorganisms can be mutually beneficial, which gives them an advantage in surviving critical conditions. Microorganisms stimulate the plant’s growth and, at the same time, transform soil pollutants into a more accessible form.

Pollutant-resistant bacteria and fungi can be isolated from the rhizosphere of pollution-resistant plants [51]. They are of particular value for biotechnologies to remediate lands contaminated with heavy metals and toxic organic compounds [52]. Table 2 shows strains of microorganisms that are currently of practical interest in the rehabilitation of lands contaminated by active industrial development and are of strategic importance for the economic development of Russian regions [16, 53–67].

In addition to the strains listed in Table 2, more active consortia can be created to produce new soil varieties that are effective and safe for the biota of microbial communities, plants, and soil animals. Such consortia improve the soil’s bioactivity and ecological functions.

Soil bioremediation by plants. All plants assimilate very small quantities of copper, manganese, iron, nickel, and zinc. Along with this, there are plants that are capable of absorbing highly toxic heavy metals, such as cadmium, arsenic, lead, mercury, and others, without serious damage to their growth. They are called hyperaccumulators and are able to accumulate pollutants in large quantities without signs of phytotoxicity in the aerial parts of plants. Metal hyperaccumulators absorb at least 100 mg/kg of arsenic and cadmium and 1000 mg/kg of cobalt, copper, chromium, manganese, nickel, and lead. These plants include Pteris vittata, Bidens pilosa, Jatropha curcas, and Helianthus annuus [68–71]. They can resist the harmful effects of heavy metals by accumulating and suppressing them inside cells.

Exposure to toxicants changes the expression of genes responsible for the synthesis of transporter proteins that capture and transfer metals [72]. In Siberia, and Kemerovo Oblast in particular, H. annuus is the most available plant of those listed. There are several families of genes responsible for metal transport. These include macrophage proteins (Nramps), heavy metal ATPases, cation diffusion catalysts (CDFS), cationic antiporters, Zn-regulated transporter (ZRT), and the ZIP family [73].

Pollutants are adsorbed by plants in two ways – by symplastic and apoplastic transport. In the case of symplastic transport, heavy metals diffuse into the roots’ endothermal cells through the plasma membrane. Ions can be transported by such carriers as proteins or organic acids, e.g., oxalic acid in combination with aluminum. In the case of apoplastic transport, metals are located in the free space between cells in non-cationic forms [39]. Special carrier proteins help pollutants to diffuse across the plasma membrane. There are special carriers for iron, zinc, and other metals [72, 74]. Various substances produced by plants, such as metallothioneins, glutathione, and phytochelatins, bind metal ions and are transported to vacuoles or shoots [74].

In hyperaccumulator plants, chelates are transported to shoots by membrane proteins: MATE, ATPase, and oligopeptide carrier proteins [72]. There, they are stored in vacuoles of parenchymal and epidermal leaf cells, which occupy 60 to 95% of the cell volume [75].

The problem with toxicant absorption by plants is that not all metals are absorbed in equal amounts. Cadmium and zinc are more readily available, which depends on the mobility of metal ions. Therefore, for better assimilation of elements, the soil conditions need to be adjusted, namely redox potential (pH) and temperature. In addition to these factors, plants themselves create conditions for better absorption of heavy metals. In particular, they secrete phytosiderophores and carboxylates, as well as acidify the rhizosphere for better release of ions from the soil [73].

Soil bioremediation by microorganisms. Microorganisms use various mechanisms for the transformation of pollutants. To survive in toxic environments, they transform compounds into safer substances. Thus, toxicants can be removed both inside and outside the plant’s cells and tissues. To neutralize pollutants, microorganisms generate substances that are released into the environment and enhance the processes of cleaning soil from pollutants [76].

Some bacteria (P. aeruginosa, P. fluorescens, Haemophilus spp.) use various cellular enzymes (laccases, peroxidases, phosphatases, nitrilases, nitroreductases, etc.) and are therefore effective in soil remediation [77].

Soil contaminants can be retained through their attachment to the membrane of a microorganism or absorption by inclusions in the form of bodies [78, 79]. At the intra- and extracellular level, toxic chemical compounds can be immobilized through the formation of minerals.

Another important mechanism for soil remediation is using microorganisms to generate exopolymer substances. For example, polysaccharides bind pollutants and they can be simultaneously removed from polluted environments during flocculation. The composition and properties of such polymers depend on the factors listed above, as well as the availability of various useful substances and the contents of salts and heavy metals in the soil [80].

Interaction between plants and microorganisms for bioremediation. An effective mechanism for cleaning transformed landscapes is to use microorganisms that promote plant growth in a polluted environment. They help capture nitrogen and create phytohormones, as well as produce antibiotics for plant protection. For example, introducing Sinorhizonium meliloti in the zone of plant roots increases the level of photosynthetic proteins.

Figure 2 shows the influence of biotic and abiotic factors on plants.

Bacteria help plants survive under stress conditions (drought, nutritional deficiencies, toxicants). Their survival is facilitated by metabolites such as amino acids, isoflavonoids, flavonoids, and fatty acids. Bacteria can reproduce in mycorrhizal and non-mycorrhizal roots. In a stressful environment, they stimulate the production of special transport proteins and chaperones by plants. For example, the GroEL and DnaK proteins benefit the body under such stress conditions as temperature, drought, and exposure to toxicants [51].

Intensive plant growth is due to bacteria’s ability to produce substances such as auxin, cytokinin, gibberellin, hydrogen cyanide, siderophores, indoleacetic acid, and others [81]. In addition, rhizobacteria are able to prevent the effects of unwanted pathogens and insects [79]. Host plants help these bacteria reproduce by providing them with bioactive substances (flavonoids, glycosides, fatty acids, and others) [82].

Prospects for using the microorganism-plant system for soil decontamination. The benefit of the microorganism-plant system is in reducing the anthropogenic impact on both industrially transformed landscapes and agrogenic soils.

Heavy metals pose a great danger to human and animal health. Pinter et al. found that phytoremediation was enhanced by a combined use of As-resistant grapevine species and microorganisms such as Bacillus licheniformis, Micrococcus luteus and P. fluorescens. This activated siderophore production, phosphate solubilization, and nitrogen fixation [83].

In another study, Jiang et al. isolated microorganisms that improve plant adaptation to the environment from the rhizosphere of plants growing in polluted areas of chemical and oil refineries. In particular, they isolated Pseudomonas, Cupriavidus, and Bacillus from the rhizosphere of Boehmeria nivea. These bacteria are resistant to Pb2+ > Zn2+ > Cu2+> Cd2+ and therefore help plants survive in the soil with high concentrations of heavy metals [84].

Jiang et al. studied the effect of arbuscular mycorrhizal fungi G. versiforme and R. intraradices on the growth, Cd absorption, and antioxidant properties of Japanese honeysuckle (Lonicera japonica L.). They found a decreased concentration of cadmium in the plant’s shoots and roots. Mycorrhizal fungi increased the biomass of shoots and roots, contributed to the accumulation of phosphorus, and activated such enzymes as catalase (CAT), ascorbate peroxidase (APX), glutathione reductase (GR), and others [85].

A promising symbiosis for soil remediation is between hyperaccumulators, grain crops, and mycorrhizal fungi. Studies by Yang et al. showed that a combined use of rice crops, hyperaccumulator Solanum nigrum L., and arbuscular mycorrhiza lowered the concentration of cadmium in this strategic culture to 64.5%. Low bioaccumulation was also due to decreased expression of the Nramp5 gene and decreased activation of the HMA3 gene in rice roots. In addition, a decline in pH was observed in the plant’s rhizosphere. These studies are promising for agricultural production [86].

In another study, pepper (C. annuum L.) was inoculated with arbuscular mycorrhizal fungi F. mosseae and R. intraradices in the soil that contained copper (8 mM). It resulted in a high accumulation of dry biomass and a large leaf area (30 and 50%, respectively) [67].

The presence of arsenic in groundwater can have negative consequences. Mallick et al. identified a microbial consortium of resistant halophilic strains Kocuria flava AB402 and Bacillus vietnamensis AB403 from the rhizosphere of mangrove thickets. These microorganisms were resistant to arsenic concentrations from 20 to 35 mM. Also, the consortium adsorbed arsenic both inside cells and on the surface of biofilms. The strains facilitated better germination of rice seedlings and reduced toxicity [87].

Lyubun and Chernyshova studied the influence of Aeromonas sp. MG3, Alcaligenes sp. P2, Acinetobacter sp. K7, and Azospirillum brasilense Sp245 on the growth of, and arsenic absorption by, various plants. In particular, they selected sugar sorghum (Sorghum saccharatum L.), Sudan grass (Sorghum sudanense L.) and sunflower (H. annuus L.). The addition of arsenic had a negative effect of the plants’ growth and development, reducing their biomass and height by 30–50%. However, their bioproductivity was restored by the rhizobacteria introduced into the soil. In particular, the use of A. brasilense Sp245 and Acinetobacter sp. K7 reduced the level of arsenic in the sunflower biomass [88].

Well studied is the positive effect of legumes and rhizobia on plant resistance to pollutants. Current studies are looking for new combinations with rhizobacteria. For example, a combined use of P. mucilaginosus rhizobacteria and S. meliloti rhizobia resulted in the absorption of copper by alfalfa. The microorganisms decreased lipid peroxidation and radicals accumulation, improving the plant’s antioxidant properties and survival rate. In addition, the consortium enhanced the biochemical properties of the soil, contributing to increased contents of nitrogen, available phosphorus, and organic matter. Finally, the rhizosphere microorganisms became more diverse [89].

Shen et al., who used M. sativa L. together with rhizobia and urea (nitrogen source) observed the plant’s resistance to copper. Nitrogen content was the dominant factor of the pollutant’s absorption. The scientists concluded that the combination of rhizobia with urea had a beneficial effect on soil remediation. As a result, copper consumption was 89.3% higher in the shoots and 1.5 times as high in the roots, compared to the control. In addition, rhizobia improved the plant’s tolerance to oxidative stress, activated catalase, superoxide dismutase, and peroxidase in the roots and shoots, and increased the content of chlorophyll in the green organs [90].

In another study, castor bean was cultivated on a substrate saturated with lead and zinc, which resulted in a significantly smaller root surface area. The plant’s inoculation with a bacterial mix, including phosphatesolubilizing Actinobacteria, contributed to its growth and good development of the root system, regardless of the presence of lead or zinc [91].

An association of arbuscular mycorrhizal fungi can also be effective in the phytoremediation of soil contaminated with hexavalent chromium [92]. Kullu et al. have found that Rhizophagus irregularis promotes the bioaccumulation of chromium by Brachiaria mutica (paragrass or buffalo grass). Fungal inoculation decreased the degree of soil contamination and made the pollutant more bioavailable for the plant. Mycorrhiza has a positive effect on plants growing in the soil contaminated with 60 mg/kg of hexavalent chromium. The experiment by Kullu et al. showed increased contents of carotenoids, chlorophyll, proline, protein, and protein-enzymes (ascorbate peroxidase, catalase, and glutathione peroxidase). In addition, the plant had improved electron transfer and photosynthetic characteristics. The scientists concluded that R. irregularis was compatible with the B. mutica population [93].

Islam and Yasmeen evaluated the effect of P. aeruginosa on wheat’s resistance to oxidative stress caused by 1500 mg/kg of zinc. The study showed that adding the rhizobacteria to the plant’s rhizosphere increased the content of antioxidant enzymes, phenolic compounds, and ascorbic acid. This reduced the pollutant’s adverse effect on wheat biomass [60].

Another experiment determined the reaction of a consortium of E. ludwigii (HG 2) and K. pneumoniae (HG 3) to soil contamination with 75 μM of mercury. This resulted in increased biomass and relative water content in wheat, compared to the control [61].

The above studies have shown the benefits of microbiological associations in remediating natural, agrogenic, and industrial lands destroyed or contaminated with heavy metals and organic toxicants.


Anthropogenic impact in industrially developed regions leads to complete transformation of natural landscapes. This has a negative effect on all living systems (plants, animals, and microbocenoses) and causes medical and social problems associated with an increased incidence of all diseases, including the most severe ones.

Our review of scientific literature revealed a variety of methods for soil reclamation and remediation. The most promising and accessible methods are those involving plant communities. Plants can utilize toxicants, convert them into less stable compounds or transfer them to mineral complexes.

Another promising method is to introduce consortia of various microorganisms into the plant’s rhizoplane. This approach is effective due to symbiotic interaction. On the one hand, microorganisms convert hard-to-reach minerals and heavy metals into other forms digestible for plants. On the other hand, they actively use plant metabolites for their own life support.

Examples from scientific literature show that consortia can develop bioactive substances, vitamins, and phytohormones for living systems to increase their stress resistance to biotic and abiotic environmental factors.

Rhizobacteria, rhizobia, mycorrhizal fungi, and their consortia have proved to be the most efficient in technogenic land remediation.

The authors declare that there is no conflict of interest.
This work was part of the state assignment on “Developing approaches to phytoremediation of post-technogenic landscapes using “omix” technology plant growth promoting rhizobacteria (PGPB)”; supplementary agreement No. 075-03-2021-189/4 dated 30.09.2021 (internal No. 075-GZ/H4140/679/4). The research was conducted on the equipment of the Research Equipment Sharing Center of Kemerovo State University.
  1. Dobrovolʹskiy GV. Degradatsiya i okhrana pochv [Soil degradation and protection]. Moscow: Lomonosov Moscow State University; 2002. 654 p. (In Russ.).
  2. Kudeyarov VN, Sokolov MS, Glinushkin AP. The soils of agrocenosis in Russia: current status, measures for improvement and rational use. Agrohimia. 2017;(6):3–11. (In Russ.).
  3. Androkhanov VA, Kulyapina ED, Kurachev VM. The soils of technogenic landscapes: genesis and evolution. Novosibirsk: Siberian Branch of the RAS; 2004. 151 p. (In Russ.).
  4. Androkhanov VA. Pochvenno-ehkologicheskoe sostoyanie tekhnogennykh landshaftov: dinamika i otsenka [Ecological state of technogenic landscapes: dynamics and assessment]. Novosibirsk: Siberian Branch of the RAS; 2010. 224 p. (In Russ.).
  5. Belozertseva IA, Granina NI. Influence of investigation, extraction and processing of minerals on ground of Siberia. Fundamental research. 2015;(10–2):238–242. (In Russ.).
  6. Baltic Sea hot spots – Hazards and possibilities for the Baltic Sea region. Coalition Clean Baltic; 2002. 47 p.
  7. Yanovsky AB. Results of structural reorganization and technological reequipment of the coal industry of the Russian federation and objectives for prospective development. Ugol’. 2019;(8):8–16.
  8. Baştabak B, Gödekmerdan E, Koçar G. A holistic approach to soil contamination and sustainable phytoremediation with energy crops in the Aegean Region of Turkey. Chemosphere. 2021:276.
  9. Fichtner A, von Oheimb G, Hardtle W, Wilken C, Gutknecht JLM. Effects of anthropogenic disturbances on soil microbial communities in oak forests persist for more than 100 years. Soil Biology and Biochemistry. 2014;70:79–87.
  10. Homburg JA, Sandor JA. Anthropogenic effects on soil quality of ancient agricultural systems of the American Southwest. Catena. 2011;85(2):144–154.
  11. Pundytė N, Baltrėnaitė E, Pereira P, Paliulis D. Anthropogenic effects on heavy metals and macronutrients accumulation in soil and wood of Pinus sylvestris L. Journal of Environmental Engineering and Landscape Management. 2011;19(1):34–43.
  12. Wall DH, Nielsen UN, Six J. Soil biodiversity and human health. Nature. 2015;528(7580):69–76.
  13. Ye F, Ma MH, Wu SJ, Jiang Y, Zhu GB, Zhang H, et al. Soil properties and distribution in the riparian zone: the effects of fluctuations in water and anthropogenic disturbances. European Journal of Soil Science. 2019;70(3):664–673.
  14. Chen J, Liu Y-Q, Yan X-W, Wei G-H, Zhang J-H, Fang L-C. Rhizobium inoculation enhances copper tolerance by affecting copper uptake and regulating the ascorbate-glutathione cycle and phytochelatin biosynthesis-related gene expression in Medicago sativa seedlings. Ecotoxicology and Environmental Safety. 2018;162:312–323.
  15. Wang Y, Wang R, Fan L, Chen T, Bai Y, Yu Q, et al. Assessment of multiple exposure to chemical elements and health risks among residents near Huodehong lead-zinc mining area in Yunnan, Southwest China. Chemosphere. 2017;174:613–627.
  16. Mun SA, Zinchuk SF. Assessment of environmentally dangerous areas and cancer morbidity in the Kemerovo region depending on the air pollution. Modern problems of science and education. 2015;(6). (In Russ.).
  17. Gomes HI, Dias-Ferreira C, Ribeiro AB. Electrokinetic remediation of organochlorines in soil: Enhancement techniques and integration with other remediation technologies. Chemosphere. 2012;87(10):1077–1090.
  18. Kambo HS, Dutta A. A comparative review of biochar and hydrochar in terms of production, physico-chemical properties and applications. Renewable and Sustainable Energy Reviews. 2015;45:359–378.
  19. Trujillo-Reyes J, Peralta-Videa JR, Gardea-Torresdey JL. Supported and unsupported nanomaterials for water and soil remediation: Are they a useful solution for worldwide pollution? Journal of Hazardous Materials. 2014;280:487–503.
  20. Wang Y, Luo Y, Zeng G, Wu X, Wu B, Li X, et al. Characteristics and in situ remediation effects of heavy metal immobilizing bacteria on cadmium and nickel co-contaminated soil. Ecotoxicology and Environmental Safety. 2020;192.
  21. Xu J, Bravo AG, Lagerkvist A, Bertilsson S, Sjöblom R, Kumpiene J. Sources and remediation techniques for mercury contaminated soil. Environment International. 2015;74:42–53.
  22. Murzakmatov RT, Shishikin AS, Borisov AN. Specifics of stand formation at coalmine dumps in forest-steppe zone. Siberian Journal of Forest Science. 2018;(1):37–49. (In Russ.). .
  23. Mandal P. An insight of environmental contamination of arsenic on animal health. Emerging Contaminants. 2017;3(1):17–22.
  24. Pandey P, Dubey RS. Metal toxicity in rice and strategies for improving stress tolerance. In: Hasanuzzaman M, Fujita M, Nahar K, Biswas JK, editors. Advances in rice research for abiotic stress tolerance. Woodhead Publishing; 2019. pp. 313–339.
  25. Nevedrov NP, Dyukanova EN, Nevedrova NYu. The concentration of heavy metals in the superficial horizons of soils in functional areas in Kursk cenourban agglomeration. Belgorod State University Scientific Bulletin. Natural Sciences. 2016;35(11):139–145. (In Russ.).
  26. Nejad ZD, Jung MC, Kim K-H. Remediation of soils contaminated with heavy metals with an emphasis on immobilization technology. Environmental Geochemistry and Health. 2018;40(3):927–953.
  27. Ilʹin VB, Syso AI. Mikroehlementy i tyazhelye metally v pochvakh i rasteniyakh Novosibirskoy oblasti [Trace elements and heavy metals in soils and plants of the Novosibirsk Region]. Novosibirsk: Siberian Branch of the RAS; 2001. 231 p. (In Russ.).
  28. Pronina NB. Ehkologicheskie stressy (prichiny, klassifikatsiya, testirovanie, fiziologo-biokhimicheskie mekhanizmy) [Environmental stresses (causes, classification, testing, physiological and biochemical mechanisms)]. Moscow: MSKHA; 2000. 310 p. (In Russ.).
  29. Selyukova SV. Heavy metals in agrocenoses. Achievements of Science and Technology in Agro-Industrial Complex. 2020;34(8):85–93. (In Russ.).
  30. Li H, Xu W, Dai M, Wang Z, Dong X, Fang T. Assessing heavy metal pollution in paddy soil from coal mining area, Anhui, China. Environmental Monitoring and Assessment. 2019;191(8).
  31. Li F, Li X, Hou L, Shao, A. Impact of the coal mining on the spatial distribution of potentially toxic metals in farmland tillage soil. Scientific Reports. 2018;8(1).
  32. Xiuzhen T, Changyuan T, Pan W, Chipeng Z, Zhikang W. Distribution and food exposure risk assessment of heavy metals immature rice on the coal mining area Guizhou TAO. Ecology and Environmental Sciences. 2017;(26):1216–1220.
  33. Szynkowska MI, Pawlaczyk A, Maćkiewicz E. Bioaccumulation and biomagnification of trace elements in the environment. In: Chojnacka K, Saeid A, editors. Recent advances in trace elements. Wiley Blackwell; 2018. pp. 251–276.
  34. Ghori N-H, Ghori T, Hayat MQ, Imadi SR, Gul A, Altay V, et al. Heavy metal stress and responses in plants. International Journal of Environmental Science and Technology. 2019;16(3):1807–1828.
  35. Ashraf S, Ali Q, Zahir ZA, Ashraf S, Asghar HN. Phytoremediation: Environmentally sustainable way for reclamation of heavy metal polluted soils. Ecotoxicology and Environmental Safety. 2019;174:714–727.
  36. Asati A, Pichhode M, Nikhil K. Effect of heavy metals on plants: An overview. International Journal of Application or Innovation in Engineering and Management. 2016;5(3):56–66.
  37. Morcillo P, Esteban MÁ, Cuesta A. Heavy metals produce toxicity, oxidative stress and apoptosis in the marine teleost fish SAF-1 cell line. Chemosphere. 2016;144:225–233.
  38. Wijayawardena MAA, Megharaj M, Naidu, R. Exposure, toxicity, health impacts, and bioavailability of heavy metal mixtures. Advances in Agronomy 2016;138:175–234.
  39. Shah V, Daverey A. Phytoremediation: A multidisciplinary approach to clean up heavy metal contaminated soil. Environmental Technology and Innovation. 2020;18.
  40. Ansari AA, Naeem M, Gill SS, AlZuaibr FM. Phytoremediation of contaminated waters: An eco-friendly technology based on aquatic macrophytes application. Egyptian Journal of Aquatic Research. 2020;46(4):371–376.
  41. Petunkina LO, Zaushintsena AV, Shatilov DI. Optimizatsiya v sootnoshenii rekulʹtivantov dlya tselevogo ispolʹzovaniya na ugledobyvayushchem predpriyatii [Optimal ratios of recultivators for targeted use at a coal mining enterprise]. Ehkologicheskie problemy promyshlenno razvitykh i resursodobyvayushchikh regionov: puti resheniya. Sbornik trudov Vserossiyskoy molodezhnoy nauchno-prakticheskoy konferentsii [Environmental problems of industrially developed and resource regions: solutions. Proceedings of the All-Russian Youth Scientific and Practical Conference]; 2016; Kemerovo. Kemerovo: T.F. Gorbachev Kuzbass State Technical University; 2016. (In Russ.).
  42. Smit SEh, Rid DDzh. Mikoriznyy simbioz [Mycorrhizal symbiosis]. Moscow: Publishing House KMK; 2012. 776 p. (In Russ.).
  43. Wang B, Qiu Y-L. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza. 2006;16(5):299–363.
  44. Patra DK, Pradhan C, Patra HK. Toxic metal decontamination by phytoremediation approach: Concept, challenges, opportunities and future perspectives. Environmental Technology and Innovation. 2020;18.
  45. Cristaldi A, Conti GO, Jho EH, Zuccarello P, Grasso A, Copat C, et al. Phytoremediation of contaminated soils by heavy metals and PAHs. A brief review. Environmental Technology and Innovation. 2017;8:309–326.
  46. Yan L, Le QV, Sonne C, Yang Y, Yang H, Gu H, et al. Phytoremediation of radionuclides in soil, sediments and water. Journal of Hazardous Materials. 2021;407.
  47. Radziemska M, Gusiatin ZM, Bilgin A. Potential of using immobilizing agents in aided phytostabilization on simulated contamination of soil with lead. Ecological Engineering. 2017;102:490–500.
  48. Limmer M, Burken J. Phytovolatilization of organic contaminants. Environmental Science and Technology. 2016;50(13):6632–6643.
  49. Sharma P, Pandey AK, Udayan A, Kumar S. Role of microbial community and metal-binding proteins in phytoremediation of heavy metals from industrial wastewater. Bioresource Technology. 2021;326.
  50. Wilson-Kokes L, Skousen J. Nutrient concentrations in tree leaves on brown and gray reclaimed mine soils in West Virginia. Science of the Total Environment. 2014;481:418–424.
  51. Sharma M, Sudheer S, Usmani Z, Rani R, Gupta P. Deciphering the omics of plant-microbe interaction: Perspectives and new insights. Current Genomics. 2020;21(5):343–362.
  52. Tabassum B, Khan A, Tariq M, Ramzan M, Khan MSI, Shahid N, et al. Bottlenecks in commercialisation and future prospects of PGPR. Applied Soil Ecology. 2017;121:102–117.
  53. Ureche MAL, Pérez-Rodriguez MM, Ortiz R, Monasterio RP, Cohen AC. Rhizobacteria improve the germination and modify the phenolic compound profile of pepper (Capsicum annum L.). Rhizosphere. 2021;18.
  54. Essalimi B, Esserti S, Rifai LA, Koussa T, Makroum K, Belfaiza M, et al. Enhancement of plant growth, acclimatization, salt stress tolerance and verticillium wilt disease resistance using plant growth-promoting rhizobacteria (PGPR) associated with plum trees (Prunus domestica). Scientia Horticulturae. 2022;291.
  55. Rasool A, Mir MI, Zulfajri M, Hanafiah MM, Unnisa SA, Mahboob M. Plant growth promoting and antifungal asset of indigenous rhizobacteria secluded from saffron (Crocus sativus L.) rhizosphere. Microbial Pathogenesis. 2021;150.
  56. AlAli HA, Khalifa A, Al-Malki M. Plant growth-promoting rhizobacteria from Ocimum basilicum improve growthof Phaseolus vulgaris and Abelmoschus esculentus. South African Journal of Botany. 2021;139:200–209.
  57. Sultana S, Alam S, Karim MM. Screening of siderophore-producing salt-tolerant rhizobacteria suitable for supporting plant growth in saline soils with iron limitation. Journal of Agriculture and Food Research. 2021;4.
  58. Al Sbani NH, Abdullah SRS, Idris M, Hasan HA, Halmi MIE, Jehawi OH, et al. PAH-degrading rhizobacteria of Lepironia articulata for phytoremediation enhancement. Journal of Water Process Engineering. 2021;39.
  59. Kamaruzzaman MA, Abdullah SRS, Hasan HA, Hassan M, Othman AR, Idris M. Characterisation of Pb-resistant plant growth-promoting rhizobacteria (PGPR) from Scirpus grossus. Biocatalysis and Agricultural Biotechnology. 2020;23.
  60. Islam F, Yasmeen T, Ali Q, Ali S, Arif MS, Hussain S, et al. Influence of Pseudomonas aeruginosa as PGPR on oxidative stress tolerance in wheat under Zn stress. Ecotoxicology and Environmental Safety. 2014;104(1):285–293.
  61. Gontia-Mishra I, Sapre S, Sharma A, Tiwari S. Alleviation of mercury toxicity in wheat by the interaction of mercurytolerant plant growth-promoting rhizobacteria. Journal of Plant Growth Regulation. 2016;35(4):1000–1012.
  62. Kholssi R, Marks EAN, Miñon J, Mate AP, Sacristan G, Montero O, et al. A consortium of cyanobacteria and plant growth promoting rhizobacteria for wheat growth improvement in a hydroponic system. South African Journal of Botany. 2021;142;247–258.
  63. Bontemps C, Rogel MA, Wiechmann A, Mussabekova A, Moody S, Simon MF, et al. Endemic Mimosa species from Mexico prefer alphaproteobacterial rhizobial symbionts. New Phytologist. 2016;209(1):319–333.
  64. Poole P, Ramachandran V, Terpolilli J. Rhizobia: from saprophytes to endosymbionts. Nature Reviews Microbiology. 2018;16(5):291–303.
  65. Guo X, Yuan L, Shakeel M, Wan Y, Song Z, Wang D. Screening of the plant growth-promoting mycorrhizal fungi in Guizhou blueberry. Rhizosphere. 2021;19.
  66. Jiang Q-Y, Zhuo F, Long S-H, Zhao H-D, Yang D-J, Ye Z-H, et al. Can arbuscular mycorrhizal fungi reduce Cd uptake and alleviate Cd toxicity of Lonicera japonica grown in Cd-added soils? Scientific Reports. 2016;6.
  67. Ruscitti M, Arango M, Beltrano J. Improvement of copper stress tolerance in pepper plants (Capsicum annuum L.) by inoculation with arbuscular mycorrhizal fungi. Theoretical and Experimental Plant Physiology. 2017;29(1):37–49.
  68. Marrugo-Negrete J, Durango-Hernandez J, Pinedo-Hernandez J, Olivero-Verbel J, Díez S. Phytoremediation of mercury-contaminated soils by Jatropha curcas. Chemosphere. 2015;127:58–63.
  69. Han Y-H, Liu X, Rathinasabapathi B, Li H-B, Chen Y, Ma LQ. Mechanisms of efficient As solubilization in soils and As accumulation by As-hyperaccumulator Pteris vittata. Environmental Pollution. 2017;227:569–577.
  70. Dai H, Wei S, Twardowska I, Han R, Xu L. Hyperaccumulating potential of Bidens pilosa L. for Cd and elucidation of its translocation behavior based on cell membrane permeability. Environmental Science and Pollution Research. 2017;24(29):23161–23167.
  71. Forte J, Mutiti S. Phytoremediation potential of Helianthus annuus and Hydrangea paniculata in copper and leadcontaminated soil. Water, Air, and Soil Pollution. 2017;228(2).
  72. Chandra R, Kumar V, Singh K. Hyperaccumulator versus nonhyperaccumulator plants for environmental waste management. In: Chandra R, Dubey NK, Kumar V, editors. Phytoremediation of environmental pollutants. New York: CRC Press; 2017. pp. 43–80.
  73. Thakur S, Singh L, Wahid ZA, Siddiqui MF, Atnaw SM, Din MFM. Plant-driven removal of heavy metals from soil: uptake, translocation, tolerance mechanism, challenges, and future perspectives. Environmental Monitoring and Assessment. 2016;188(4).
  74. Pinto E, Aguiar AARM, Ferreira IMPLVO. Influence of soil chemistry and plant physiology in the phytoremediation of Cu, Mn, and Zn. Critical Reviews in Plant Sciences. 2014;33(5):351–373.
  75. Sharma SS, Dietz K-J, Mimura T. Vacuolar compartmentalization as indispensable component of heavy metal detoxification in plants. Plant Cell and Environment. 2016;39(5):1112–1126.
  76. Alvarez A, Saez JM, Davila Costa JS, Colin VL, Fuentes MS, Cuozzo SA, et al. Actinobacteria: Current research and perspectives for bioremediation of pesticides and heavy metals. Chemosphere. 2017;166:41–62.
  77. Kotoky R, Rajkumari J, Pandey P. The rhizosphere microbiome: Significance in rhizoremediation of polyaromatic hydrocarbon contaminated soil. Journal of Environmental Management. 2018;217:858–870.
  78. Thavamani P, Samkumar RA, Satheesh V, Subashchandrabose SR, Ramadass K, Naidu R, et al. Microbes from mined sites: Harnessing their potential for reclamation of derelict mine sites. Environmental Pollution. 2017;230:495–505.
  79. Romano-Armada N, Yañez-Yazlle MF, Irazusta VP, Rajal VB, Moraga NB. Potential of bioremediation and PGP traits in Streptomyces as strategies for bio-reclamation of salt-affected soils for agriculture. Pathogens. 2020;9(2).
  80. Martínez FL, Orce IG, Rajal VB, Irazusta VP. Salar del Hombre Muerto, source of lithium-tolerant bacteria. Environmental Geochemistry and Health. 2019;41(2):529–543.
  81. Laranjeira S, Fernandes-Silva A, Reis S, Torcato C, Raimundo F, Ferreira L, et al. Inoculation of plant growth promoting bacteria and arbuscular mycorrhizal fungi improve chickpea performance under water deficit conditions. Applied Soil Ecology. 2021;164.
  82. Toussaint J-P, Pham TTM, Barriault D, Sylvestre M. Plant exudates promote PCB degradation by a rhodococcal rhizobacteria. Applied Microbiology and Biotechnology. 2012;95(6):1589–1603.
  83. Pinter IF, Salomon MV, Berli F, Bottini R, Piccoli P. Characterization of the As(III) tolerance conferred by plant growth promoting rhizobacteria to in vitro-grown grapevine. Applied Soil Ecology. 2017;109:60–68.
  84. Jiang J, Pan C, Xiao A, Yang X, Zhang G. Isolation, identification, and environmental adaptability of heavy-metalresistant bacteria from ramie rhizosphere soil around mine refinery. 3 Biotech. 2017;7(1).
  85. Jiang Q-Y, Zhuo F, Long S-H, Zhao H-D, Yang D-J, Ye Z-H, et al. Can arbuscular mycorrhizal fungi reduce Cd uptake and alleviate Cd toxicity of Lonicera japonica grown in Cd-added soils? Scientific Reports. 2016;6.
  86. Yang X, Qin J, Li J, Lai Z, Li H. Upland rice intercropping with Solanum nigrum inoculated with arbuscular mycorrhizal fungi reduces grain Cd while promoting phytoremediation of Cd-contaminated soil. Journal of Hazardous Materials. 2021;406.
  87. Mallick I, Bhattacharyya C, Mukherji S, Dey D, Sarkar SC, Mukhopadhyay UK, et al. Effective rhizoinoculation and biofilm formation by arsenic immobilizing halophilic plant growth promoting bacteria (PGPB) isolated from mangrove rhizosphere: A step towards arsenic rhizoremediation. Science of the Total Environment. 2018;610–611:1239–1250.
  88. Lyubun Y, Chernyshova M. Use of rhizobacteria to inoculate agricultural crops grown on arsenic-polluted soil. Journal of Biotechnology. 2010;150.
  89. Ju W, Liu L, Fang L, Cui Y, Duan C, Wu H. Impact of co-inoculation with plant-growth-promoting rhizobacteria and rhizobium on the biochemical responses of alfalfa-soil system in copper contaminated soil. Ecotoxicology and Environmental Safety. 2019;167:218–226.
  90. Shen G, Ju W, Liu Y, Guo X, Zhao W, Fang L. Impact of urea addition and rhizobium inoculation on plant resistance in metal contaminated soil. International Journal of Environmental Research and Public Health. 2019;16(11).
  91. Li X, Feng C, Chen L, Liu F, Wang L, Luo K, et al. Cultivable rhizobacteria improve castor bean seedlings root and plant growth in Pb–Zn treated soil. Rhizosphere. 2021;19.
  92. Yadav KK, Gupta N, Kumar A, Reece LM, Singh N, Rezania S, et al. Mechanistic understanding and holistic approach of phytoremediation: A review on application and future prospects. Ecological Engineering. 2018;120:274–298.
  93. Kullu B, Patra DK, Acharya S, Pradhan C, Patra HK. AM fungi mediated bioaccumulation of hexavalent chromium in Brachiaria mutica-a mycorrhizal phytoremediation approach. Chemosphere. 2020;258.
Как цитировать?
Drozdova MYu, Pozdnyakova AV, Osintseva MA, Burova NV, Minina VI. The microorganism-plant system for remediation of soil exposed to coal mining. Foods and Raw Materials. 2021;9(2):406–418.
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