Аннотация и ключевые слова
Аннотация (русский):
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
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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.
Drozdova M.Yu. et al. Foods and Raw Materials, 2021, vol. 9, no. 2, pp. 406–418
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
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
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
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].
Drozdova M.Yu. et al. Foods and Raw Materials, 2021, vol. 9, no. 2, pp. 406–418
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
Drozdova M.Yu. et al. Foods and Raw Materials, 2021, vol. 9, no. 2, pp. 406–418
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,
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
Figure 1 Basic phytoremediation processes [44–50]
Table 1 Pollutant transformation processes in plants
Stages Process description
Rhizofiltration Pollutants are adsorbed by plant roots with a developed fibrous system. Plants secrete special organic
compounds in order to attract microbial communities [44].
Rhizodegradation Harmful substances are decomposed by various microorganisms, including bacteria, fungi, and yeast, which
live in the plant’s root system. This process removes such contaminants as pesticides, oil, and PCBs [45, 46].
Phytostabilization Harmful substances are immobilized in the soil and prevented from entering groundwater and then the food
chain. Stabilization is enabled by pollutants sorption in the plant’s rhizosphere [47].
Phytovolatilization Plants convert pollutants into volatile forms that enter the atmosphere [48].
Phytodegradation Organic substances are biodegraded in the plant under the action of various enzymes such as peroxidase,
dehalogenase, nitroreductase, and others [35, 49].
Phytoextraction The plant’s roots accumulate toxicants which then enter its aerial parts [35].
Drozdova M.Yu. et al. Foods and Raw Materials, 2021, vol. 9, no. 2, pp. 406–418
consortia improve the soil’s bioactivity and ecological
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
Table 2 Microorganisms for remediation of transformed soils
Microorganisms Source of extraction Positive effect on the plant Reference
Cellulosimicrobium 60I1 and Pseudomonas 42P4 Capsicum annuum L. Increased growth rate,
protection against abiotic
Pseudomonas stutzeri Pr7 and Bacillus toyonensis Pr8 Prunus domestica L. Increased growth rate,
antifungal activity, improved
disease resistance
Brevibacterium frigoritolerans (AIS-3), Alcaligenes faecalis
subsp. Phenolicus (AIS-8) and Bacillus aryabhattai (AIS-10)
Crocus sativus L. Increased growth rate,
antifungal activity
Pseudomonas alcaliphila and Pseudomonas hunanensis Ocimum basilicum L. Improved growth [56]
B. aryabhattai MS3 Rice root zone Resistance to salt stress
and iron restriction
Pseudomonas toyotomiensis ND1 (E), Microbacterium resistens
ND2 (G), and Bacillus pumilus. train ND3 (I)
Lepironia articulata L. Biodegradation
of polycyclic aromatic
Aeromonas taiwanensis isolate 5E, Bcillus sp. isolate 7G,
Bacillus cereus isolate 8H and 3Ca, Bacillus velezensis isolate
9I, Bacillus proteolyticus isolate 4D, Bacillus stratosphericus
isolate 14N, Bacillus megaterium isolate 11K, Pseudomonas sp.
isolate 12L, Enterobacter cloacae
Scirpus grossus L. Improved disease
Pseudomonas aeruginosa Arable land exposed to
industrial effluent
Resistance to oxidative
stress, increased chlorophyll
content, improved growth,
zinc resistance
Enterobacter ludwigii (HG2) and Klebsiella pneumoniae Rhizosphere of plants
from contaminated
Improved growth, resistance
to mercury-caused oxidative
Consortium of cyanobacteria: Calothrix sp. and Anabaena
cylindrica and rhizobacteria: Chryseobacterium balustinum,
Pseudomonas simiae, and Pseudomonas fluorescens
Irrigated field horizon Improved growth [62]
alpha proteobacteria from the genera Rhizobium and Ensifer Mimosa spp. Nitrogen fixation [63]
Sinorhizobium medicae Medicago sativa L. Nitrogen fixation [64]
Rhizobium leguminosarum bv. Trifolii Trifollium spp. Nitrogen fixation [64]
Mycorrhizal fungi:
42 genera of endophytic fungi, with a prevalence
of Chaetomium spp. and Fusarium spp.
Blueberry Improved growth [65]
Glomus versiforme and Rhizophagus intraradices Zea mays L. Resistance to cadmiumcaused
oxidative stress
Funneliformis mosseae, R. intraradices Trifolium repens L. Improved growth,
resistance to coppercaused
oxidative stress
Drozdova M.Yu. et al. Foods and Raw Materials, 2021, vol. 9, no. 2, pp. 406–418
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
Figure 2 Interaction of plants with biotic and abiotic factors
Drozdova M.Yu. et al. Foods and Raw Materials, 2021, vol. 9, no. 2, pp. 406–418
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.
Drozdova M.Yu. et al. Foods and Raw Materials, 2021, vol. 9, no. 2, pp. 406–418
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
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
Rhizobacteria, rhizobia, mycorrhizal fungi, and
their consortia have proved to be the most efficient in
technogenic land remediation.
The authors were equally involved in writing the
manuscript and are equally responsible for plagiarism.
The authors declare that there is no conflict of

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