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  <journal-meta>
   <journal-id journal-id-type="publisher-id">Foods and Raw Materials</journal-id>
   <journal-title-group>
    <journal-title xml:lang="en">Foods and Raw Materials</journal-title>
    <trans-title-group xml:lang="ru">
     <trans-title>Foods and Raw Materials</trans-title>
    </trans-title-group>
   </journal-title-group>
   <issn publication-format="print">2308-4057</issn>
   <issn publication-format="online">2310-9599</issn>
  </journal-meta>
  <article-meta>
   <article-id pub-id-type="publisher-id">46739</article-id>
   <article-id pub-id-type="doi">10.21603/2308-4057-2021-2-406-418</article-id>
   <article-categories>
    <subj-group subj-group-type="toc-heading" xml:lang="ru">
     <subject>Review Article</subject>
    </subj-group>
    <subj-group subj-group-type="toc-heading" xml:lang="en">
     <subject>Review Article</subject>
    </subj-group>
    <subj-group>
     <subject>Review Article</subject>
    </subj-group>
   </article-categories>
   <title-group>
    <article-title xml:lang="en">The microorganism-plant system for remediation of soil exposed to coal mining</article-title>
    <trans-title-group xml:lang="ru">
     <trans-title>The microorganism-plant system for remediation of soil exposed to coal mining</trans-title>
    </trans-title-group>
   </title-group>
   <contrib-group content-type="authors">
    <contrib contrib-type="author">
     <contrib-id contrib-id-type="orcid">https://orcid.org/0000-0002-9499-9470</contrib-id>
     <name-alternatives>
      <name xml:lang="ru">
       <surname>Drozdova</surname>
       <given-names>Margarita Yu.</given-names>
      </name>
      <name xml:lang="en">
       <surname>Drozdova</surname>
       <given-names>Margarita Yu.</given-names>
      </name>
     </name-alternatives>
     <email>drozdowa.margarita.00@yandex.ru</email>
     <xref ref-type="aff" rid="aff-1"/>
    </contrib>
    <contrib contrib-type="author">
     <contrib-id contrib-id-type="orcid">https://orcid.org/0000-0002-6854-0850</contrib-id>
     <name-alternatives>
      <name xml:lang="ru">
       <surname>Pozdnyakova</surname>
       <given-names>Anna V.</given-names>
      </name>
      <name xml:lang="en">
       <surname>Pozdnyakova</surname>
       <given-names>Anna V.</given-names>
      </name>
     </name-alternatives>
     <xref ref-type="aff" rid="aff-2"/>
    </contrib>
    <contrib contrib-type="author">
     <contrib-id contrib-id-type="orcid">https://orcid.org/0000-0002-4045-8054</contrib-id>
     <name-alternatives>
      <name xml:lang="ru">
       <surname>Osintseva</surname>
       <given-names>Maria A.</given-names>
      </name>
      <name xml:lang="en">
       <surname>Osintseva</surname>
       <given-names>Maria A.</given-names>
      </name>
     </name-alternatives>
     <xref ref-type="aff" rid="aff-3"/>
    </contrib>
    <contrib contrib-type="author">
     <name-alternatives>
      <name xml:lang="ru">
       <surname>Burova</surname>
       <given-names>Nadezhda V.</given-names>
      </name>
      <name xml:lang="en">
       <surname>Burova</surname>
       <given-names>Nadezhda V.</given-names>
      </name>
     </name-alternatives>
     <xref ref-type="aff" rid="aff-4"/>
    </contrib>
    <contrib contrib-type="author">
     <contrib-id contrib-id-type="orcid">https://orcid.org/0000-0003-3485-9123</contrib-id>
     <name-alternatives>
      <name xml:lang="ru">
       <surname>Minina</surname>
       <given-names>Varvara I.</given-names>
      </name>
      <name xml:lang="en">
       <surname>Minina</surname>
       <given-names>Varvara I.</given-names>
      </name>
     </name-alternatives>
     <xref ref-type="aff" rid="aff-5"/>
    </contrib>
   </contrib-group>
   <aff-alternatives id="aff-1">
    <aff>
     <institution xml:lang="ru">Kemerovo State University</institution>
     <city>Kemerovo</city>
     <country>Россия</country>
    </aff>
    <aff>
     <institution xml:lang="en">Kemerovo State University</institution>
     <city>Kemerovo</city>
     <country>Russian Federation</country>
    </aff>
   </aff-alternatives>
   <aff-alternatives id="aff-2">
    <aff>
     <institution xml:lang="ru">Kemerovo State University</institution>
     <city>Kemerovo</city>
     <country>Россия</country>
    </aff>
    <aff>
     <institution xml:lang="en">Kemerovo State University</institution>
     <city>Kemerovo</city>
     <country>Russian Federation</country>
    </aff>
   </aff-alternatives>
   <aff-alternatives id="aff-3">
    <aff>
     <institution xml:lang="ru">Kemerovo State University</institution>
     <city>Kemerovo</city>
     <country>Россия</country>
    </aff>
    <aff>
     <institution xml:lang="en">Kemerovo State University</institution>
     <city>Kemerovo</city>
     <country>Russian Federation</country>
    </aff>
   </aff-alternatives>
   <aff-alternatives id="aff-4">
    <aff>
     <institution xml:lang="ru">Kemerovo State University</institution>
     <city>Kemerovo</city>
     <country>Россия</country>
    </aff>
    <aff>
     <institution xml:lang="en">Kemerovo State University</institution>
     <city>Kemerovo</city>
     <country>Russian Federation</country>
    </aff>
   </aff-alternatives>
   <aff-alternatives id="aff-5">
    <aff>
     <institution xml:lang="ru">Kemerovo State University</institution>
     <city>Kemerovo</city>
     <country>Россия</country>
    </aff>
    <aff>
     <institution xml:lang="en">Kemerovo State University</institution>
     <city>Kemerovo</city>
     <country>Russian Federation</country>
    </aff>
   </aff-alternatives>
   <pub-date publication-format="print" date-type="pub" iso-8601-date="2021-11-02T00:00:00+03:00">
    <day>02</day>
    <month>11</month>
    <year>2021</year>
   </pub-date>
   <pub-date publication-format="electronic" date-type="pub" iso-8601-date="2021-11-02T00:00:00+03:00">
    <day>02</day>
    <month>11</month>
    <year>2021</year>
   </pub-date>
   <volume>9</volume>
   <issue>2</issue>
   <fpage>406</fpage>
   <lpage>418</lpage>
   <history>
    <date date-type="received" iso-8601-date="2021-10-05T00:00:00+03:00">
     <day>05</day>
     <month>10</month>
     <year>2021</year>
    </date>
    <date date-type="accepted" iso-8601-date="2021-10-27T00:00:00+03:00">
     <day>27</day>
     <month>10</month>
     <year>2021</year>
    </date>
   </history>
   <self-uri xlink:href="http://jfrm.ru/en/issues/1879/1972/">http://jfrm.ru/en/issues/1879/1972/</self-uri>
   <abstract xml:lang="ru">
    <p>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.&#13;
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.&#13;
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.&#13;
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.</p>
   </abstract>
   <trans-abstract xml:lang="en">
    <p>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.&#13;
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.&#13;
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.&#13;
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.</p>
   </trans-abstract>
   <kwd-group xml:lang="ru">
    <kwd>Technogenic landscapes</kwd>
    <kwd>heavy metals</kwd>
    <kwd>pollutants</kwd>
    <kwd>phytoremediation</kwd>
    <kwd>remediation</kwd>
    <kwd>mycorrhizal fungi</kwd>
    <kwd>rhizogenic microorganisms</kwd>
   </kwd-group>
   <kwd-group xml:lang="en">
    <kwd>Technogenic landscapes</kwd>
    <kwd>heavy metals</kwd>
    <kwd>pollutants</kwd>
    <kwd>phytoremediation</kwd>
    <kwd>remediation</kwd>
    <kwd>mycorrhizal fungi</kwd>
    <kwd>rhizogenic microorganisms</kwd>
   </kwd-group>
   <funding-group>
    <funding-statement xml:lang="ru">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).</funding-statement>
    <funding-statement xml:lang="en">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).</funding-statement>
   </funding-group>
  </article-meta>
 </front>
 <body>
  <p>INTRODUCTIONAreas of anthropogenically transformed soilscontinue to expand throughout the world. Soiltransformation is caused by degradation or completedestruction of topsoil as a result of deforestation, windand water erosion, pesticide pollution, mining, industrialand civil construction, and growing urbanization [1–6].Russia accounts for 15% of coal production andexport in the world [7]. One of its regions, KemerovoOblast-Kuzbass, has about 100 coal mines, of which halfare open-pit mines. In the first half of 2021, it produced116.84 million tons of high-quality coal, up 8% from theprevious year.Extraction of coal and other minerals transformstopsoil drastically, especially in case of opencast mining.407Drozdova M.Yu. et al. Foods and Raw Materials, 2021, vol. 9, no. 2, pp. 406–418Drilling and blasting are accompanied by enormous dustemissions that contain toxic pollutants, including heavymetals and carcinogenic gas (benzo(a)pyrene) [8–15].Large amounts of methane and carbon dioxide releasedinto the atmosphere have a greenhouse effect and changethe thermal regime, vegetation, and topsoil of the area.All this exacerbates health problems, such as a growthin oncological and cardiovascular diseases, as well ascongenital malformations [16].Active mining causes a serious ecologicalimbalance. In particular, it transforms or destroysnatural landscapes and creates new anthropogenicforms with different physical, chemical, and biologicalproperties. According to Rosprirodnadzor (Russia’senvironmental watchdog), the country had 194 225hectares of disturbed lands by 2019. Back in 2015, theCenter for Hygiene and Epidemiology in KemerovoOblast and the Kemerovo Center for Hydrometeorologyand Environmental Monitoring confirmed a strongcorrelation between increased coal mining, industrialproduction, and total emission of pollutants into the air.They identified eight ecologically vulnerable districts:Yaysky, Topkinsky, Tisulsky, Leninsk-Kuznetsky,Guryevsky, Prokopyevsky, Novokuznetsky, andMezhdurechensky.The above factors call for research that appliesmodern methods to monitor technogenic landscapesand introduce the latest complementary technologiesfor their remediation [17–21]. This can be doneby using living systems: plants and soil animalsand microorganisms. Of great importance areplant-microbial complexes: arbuscular ecto- andendomycorrhizae, symbiotic associations of plants andnitrogen-fixing prokaryotes, as well as rhizobial andcyanobacterial symbioses.Our aim was to assess the use of soil and rhizospheremicroorganisms for remediating technogenic soils inRussia’s coal-mining regions.STUDY OBJECT AND METHODSWe studied the scientific articles published over thepast five years, as well as those cited in Scopus and Webof Science.RESULTS AND DISCUSSIONThe Institute of Soil Science and Agrochemistry(Siberian Branch of the Russian Academy of Sciences)has developed theoretical and practical foundations forimproving the methods of recultivating technogenicsoils [3]. Unfortunately, the geobotanical approach todisturbed territories still prevails, with reclamation ofdumps by pine trees or perennial grasses [22]. Alongwith that, it is important to scientifically substantiatethe latest reclamation technologies, taking into accountthe biosystems of undisturbed soils in a particulargeographical zone.Until 2000, external dumps had been selectivelyformed during the exploitation of coal deposits.Overburden was selectively placed into the body ofthe dump. This method of reclamation was used toensure the rational use of the area’s land and developa harmonious anthropogenic landscape that met theecological, socioeconomic, and sanitary requirements byusing the fertile soil layer and potentially fertile species.Today, this method is not as common. The biologicalstage of forest and agricultural reclamation is noteffective due to the water regime and, consequently,insufficient moisture supply to the biota. Low moisturein the root layer and the presence of highly toxic heavymetals and other pollutants result in poor survivalamong trees and poor germination of perennial grassseeds.Irreversible soil degradation caused by technogenesismay have severe consequences for living systems.Of great concern is chemical pollution of landscapes,especially with heavy metals that are deposited andadsorbed in soil [23–27]. When the contents of metalsexceed the ecological capacity or change the redoxpotential (pH), pollutants are released. The humanbody 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 conditionallyessential (Cd, Pb, Sn, and Rb). They were found in lowconcentrations in plant and animal tissues, but theyare highly dangerous for human health even in thesmallest amounts [28]. Almost all regions of the worldhave a chemically “aggressive” environment. However,biochemical anomalies are more common in the zonesof industrial development of natural landscapes,during mineral extraction, and in urban industrialagglomerations. Agrogenic lands are polluted throughexcessive use of pesticides [29].According to Li et al., mining operations in Chinaresulted in increased copper and cadmium contentsin the soil used to grow rice. The environmental loadchanged in decreasing order from lead to chromium:Pb &gt; Cd &gt; Ni &gt; As &gt; Zn &gt; Cu &gt; Cr [30]. Moreover,lead, chromium, and cadmium exceeded the maximumpermissible concentrations in crop production2–8 times [31, 32]. Lead has the longest period ofclearance from the soil-plant system. Plants receiveits excessive quantities from soil. As a result, leadinhibits their respiration, suppresses photosynthesis,and sometimes increases the amount cadmium, whiledecreasing the intake of zinc, calcium, phosphorus, andsulfur.It has also been found that during coaltransportation, many pollutants are deposited onthe transport routes along with dust. Heavy metalsaccumulate in soils for a long time. Their excessiveamounts affect plant growth, metabolism, physiology,and aging. Plants have stress control mechanismsresponsible for maintaining homeostasis of the basicmetals that they require. These mechanisms makeplants tolerant to metal contamination by formingless toxic metal complexes with active metabolitesexcreted through the root system. Other mechanisms aretriggered by specific stress [31].408Drozdova M.Yu. et al. Foods and Raw Materials, 2021, vol. 9, no. 2, pp. 406–418Arsenic is the most dangerous inorganic substance.It does not immediately cause symptoms of poisoningin animals, but its concentrations in their blood,hair, hooves, and urine remain high in contaminatedareas. It belongs to a special group of conditionallyessential elements since it acts at the ionic level or aspart of nonspecific molecules or ions that penetrate theorganism of living systems.Heavy metals in soil have a detrimental effecton living organisms as a result of bioaccumulationand biomagnification [33]. Due to their impact onphysiological and biochemical processes, most pollutantsare toxic to plants [34]. The extent of toxicity dependson their content in soil, which can vary from 1 to 100000 mg/kg [35, 36]. Heavy metals are also dangerousbecause they can replace the ions of the main metals thatliving systems and humans need [37, 38]. This disturbsmetabolic processes and biochemical reactions duringfood consumption and removes metabolites from thebody. Excessive accumulation of heavy metals causesprotein compounds to break down at the molecular level,ruptures peptide bonds, increases free radicals, andseverely damages vulnerable organs (brain, kidneys,liver, and blood vessels).Phytoremediation is a well-known method ofcleaning contaminated soil by extracting pollutantsthrough the roots of trees, shrubs, and herbaceousplants [17, 39]. The results depend on the plants’tolerance to pollutants, the volume of biomass, andthe efficiency of pollutant transportation from rootsto shoots. Absorbed by the root system of plants,toxic elements accumulate in their tissues and aresubsequently decomposed or converted into saferforms [40].Russian and foreign researchers have recentlydeveloped efficient technologies to improve soil byphysical and chemical methods [10–14]. For example,scientists in Kemerovo Oblast have proposed combininga bioorganic remediation agent from industrial wastewith a technical agent to improve soil physicochemicallyand obtain a pollutant-free biomass of perennial grasses[41]. In another study, Altunina et al. developed aland reclamation method based on biocryogels. Theyhave high porosity, good mechanical strength, stabilityin any biotechnological environment, and thermalresistance. Plants in cryostructured soil develop a goodroot system and do not inhibit soil microflora (www.ipc.tsc.ru).Soil can also be remediated by sorbents producedfrom environmentally friendly materials, such as humicacids from naturally oxidized coals [25]. The cleaningmechanism is based on the introduction of reactioncenters into the composition of humic acids to bind withmetal ions.A mixture of dry lime and sapropel (5:1) can beused as an active natural sorbent. It is applied evenlyto the surface of soil contaminated with heavy metalsin an amount of 0.5–1.5 t/ha in early spring. Thesorbent improves the redox potential (pH) and thesoil’s absorbing capacity. Increased amounts of mineraland organomineral colloids contributes to activeaccumulation and long-term immobilization (3–5 years)of toxicants in the humus horizon, preventing themigration of heavy metals to other ecosystemcomponents (patent RU 2655215C1).Many studies report using groups of microorganismswith different biological functions to remove heavymetals, radionuclides, and organic compounds fromsoils. Microbiota used to clean soils, wastewater,bottom sediments, and overburden from pollution areable to extract elements and compounds from adjacentenvironments, convert them into less hazardous wasteproducts or transport them to plant tissues as nutrition.The most efficient groups of microorganisms are thosewith high symbiotic activity in relation to plants ofdifferent classes, families, genera, and species.Structurally largest is a group of arbuscularmycorrhiza with characteristic morphologicalstructures in the cells of the root cortex and somemycotallia in the form of arbuscules or vesicles [12].It has been established that by interacting witharbuscular mycorrhiza, host plants are often activelynourished with nitrogen and phosphorus [11, 13]. Justas important are groups of proteobacteria from thegenera Agrobacterium, Azospirillum, Azotobacter,Burkholderia, Bradyrizobium, Enterobacter, Pseudomonas,Klebsiella, Rizobium (Gram-negative), Bacillus,Brevibacillus, Paenibacillus (Gram-positive), aswell as Gram-positive actinomycetes (Rhodococcus,Streptomyces, Arhtrobacter).Mycorrhizal chains can form in soil to transportand exchange various substances, including mineralforms of nitrogen, phosphorus, and organic formsof C3 and C4 plants. Many representatives of theabove genera produce phytohormones, vitamins, andbioactive substances that stimulate plant growth,inhibit phytopathogenic diseases and harm frominsects, and increase the tolerance to soil salinity, airand soil drought, and oxidative stress [12–16, 22–26].Mycorrhizal chains are also involved in the removal oftoxic elements by precipitating or accumulating themboth inside cells and in the extracellular space. Theactivity of mycorrhizal networks is strongly influencedby soil animals: mites, amoeba, collembola, lumbricids,and others [42, 43].Mycorrhiza can be identified in plant groups andcommunities in any ecological zone of the world. Theirdevelopment depends on abiotic and biotic factors, suchas moisture and heat supply of the soil and atmosphere,altitudes above sea level, atmospheric pressure, varietyof vegetation, and the presence of phytopathogenicinfection or harmful animals (invertebrates andvertebrates). These factors are interdependent and canexert varying degrees of environmental pressure on thedevelopment of mycorrhizal networks in the rhizoplaneof plants. Mycorrhiza has been identified in 44% ofbryophytes, 52% of ferns, 100% of gymnosperms,and 85% of flowering plants. However, it has not been409Drozdova M.Yu. et al. Foods and Raw Materials, 2021, vol. 9, no. 2, pp. 406–418found in the families Caryophyllaceae, Cyperaceae,Brassicaceae, Chenopodiaceae, and others.Well studied is the interaction of plants and nitrogenfixingprokaryotes at the level of symbiotic, associative,and non-symbiotic nitrogen fixation. Lack of nitrogen inthe soil limits the bioproductivity of many plant species.Plants absorb nitrogen from the soil in the form ofnitrates, ammonium, and amino acids that are availableto them as a result of the microbiological destructionof organic litter (leaves, branches, fruits, etc.) ornitrogen fixation. Symbiotic nitrogen fixation occurs inspecialized structures of plants. Associative nitrogenfixation takes place in the rhizoplane or rhizosphereof roots and on the surface of leaves. Non-symbioticnitrogen fixation occurs through external sources oforganic matter or photosynthesis in cyanobacteria.The type of rhizobial symbiosis is associated withprokaryotes of the order Rhizobiales and plants fromthe Fabaceae family and Ulmaceae family (Parasponiassp.). Thanks to the short-lived nitrogen-fixingnodules on the plant roots, they are able to collect up to450–550 kg/ha of nitrogen per year. These bacteria areactive in wide pH ranges (5.0–8.5). In Siberia, activenitrogen-fixing nodules can be found on many species ofclover, astragalus and other plants.Actinorhizas of the order Frankia come intosymbiosis with over 200 species of dicotyledonousplants, including woody ones. These long-lived rootnodules collect up to 225 kg/ha of nitrogen per year.They can grow on pioneer substrates and easily functioneven in acidic boggy soils.Cyanobacteria are mainly of the Nostoc genus andsometimes of the Anabaena genus. They are localizedin the Azolla L. cavity, in intercellular spaces of cycadbark, on plant stems, and leaf petioles. Moisture and heatare the main conditions for their activation. Maximumnitrogen fixation is up to 720 kg/ha in Australia andmuch less in the boreal zone.Actinorhizal plants are of the families Betulaceae,Elaefgnaceae, Rozaceae, Datiscaceae, Ramnaceae andother species. Flowering plants that come into symbiosiswith cyanobacteria belong to the Gunneraceaegenus and are common for the southern hemisphere.Cyanobacteria function mainly under aerobic conditionsand can use their own photosynthesis or sources oforganic matter.Any type of symbiosis between plants andmicroorganisms can be used to clean the soilfrom pollutants. Figure 1 shows the main soilphytoremediation processes using microorganisms asplant symbionts.Table 1 shows the main stages and processes in theplant during the transformation of toxicants [35, 44–49].Plants and microorganisms can be mutuallybeneficial, which gives them an advantage in survivingcritical conditions. Microorganisms stimulate the plant’sgrowth and, at the same time, transform soil pollutantsinto a more accessible form.Pollutant-resistant bacteria and fungi can be isolatedfrom the rhizosphere of pollution-resistant plants [51].They are of particular value for biotechnologies toremediate lands contaminated with heavy metals andtoxic organic compounds [52]. Table 2 shows strains ofmicroorganisms that are currently of practical interestin the rehabilitation of lands contaminated by activeindustrial development and are of strategic importancefor the economic development of Russian regions [16,53–67].In addition to the strains listed in Table 2, moreactive consortia can be created to produce new soilvarieties that are effective and safe for the biota ofmicrobial communities, plants, and soil animals. SuchFigure 1 Basic phytoremediation processes [44–50]Table 1 Pollutant transformation processes in plantsStages Process descriptionRhizofiltration Pollutants are adsorbed by plant roots with a developed fibrous system. Plants secrete special organiccompounds in order to attract microbial communities [44].Rhizodegradation Harmful substances are decomposed by various microorganisms, including bacteria, fungi, and yeast, whichlive 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 foodchain. 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].410Drozdova M.Yu. et al. Foods and Raw Materials, 2021, vol. 9, no. 2, pp. 406–418consortia improve the soil’s bioactivity and ecologicalfunctions.Soil bioremediation by plants. All plants assimilatevery small quantities of copper, manganese, iron,nickel, and zinc. Along with this, there are plants thatare capable of absorbing highly toxic heavy metals,such as cadmium, arsenic, lead, mercury, and others,without serious damage to their growth. They are calledhyperaccumulators and are able to accumulate pollutantsin large quantities without signs of phytotoxicity in theaerial parts of plants. Metal hyperaccumulators absorbat least 100 mg/kg of arsenic and cadmium and 1000mg/kg of cobalt, copper, chromium, manganese, nickel,and lead. These plants include Pteris vittata, Bidenspilosa, Jatropha curcas, and Helianthus annuus [68–71].They can resist the harmful effects of heavy metals byaccumulating and suppressing them inside cells.Exposure to toxicants changes the expression ofgenes responsible for the synthesis of transporterproteins that capture and transfer metals [72]. In Siberia,and Kemerovo Oblast in particular, H. annuus is themost available plant of those listed. There are severalfamilies of genes responsible for metal transport. Theseinclude macrophage proteins (Nramps), heavy metalATPases, cation diffusion catalysts (CDFS), cationicantiporters, Zn-regulated transporter (ZRT), and the ZIPfamily [73].Pollutants are adsorbed by plants in two ways –by symplastic and apoplastic transport. In the case ofsymplastic transport, heavy metals diffuse into theTable 2 Microorganisms for remediation of transformed soilsMicroorganisms Source of extraction Positive effect on the plant ReferenceRhizobacteria:Cellulosimicrobium 60I1 and Pseudomonas 42P4 Capsicum annuum L. Increased growth rate,protection against abioticstress[53]Pseudomonas stutzeri Pr7 and Bacillus toyonensis Pr8 Prunus domestica L. Increased growth rate,antifungal activity, improveddisease resistance[54]Brevibacterium frigoritolerans (AIS-3), Alcaligenes faecalissubsp. Phenolicus (AIS-8) and Bacillus aryabhattai (AIS-10)Crocus sativus L. Increased growth rate,antifungal activity[55]Pseudomonas alcaliphila and Pseudomonas hunanensis Ocimum basilicum L. Improved growth [56]B. aryabhattai MS3 Rice root zone Resistance to salt stressand iron restriction[57]Pseudomonas toyotomiensis ND1 (E), Microbacterium resistensND2 (G), and Bacillus pumilus. train ND3 (I)Lepironia articulata L. Biodegradationof polycyclic aromatichydrocarbons[58]Aeromonas taiwanensis isolate 5E, Bcillus sp. isolate 7G,Bacillus cereus isolate 8H and 3Ca, Bacillus velezensis isolate9I, Bacillus proteolyticus isolate 4D, Bacillus stratosphericusisolate 14N, Bacillus megaterium isolate 11K, Pseudomonas sp.isolate 12L, Enterobacter cloacaeScirpus grossus L. Improved diseaseresistance[59]Pseudomonas aeruginosa Arable land exposed toindustrial effluentResistance to oxidativestress, increased chlorophyllcontent, improved growth,zinc resistance[60]Enterobacter ludwigii (HG2) and Klebsiella pneumoniae Rhizosphere of plantsfrom contaminatedareasImproved growth, resistanceto mercury-caused oxidativestress[61]Consortium of cyanobacteria: Calothrix sp. and Anabaenacylindrica and rhizobacteria: Chryseobacterium balustinum,Pseudomonas simiae, and Pseudomonas fluorescensIrrigated field horizon Improved growth [62]Rhizobia: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 prevalenceof Chaetomium spp. and Fusarium spp.Blueberry Improved growth [65]Glomus versiforme and Rhizophagus intraradices Zea mays L. Resistance to cadmiumcausedoxidative stress[66Funneliformis mosseae, R. intraradices Trifolium repens L. Improved growth,resistance to coppercausedoxidative stress[67]411Drozdova M.Yu. et al. Foods and Raw Materials, 2021, vol. 9, no. 2, pp. 406–418roots’ endothermal cells through the plasma membrane.Ions can be transported by such carriers as proteins ororganic acids, e.g., oxalic acid in combination withaluminum. In the case of apoplastic transport, metals arelocated in the free space between cells in non-cationicforms [39]. Special carrier proteins help pollutants todiffuse across the plasma membrane. There are specialcarriers for iron, zinc, and other metals [72, 74]. Varioussubstances produced by plants, such as metallothioneins,glutathione, and phytochelatins, bind metal ions and aretransported to vacuoles or shoots [74].In hyperaccumulator plants, chelates are transportedto shoots by membrane proteins: MATE, ATPase, andoligopeptide carrier proteins [72]. There, they are storedin vacuoles of parenchymal and epidermal leaf cells,which occupy 60 to 95% of the cell volume [75].The problem with toxicant absorption by plantsis 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, thesoil conditions need to be adjusted, namely redoxpotential (pH) and temperature. In addition to thesefactors, plants themselves create conditions for betterabsorption of heavy metals. In particular, they secretephytosiderophores and carboxylates, as well as acidifythe rhizosphere for better release of ions from thesoil [73].Soil bioremediation by microorganisms.Microorganisms use various mechanisms for thetransformation of pollutants. To survive in toxicenvironments, they transform compounds into safersubstances. Thus, toxicants can be removed both insideand outside the plant’s cells and tissues. To neutralizepollutants, microorganisms generate substances that arereleased into the environment and enhance the processesof 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 soilremediation [77].Soil contaminants can be retained through theirattachment to the membrane of a microorganism orabsorption by inclusions in the form of bodies [78, 79].At the intra- and extracellular level, toxic chemicalcompounds can be immobilized through the formationof minerals.Another important mechanism for soil remediationis using microorganisms to generate exopolymersubstances. For example, polysaccharides bind pollutantsand they can be simultaneously removed from pollutedenvironments during flocculation. The compositionand properties of such polymers depend on the factorslisted above, as well as the availability of various usefulsubstances and the contents of salts and heavy metals inthe soil [80].Interaction between plants and microorganismsfor bioremediation. An effective mechanism forcleaning transformed landscapes is to use microorganismsthat promote plant growth in a pollutedenvironment. They help capture nitrogen and createphytohormones, as well as produce antibiotics for plantprotection. For example, introducing Sinorhizoniummeliloti in the zone of plant roots increases the level ofphotosynthetic proteins.Figure 2 shows the influence of biotic and abioticfactors on plants.Bacteria help plants survive under stress conditions(drought, nutritional deficiencies, toxicants). Theirsurvival is facilitated by metabolites such as aminoacids, isoflavonoids, flavonoids, and fatty acids. Bacteriacan reproduce in mycorrhizal and non-mycorrhizalroots. In a stressful environment, they stimulate theproduction of special transport proteins and chaperonesby plants. For example, the GroEL and DnaK proteinsbenefit the body under such stress conditions astemperature, drought, and exposure to toxicants [51].Intensive plant growth is due to bacteria’s abilityto produce substances such as auxin, cytokinin,gibberellin, hydrogen cyanide, siderophores, indoleaceticacid, and others [81]. In addition, rhizobacteriaare able to prevent the effects of unwanted pathogensand insects [79]. Host plants help these bacteriareproduce by providing them with bioactive substances(flavonoids, glycosides, fatty acids, and others) [82].Prospects for using the microorganism-plantsystem for soil decontamination. The benefit ofthe microorganism-plant system is in reducing theanthropogenic impact on both industrially transformedlandscapes and agrogenic soils.Heavy metals pose a great danger to human andanimal health. Pinter et al. found that phytoremediationwas enhanced by a combined use of As-resistantgrapevine species and microorganisms such as Bacilluslicheniformis, Micrococcus luteus and P. fluorescens.This activated siderophore production, phosphatesolubilization, and nitrogen fixation [83].In another study, Jiang et al. isolated microorganismsthat improve plant adaptation to the environment fromFigure 2 Interaction of plants with biotic and abiotic factors412Drozdova M.Yu. et al. Foods and Raw Materials, 2021, vol. 9, no. 2, pp. 406–418the rhizosphere of plants growing in polluted areas ofchemical and oil refineries. In particular, they isolatedPseudomonas, Cupriavidus, and Bacillus from therhizosphere of Boehmeria nivea. These bacteria areresistant to Pb2+ &gt; Zn2+ &gt; Cu2+&gt; Cd2+ and therefore helpplants survive in the soil with high concentrations ofheavy metals [84].Jiang et al. studied the effect of arbuscularmycorrhizal fungi G. versiforme and R. intraradices onthe growth, Cd absorption, and antioxidant propertiesof Japanese honeysuckle (Lonicera japonica L.).They found a decreased concentration of cadmiumin the plant’s shoots and roots. Mycorrhizal fungiincreased the biomass of shoots and roots, contributedto the accumulation of phosphorus, and activated suchenzymes as catalase (CAT), ascorbate peroxidase (APX),glutathione reductase (GR), and others [85].A promising symbiosis for soil remediationis between hyperaccumulators, grain crops, andmycorrhizal fungi. Studies by Yang et al. showed that acombined use of rice crops, hyperaccumulator Solanumnigrum L., and arbuscular mycorrhiza lowered theconcentration of cadmium in this strategic culture to64.5%. Low bioaccumulation was also due to decreasedexpression of the Nramp5 gene and decreased activationof the HMA3 gene in rice roots. In addition, a declinein pH was observed in the plant’s rhizosphere. Thesestudies are promising for agricultural production [86].In another study, pepper (C. annuum L.) wasinoculated with arbuscular mycorrhizal fungiF. mosseae and R. intraradices in the soil that containedcopper (8 mM). It resulted in a high accumulationof dry biomass and a large leaf area (30 and 50%,respectively) [67].The presence of arsenic in groundwater can havenegative consequences. Mallick et al. identified amicrobial consortium of resistant halophilic strainsKocuria flava AB402 and Bacillus vietnamensis AB403from the rhizosphere of mangrove thickets. Thesemicroorganisms were resistant to arsenic concentrationsfrom 20 to 35 mM. Also, the consortium adsorbedarsenic both inside cells and on the surface of biofilms.The strains facilitated better germination of riceseedlings and reduced toxicity [87].Lyubun and Chernyshova studied the influence ofAeromonas sp. MG3, Alcaligenes sp. P2, Acinetobactersp. K7, and Azospirillum brasilense Sp245 on thegrowth of, and arsenic absorption by, various plants.In particular, they selected sugar sorghum (Sorghumsaccharatum L.), Sudan grass (Sorghum sudanense L.)and sunflower (H. annuus L.). The addition of arsenichad a negative effect of the plants’ growth anddevelopment, reducing their biomass and height by 30–50%. However, their bioproductivity was restored bythe rhizobacteria introduced into the soil. In particular,the use of A. brasilense Sp245 and Acinetobactersp. K7 reduced the level of arsenic in the sunflowerbiomass [88].Well studied is the positive effect of legumesand rhizobia on plant resistance to pollutants.Current studies are looking for new combinationswith rhizobacteria. For example, a combined use ofP. mucilaginosus rhizobacteria and S. meliloti rhizobiaresulted in the absorption of copper by alfalfa. Themicroorganisms decreased lipid peroxidation andradicals accumulation, improving the plant’s antioxidantproperties and survival rate. In addition, the consortiumenhanced the biochemical properties of the soil,contributing to increased contents of nitrogen, availablephosphorus, and organic matter. Finally, the rhizospheremicroorganisms became more diverse [89].Shen et al., who used M. sativa L. together withrhizobia and urea (nitrogen source) observed the plant’sresistance to copper. Nitrogen content was the dominantfactor of the pollutant’s absorption. The scientistsconcluded that the combination of rhizobia with ureahad a beneficial effect on soil remediation. As a result,copper consumption was 89.3% higher in the shoots and1.5 times as high in the roots, compared to the control.In addition, rhizobia improved the plant’s toleranceto oxidative stress, activated catalase, superoxidedismutase, and peroxidase in the roots and shoots,and increased the content of chlorophyll in the greenorgans [90].In another study, castor bean was cultivated on asubstrate saturated with lead and zinc, which resultedin a significantly smaller root surface area. The plant’sinoculation with a bacterial mix, including phosphatesolubilizingActinobacteria, contributed to its growthand good development of the root system, regardless ofthe presence of lead or zinc [91].An association of arbuscular mycorrhizal fungican also be effective in the phytoremediation of soilcontaminated with hexavalent chromium [92]. Kulluet al. have found that Rhizophagus irregularis promotesthe bioaccumulation of chromium by Brachiariamutica (paragrass or buffalo grass). Fungal inoculationdecreased the degree of soil contamination andmade the pollutant more bioavailable for the plant.Mycorrhiza has a positive effect on plants growingin the soil contaminated with 60 mg/kg of hexavalentchromium. The experiment by Kullu et al. showedincreased contents of carotenoids, chlorophyll,proline, protein, and protein-enzymes (ascorbateperoxidase, catalase, and glutathione peroxidase). Inaddition, the plant had improved electron transfer andphotosynthetic characteristics. The scientists concludedthat R. irregularis was compatible with the B. muticapopulation [93].Islam and Yasmeen evaluated the effect ofP. aeruginosa on wheat’s resistance to oxidative stresscaused by 1500 mg/kg of zinc. The study showed thatadding the rhizobacteria to the plant’s rhizosphereincreased the content of antioxidant enzymes, phenoliccompounds, and ascorbic acid. This reduced thepollutant’s adverse effect on wheat biomass [60].Another experiment determined the reaction of aconsortium of E. ludwigii (HG 2) and K. pneumoniae(HG 3) to soil contamination with 75 μM of mercury.413Drozdova M.Yu. et al. Foods and Raw Materials, 2021, vol. 9, no. 2, pp. 406–418This resulted in increased biomass and relative watercontent in wheat, compared to the control [61].The above studies have shown the benefitsof microbiological associations in remediatingnatural, agrogenic, and industrial lands destroyedor contaminated with heavy metals and organictoxicants.CONCLUSIONAnthropogenic impact in industrially developedregions leads to complete transformation of naturallandscapes. This has a negative effect on all livingsystems (plants, animals, and microbocenoses) andcauses medical and social problems associated with anincreased incidence of all diseases, including the mostsevere ones.Our review of scientific literature revealed a varietyof methods for soil reclamation and remediation.The most promising and accessible methods arethose involving plant communities. Plants can utilizetoxicants, convert them into less stable compounds ortransfer them to mineral complexes.Another promising method is to introduce consortiaof various microorganisms into the plant’s rhizoplane.This approach is effective due to symbiotic interaction.On the one hand, microorganisms convert hard-to-reachminerals and heavy metals into other forms digestiblefor plants. On the other hand, they actively use plantmetabolites for their own life support.Examples from scientific literature show thatconsortia can develop bioactive substances, vitamins,and phytohormones for living systems to increase theirstress resistance to biotic and abiotic environmentalfactors.Rhizobacteria, rhizobia, mycorrhizal fungi, andtheir consortia have proved to be the most efficient intechnogenic land remediation.CONTRIBUTIONThe authors were equally involved in writing themanuscript and are equally responsible for plagiarism.CONFLICT OF INTERESTThe authors declare that there is no conflict ofinterest.</p>
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