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Review

Soil Contamination by Heavy Metals and Radionuclides and Related Bioremediation Techniques: A Review

by
Yelizaveta Chernysh
1,2,*,
Viktoriia Chubur
1,2,
Iryna Ablieieva
1,3,
Polina Skvortsova
1,
Olena Yakhnenko
1,
Maksym Skydanenko
1,
Leonid Plyatsuk
1 and
Hynek Roubík
2,*
1
Departament of Ecology and Environmental Protection Technologies, Sumy State University, Kharkivska st. 116, 40007 Sumy, Ukraine
2
Department of Sustainable Technologies, Faculty of Tropical AgriSciences, Czech University of Life Sciences Prague, Kamýcká 129, 16500 Prague, Czech Republic
3
Department of Thematic Studies, Faculty of Arts and Sciences, Linköping University, SE-581 83 Linköping, Sweden
*
Authors to whom correspondence should be addressed.
Soil Syst. 2024, 8(2), 36; https://doi.org/10.3390/soilsystems8020036
Submission received: 15 February 2024 / Revised: 15 March 2024 / Accepted: 18 March 2024 / Published: 22 March 2024
(This article belongs to the Special Issue Research on Heavy Metals in Soils and Sediments)
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Abstract

:
The migration of heavy metals and radionuclides is interrelated, and this study focusses on the interaction and complex influence of various toxicants. The rehabilitation of radioactively contaminated territories has a complex character and is based on scientifically supported measures to restore industrial, economic, and sociopsychological relations. We aim for the achievement of pre-emergency levels of hygienic norms of radioactive contamination of output products. This, in its sum, allows for further economic activity in these territories without restrictions on the basis of natural actions of autoremediation. Biosorption technologies based on bacterial biomass remain a promising direction for the remediation of soils contaminated with radionuclides and heavy metals that help immobilise and consolidate contaminants. A comprehensive understanding of the biosorption capacity of various preparations allows for the selection of more effective techniques for the elimination of contaminants, as well as the overcoming of differences between laboratory results and industrial use. Observation and monitoring make it possible to evaluate the migration process of heavy metals and radionuclides and identify regions with a disturbed balance of harmful substances. The promising direction of the soil application of phosphogypsum, a by-product of the chemical industry, in bioremediation processes is considered.

1. Introduction

The pollution of soils by toxicants of different natures and origins is a current issue, as it disrupts the homeostasis of ecosystems. The soil is the starting point of the food chain, where all nutrients accumulate. Therefore, one of the most dangerous types of pollution associated with radioactive contamination and heavy metal contamination requires significant efforts in soil remediation [1,2].
An analysis of radioactive contamination of the territory of Europe with cesium-137 shows that about 35% of radionuclide fallout after the Chernobyl radiation accident on the European continent is located in the territory of Belarus. The contamination of Belarusian territory with cesium-137 with a density greater than 37 kBq/m2 amounted to 23% of the entire country’s area; for Ukraine, ~5%. In Ukraine, more than 3.5 million hectares of forest land is radioactively contaminated by accidental emissions from the Chornobyl nuclear power plant. A complex set of factors determines the current radiation situation in radioactively contaminated forests, in particular, the density of radioactive soil contamination, the composition of radionuclides, the physical and agrochemical properties of soils, etc., which determine the intensity of the biological circulation of radionuclides in ecosystems [3].
In research by Morooka et al. [4], areas affected by nuclear power plant (NPP) disasters are presented. Thus, 31 radioactive particles from surface soils were detected in an area 3.9 km northwest of the Fukushima-1 NPP. 134+137Cs had the highest activity ever recorded for Fukushima-1 NPP (6.1 × 105 and 2.5 × 106 Bq per particle after decay correction until March 2011). Taking into account their large size (120 μm), the impact of these particles on human health will be minimal, including radiation during static skin contact [4].
The polluting of soils with heavy metals and radionuclides can be natural or anthropogenic. Furthermore, different heavy metals have a specific accumulation rate and bioavailability based on the physical and chemical properties of soils; therefore, they have a different biomagnification rate, impact on human health, and ecological risk level [5]. In this regard, it is important to identify the main sources, fate, and specific features in the distribution of heavy metals and radionuclides in soils.
A complex interplay of biogeochemical processes, affected by factors such as pH, clay content, and redox potential, controls the transport and chemical stability of metallic contaminants in soil and sediment deposits. The transfer of heavy metals from the soil to plants depends on quantity factors, intensity factors, and reaction kinetics. These factors represent indicators of the overall quantity of potentially available elements, the activity and ionic ratios of elements in the soil solution, and the rate of transition of elements from the solid phase to the liquid phase and within the roots of the plant. Physical clay (particles < 0.01 mm) and silt particles (particles < 0.001 mm), which have a higher absorption capacity compared to larger fractions, have the greatest impact on the radionuclide mobility in soils. The addition of a silt fraction from chernozem or sod–podzolic soils to sand reduces the accumulation of Sr in oats and wheat by 1.5–2 times, and this effect is more significant for 137Cs. The transfer of 90Sr from soil to plants is four times higher on sandy soils compared to loamy soils. Similarly, the transfer rates for 137Cs and 60Co are 100 times and 40 times higher, respectively, on sandy soils [6]. According to the sorption efficiency of these isotopes, the soil is arranged in the following order: sod–podzolic soils (Albeluvisols), grey soils (Calcisols), yellow soils, red soils (Ferralsols, Alisols, and Acrisols), chestnut soils (Kastanozems), and black soils (Chernozem). Substantial transfer of radiocaesium to plants in sandy and sandy loam soils with a low content of clay minerals and organic matter has been reported [7]. However, within the same soil group, the nature of the uptake of 137Cs into plants may vary depending on the absorption capacity of the soil, the content of macro and microelements, and the pH of the soil solution. The sorption of 137Cs in the soil depends on the clay mineral content of the soil and K-saturation.
This effect of fine soil fractions is associated with a stronger fixation of radionuclides in them, which, in turn, is due to a larger specific surface of clay and silt particles and changes in the chemical properties of the soil: the content of exchangeable cations and organic matter, as well as the absorption capacity, increases [6]. In general, the effect of soil properties on the biological rate of radionuclides can be described as follows: the transfer of radionuclides to plants increases with a decrease in the content of clay, silt, organic matter, and the absorption capacity in the soil [8,9].
Adsorbed radionuclides are more strongly retained by organic mineral complexes than when sorbed in minerals of a different nature [10,11].
Summarising several studies, two soil management directions can be outlined:
  • Incorporating soil amendments can effectively fixate toxicants [12,13].
  • Supplying the soil with deficient nutrients is a method that helps plants resist heavy metal stress [14,15].
The type of soil should be taken into account for its effective treatment. For example, on loamy soils, the use of almost all types of fertilisers will increase yields and reduce the level of radioactive substances in plant products. On poorly mineralised and hydromorphic soils, the absorption of some radioactive substances can sometimes increase with the application of mineral fertilisers. Research on new fertiliser compositions (also biosolids) based on a combination of organic and mineral components of sustainable raw materials to increase the stability of soil–plant systems remains relevant [16,17]. Furthermore, resistance of the soil–plant system to radionuclides and heavy metals refers to the ability of the system to limit the mobility of chemical pollutants due to the inherent buffering properties of the soil, thus controlling the transition of the latter to the aerial part of the plant [18].
The migration of heavy metals and radionuclides is interrelated, and this study focusses on the interaction and complex influence of various toxicants. Therefore, this research aimed to review the problems of the rehabilitation of contaminated ecosystems and the areas of application of bioremediation processes for this purpose. According to the goal, the task was set as follows:
  • Review of the state of ecosystems contaminated with heavy metals and radionuclides.
  • Identification of the advantages and disadvantages of using biosorption technologies for the joint fixation of heavy metals and radionuclides.
  • Substantiation of the possibility of using phosphogypsum for soil bioremediation.

2. Methodological Approach

To implement the objectives of the review, taking into account the analysis of the general scheme of the pollution cycle to structure the impact and means of reducing it, a bibliometric analysis was used using data from the Scopus and Web of Science databases. For the systematisation of data and their management, Mendeley software (Elsevier, Amsterdam, The Netherlands) was used.
Therefore, the methodological approach to the literature analysis consists of the following steps described in the flowchart in Figure 1.
To validate the approach of using phosphogypsum in bioremediation, a comparative analysis of the elemental composition of phosphogypsum of various origins and locations was conducted in different regions of the world. This analysis was based on the results of research on Ukrainian phosphogypsum, as well as previous studies by other authors in different countries and regions around the world. This allowed for the synthesis of existing information on the subject and provided a rationale for recommending the genesis of suitable phosphogypsum for use in bioremediation processes. The main stages of the analysis are illustrated in Figure 2.
The ICP-OES method was used to analyse the elemental composition of phosphogypsum. The measurement protocol is shown in Table 1.

3. Review of the State of Ecosystems Contaminated with Heavy Metals and Radionuclides

3.1. Sources of Radionuclides and Heavy Metals in the Ecosystem

Soil is a complex mixture and a non-renewable natural resource, as it can only be restored on a geological timescale. Heavy metals, unlike biological compounds, are rarely biodegradable and therefore accumulate in the environment. Heavy metals in the soil have a toxicological effect on soil microorganisms, leading to a decrease in abundance and activity [8,19]. The relatively long half-life of radionuclides contributes to their long-term presence in the environment, leading to various health complications, such as cancer [20].
Table 2 shows that the mentioned metals have a common anthropogenic source. These activities have led to increased concentrations of heavy metals in the soil, contributing significantly to their occurrence in the environment [21,22].
The application of mineral fertilisers contributes to the increase in these elements (Cd, Pb, etc.) in the soil. Cu, Cr, As, Hg, Mn, Pb, or Zn enter the soil, along with other toxic chemicals, such as pesticides. The application of a wide variety of biosolids, such as livestock manure, composts, and sewage sludge, to the soil unintentionally leads to the accumulation of heavy metals such as As, Cd, Cr, Cu, Pb, Hg, Ni, Se, Mo, Zn, Tl, Sb, etc., in the soil [40,41]. The extensive mining and smelting of Pb and Zn ore have resulted in soil contamination that poses a risk to human and ecological health [42].

3.2. Monitoring of Radionuclides and Heavy Metals in Ecosystems and Impact on Humans: Ukraine CASE Study

Monitoring radioactive substances and heavy metals in the environment is essential since pollutants can accumulate and migrate in the elements of the trophic chain. Soil is an indicator of the ecological state of the environment. Proper organisation of background monitoring of contaminated areas allows for an effective assessment of the state of environmental objects, development of methods for biological soil remediation, and prediction of the future state of the biological environment. Therefore, the authors investigated [43] the migration and accumulation of heavy metals and radionuclides in the most significant protected areas of the Transcarpathian region and identified the main possible factors that affect the environmental monitoring process. As stated in Savchuk et al. [44], years after the Chernobyl disaster, the environmental situation in the Polesie zone of Ukraine remains difficult, as confirmed by the increased content of heavy metals in feed, milk, beef, and pork. The highest concentration of Pb was detected in coarse feed and sunflower cake and meal (2462 mg/kg and 1639 mg/kg); 41.9% and 60.0% of samples of these types of feed, respectively, had exceeded the maximum allowed concentrations of Cd.
The study revealed that coal mining in Jiangxi Province, China, causes radioactive uranium contamination and heavy metal contamination with zinc and cadmium in the soil, and the proposed in situ leaching method can be used to remediate contaminated soils, but with attention paid to the potential environmental risks to the soil [45]. The study by Mohuba et al. [46], conducted in the Thyspunt area of South Africa’s Eastern Cape province, a potential site for a nuclear power plant, revealed elevated levels of radionuclides, including 238U, 235U, 234U, 226Ra, 232Th, and 210Pb, mainly in rock formations of shale and quartzite due to the natural geochemistry of these rocks. This indicates the potential health risks associated with the ingestion of groundwater commonly used in the area. The study by Baghdady et al. [47] in the Bahariya Oasis of Egypt, located near large iron mines, identified elevated levels of Ba, Cr, Cu, Fe, and V in cultivated soils and Al, Cr, Cu, and V in uncultivated soils, exceeding acceptable limits, with the highest concentrations recorded in the northern oases near iron mines, while the highest values of activity concentrations, i.e., 40 K, were recorded in uncultivated soils rich in evaporites. The study by Mitrovic et al. [48] observed a significant decrease in soil 137Cs activity levels over a ten-year study period (2007–2017) in Palilula, Belgrade, with values declining from 16 Bq/kg to 3.9 Bq/kg; and in Surcin, Belgrade, from 18 Bq/kg to 12 Bq/kg. The study also identified variations in soil heavy metal concentrations and attributed the primary source of radionuclides and heavy metals to the widespread use of mineral phosphate fertilisers in agricultural fields.
In the context of the analysis performed, it is possible to define the main aspects of the effectiveness of soil-monitoring implementation [49]:
-
Availability of sufficient areas that are subject to minimal anthropogenic impact (for example, biosphere reserves, nature reserves, and national nature parks);
-
Selection of background monitoring criteria that would take into account the prevalence of individual substances in nature, their migration in the natural environment, and the presence of potential sources of their anthropogenic intake;
-
Selection of effective methods for monitoring the state parameters of environmental objects.
The impact of the Chornobyl accident is not limited to the exclusion zone. Studies were carried out in different regions of Ukraine and protected areas to establish the migration processes of radionuclides and heavy metals and the possible relationships between them. The determination of the heavy metal content in soils in the Carpathian Mountains region and bottom sediments and the absolute activity of gamma-active nuclides was measured by Symkanych et al. [43]. Based on the data obtained, a map of the distribution of the total gross content of heavy metals and radionuclides was formed, which allowed for the evaluation of the migration process and the identification of regions with a disturbed balance of harmful substances.
According to the data of Lee et al. [50], the monitoring of radioactive pollutants, mainly lying at a depth of 15 cm of the soil surface layer, can be carried out using several radiochemical analytical methods: plasma or laser spectrometry; and scintillation or semiconductor spectrometry. Plasma or laser spectrometry can effectively detect vertical variations in surface contamination only at a depth of about 10 cm because of its minimal penetration depth. Therefore, mobile scintillator spectrometry was proposed to comprehensively characterise the radioactive contamination of decommissioned nuclear facilities. In the study by Lee et al. [50], a mobile in situ scanning system, consisting of a gamma-ray spectrometer, was developed and tested for application in nuclear decommissioning sites. The results demonstrated its potential as an integrated performance-assessment tool for in situ monitoring at nuclear decommissioning sites.
Minimising the pollution of agricultural products is the main direction of the state in ensuring environmental safety and public health, as radionuclides enter the human body during the consumption of contaminated products. This relationship characterises the trophic chain: radioactive fallout–soil–agricultural plants–farm animals–humans [51].
It is possible to form three main migration flows of radionuclides that fell on the territory of Ukraine (Figure 3) [50,51,52].
The set of measures that prevents the entry of radionuclides into agricultural products includes the following [7,53]:
-
Natural autorehabilitation (radioactive decay, and fixation and redistribution of radionuclides in the soil);
-
Strengthening of biogeochemical barriers to fix radionuclides in soils, reducing the risk of radiation contamination of food;
-
Strengthening the radioecological monitoring of soils and agricultural products, radiological control, and compliance with recommendations for agricultural production.
The restoration of radioactive soils is carried out using methods based on such strategies as dry separation, soil washing, flotation separation, thermal desorption, electrokinetic remediation, phytoremediation, etc. The main factors that help to select soil-cleaning methods effectively include soil type, particle size, percentage of fine particles, and radionuclide characteristics [54].
The characteristics and composition of radioactive particles depend on the source of release, and emission scenarios affect the properties of these particles, which is directly essential for the transfer to the environment. Radioactive particles in the bio-environment can come in a variety of physical and chemical forms, ranging from low-molecular-weight particles, colloids, or nanoparticles to pseudocolloids, particles, and fragments. Therefore, information on the types of radionuclides that transform over time is important for assessing the state of contaminated areas and irradiated organisms [55,56]. Radioactive particles can also carry a certain amount of radioactivity and be point sources of radiological danger [57].
For the sorption of radionuclides and heavy metals, various matrices can be used. Basic rock-forming minerals (framework aluminosilicates) are better suited for immobilisation of radionuclides of alkaline and alkaline-earth element groups, as well as halogens, and the use of accessory minerals (phosphates, titanates, and titanium zirconate). As reviewed in our previous studies [14], matrix materials such as phosphates, zirconolites, and sphenes can be recommended for use. In more detail, it is worth dwelling on biosorption methods of ecosystem remediation, which are of increasing interest in applied technologies of radionuclide and heavy metal fixation.

4. Biotechnologies for Integrated Fixation of Heavy Metals and Radionuclides: Identification of Advantages and Disadvantages

4.1. Soil Bioremediation Methods

The soil rehabilitation process of microbes is carried out using mechanisms such as bioprecipitation, biosorption, bioaccumulation, bio-assimilation, bio-extraction, biodegradation, and biotransformation [58,59,60,61,62,63]. Some methods for fixing heavy metals and radionuclides are shown in Figure 4. In situ remediation, which involves treating the contaminated site directly in place, can be further subdivided into intrinsic bioremediation and engineered bioremediation. Intrinsic bioremediation occurs naturally without human intervention, while engineered bioremediation involves manipulating the environment to accelerate the degradation of the contaminant [64].
The connection between engineered bioremediation methods and physical and chemical treatment methods is to complement each other. Therefore, stage-by-stage soil remediation is needed, including physical, chemical, and biological treatment methods. Physical and chemical methods can precede biological methods and serve as a preliminary stage. Groudeva et al. [59] investigated the dissolution and removal of contaminants from soil using Na2CO3 and NaHCO3 solutions, linked to the activity of heterotrophic and basophilic chemo-lithotrophic microorganisms. This activity was intensified by the corresponding changes in environmental factors, such as water, oxygen, and nutrient levels. Furthermore, dissolved-impurities soil leachates were efficiently treated using a nearby natural wetland ecosystem [59].
In the context of mechanical and physicochemical soil remediation methods, the contaminated soil fraction is excavated and then transported to a designated disposal site, where it is stored and treated, incurring additional space requirements and transportation costs [60]. This approach has the disadvantage that it essentially relocates contamination to another location, necessitating ongoing monitoring of the previously contaminated soil and the surrounding environment. Furthermore, during the removal and transport of contaminated soil, there is a risk of spreading contaminated soil and dust particles.
Chemical or physicochemical remediation can be used as a standalone method (when heavy metal concentrations are less than 100 mg/L), but it is more advisable to use it as a preliminary step before biological remediation. The latter approach allows for the removal of heavy metals from an environment with concentrations significantly lower, but exceeding background levels due to pollution [61].
The chemical and physicochemical methods in the separate application require soil treatment with certain reagents and subsequent leaching with an organic or inorganic solvent, which can lead to deterioration of soil properties, creating an additional factor of destruction of natural soil properties, excluding the possibility of their further use [45].
There are many factors to consider when using physicochemical methods, e.g., pH, temperature, time, nature of the desorbing agent, etc., making the physicochemical method not always suitable, effective, or economically feasible [32]. For example, ion exchange, as a chemical treatment method, can be used to remove various types of metals from the soil but requires the replacement of ion exchange materials and can be expensive [56,63,65].
Compared to organic contaminants, heavy metals and radionuclides in soil cannot be destroyed but must either be converted into a stable form or removed. For this purpose, it is appropriate to use chemical methods to clean soils contaminated with heavy metals and radionuclides, which allow the reaction mixture to be applied directly to the contaminated area, while the topsoil that is being cleaned does not have a significant impact on the functioning of the ecosystem in general [66].
One such approach for the purification of heavy metal-contaminated chernozem soils involves the incorporation of a residual mixture of organic and mineral compost. In this scenario, pollutants are not extracted from the soil; instead, they are temporarily transformed into less readily available forms for plants over a specific duration, typically 4–5 years. However, this method itself does not provide a solution to the problem of removing pollutants from soils but can be combined with biological methods to achieve a positive effect.
The biological soil remediation of heavy metals and radionuclides is achieved through biotransformation. Microorganisms, such as bacteria, fungi, and microscopic algae that reside in the soil, are effective biotic entities that are capable of efficiently absorbing or transforming heavy metal and radionuclide compounds [67].
Heavy metals that penetrate living cells exhibit their toxic effects primarily in the form of ions. However, if heavy metals and radionuclides are transformed into bound forms through various means, they lose their toxic properties [68]. Consequently, heavy metals deposited in the cell wall in a crystalline or poorly soluble compound form become non-toxic to microorganisms but are eventually removed from the environment as a result of biological remediation.
The mechanisms through which microorganisms interact most frequently with heavy metals include biosorption (the sorption of metals on cell surfaces through physicochemical mechanisms), bioleaching (the mobilisation of heavy metals through the excretion of organic acids or methylation), biomineralization (the immobilisation of heavy metals through the formation of insoluble sulphides or polymeric complexes), bioaccumulation (intracellular accumulation), and enzyme transformation catalysis (oxidation-reduction reactions) (Figure 4) [69,70].
Biological methods of soil remediation offer partial solutions to challenges in this field. From an economic point of view, they provide benefits by avoiding the need for significant one-time investments. The associated costs can be spread over several years. These methods also eliminate the requirement for mandatory soil excavation and can be applied to larger areas. Furthermore, they avoid the introduction of specific harmful chemical mixtures, solutions, or reagents into the soil, thus preventing secondary pollution [71,72]. The general disadvantages of biological methods are their delayed effectiveness; long duration; and dependence on climatic conditions, including the rate of development of bioremediation organisms and biotransformations carried out by microorganisms in climatic conditions with variable temperature and humidity throughout the year [73,74].
Table 3 presents a classification of soil bioremediation methods. The approach chosen may vary depending on the concentration and type of target metals. It is also essential to consider an ecosystem-based approach within the context of interconnectedness because the soil environment interacts with water resources and the atmosphere, influenced by the biochemical activities of organisms in the natural components of the ecosystem [75,76,77].
Bioremediation-based processes can be considered a promising area based on the transformation of heavy metals and radionuclides into a less dangerous state and, at the same time, provide sustainable restoration of the environment. Thus, as part of the study of transformations of metals such as Pb, Zn, and Cd by Thakare et al., a number of regularities were identified. Metals cannot be decomposed by microorganisms involved in contaminated soil rehabilitation, but they can be changed from one oxidised form to another, allowing them to become fixed in insoluble form and be removed from biogeochemical cycles of migration in the environment [112].
Heavy-metal ions and radionuclides can usually be adsorbed by functional groups such as carbonyl, carboxyl, sulfhydryl, phosphate, sulphate, amino, and hydroxyl groups on the bacterial surface. The ability of bacteria to absorb heavy-metal ions generally varies from 1 mg/g to 500 mg/g [113]. Extracellular polymer substances consisting of proteins, lipids, nucleic acids, and complex carbohydrates play an important role in the adsorption of heavy-metal ions. These substances on the surface of the bacterial cell can prevent heavy metal toxicity and penetration into the inner cell region [112]. When studying the effect of metals on soil biological properties, it is feasible to use a set of methods, such as microbial biomass, C and N mineralisation, respiration, and enzyme activity, that will allow for a complete evaluation of this interaction [114].
In general, the following types of microorganisms are used in the bioremediation methodology [78]: Bacillus sp., Lysinibacillus sp., Rhodococcus sp., Ascomycota, Basidiomycota, Perenniporia subtephropora, Daldinia starbaeckii, Phanerochaete concrescens, etc.

4.2. Biosorption Technologies and Their Aspects of Realisation

Today, biosorption has been accepted as an environmentally friendly alternative green technology for the removal of various human-made pollutants, with the help of microbes such as bacteria, fungi, algae, and yeast. Pollutants are substances that do not decompose, are relatively unyielding, are insoluble in water, are impervious to microbial cells, and are harmful to lower and higher classes of living organisms. Desorbing eluents can be used to remove adsorbed pollutants, and biosorbent regeneration can be carried out by chemical, thermal, or electrochemical methods [115].
Fundamental to understanding the biosorption process is knowledge of the mechanism of the process. Based on cellular metabolism, biosorption mechanisms can be classified into independent and dependent mechanisms. Based on the location of biosorption, the following are distinguished [116,117,118,119,120,121]: (i) intracellular accumulation, (ii) extracellular accumulation and deposition, and (iii) cell surface sorption and deposition. The mechanisms belonging to the first two groups depend on metabolism and are caused by the processes of complexation, precipitation, and ion exchange; and the last group of mechanisms are also adsorption (physical and chemisorption).
The process of adsorption involves the attraction of other dissolved particles to the surface of a solid substance (adsorbent), primarily through adhesion, electrostatic attraction, and ion exchange. The adsorbent “fixes” all contaminants in its structure and thus purifies the sample [116].
An integrated approach is necessary for the restoration, regeneration, revegetation, and management of areas with a high level of anthropogenic loads, such as areas contaminated with heavy metals and radionuclides. Methods can be applied effectively for soil restoration, including some green activities, such as phytoremediation, and an appropriate soil cleanup process can be established. The enhancement of phytoremediation takes place through organic additives, namely agricultural waste and pretreated sewage sludge, biochar, humic substances, plant extracts, exudates, etc. [117].
At the same time, the commercialisation of biosorption technologies is hindered by technical problems associated with the operation and regeneration of native biosorbents. This problem is partially solved by immobilising microorganisms in a solid inert carrier, such as biochar, zeolites, and vermiculite, or by including them in an alginate gel. In this case, it becomes possible to apply a dynamic sorption process, the so-called “column variant” [118,119,120,121]. However, the sorption capacity of the biosorbent decreases significantly in comparison to static biosorption. Furthermore, there are still problems with biosorbent regeneration and replacement in the event of complete depletion.
The key advantages and disadvantages of biosorption technologies are shown in Figure 5. Biosorption is well suited for use in large areas of contaminated soil where other remediation methods are not economically feasible or difficult to implement practically and where soil productivity can be restored over long periods of time. It can be combined with other technologies, such as phytoremediation, for the final closure of the site with vegetation. In emergency situations or military action that involves the release of high concentrations of pollutants into the ecosystem, it is initially necessary to use physicochemical methods to quickly stop vertical and horizontal migration into natural components. Biosorption technology has some limitations that should be considered before choosing it for the remediation of areas contaminated with heavy metals and radionuclides: the prolonged duration of territorial restoration and the fixation and transformation of pollutants into less toxic forms have a long-term positive effect, but there is a potential risk of contamination through the food chain.
A biostimulation approach is used to improve biosorption processes. It includes stimulating the growth of microorganisms in a contaminated soil area to introduce pH-correcting substances, nutrients, surfactants, and oxygen [122], which requires further research.
However, it should be noted that there is a lack of information on the synergistic or inhibitory effect on the sorption processes of metal ions in multicomponent solutions with different ionic strengths, effective methods of immobilisation of microorganisms for the implementation of flow biosorption processes, selectivity and ways to increase it in the concentration of heavy metals, etc. This indicates the need to create a research algorithm for the study of biosorption processes using microorganisms.
Thus, to date, the following directions are relevant [60,123,124,125,126,127,128]:
-
Studies of microorganisms of different physiological groups (including the use of genetically modified strains) on the ability to sorb and transform soluble forms of heavy metals and radioactive elements into insoluble ones;
-
Bacterial reduction processes of technetium, chromium, and uranium when used as final electron acceptors in bacterial energy metabolism for the purpose of their detoxification in systems with neutral, acidic, and alkaline pH values;
-
Determining the products of bacterial transformation of radionuclides and heavy metals formed under different conditions;
-
Possibilities of reducing the toxic effects of heavy metals and radionuclides on soil microorganisms;
-
Development of nanobioremediation technology.

5. Possibility of Using Phosphogypsum for Soil Bioremediation

The use of phosphogypsum is associated with challenges that have gained increasing importance [129], as shown in Figure 6. Furthermore, it should be noted that phosphogypsum may be contaminated with radionuclides [130]. According to EPA data, phosphogypsum contains significant quantities of uranium and its decay products, such as radium-226, attributed to its presence in phosphate ores. The concentration of uranium in phosphate ores identified in the United States varies within the range of 0.26 to 3.7 Bq/g (7 to 100 pCi/g) [131]. However, various raw materials are used in different countries and regions globally; consequently, not all phosphogypsum exhibits elevated levels of radioactivity [129,132].
In order to address the development of environmentally friendly technologies for the use of phosphogypsum within the context of the bionics concept that integrates biological methods and structures for engineering solutions and technological approaches, it is necessary to improve the technical solutions and technologies for phosphogypsum utilisation in potential soil applications. A crucial element involves precise control over the composition of the soil solution through in situ synthesis of essential compounds directly within the soil. Given the present issue of soil degradation, there is a pressing need to actively explore novel soil management strategies. Furthermore, the effective resolution of this problem requires the availability of suitable design tools [18].
We emphasise the use of phosphogypsum, which does not have significant radioactive contamination, in bioprocesses. Therefore, Figure 7 shows the main elements of phosphogypsum that positively affect soil properties [133,134]. Furthermore, phosphogypsum has an impact on the growth of microorganisms, which has been confirmed by several studies [135,136,137,138,139]. Through the regulation of soil moisture, it is possible to significantly reduce the leaching of unproductive substances and address issues related to the hydromorphic regime of the soil, including the degradation of organic matter and the reduction of sulphate to sulphides. Moisture control also enhances the protective effect of the geochemical barrier “soil–rhizosphere”, effectively retaining harmful compounds within soil solution, particularly for Pb, Cd, and Sr [140].
Figure 8 shows the distribution of countries according to their publication activity in the phosphogypsum research documented in the Scopus database. Distribution of countries by publication activity in the field of phosphogypsum research according to the Scopus database.
Table 4 and Table 5 show a comparative analysis of the concentrations of elements in phosphogypsum from different countries.
Table 4 shows that the main components of calcium and sulphur oxides fluctuate in significant intervals in phosphogypsum samples from different regions of the world, with calcium in the range of 17.7–45.9 wt% and sulphur in the range of 17–51.4 wt%, respectively. At the same time, components such as iron, potassium, aluminium, magnesium, and manganese also have a significant difference in the amount of content in phosphogypsum from different locations of generation in the world. This is due to the technological process of production, but the special influence on changes in the content of trace elements is influenced by the raw materials used (phosphates and apatites).
In terms of the content of radionuclide isotopes, the data vary significantly depending on the region of phosphogypsum deposition. A review of previous studies [130,141,142] showed that radioactivity varies according to the type of phosphate ore and is mainly caused by the decay series U-238 and Th-232. Since U-235 is not as common in nature as U-238, the radiation of this decay series is not considered a threat [143]. However, the information about harmful impurities in phosphogypsum related to its environmental impact is not yet fully understood, which requires scientific evaluation in the future and the expansion of research in this area [144].
Therefore, it is worth concluding that Ukrainian phosphogypsum (in particular, from the Sumy region, since its samples were studied) is the most environmentally acceptable for bioremediation processes (Table 4 and Table 5):
-
Heavy metals (e.g., As, Pb, and Cr) have lower concentrations in phosphogypsum from the Sumy region than in phosphogypsum from China, Spain, the USA, and Brazil;
-
Some rare earth elements (such as La, Ce, Pr, and Y) are represented in phosphogypsum from the Sumy region (Ukraine) and less represented in phosphogypsum from other regions of the world.
However, this conclusion requires several further studies on the testing of Sumy phosphogypsum on different types of soil in bioremediation practice.
Table 4. Concentrations of major elements in phosphogypsum.
Table 4. Concentrations of major elements in phosphogypsum.
wt.%Ukraine aChina bUnited States cSpain dBrazil eIndia fMorocco gPoland hTunisia iFrance jGreece k
CaO22.9–31.431.6–43.322.7–39.4 17.7–32.631–3630.9–38.932.2–3529.6–42.730.7–37.231.3–33.434.30
SO329.8–3634–4922.9–51.930.7–4644.544.2–52.917–45.142.1–56.537.5–47n.m.41.50
SiO213.1–24.73.6–15.33.2–51.3n.m.0.80.5–4.30.3–9.70.4–1.81.0–3.80.6–1.5n.m.
Al2O30.96–2.520.08–2.590.069–1.14n.m.0.11–0.20.1–0.770.13–0.770.18–1.70.04–0.110.11–0.31n.m.
P2O50.63–0.790.68–1.820.5–3.80.49–1.180.07–1.290.82–1.040.59–1.621.50.8–1.690.36–0.69n.m.
Fe2O30.41–0.940.05–1.950,13–1.15n.m.0.25–0.770.1–0.560.15–0.830.06–0.200.03–0.13n.m.0.84
K2O0.1–0.320.17–0.330.02–0.90.020.040.030.05–0.4n.m.0.01–0.03n.m.n.m.
TiO20.05–0.170.04–0.270.03–0.46n.m.0.18–0.520.02–0.050.01–0.03n.m.n.m.n.m.n.m.
Na2O0.02–0.070.050.11–1.420.020.02–0.090.03–0.110.14–0.55n.m.0.05–0.290.02–0.19n.m.
MnO0.010.08–0.180.06–0.07n.m.0.004–0.017n.m.0.01n.m.n.m.0.0002–0.0004n.m.
MgO0.010.01–0.230.03–0.13n.m.0.02–0.760.02–0.560.21–0.54n.m.0.01–0.07n.m.0.13
a Ukraine (author’s results); b China [145,146,147,148,149]; c United States [150,151,152]; d Spain [153,154]; e Brazil [155,156,157]; f India [158,159,160]; g Morocco [161,162,163,164,165]; h Poland [166,167,168,169,170]; i Tunisia [171,172,173,174]; j France [175]; k Greece [176,177]; n.m., not measured.
Table 5. Concentrations of trace elements in phosphogypsum.
Table 5. Concentrations of trace elements in phosphogypsum.
ppmUkraine aChina bUnited States cSpain dBrazil eIndia fMorocco gPoland hTunisia iFrance jGreece k
Cu3.6–7.027.62.5–35.12.5–116.3–9n.m.1.5–2.93.396–9.65.4–17.513
As<4.967.150.77–20.10.6–8.56n.m.n.m.1.84–1.948.051n.m.0.61–17
Pb4.6–4.728.152.06–11.41.99–10.87.2–310.070.17–1.710.40.91.68–4.5711
Zn3.2–19.737.51.19–32.11.92–13.14.4–85.1n.m.3–28n.m.9–137n.m.12–123
Cr4.6–11.9371.69–20.23.59–20.311.1–14.72.735.85–115.96–13n.m.15.8–153
Ni1.4–1.716.60.21–17.790.87–2.675.4–1114.481.2–3003.60.94–4.1n.m.21
Cd1.19–6.360.480.28–10.81.39–2.83<0.1n.m.0.8–7.381.78–17.71.2–2.10.98–6.67
V1.6–2.227.50.38–10.72.9–12.86.9–9.2n.m.1.94–5n.m.2–31.43–3.91n.m.
Ga0.49–0.78n.m.n.m.n.m.9–10.4n.m.n.m.n.m.0.87n.m.n.m.
Sr981n.m.1.05–899360–5964884.9–6179.1n.m.530–778n.m.n.m.813.2–1275172–470
Ba20.5–27.221530.3–88.937767.1–6104n.m.23–63.3n.m.1092.36–215.638.3–331
Y197.2–148.87443.36106–14290–105.3n.m.127n.m.53.234.65–100.7n.m.
La195.3–137.136.5–4636.38n.m.921.1–1969n.m.60.74046.312.96–43.3524.9–30.5
Ce282.1–20030.6–3263.8419.5–81.22109.1–3547n.m.395374.46.53–18.7219.2–60.7
Pr46.7–33.455.01n.m.256.1–276.2n.m.118n.m.1.9–6.9n.m.
Eu0.98n.m.1.4n.m.23.7–25.9n.m.2.482n.m.0.49–1.70.85–1.08
Cs0.38n.m.n.m.n.m.<0.1n.m.n.m.n.m.0.05n.m.0.09–4.82
Th3.3–5.8n.m.n.m.1.167.2–81n.m.3.04–3.27n.m.0.740.22–1.390.59–10.1
a Ukraine (author’s results); b China [145,146,147,148,149]; c United States [150,151,152]; d Spain [153,154]; e Brazil [155,156,157]; f India [158,159,160]; g Morocco [161,162,163,164,165]; h Poland [166,167,168,169,170]; i Tunisia [171,172,173,174]; j France [175]; k Greece [176,177]; n.m., not measured.
The selective removal of Na+ and Cl− from soil, without affecting other macroelement ions, is an integral aspect of the scientific and technical field known as biogeosystem engineering. Biogeosystem engineering deals with engineering solutions and technologies, unprecedented in nature, aimed at managing the cycling of biogeochemical substances in gaseous, liquid, and solid phases. Its primary focus is the ecologically safe use of substances in soils, the improvement of resources and food products, and the solution of the production and environmental challenges in the noosphere through a unified technological cycle based on the principle of natural consistency. In the context of ensuring a quality environment for healthy living, the issue of phosphogypsum involves considering methods for its neutralisation as a more environmentally friendly alternative to the disposal in storage facilities [18,178]. However, for the reclamation of saline soils, neutralising phosphogypsum should be avoided, as its residual acids enhance the solubility of calcium compounds in the soil, promoting sodium displacement by calcium. Therefore, the supply of phosphogypsum to consumers in reusable containers for soil application appears to be a rational solution. Mixing phosphogypsum with ash from a power plant appears promising for optimising the use of by-products [179]. The lower the coal quality, the higher the CaO content in the ash, leading to a higher level of phosphogypsum neutralisation. Simultaneously, both materials can be recirculated in the soil.
In our previous study, Chernysh et al. [18], the introduction of phosphogypsum into the process of anaerobic fermentation of sustainable feedstock (sewage sludge, etc.) leads to the introduction of additional macroanalogues into the organo-mineral structure of digestate. It should be noted that the introduction of phosphorus and calcium compounds contained in phosphogypsum intensified the process of fixation of heavy metals and radionuclides in the sludge. As a result, calcium and potassium hydrogen phosphate compounds, which have the ability to adsorb radionuclides, were found in the mineral composition of the digestate [18].
The factors that influence the migration of radionuclides into the ecosystem and the impact of the organo-mineral complex on the fixation of heavy metals and radionuclides in soils are described in Figure 9.
Thus, the uptake of radionuclides by plants and their accumulation by chemicals in crop fields are largely dependent on the amount of their chemical analogues in the environment. An increase in the exchange capacity usually leads to an increase in the adsorption strength of radionuclide traces. Therefore, the accumulation of 137Cs by plants in most cases is inversely proportional to the absorption capacity of the soil and the amount of exchangeable K in it, and for 90Sr [3]. The uptake of 90Sr and 137Cs by plants decreases with an increase in the content of calcium and potassium in the soil or growing medium [18].

6. Conclusions

A review of studies of heavy metal content was conducted in radioactively contaminated areas. In particular, the sources of heavy metals and radionuclides in the soil and their impact on ecosystem services with inclusion in food chains were identified. This article discusses the important issue that is the remediation of soils contaminated with heavy metals and radionuclides, especially if these toxicants are present simultaneously in contaminated areas. Therefore, remediation methods should take into account the specificity of both of them.
The advantages and disadvantages of immobilising heavy metals and radionuclides are identified using biosorption methods. Technical problems associated with the use and regeneration of local biosorbents have hindered the commercialisation of biosorption technologies. The immobilisation of biomass on solid inert carriers (e.g., biochar, zeolite, and vermiculite) can partially solve this problem. However, the issue of regeneration and replacement of the biosorbent in case of its complete exhaustion arises. In addition, the directions for the use of phosphogypsum as a sorption carrier for soil bioremediation were determined. It is necessary to take into account the neutralisation of phosphogypsum in this field as a promising one, which requires further research within the framework of the development of the biogeosystem approach. It should be noted that the post-war restoration of the contaminated territories of Ukraine is a complex and strategic task within the framework of the global issue of food security.

Author Contributions

Conceptualisation, Y.C.; validation, H.R.; formal analysis, P.S., V.C. and M.S.; investigation, V.C. and P.S.; writing—original draft preparation, Y.C.; writing—review and editing, I.A., V.C., P.S., O.Y., L.P. and H.R.; visualization, I.A., P.S. and V.C.; funding acquisition, Y.C. and H.R.; supervision, H.R. All authors have read and agreed to the published version of the manuscript.

Funding

This project, “Phosphogypsum as a mineral resource for bioprocesses”, received funding through the MSCA4Ukraine project, which is funded by the European Union (Y.Ch.). This research project was carried out as planned research projects of the Department of Ecology and Environmental Protection Technologies of Sumy State University, related to the topics “Assessment of the technogenic load of the region with changes in industrial infrastructure” according to the scientific and technical programme of the Ministry of Education and Science of Ukraine (state registration no 0121U114478). Finally, we would like to acknowledge Technology Agency of the Czech Republic (Grant Number TH79020003; support for this project is offered under the coordination of the ERA-MIN3 action, which received funding from the European Union under the Horizon 2020 Programme (European Commission Grant Agreement No. 101003575).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data sets generated during and/or analysed during the current study are available from the corresponding author on request.

Conflicts of Interest

The authors declare that they have no competing interests.

References

  1. Zhang, J.; Chen, Q.; Tian, L.; Shi, K.; Wu, M. Environmental-Friendly Remediation Technology and Its Application in Heavy Metal Polluted Soil. Mater. Rep. 2023, 37, 21030018-11. [Google Scholar]
  2. Bhaduri, D.; Sihi, D.; Bhowmik, A.; Verma, B.C.; Munda, S.; Dari, B. A Review on Effective Soil Health Bio-Indicators for Ecosystem Restoration and Sustainability. Front. Microbiol. 2022, 13, 938481. [Google Scholar] [CrossRef] [PubMed]
  3. Chornobyl Radiation Ecological Biosphere Reserve. History of Creation. Available online: https://zapovidnyk.org.ua/index.php?fn=istor (accessed on 22 January 2023).
  4. Morooka, K.; Kurihara, E.; Takehara, M.; Takami, R.; Fueda, K.; Horie, K.; Takehara, M.; Yamasaki, S.; Ohnuki, T.; Grambow, B.; et al. New Highly Radioactive Particles Derived from Fukushima Daiichi Reactor Unit 1: Properties and Environmental Impacts. Sci. Total Environ. 2021, 773, 145639. [Google Scholar] [CrossRef] [PubMed]
  5. Akbay, C.; Aytop, H.; Dikici, H. Evaluation of Radioactive and Heavy Metal Pollution in Agricultural Soil Surrounding the Lignite-Fired Thermal Power Plant Using Pollution Indices. Int. J. Environ. Health Res. 2023, 33, 1490–1501. [Google Scholar] [CrossRef] [PubMed]
  6. Melnychuk, A.O.; Tarariko, M.Y. Eco-Energy and Economic Efficiency of Alternative Fertilization Systems on Radioactively Contaminated Soils of Polissya of Ukraine. Agroecol. J. Sci. Theor. 2015, 1, 121–125. [Google Scholar] [CrossRef]
  7. Bulyhin, S.Y.; Vitvitskyi, S.V.; Bulanyi, O.V.; Tonkha, O.L. Monitoring of Quality of Soils; Publishing House of the National University of Life and Environmental Sciences of Ukraine: Kyiv, Ukraine, 2019; 421p. [Google Scholar]
  8. Feng, G.; Yong, J.; Liu, Q.; Chen, H.; Mao, P. Response of Soil Microbial Communities to Natural Radionuclides along Specific-Activity Gradients. Ecotoxicol. Environ. Saf. 2022, 246, 114156. [Google Scholar] [CrossRef] [PubMed]
  9. Horvath, M.; Heltai, G.; Várhegyi, A.; Mbokazi, L.A. Study on the Possible Relationship between Physico-Chemical Properties of the Covering Soil and the Mobility of Radionuclides and Potentially Toxic Elements in a Recultivated Spoil Bank. Minerals 2022, 12, 1534. [Google Scholar] [CrossRef]
  10. Dinis, M.D.L.; Fiúza, A.; Góis, J.; de Carvalho, J.S.; Meira Castro, A.C. Assessment of Natural Radioactivity, Heavy Metals, and Particulate Matter in Air and Soil around a Coal-Fired Power Plant—An Integrated Approach. Atmosphere 2021, 12, 1433. [Google Scholar] [CrossRef]
  11. Kim, J.H.; Anwer, H.; Kim, Y.S.; Park, J.-W. Decontamination of Radioactive Cesium-Contaminated Soil/Concrete with Washing and Washing Supernatant—Critical Review. Chemosphere 2021, 280, 130419. [Google Scholar] [CrossRef]
  12. Yang, L.; Fan, L.; Huang, B.; Xin, J. Efficiency and mechanisms of fermented horse manure, vermicompost, bamboo biochar, and fly ash on Cd accumulation in rice. Environ. Sci. Pollut. Res. Int. 2020, 27, 27859–27869. [Google Scholar] [CrossRef]
  13. Yin, A.; Shen, C.; Huang, Y.; Yue, M.; Huang, B.; Xin, J. Reduction of Cd accumulation in Se-biofortified rice by using fermented manure and fly ash. Environ. Sci. Pollut. Res. Int. 2020, 27, 39391–39401. [Google Scholar] [CrossRef]
  14. Shen, C.; Fu, H.; Huang, B.; Liao, Q.; Huang, Y.; Wang, Y.; Wang, Y.; Xin, J. Physiological and molecular mechanisms of boron in alleviating cadmium toxicity in Capsicum annuum. Sci. Total Environ. 2023, 903, 166264. [Google Scholar] [CrossRef]
  15. Huang, B.; Liao, Q.; Fu, H.; Ye, Z.; Mao, Y.; Luo, J.; Wang, Y.; Yuan, H.; Xin, J. Effect of potassium intake on cadmium transporters and root cell wall biosynthesis in sweet potato. Ecotoxicol. Environm. Saf. 2023, 250, 114501. [Google Scholar] [CrossRef]
  16. Selim, H.M. (Ed.) Phosphate in Soils; CRC Press: Boca Raton, FL, USA, 2018. [Google Scholar]
  17. Pozzebon, E.A.; Seifert, L. Emerging Environmental Health Risks Associated with the Land Application of Biosolids: A Scoping Review. Environ. Health 2023, 22, 57. [Google Scholar] [CrossRef]
  18. Chernysh, Y.; Balintova, M.; Shtepa, V.; Skvortsova, P.; Skydanenko, M.; Fukui, M. Integration of Processes of Radionuclide-Contaminated Territories Decontamination in the Framework of Their Ecological-Socio-Economic Rehabilitation. Ecol. Eng. Environ. Technol. 2022, 23, 110–124. [Google Scholar] [CrossRef]
  19. Awasthi, G.; Nagar, V.; Mandzhieva, S.; Minkina, T.; Sankhla, M.S.; Pandit, P.P.; Aseri, V.; Awasthi, K.K.; Rajput, V.D.; Bauer, T.; et al. Sustainable Amelioration of Heavy Metals in Soil Ecosystem: Existing Developments to Emerging Trends. Minerals 2022, 12, 1. [Google Scholar] [CrossRef]
  20. Basu, S.; Banerjee, P.; Banerjee, S.; Ghosh, B.; Bhattacharjee, A.; Roy, D.; Singh, P.; Kumar, A.A. Bioremediation Strategies to Overcome Heavy Metals and Radionuclides from the Environment. In Development in Wastewater Treatment Research and Processes; Elsevier: Amsterdam, The Netherlands, 2022; pp. 287–302. [Google Scholar] [CrossRef]
  21. Bakshi, S.; Banik, C.; He, Z. The Impact of Heavy Metal Contamination on Soil Health. In Managing Soil Health for Sustainable Agriculture; Reicosky, D., Ed.; Burleigh Dodds Science Publishing: Cambridge, UK, 2018; Volume 2, pp. 1–36. [Google Scholar]
  22. Nyiramigisha, P.; Komariah, A.; Sajidan, M. Harmful Impacts of Heavy Metal Contamination in the Soil and Crops Grown Around Dumpsites. Rev. Agric. Sci. 2021, 9, 271–282. [Google Scholar] [CrossRef] [PubMed]
  23. Somani, M.; Datta, M.; Gupta, S.K.; Sreekrishnan, T.R.; Ramana, G.V. Comprehensive Assessment of the Leachate Quality and Its Pollution Potential from Six Municipal Waste Dumpsites of India. Bioresour. Technol. Rep. 2019, 6, 198–206. [Google Scholar] [CrossRef]
  24. Ramelli, G.P.; Taddeo, I.; Herrmann, U.; Weber, P. Toxicological Profile for Cadmium: U.S. Department of Health and Human Services Public Health Service Agency for Toxic Substances and Disease Registry. Eur. J. Paediatr. Neurol. 2012, 13, 105–180. [Google Scholar] [CrossRef]
  25. Rezapour, S.; Samadi, A.; Kalavrouziotis, I.K.; Ghaemian, N. Impact of the Uncontrolled Leakage of Leachate from a Municipal Solid Waste Landfill on Soil in a Cultivated-Calcareous Environment. Waste Manag. 2018, 82, 51–61. [Google Scholar] [CrossRef] [PubMed]
  26. Khan, A.; Khan, S.; Khan, M.A.; Qamar, Z.; Waqas, M. The Uptake and Bioaccumulation of Heavy Metals by Food Plants, Their Effects on Plants Nutrients, and Associated Health Risk: A Review. Environ. Sci. Pollut. Res. 2015, 22, 13772–13799. [Google Scholar] [CrossRef] [PubMed]
  27. Rashid, A.; Ayub, M.; Ullah, Z.; Ali, A.; Sardar, T.; Iqbal, J.; Gao, X.; Bundschuh, J.; Li, C.; Khattak, S.A.; et al. Groundwater Quality, Health Risk Assessment, and Source Distribution of Heavy Metals Contamination around Chromite Mines: Application of GIS, Sustainable Groundwater Management, Geostatistics, PCAMLR, and PMF Receptor Model. Int. J. Environ. Res. Public Health 2023, 20, 2113. [Google Scholar] [CrossRef] [PubMed]
  28. Raheem, A.; Sikarwar, V.S.; He, J.; Dastyar, W.; Dionysiou, D.D.; Wang, W.; Zhao, M. Opportunities and Challenges in Sustainable Treatment and Resource Reuse of Sewage Sludge: A Review. Chem. Eng. J. 2018, 337, 616–641. [Google Scholar] [CrossRef]
  29. Beschkov, V. Control of Pollution in the Non-Ferrous Metals Industry. In: Control of Pollution in the Non-ferrous Metals Industry. Available online: http://www.eolss.net/sample-chapters/c09/e4-14-04-05.pdf (accessed on 19 January 2023).
  30. Pan, X.; Zhang, S.; Zhong, Q.; Gong, G.; Wang, G.; Guo, X.; Xu, X. Effects of soil chemical properties and fractions of Pb, Cd, and Zn on bacterial and fungal communities. Sci. Total Environ. 2020, 715, 136904. [Google Scholar] [CrossRef] [PubMed]
  31. Zhang, J.; Sun, X.; Deng, J.; Li, G.; Li, Z.; Jiang, J.; Wu, Q.; Duan, L. Emission characteristics of heavy metals from a typical copper smelting plant. J. Hazard. Mater. 2021, 424, 127311. [Google Scholar] [CrossRef] [PubMed]
  32. Fekiacova, Z.; Cornu, S.; Pichat, S. Tracing contamination sources in soils with Cu and Zn isotopic ratios. Sci. Total Environ. 2015, 517, 96–105. [Google Scholar] [CrossRef]
  33. Müller, A.K.; Westergaard, K.; Christensen, S.; Sørensen, S.J. The effect of long-term mercury pollution on the soil microbial community. FEMS Microbiol. Ecol. 2001, 36, 11–19. [Google Scholar] [CrossRef]
  34. Pacyna, J.M.; Sundseth, K.; Pacyna, E.G. Sources and Fluxes of Harmful Metals. In Environmental Determinants of Human Health. Molecular and Integrative Toxicology; Pacyna, J., Pacyna, E., Eds.; Springer: Cham, Switzerland, 2016. [Google Scholar] [CrossRef]
  35. Environment Agency. Ferrous and Non-Ferrous Metals: Pollution Inventory Reporting. Available online: https://www.gov.uk/government/publications/pollution-inventory-reporting-guidance-notes/ferrous-and-non-ferrous-metals-pollution-inventory-reporting (accessed on 20 December 2023).
  36. Qi, M.; Wu, Y.; Zhang, S.; Li, G.; An, T. Pollution Profiles, Source Identification and Health Risk Assessment of Heavy Metals in Soil near a Non-Ferrous Metal Smelting Plant. Int. J. Environ. Res. Public. Health 2023, 20, 1004. [Google Scholar] [CrossRef]
  37. Non-Ferryytrrous Metals—AR4 WGIII Chapter 7: Industry. IPCC—Intergovernmental Panel on Climate Change. Available online: https://archive.ipcc.ch/publications_and_data/ar4/wg3/en/ch7s7-4-2.html (accessed on 20 December 2023).
  38. United Nations Environment Programme. UNEP Global Mercury Partnership Study Report on Mercury from Non-Ferrous Metals Mining and Smelting. 2021. Available online: https://www.unep.org/globalmercurypartnership/resources/report/mercury-non-ferrous-metals-mining-and-smelting (accessed on 21 December 2023).
  39. Emission Control for Non-Ferrous Industry. GEA Engineering for a Better World. Available online: https://www.gea.com/en/chemical/emission-control/non-ferrous.jsp (accessed on 20 December 2023).
  40. Basta, N.T.; Ryan, J.A.; Chaney, R.L. Trace Element Chemistry in Residual-Treated Soil: Key Concepts and Metal Bioavailability. J. Environ. Qual. 2005, 34, 49–63. [Google Scholar] [CrossRef]
  41. Rosen, V.; Chen, Y. Effects of Compost Application on Soil Vulnerability to Heavy Metal Pollution. Environ. Sci. Pollut. Res. 2018, 25, 35221–35231. [Google Scholar] [CrossRef]
  42. Raymond, A.W.; Felix, E.O. Heavy Metals in Contaminated Soils: A Review of Sources, Chemistry, Risks, and Best Available Strategies for Remediation. Int. Sch. Res. Netw. ISRN Ecol. 2012, 2011, 402647. [Google Scholar] [CrossRef]
  43. Symkanych, O.I.; Sukharev, S.M.; Delehan-Kokayko, S.V.; Maslyuk, V.T.; Svatyuk, A.N.I. Distribution of Heavy Metals and Radionuclides in the Protected Areas of Transcarpathia. Uzhhorod University Scientific Herald. Series Physics 2015, 3, 145–152. [Google Scholar]
  44. Savchuk, I.M.; Romanchuk, L.D.; Yashchuk, I.V.; Kovalyova, S.P.; Bondarchuk, L.V. Monitoring of Heavy Metals in Fodder and Animal Husbandry Products of the Polissia Zone of Ukraine. Sci. Horiz. 2022, 25, 45–54. [Google Scholar] [CrossRef]
  45. Yang, Z.; Zhang, W.; Wu, W.; Ma, Z.; Li, H.; Zhang, L. Study on Remediation Effect of Radioactive-Heavy Metal Contaminated Soil in Stone Coal Mines by Chemical Elution. Coal Sci. Technol. 2022, 50, 261–266. [Google Scholar]
  46. Mohuba, S.C.; Abiye, T.A.; Demlie, M.B.; Nhleko, S. Natural Radioactivity and Metal Concentration in the Thyspunt Area, Eastern Cape Province, South Africa. Environ. Monit. Assess. 2022, 194, 112. [Google Scholar] [CrossRef]
  47. Baghdady, A.; Awad, S.; Gad, A. Assessment of Metal Contamination and Natural Radiation Hazards in Different Soil Types Near Iron Ore Mines, Bahariya Oasis, Egypt. Arab. J. Geosci. 2018, 11, 506. [Google Scholar] [CrossRef]
  48. Mitrovic, B.; Vranjes, B.; Kostic, O.; Perovic, V.; Mitrovic, M.; Pavlovic, P. Radionuclides and Heavy Metals in Soil, Vegetables, and Medicinal Plants in Suburban Areas of the Cities of Belgrade and Pancevo, Serbia. Nucl. Technol. Radiat. Prot. 2019, 34, 278–284. [Google Scholar] [CrossRef]
  49. Cuenca, R.H.; Hagimoto, Y.; Moghaddam, M. Three-and-a-half Decades of Progress in Monitoring Soils and Soil Hydraulic Properties. Procedia Environ. Sci. 2013, 19, 384–393. [Google Scholar] [CrossRef]
  50. Lee, C.; Park, S.-W.; Kim, A.H.R. Development of Mobile Scanning System for Effective In-Situ Spatial Prediction of Radioactive Contamination at Decommissioning Sites. Nucl. Instrum. Methods Phys. Res. 2020, 966, 163833. [Google Scholar] [CrossRef]
  51. Bida, P.I.; Rudko, O.M.; Malimon, S.S.; Kushniruk, A.O.M. Introduction of Drainage and Sorption Systems on Radioactively Contaminated Peat Soils of Polissya of Ukraine. Environ. Sci. 2020, 5, 36–40. [Google Scholar] [CrossRef]
  52. Chobotko, H.M.; Landin, V.P.; Yaskovets, I.I.; Raichuk, L.A.; Shvydenko, I.K. Radiologically Critical Ecosystems and Their Role in the Formation of Contamination of Agricultural Products. Ahroekolohichnyi Zhurnal 2018, 4, 29–35. [Google Scholar] [CrossRef]
  53. Kovalyova, S.P.; Mozharivska, I.A. Heavy Metal Concentration in Soils while Growing Energy Crops in the Radioactively Contaminated Territory. Sci. Horiz. 2020, 3, 121–126. [Google Scholar] [CrossRef]
  54. Yoon, I.-H.; Park, C.W.; Kim, I.; Yang, H.-M.; Kim, S.-M.; Kim, J.-H. Characteristic and Remediation of Radioactive Soil in Nuclear Facility Sites: A Critical Review. Environ. Sci. Pollut. Res. 2021, 28, 67990–68005. [Google Scholar] [CrossRef] [PubMed]
  55. Lysenko, L.; Mishchuk, N.; Kovalchuk, V. Basic Principles and Problems in Decontamination of Natural Disperse Systems. Electrokinet. Treat. Soils. Adv. Colloid. Interface Sci. 2022, 310, 102798. [Google Scholar] [CrossRef] [PubMed]
  56. Impens, N.R.E.N.; Jensen, K.A.; Skipperud, L.; Gompel, A.V.; Vanhoudt, N. In-Depth Understanding of Local. Soil. Chemistry Reveals That Addition of Ca May Counteract the Mobilisation of 226Ra and Other Pollutants before Wetland Creation on the Grote Nete River Banks. Sci. Total Environ. 2022, 823, 153703. [Google Scholar] [CrossRef] [PubMed]
  57. Salbu, B.; Lind, O.C. Analytical Techniques for Characterizing Radioactive Particles Deposited in the Environment. J. Environ. Radioact. 2020, 211, 106078. [Google Scholar] [CrossRef] [PubMed]
  58. Arora, V.; Khosla, A.B. Conventional and Contemporary Techniques for Removal of Heavy Metals from Soil. In Biodegradation Technology of Organic and Inorganic Pollutants, 2nd ed.; Mendes, K.F., Sousa, R.N., Mielke, K.C., Eds.; IntechOpen: Rijeka, Croatia, 2021; Volume 3, pp. 154–196. [Google Scholar] [CrossRef]
  59. Groudeva, V.I.; Doycheva, A.; Krumova, K.; Groudev, S.N. Bioremediation In Situ of an Alkaline Soil Polluted with Heavy Metals. Adv. Mater. Res. 2007, 20–21, 287–290. [Google Scholar] [CrossRef]
  60. Marcon, L.; Oliveras, J.; Puntes, V.F. In Situ Nanoremediation of Soils and Groundwaters from the Nanoparticle’s Standpoint: A Review. Sci. Total Environ. 2021, 791, 148324. [Google Scholar] [CrossRef] [PubMed]
  61. Bhatt, J.; Desai, S.; Wagh, N.S.; Lakkakula, J. New Bioremediation Technologies to Remove Heavy Metals and Radionuclides. In Industrial Wastewater Reuse; Springer Nature Singapore: Singapore, 2023; pp. 267–316. [Google Scholar]
  62. Zhang, H.; Chen, Y.; Liu, S.X.; Jachimowicz, A.E.; Li, A. Big Data Research on Agricultural Soil Contamination by Zeolite Application. J. Elem. 2022, 27, 265–287. [Google Scholar] [CrossRef]
  63. Kornilovich, B.; Mishchuk, N.; Abbruzzese, K.; Pshinko, G.; Klishchenko, R. Enhanced Electrokinetic Remediation of Metals-Contaminated Clay. Colloids Surf. A Physicochem. Eng. Asp. 2005, 265, 114–123. [Google Scholar] [CrossRef]
  64. Megharaj, M.; Venkateswarlu, K.; Naidu, R. Bioremediation. In Encyclopedia of Toxicology; Elsevier: Amsterdam, The Netherlands, 2014; pp. 485–489. [Google Scholar] [CrossRef]
  65. Nadaf, M.; Jadav, K.D.; Gingine, V. Decontamination of Soil by Electro Kinetic Treatment; Lecture Notes in Civil Engineering; Springer: Singapore, 2021; pp. 91–103. [Google Scholar] [CrossRef]
  66. Olodovskii, P. Theory of the Effect of Inhibition of the Transfer of Radionuclides and Heavy Metals from Soil to Plants by an Ameliorant. V. Calculation of the Binding Energy of Exchange Ions in Disperse Systems with Low pH. J. Eng. Phys. Thermophys. 2001, 74, 243–249. [Google Scholar] [CrossRef]
  67. Sethi, S. Holistic Approach to Remediate Heavy Metals and Radionuclides. In Industrial Wastewater Reuse; Springer Nature: Singapore, 2023; pp. 113–132. [Google Scholar] [CrossRef]
  68. Chandra, D.; General, T.; Nisha; Chandra, S. Microorganisms: An Asset for Decontamination of Soil. In Smart Bioremediation Technologies; Academic Press: Cambridge, MA, USA, 2019; pp. 319–345. [Google Scholar]
  69. Gadd, G.M. Heavy Metal Pollutants: Environmental and Biotechnological Aspects. In Reference Module in Life Sciences; Elsevier: Amsterdam, The Netherlands, 2019. [Google Scholar]
  70. Mishra, M.; Mohan, D. Bioremediation of Contaminated Soils: An Overview. In Adaptive Soil Management: From Theory to Practices; Springer: Singapore, 2017; pp. 323–337. [Google Scholar]
  71. Singh, B.S.M.; Singh, D.; Dhal, N.K. Enhanced Phytoremediation Strategy for Sustainable Management of Heavy Metals and Radionuclides. Case Stud. Chem. Environ. Eng. 2022, 5, 100176. [Google Scholar] [CrossRef]
  72. Devedee, A.K.; Sahoo, M.; Choudhary, K.; Singh, M.; Ghanshyam. Bioremediation of Soil: An Overview. In Microbes and Microbial Biotechnology for Green Remediation; Elsevier: Amsterdam, The Netherlands, 2022; pp. 13–27. [Google Scholar]
  73. Phian, S.; Nagar, S.; Kaur, J.; Rawat, C.D. Emerging Issues and Challenges for Microbes-Assisted Remediation. In Microbes and Microbial Biotechnology for Green Remediation; Elsevier: Amsterdam, The Netherlands, 2022; pp. 47–89. [Google Scholar]
  74. Xing, Y.; Tan, S.; Liu, S.; Xu, S.; Wan, W.; Huang, Q.; Chen, W. Effective Immobilization of Heavy Metals via Reactive Barrier by Rhizosphere Bacteria and Their Biofilms. Environ. Res. 2022, 207, 112080. [Google Scholar] [CrossRef]
  75. Chen, P.; Liu, Y.; Sun, G.-X. Evaluation of Water Management on Arsenic Methylation and Volatilization in Arsenic-Contaminated Soils Strengthened by Bioaugmentation and Biostimulation. J. Environ. Sci. 2024, 137, 515–526. [Google Scholar] [CrossRef]
  76. Khalid, M.; Liu, X.; ur Rahman, S.; Rehman, A.; Zhao, C.; Li, X.; Yucheng, B.; Hui, N. Responses of Microbial Communities in Rhizocompartments of King Grass to Phytoremediation of Cadmium-Contaminated Soil. Sci. Total Environ. 2023, 904, 167226. [Google Scholar] [CrossRef] [PubMed]
  77. Li, S.; Wu, X.; Xie, J. Biomineralization Technology for Solidification/Stabilization of Heavy Metals in Ecosystem: Status and Perspective. Front. Ecol. Evol. 2023, 11, 1189356. [Google Scholar] [CrossRef]
  78. Mendoza-Burguete, Y.; de la Luz Pérez-Rea, M.; Ledesma-García, J.; Campos-Guillén, J.; Ramos-López, M.A.; Guzmán, C.; Rodríguez-Morales, J.A. Global Situation of Bioremediation of Leachate-Contaminated Soils by Treatment with Microorganisms: A Systematic Review. Microorganisms 2023, 11, 857. [Google Scholar] [CrossRef] [PubMed]
  79. Lai, H.-J.; Ding, X.-Z.; Cui, M.-J.; Zheng, J.-J.; Chen, Z.-B.; Pei, J.-L.; Zhang, J.-W. Mechanisms and Influencing Factors of Biomineralization Based Heavy Metal Remediation: A Review. Biogeotechnics 2023, 1, 100039. [Google Scholar] [CrossRef]
  80. Li, M.; Cheng, X.; Guo, H. Heavy metal removal by biomineralization of urease producing bacteria isolated from soil. Int. Biodeterior. Biodegrad. 2013, 76, 81–85. [Google Scholar] [CrossRef]
  81. Lopez-Fernandez, M.; Jroundi, F.; Ruiz-Fresneda, M.A.; Merroun, M.L. Microbial interaction with and tolerance of radionuclides: Underlying mechanisms and biotechnological applications. Microb. Biotechnol. 2020, 14, 810–828. [Google Scholar] [CrossRef] [PubMed]
  82. Zhang, W.; Zhang, H.; Xu, R.; Qin, H.; Liu, H.; Zhao, K. Heavy metal bioremediation using microbially induced carbonate precipitation: Key factors and enhancement strategies. Front. Microbiol. 2023, 14, 1116970. [Google Scholar] [CrossRef]
  83. Renshaw, J.; Mackay, R.; Macaskie, L. Immobilization of Metals and Radionuclides by Microbial Biomineralization Processes. Available online: https://www.birmingham.ac.uk/Documents/college-les/gees/biomineralizationprocesses.pdf (accessed on 21 December 2023).
  84. Priya, A.K.; Gnanasekaran, L.; Dutta, K.; Rajendran, S.; Balakrishnan, D.; Soto-Moscoso, M. Biosorption of Heavy Metals by Microorganisms: Evaluation of Different Underlying Mechanisms. Chemosphere 2022, 307, 135957. [Google Scholar] [CrossRef]
  85. Vasconcellos, S.; Paganotti, A.; Vital, V.G.; Santos Lima, L.M.; Paiva, G.M.S.; de Lima, L.F.; Moreira, E.; Sousa, L.O.; Guerini, G.G.; Santos, V.T.; et al. Biotransformation of Metal-Rich Effluents and Potential Recycle Applications. In Bioremediation for Global Environmental Conservation; IntechOpen: Rijeka, Croatia, 2023. [Google Scholar] [CrossRef]
  86. White, C.; Wilkinson, S.C.; Gadd, G.M. The role of microorganisms in biosorption of toxic metals and radionuclides. Int. Biodeterior. Biodegrad. 1995, 35, 17–40. [Google Scholar] [CrossRef]
  87. Gavrilescu, M. Removal of heavy metals from the environment by biosorption. Eng. Life Sci. 2004, 4, 219–232. [Google Scholar] [CrossRef]
  88. Das, N. Remediation of Radionuclide Pollutants through Biosorption—An Overview. Clean. Soil. Air Water 2012, 40, 16–23. [Google Scholar] [CrossRef]
  89. Kotrba, P. Microbial Biosorption of Metals—General Introduction. In Microbial Biosorption of Metals; Kotrba, P., Mackova, M., Macek, T., Eds.; Springer: Dordrecht, The Netherlands, 2011. [Google Scholar] [CrossRef]
  90. Zabochnicka-Świątek, M.; Krzywonos, M. Potentials of Biosorption and Bioaccumulation Processes for Heavy Metal Removal. Pol. J. Environ. Studies. 2014, 23, 551–561. [Google Scholar]
  91. Mathew, A.T.; Saravanakumar, M.P. Removal of Bisphenol A and Methylene Blue by α -MnO2 Nanorods: Impact of Ultrasonication, Mechanism, Isotherm, and Kinetic Models. J. Hazard. Toxic Radioact. Waste 2021, 25, 04021005. [Google Scholar] [CrossRef]
  92. Fomina, M.; Gadd, G.M. Biosorption: Current perspectives on concept, definition and application. Bioresour. Technol. 2014, 160, 3–14. [Google Scholar] [CrossRef] [PubMed]
  93. Janyasuthwiong, S.; Rene, E.R. Bioprecipitation—A Promising Technique for Heavy Metal Removal and Recovery from Contaminated Wastewater Streams. MOJ Civil. Eng. 2017, 2, 191–193. [Google Scholar] [CrossRef]
  94. Kim, Y.; Kwon, S.; Roh, Y. Effect of Divalent Cations (Cu, Zn, Pb, Cd, and Sr) on Microbially Induced Calcium Carbonate Precipitation and Mineralogical Properties. Front. Microbiol. 2021, 12, 646748. [Google Scholar] [CrossRef]
  95. Pande, V.; Pandey, S.C.; Sati, D.; Bhatt, P.; Samant, M. Microbial Interventions in Bioremediation of Heavy Metal Contaminants in Agroecosystem. Front. Microbiol. 2022, 13, 824084. [Google Scholar] [CrossRef] [PubMed]
  96. Xu, Q.; Wu, B.; Chai, X. In Situ Remediation Technology for Heavy Metal Contaminated Sediment: A Review. Int. J. Environ. Res. Public Health 2022, 19, 16767. [Google Scholar] [CrossRef] [PubMed]
  97. Mugwar, A. Bioprecipitation of Heavy Metals and Radionuclides with Calcium Carbonate in Aqueous Solutions and Particulate Media. Cardiff University. 2015. Available online: https://www.semanticscholar.org/paper/Bioprecipitation-of-heavy-metals-andradionuclides-Mugwar/a0070cd67b0c051e674db74c8257ad955d79c308 (accessed on 21 December 2023).
  98. Kumari, D.; Qian, X.Y.; Pan, X.; Achal, V.; Li, Q.; Gadd, G.M. Microbially-induced Carbonate Precipitation for Immobilization of Toxic Metals. Adv. Appl. Microbiol. 2016, 94, 79–108. [Google Scholar] [CrossRef] [PubMed]
  99. Nnaji, N.D.; Onyeaka, H.; Miri, T.; Ugwa, C. Bioaccumulation for Heavy Metal Removal: A Review. SN Appl. Sci. 2023, 5, 125. [Google Scholar] [CrossRef]
  100. Rahmat, M.A.; Ismail, A.F.; Rodzi, N.D.; Aziman, E.S.; Idris, W.M.R.; Lihan, T. Assessment of natural radionuclides and heavy metals contamination to the environment: Case study of Malaysian unregulated tin-tailing processing industry. Nucl. Eng. Technol. 2022, 54, 2230–2243. [Google Scholar] [CrossRef]
  101. Zalewska, T.; Saniewski, M. Bioaccumulation of gamma emitting radionuclides in red algae from the Baltic Sea under laboratory conditions. Oceanologia 2011, 53, 631–650. [Google Scholar] [CrossRef]
  102. Abdelkarim, M.S.; Imam, N. Radiation hazards and extremophiles bioaccumulation of radionuclides from hypersaline lakes and hot springs. Int. J. Environ. Sci. Technol. 2023, 21, 3021–3036. [Google Scholar] [CrossRef]
  103. Borghei, S.M.; Arjmandi, R.; Moogouei, R. Bioaccumulation of Radionuclide Metals in Plants: A Case Study of Cesium. In Radionuclide Contamination and Remediation Through Plants; Springer International Publishing: Cham, Switzerland, 2014; pp. 177–195. [Google Scholar] [CrossRef]
  104. Srisuksawad, K.; Prasertchiewchan, N. Experimental Studies on the Bioaccumulation of Selected Heavy Metals and Radionuclides in the Blood Cockle Anadara granosa of the Bang Pakong Estuary. Environ. Bioindic. 2007, 2, 253–263. [Google Scholar] [CrossRef]
  105. Tykva, R. Sources of Environmental Radionuclides and Recent Results in Analyses of Bioaccumulation. A review. Nukleonika 2004, 49. Available online: https://bibliotekanauki.pl/articles/147281 (accessed on 22 December 2023).
  106. Diaz-Bone, R.; Van de Wiele, T. Biotransformation of metal(loid)s by intestinal microorganisms. Pure Appl. Chemistry. 2010, 82, 409–427. [Google Scholar] [CrossRef]
  107. Jabbar, T.; Wallner, G. Biotransformation of Radionuclides: Trends and Challenges. In Radionuclides in the Environment; Walther, C., Gupta, D., Eds.; Springer: Cham, Switzerland, 2015. [Google Scholar] [CrossRef]
  108. Lloyd, J.R.; Lovley, D.R. Microbial detoxification of metals and radionuclides. Curr. Opin. Biotechnol. 2001, 12, 248–253. [Google Scholar] [CrossRef] [PubMed]
  109. Francis, A. Microbial Transformations of Radionuclides and Environmental Restoration through Bioremediation. Symposium on “Emerging Trends in Separation Science and Technology” SESTEC 2006 Bhabha Atomic Research Center (BARC), Trombay, Mumbai. Brookhaven National Laboratory. 2006, pp. 1–15. Available online: https://citeseerx.ist.psu.edu/document?repid=rep1&type=pdf&doi=fdce929bc2c9995a1567fc17853c0b6b443cd3c8 (accessed on 22 December 2023).
  110. Mani, D.; Kumar, C. Biotechnological advances in bioremediation of heavy metals contaminated ecosystems: An overview with special reference to phytoremediation. Int. J. Environ. Sci. Technol. 2014, 11, 843–872. [Google Scholar] [CrossRef]
  111. Gadd, G.M. Geomicrobiology of Metal and Mineral Transformations in the Environment. Extremophiles. Encyclopedia of Life Support Systems. Available online: https://www.eolss.net/sample-chapters/c03/E6-38-18.pdf (accessed on 22 December 2023).
  112. Thakare, M.; Sarma, H.; Datar, S.; Roy, A.; Pawar, P.; Gupta, K.; Pandit, S.; Prasad, R. Understanding the Holistic Approach to Plant-Microbe Remediation Technologies for Removing Heavy Metals and Radionuclides from Soil. Curr. Res. Biotechnol. 2021, 3, 84–98. [Google Scholar] [CrossRef]
  113. Harher, Y.K.; Voitsekhovych, O.V. Twenty-Five Years since the Chornobyl Disaster. Security of the Future; National Report of Ukraine; KIM: Kyiv, Ukraine, 2011; pp. 39–42. [Google Scholar]
  114. Chibuike, G.U.; Obiora, S.C. Heavy Metal Polluted Soils: Effect on Plants and Bioremediation Methods. Appl. Environ. Soil. Sci. 2014, 752708. [Google Scholar] [CrossRef]
  115. Yaashikaa, P.R.; Senthil Kumar, P.; Saravanan, A.; Vo, D.-V.N. Advances in Biosorbents for Removal of Environmental Pollutants: A Review on Pretreatment, Removal Mechanism, and Future Outlook. J. Hazard. Mater. 2021, 420, 126596. [Google Scholar] [CrossRef]
  116. Kumar, M.; Seth, A.; Singh, A.K.; Rajput, M.S.; Sikandar, A.M. Remediation Strategies for Heavy Metals Contaminated Ecosystem: A Review. J. Environ. Sustain. 2021, 12, 100155. [Google Scholar] [CrossRef]
  117. Priyadarshanee, M.; Das, S. Biosorption and Removal of Toxic Heavy Metals by Metal Tolerating Bacteria for Bioremediation of Metal Contamination: A Comprehensive Review. J. Environ. Chem. Eng. 2021, 9, 104686. [Google Scholar] [CrossRef]
  118. Han, J.; Zhang, J.; Meng, J.; Cai, Y.; Cheng, M.; Wu, S.; Li, Z. Characterization of Modified Rice Straw Biochar in Immobilizing Bacillus subtilis 168 and Evaluation on Its Role as a Novel Agent for Zearalenone-Removal Delivery. J. Hazard. Mater. 2023, 453, 131424. [Google Scholar] [CrossRef]
  119. Li, M.; Yao, J.; Sunahara, G.; Hawari, J.; Duran, R.; Liu, J.; Liu, B.; Cao, Y.; Pang, W.; Li, H.; et al. Novel Microbial Consortia Facilitate Metalliferous Immobilization in Non-Ferrous Metal(loid)s Contaminated Smelter Soil: Efficiency and Mechanisms. Environ. Pollut. 2022, 313, 120042. [Google Scholar] [CrossRef]
  120. Zhang, Y.; Majeed, Z.; Tian, M.; Xie, Y.; Zheng, K.; Luo, Z.; Li, C.; Zhao, C. Application of Hydrogen-Bonded Organic Frameworks in Environmental Remediation. Separations 2023, 10, 196. [Google Scholar] [CrossRef]
  121. Qi, X.; Xiao, S.; Chen, X.; Ali, I.; Gou, J.; Wang, D.; Zhu, B.; Zhu, W.; Shang, R.; Han, M. Biochar-Based Microbial Agent Reduces U and Cd Accumulation in Vegetables and Improves Rhizosphere Microecology. J. Hazard. Mater. 2022, 436, 129147. [Google Scholar] [CrossRef]
  122. Oziegbe, O.; Oluduro, A.O.; Oziegbe, E.J.; Ahuekwe, E.F.; Olorunsola, S.J. Assessment of Heavy Metal Bioremediation Potential of Bacterial Isolates from Landfill Soils. Saudi J. Biol. Sci. 2021, 28, 3948–3956. [Google Scholar] [CrossRef]
  123. Maqsood, Q.; Sumrin, A.; Waseem, R.; Hussain, M.; Imtiaz, M.; Hussain, N. Bioengineered Microbial Strains for Detoxification of Toxic Environmental Pollutants. Environ. Res. 2023, 227, 115665. [Google Scholar] [CrossRef]
  124. Salah-Tazdaït, R.; Tazdaït, D. Phyto and Microbial Remediation of Heavy Metals and Radionuclides in the Environment; Routledge: London, UK, 2022. [Google Scholar]
  125. Singha, S.; Chatterjee, S. Soil Pollution by Industrial Effluents, Solid Wastes, and Reclamation Strategies by Microorganisms. In Microbes and Microbial Biotechnology for Green Remediation; Springer International Publishing: Cham, Switzerland, 2022; pp. 471–488. [Google Scholar]
  126. Chen, Z.; Li, Q.; Yang, Y.; Sun, J.; Li, G.; Liu, X.; Shu, S.; Li, X.; Liao, H. Uranium Removal from a Radioactive Contaminated Soil by Defined Bioleaching Bacteria. J. Radioanal. Nucl. Chem. 2022, 331, 439–449. [Google Scholar] [CrossRef]
  127. Bryukhanov, A.L.; Khijniak, T.V. The Application of Sulfate-Reducing Bacteria in the Bioremediation of Heavy Metals and Metalloids. Appl. Biochem. Microbiol. 2022, 58 (Suppl. S1), S1–S15. [Google Scholar] [CrossRef]
  128. Aslam, F.; Mazhar, S. Nano-Bioremediation of Heavy Metals from Environment Using a Green Synthesis Approach. Int. J. Adv. Appl. Sci. 2023, 12, 7. [Google Scholar] [CrossRef]
  129. Bilal, E.; Bellefqih, H.; Bourgier, V.; Mazouz, H.; Dumitraş, D.-G.; Bard, F.; Laborde, M.; Caspar, J.P.; Guilhot, B.; Iatan, E.-L.; et al. Phosphogypsum Circular Economy Considerations: A Critical Review from More than 65 Storage Sites Worldwide. J. Clean. Prod. 2023, 414, 137561. [Google Scholar] [CrossRef]
  130. Diwa, R.R.; Tabora, E.U.; Palattao, B.L.; Haneklaus, N.H.; Vargas, E.P.; Reyes, R.Y.; Ramirez, J.D. Evaluating radiation risks and resource opportunities associated with phosphogypsum in the Philippines. J. Radioanal. Nucl. Chem. 2022, 331, 967–974. [Google Scholar] [CrossRef]
  131. TENORM: Fertilizer and Fertilizer Production Wastes. U.S. Environmental Protection Agency. Available online: https://www.epa.gov/radiation/tenorm-fertilizer-and-fertilizer-production-wastes (accessed on 22 December 2023).
  132. Plyatsuk, L.; Balintova, M.; Chernysh, Y.; Demcak, S.; Holub, M.; Yakhnenko, E. Influence of Phosphogypsum Dump on the Soil Ecosystem in the Sumy region (Ukraine). Appl. Sci. 2019, 9, 5559. [Google Scholar] [CrossRef]
  133. Mahmoud, E.; Ghoneim, A.M.; Seleem, M.; Zuhair, R.; El-Refaey, A.; Khalafallah, N. Phosphogypsum and Poultry Manure Enhance Diversity of Soil Fauna, Soil Fertility, and Barley (Hordeum aestivum L.) Grown in Calcareous Soils. Sci. Rep. 2023, 13, 9944. [Google Scholar] [CrossRef] [PubMed]
  134. Qi, J.; Zhu, H.; Zhou, P.; Wang, X.; Wang, Z.; Yang, S.; Yang, D.; Li, B. Application of Phosphogypsum in Soilization: A Review. Int. J. Environ. Sci. Technol. 2023, 20, 10449–10464. [Google Scholar] [CrossRef]
  135. Li, C.; Dong, Y.; Yi, Y.; Tian, J.; Xuan, C.; Wang, Y.; Wen, Y.; Cao, J. Effects of Phosphogypsum on Enzyme Activity and Microbial Community in Acid Soil. Sci. Rep. 2023, 13, 6189. [Google Scholar] [CrossRef] [PubMed]
  136. Ben Mefteh, A.; Bouket, L.; Daoud, A.; Luptakova, L.; Alenezi, F.N.; Gharsallah, N.; Belbahri, L. Metagenomic Insights and Genomic Analysis of Phosphogypsum and Its Associated Plant Endophytic Microbiomes Reveals Valuable Actors for Waste Bioremediation. Microorganisms 2019, 7, 382. [Google Scholar] [CrossRef]
  137. Lei, L.; Gu, J.; Wang, X.; Song, Z.; Wang, J.; Yu, J.; Hu, T.; Dai, X.; Xie, J.; Zhao, W. Microbial Succession and Molecular Ecological Networks Response to the Addition of Superphosphate and Phosphogypsum during Swine Manure Composting. J. Environ. Manag. 2021, 279, 111560. [Google Scholar] [CrossRef] [PubMed]
  138. Trifi, H.; Najjari, A.; Achouak, W.; Barakat, M.; Ghedira, K.; Mrad, F.; Saidi, M.; Sghaier, H. Metataxonomics of Tunisian Phosphogypsum Based on Five Bioinformatics Pipelines: Insights for Bioremediation. Genomics 2020, 112, 981–989. [Google Scholar] [CrossRef]
  139. Chernysh, Y.; Hasegawa, K. Improvement of the Model System to Develop Eco-Friendly Bio-Utilization of Phosphogypsum; Lecture Notes in Mechanical Engineering; Springer: Cham, Switzerland, 2020; pp. 357–366. [Google Scholar]
  140. Ulianchuk-Martyniuk, O.V.; Michuta, O.R.; Ivanchuk, N.V. Finite Element Analysis of the Diffusion Model of the Bioclogging of the Geobarrier. Eurasian J. Math. Comput. Appl. 2021, 9, 100–111. [Google Scholar] [CrossRef]
  141. Yimer, A.M.; Assen, A.H.; Mghaimimi, I.E.L.; Lakbita, O.; Adil, K.; Belmabkhout, Y. Unlocking the potential of phosphogypsum waste: Unified synthesis of functional metal-organic frameworks and zeolite via a sustainable valorization route. Chem. Eng. J. 2024, 479, 147902. [Google Scholar] [CrossRef]
  142. Ait Brahim, J.; Merroune, A.; Mazouz, H.; Beniazza, R. Recovery of rare earth elements and sulfuric acid solution from phosphate byproducts via hydrofluoric acid conversion. J. Ind. Eng. Chem. 2023, 127, 446–453. [Google Scholar] [CrossRef]
  143. Akfas, F.; Elghali, A.; Aboulaich, A.; Munoz, M.; Benzaazoua, M.; Bodinier, J.-L. Exploring the potential reuse of phosphogypsum: A waste or a resource? Sci. Total Environ. 2024, 908, 168196. [Google Scholar] [CrossRef]
  144. Wei, Z.; Deng, Z. Research hotspots and trends of comprehensive utilization of phosphogypsum: Bibliometric analysis. J. Environ. Radioact. 2022, 242, 106778. [Google Scholar] [CrossRef]
  145. Wang, J.; Dong, F.; Wang, Z.; Yang, F.; Du, M.; Fu, K.; Wang, Z. A novel method for purification of phosphogypsum. Physicochem. Probl. Miner. Process. 2020, 56, 975–983. [Google Scholar] [CrossRef]
  146. Zou, C.; Shi, Z.; Yang, Y.; Zhang, J.; Hou, Y.; Zhang, N. The Characteristics, Enrichment, and Migration Mechanism of Cadmium in Phosphate Rock and Phosphogypsum of the Qingping Phosphate Deposit, Southwest China. Minerals 2023, 13, 107. [Google Scholar] [CrossRef]
  147. Guan, Q.; Sui, Y.; Liu, C.; Wang, Y.; Zeng, C.; Yu, W.; Gao, Z.; Zang, Z.; Chi, R.-A. Characterization and Leaching Kinetics of Rare Earth Elements from Phosphogypsum in Hydrochloric Acid. Minerals 2022, 12, 703. [Google Scholar] [CrossRef]
  148. Zhou, B.; Zhu, H.; Xu, S.; Du, G.; Shi, S.; Liu, M.; Xing, F.; Ren, J. Effect of phosphogypsum on the properties of magnesium phosphate cement paste with low magnesium-to-phosphate ratio. Sci. Total Environ. 2021, 798, 149262. [Google Scholar] [CrossRef] [PubMed]
  149. Wu, F.; Liu, S.; Qu, G.; Chen, B.; Zhao, C.; Liu, L.; Li, J.; Ren, Y. Highly targeted solidification behavior of hazardous components in phosphogypsum. Chem. Eng. J. Adv. 2022, 9, 100227. [Google Scholar] [CrossRef]
  150. Weiksnar, K.D.; Clavier, K.A.; Robey, N.M.; Townsend, T.G. Changes in trace metal concentrations throughout the phosphogypsum lifecycle. Sci. Total Environ. 2022, 851, 158163. [Google Scholar] [CrossRef]
  151. Liang, H.; Zhang, P.; Jin, Z.; DePaoli, D. Rare earths recovery and gypsum upgrade from Florida phosphogypsum. Miner. Metall. Process. 2017, 34, 201–206. [Google Scholar] [CrossRef]
  152. Al-Thyabat, S.; Zhang, P. REE extraction from phosphoric acid, phosphoric acid sludge, and phosphogypsum. Miner. Process. Extr. Metall. 2015, 124, 143–150. [Google Scholar] [CrossRef]
  153. Romero-Hermida, M.I.; Flores-Alés, V.; Hurtado-Bermúdez, S.J.; Santos, A.; Esquivias, L. Environmental Impact of Phosphogypsum-Derived Building Materials. Int. J. Environ. Res. Public Health 2020, 17, 4248. [Google Scholar] [CrossRef]
  154. Pérez-López, R.; Nieto, J.M.; López-Coto, I.; Aguado, J.L.; Bolívar, J.P.; Santisteban, M. Dynamics of contaminants in phosphogypsum of the fertilizer industry of Huelva (SW Spain): From phosphate rock ore to the environment. Appl. Geochem. 2010, 25, 705–715. [Google Scholar] [CrossRef]
  155. Costa, R.P.; de Medeiros, M.H.G.; Rodriguez Martinez, E.D.; Quarcioni, V.A.; Suzuki, S.; Kirchheim, A.P. Effect of soluble phosphate, fluoride, and pH in Brazilian phosphogypsum used as setting retarder on Portland cement hydration. Case Stud. Constr. Mater. 2022, 17, e01413. [Google Scholar] [CrossRef]
  156. Calado, B.; Tassinari, C. Geochemistry of the upper estuarine sediments of the Santos estuary: Provenance and anthropogenic pollution. J. Geol. Surv. Braz. 2020, 3, 189–209. [Google Scholar] [CrossRef]
  157. Lütke, S.F.; Oliveira, M.L.S.; Silva, L.F.O.; Cadaval, T.R.S.; Dotto, G.L. Nanominerals assemblages and hazardous elements assessment in phosphogypsum from an abandoned phosphate fertilizer industry. Chemosphere 2020, 256, 127138. [Google Scholar] [CrossRef] [PubMed]
  158. Shah, J.; Puthiyaveetil Othayoth, S.; Pania, R.; Parikh, S.; Vaishnav, P. Efficient Recovery of Trapped Phosphorus from Waste Phosphogypsum of a Phosphoric Acid Plant. Chem. Sci. Rev. Lett. 2022, 11, 340–348. [Google Scholar] [CrossRef]
  159. Raut, S.P.; Patil, U.S.; Madurwar, M.V. Utilization of phosphogypsum and rice husk to develop sustainable bricks. Mater. Today Proc. 2022, 60, 595–601. [Google Scholar] [CrossRef]
  160. Muthukumar, P.; Shewale, M.; Asalkar, S.; Shinde, N.; Korke, P.; Anitha, M.; Gobinath, R.; Anuradha, R. Experimental study on lightweight panel using phosphogypsum. Mater. Today Proc. 2022, 49, 1852–1856. [Google Scholar] [CrossRef]
  161. Yassine, I.; Joudi, M.; Hafdi, H.; Hatimi, B.; Mouldar, J.; Bensemlali, M.; Nasrellah, H.; El Mahammedi, M.A.; Bakasse, M. Synthesis of Brushite from Phosphogypsum Industrial Waste. Biointerface Res. Appl. Chem. 2021, 12, 6580–6588. [Google Scholar] [CrossRef]
  162. Ennaciri, Y.; Bettach, M.; El Alaoui-Belghiti, H. Recovery of nano-calcium fluoride and ammonium bisulphate from phosphogypsum waste. Int. J. Environ. Stud. 2020, 77, 297–306. [Google Scholar] [CrossRef]
  163. Arhouni, F.E.; Hakkar, M.; Ouakkas, S.; Haneklaus, N.; Boukhair, A.; Nourreddine, A.; Benjelloun, M. Evaluation of the physicochemical, heavy metal and radiological contamination from phosphogypsum discharges of the phosphoric acid production unit on the coast of El Jadida Province in Morocco. J. Radioanal. Nucl. Chem. 2023, 332, 4019–4028. [Google Scholar] [CrossRef]
  164. Akfas, F.; Elghali, A.; Bodinier, J.-L.; Parat, F.; Muñoz, M. Geochemical and mineralogical characterization of phosphogypsum and leaching tests for the prediction of the mobility of trace elements. Environ. Sci. Pollut. Res. 2023, 30, 43778–43794. [Google Scholar] [CrossRef]
  165. Abouloifa, W.; Belbsir, H.; Ettaki, M.; Mounir, S.H.; El-Hami, K. Moroccan Phosphogypsum: Complete Physico-Chemical Characterization and Rheological Study of Phosphogypsum-Slurry. Chem. Afr. 2023, 6, 1605–1618. [Google Scholar] [CrossRef]
  166. Szajerski, P.; Bogobowicz, A.; Bem, H.; Gasiorowski, A. Quantitative evaluation and leaching behavior of cobalt immobilized in sulfur polymer concrete composites based on lignite fly ash, slag and phosphogypsum. J. Clean. Prod. 2019, 222, 90–102. [Google Scholar] [CrossRef]
  167. Grabas, K.; Pawełczyk, A.; Stręk, W.; Szełęg, E.; Stręk, S. Study on the Properties of Waste Apatite Phosphogypsum as a Raw Material of Prospective Applications. Waste Biomass Valor. 2019, 10, 3143–3155. [Google Scholar] [CrossRef]
  168. Gijbels, K.; Nguyen, H.; Kinnunen, P.; Samyn, P.; Schroeyers, W.; Pontikes, Y.; Schreurs, S.; Illikainen, M. Radiological and leaching assessment of an ettringite-based mortar from ladle slag and phosphogypsum. Cem. Concr. Res. 2020, 128, 105954. [Google Scholar] [CrossRef]
  169. Myka, A.; Łyszczek, R.; Zdunek, A.; Rusek, P. Thermal analysis of materials based on calcium sulphate derived from various sources. J. Therm. Anal. Calorim. 2022, 147, 9923–9934. [Google Scholar] [CrossRef]
  170. The Possibility of Obtaining Rare Earth Elements from Potential Sources in Poland. Warszawa: Institute of Nuclear Chemistry and Technology. 2019. Available online: http://www.ichtj.waw.pl/ichtj/publ/annual/anrep18.pdf#page=47 (accessed on 29 December 2023).
  171. El Zrelli, R.; Rabaoui, L.; Daghbouj, N.; Abda, H.; Castet, S.; Josse, C.; van Beek, P.; Souhaut, M.; Michel, S.; Bejaoui, N.; et al. Characterization of phosphate rock and phosphogypsum from Gabes phosphate fertilizer factories (SE Tunisia): High mining potential and implications for environmental protection. Environ. Sci. Pollut. Res. 2018, 25, 14690–14702. [Google Scholar] [CrossRef]
  172. Antar, K.; Jemal, M. A thermogravimetric study into the effects of additives and water vapor on the reduction of gypsum and Tunisian phosphogypsum with graphite or coke in a nitrogen atmosphere. J. Therm. Anal. Calorim. 2018, 132, 113–125. [Google Scholar] [CrossRef]
  173. Jalali, J.; Magdich, S.; Jarboui, R.; Loungou, M.; Ammar, E. Phosphogypsum biotransformation by aerobic bacterial flora and isolated Trichoderma asperellum from Tunisian storage piles. J. Hazard. Mater. 2016, 308, 362–373. [Google Scholar] [CrossRef]
  174. Moalla, R.; Gargouri, M.; Khmiri, F.; Kamoun, L.; Zairi, M. Phosphogypsum purification for plaster production: A process optimization using full factorial design. Environ. Eng. Res. 2017, 23, 36–45. [Google Scholar] [CrossRef]
  175. Bisone, S.; Gautier, M.; Chatain, V.; Blanc, D. Spatial distribution and leaching behavior of pollutants from phosphogypsum stocked in a gypstack: Geochemical characterization and modeling. J. Environ. Manag. 2017, 193, 567–575. [Google Scholar] [CrossRef]
  176. Gaidajis, G.; Anagnostopoulos, A.; Garidi, A.; Mylona, E.; Zevgolis, I.E. Laboratory evaluation of phosphogypsum for alternative uses. Environ. Geotech. 2018, 5, 310–323. [Google Scholar] [CrossRef]
  177. Noli, F.; Sidirelli, M.; Tsamos, P. Dispersion of radionuclides and heavy metals from phosphogypsum stacks in soil and plants at Northwestern Greece. J. Radioanal. Nucl. Chem. 2023, 332, 4213–4221. [Google Scholar] [CrossRef]
  178. Kalinitchenko, V.P.; Glinushkin, A.P.; Minkina, T.M.; Mandzhieva, S.S.; Sushkova, S.N.; Sukovatov, V.A.; Il’ina, L.P.; Makarenkov, D.A. Chemical Soil-Biological Engineering Theoretical Foundations, Technical Means, and Technology for Safe Intrasoil Waste Recycling and Long-Term Higher Soil Productivity. ACS Omega 2020, 5, 17553–17564. [Google Scholar] [CrossRef] [PubMed]
  179. Yusupov, U.; Kasimov, I.; Mukhamedgaliev, B. Contemporary Generation Additives for Modification of Cements and Other Knitting Building Materials. Int. J. Sci. Technol. Res. 2020, 9, 1191–1192. [Google Scholar]
Soilsystems 08 00036 g001
Figure 1. The methodological approach to the implementation of the topic review rehabilitation of contaminated ecosystems and the areas of application of bioremediation processes.
Figure 1. The methodological approach to the implementation of the topic review rehabilitation of contaminated ecosystems and the areas of application of bioremediation processes.
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Figure 2. The methodological approach for the comparative review of phosphogypsum.
Figure 2. The methodological approach for the comparative review of phosphogypsum.
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Figure 3. Radionuclide migration flows through the trophic chain to the human body.
Figure 3. Radionuclide migration flows through the trophic chain to the human body.
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Figure 4. Generalisation of remediation methods.
Figure 4. Generalisation of remediation methods.
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Figure 5. Characteristics of biosorption technologies.
Figure 5. Characteristics of biosorption technologies.
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Figure 6. Accumulation of phosphogypsum in the environment.
Figure 6. Accumulation of phosphogypsum in the environment.
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Figure 7. Beneficial elements in the composition of phosphogypsum (case study: phosphogypsum dump in Sumy region, Ukraine).
Figure 7. Beneficial elements in the composition of phosphogypsum (case study: phosphogypsum dump in Sumy region, Ukraine).
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Figure 8. Distribution of countries by publication activity in the field of phosphogypsum research according to the Scopus database.
Figure 8. Distribution of countries by publication activity in the field of phosphogypsum research according to the Scopus database.
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Figure 9. Influence of the organic–mineral complex on the fixation of heavy metals and radionuclides in soils.
Figure 9. Influence of the organic–mineral complex on the fixation of heavy metals and radionuclides in soils.
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Table 1. Protocol to analyse the elemental composition of phosphogypsum.
Table 1. Protocol to analyse the elemental composition of phosphogypsum.
StepDescription
1 Drying Over-drying at 40 °C for 24 h
2 Milling Fraction size smaller than 1 mm
3 DigestionEthos 1 (MLS GmbH, Leutkirch im Allgäu, Germany) microwave-assisted wet digestion system for 35 min at 210 °C
4 MeasurementInductively coupled plasma-atomic emission spectrometry (ICP-OES, Agilent 720, Agilent Technologies Inc., Santa Clara, CA, USA)
Table 2. Main sources of some heavy metals in soils.
Table 2. Main sources of some heavy metals in soils.
HMSourcesEffects on Soil References
CdNon-ferrous metal extraction, production of phosphate fertilisers, burning of fossil fuels, waste incineration, tannery industry, electroplating, and battery disposal.The disruption of metabolic functions hinders enzyme activities, reducing the availability of N and S in the soil for crops.[20,21,23,24,25]
PbEmissions from power generation, metallurgy, mechanical engineering, metalworking, electrical engineering, chemistry and petrochemistry, woodworking and pulp and paper industries, food industry, and construction-material production, as well as automotive transport. Organisms’ metabolic abnormalities affect soil enzymes and interrupt nutrient balance, reducing soil productivity.[19,21,23,26,27,28]
ZnEmissions from non-ferrous metallurgy, waste incineration plants, coal combustion, and tyre wear.Phytotoxic effects on soil fertility, diminishing microbial biomass N; and lacking essential soil macronutrients, such as phosphorus.[9,21,26,29,30]
CuEmissions of non-ferrous metallurgy enterprises; combustion of leaded gasoline, municipal incinerators, and copper mining residue.Limited amounts of soil N and S hinder crop production. Inhibit β-glycosidase more than cellulose. Diminish microbial biomass N.[21,26,27,31,32]
HgEmissions from non-ferrous metallurgy, fossil fuel burning, steel production, metal smelting.Disruption of metabolic function in organisms.[21,26,33,34]
AsBurning of fuel, emissions from power generation, production of construction materials, pharmaceutical and textile industry. As used in herbicides, insecticides, and desiccants.Disruption of metabolic function in organisms.[21,22,26,27]
CrEmissions from ferrous and non-ferrous metallurgy (alloying additives, alloys, and refractories) and mechanical engineering (electroplating).Disruption of metabolic function in organisms.[21,26,35,36]
NiEmissions from non-ferrous metallurgy, burning of fuel, waste incineration, and chemical industries.Disruption of metabolic function in organisms.[21,26,37,38,39]
Table 3. Classification of soil bioremediation methods.
Table 3. Classification of soil bioremediation methods.
MethodBrief Definition Process Features Considering Their LimitationsReferences
BiomineralisationDeposition of heavy metals as insoluble compounds. It includes two primary methods: microbiological carbonate precipitation and enzymatic carbonate precipitation.It is considered an environmentally friendly bioremediation method that is not less effective than chemical methods. However, limitations related to microorganism strains, pollutant concentrations, and soil properties must be taken into account. Further research on soils treated with biomineralization, the solidification and stabilisation (S/S) of toxicants, is necessary to understand the patterns of strength change in polluted soils treated with biomineralization. Additionally, it is important to investigate changes in the rate of heavy metal fixation and the mechanical properties of contaminated soil.[77,78,79,80,81,82,83]
BiosorptionThis is a physicochemical and metabolically independent process that relies on various mechanisms, including absorption, adsorption, ion exchange, surface complexation, and precipitation.Advantages include low cost and significantly higher efficiency in removing metals from diluted solutions. Heavy metal adsorption and removal can be performed using biomass, which can generate income for businesses that do not use biomass, such as organic waste.
Various environmental parameters, such as temperature, metal type and concentration, metal oxidation state, microbe type, metal removal method, and biosorbent concentration, can influence the ability of microorganisms to bind metals. This may have a negative impact on biosorption efficiency.		[84,85,86,87,88,89,90,91,92]
BioprecipitationIn the process of bioprecipitation, the formed metabolites react with metals present in the groundwater, resulting in the precipitation of metals, i.e., the transformation of metals from the aqueous phase to the solid phase.Bioprecipitation is more effective in treating wastewater than soils; however, the profitability of recycling or selling recovered metals can vary depending on the investments in infrastructure of the investments in infrastructure of a company. It is recommended to use it in conjunction with other biological methods.[78,93,94,95,96,97,98]
BioaccumulationActive uptake of heavy metals into cells involves the binding of toxic metals or chemical compounds inside the cellular structure.This method not only is cost-effective but also helps minimise the environmental impact of pollution. Metal bioaccumulation is particularly useful as an impact indicator, as metals are not metabolised. Metal ions initially attach to the cell surface and are later transported into the cell. This process can lead to a temporary reduction in metal ion concentration. However, it can be utilised to synthesise metal-rich nanoparticles, provided that the processing is performed in specialised bioreactors rather than in situ.[85,99,100,101,102,103,104,105]
BiotransformationBreakdown of heavy metal compounds into less toxic forms or their conversion into less toxic forms (associated with biodegradation).Photoautotrophic microbes are capable of biotransforming heavy metals into relatively biologically inaccessible and insoluble metal sulphides. By characterising the role of sulphur assimilation pathways in the biotransformation of heavy metals, we can develop more effective processes for heavy metal bioremediation. The use of additional sulphate nutrition can enhance the rate of biotransformation in aerobic microbes.[78,85,106,107,108,109,110,111]
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Chernysh, Y.; Chubur, V.; Ablieieva, I.; Skvortsova, P.; Yakhnenko, O.; Skydanenko, M.; Plyatsuk, L.; Roubík, H. Soil Contamination by Heavy Metals and Radionuclides and Related Bioremediation Techniques: A Review. Soil Syst. 2024, 8, 36. https://doi.org/10.3390/soilsystems8020036

AMA Style

Chernysh Y, Chubur V, Ablieieva I, Skvortsova P, Yakhnenko O, Skydanenko M, Plyatsuk L, Roubík H. Soil Contamination by Heavy Metals and Radionuclides and Related Bioremediation Techniques: A Review. Soil Systems. 2024; 8(2):36. https://doi.org/10.3390/soilsystems8020036

Chicago/Turabian Style

Chernysh, Yelizaveta, Viktoriia Chubur, Iryna Ablieieva, Polina Skvortsova, Olena Yakhnenko, Maksym Skydanenko, Leonid Plyatsuk, and Hynek Roubík. 2024. "Soil Contamination by Heavy Metals and Radionuclides and Related Bioremediation Techniques: A Review" Soil Systems 8, no. 2: 36. https://doi.org/10.3390/soilsystems8020036

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