Heavy Metals Removal from Contaminated Soil by Phytoremediation: History
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Priya A.K.
,
Muruganandam Muthiah
,
Sameh S. Ali
,
Michael Kornaros

Pollution from heavy metals is one of the significant environmental concerns facing the world today. Human activities, such as mining, farming, and manufacturing plant operations, can allow them access to the environment. Heavy metals polluting soil can harm crops, change the food chain, and endanger human health. Thus, the overarching goal for humans and the environment should be the avoidance of soil contamination by heavy metals. Heavy metals persistently present in the soil can be absorbed by plant tissues, enter the biosphere, and accumulate in the trophic levels of the food chain. The removal of heavy metals from contaminated soil can be accomplished using various physical, synthetic, and natural remediation techniques (both in situ and ex situ). The most controllable (affordable and eco-friendly) method among these is phytoremediation. The removal of heavy metal defilements can be accomplished using phytoremediation techniques, including phytoextraction, phytovolatilization, phytostabilization, and phytofiltration.

  • biotechnological methods
  • genetic modifications
  • heavy metal degradation
  • phytoremediation
  • remediation techniques

1. Heavy Metal Sources in the Environment

Due to the potential for bioaccumulation and poisoning of living organic entities, heavy metal (HM) contamination has drawn attention across the world [1]. The effects of HM contamination in the environment significantly impact biological systems both in terrestrial and marine ecosystems [2]. In addition to diffuse sources, point sources of contamination, such as mining, smelting, and manufacturing, can also contribute to heavy metal contamination in soil and water. These activities can release high concentrations of heavy metals into the environment and can result in localized contamination of soil, water, and air [3]. These water contaminations are most dangerous and harmful to human and natural environments [1]. Various sources of heavy metals and their environmental pathways are shown in Figure 1.
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Figure 1. Various sources of heavy metals and their environmental pathways.
Heavy metal contamination of soil can arise from both natural and anthropogenic sources. Heavy metals in contaminated areas can typically be obtained from parent soil, also referred to as a lithogenic source. Numerous heavy metals do not exist separately; instead, they exist as synthetic structures that can be readily and directly absorbed by living cells and tissues [4]. Zn, Hg, Cd, Pb, Cu, Ni, As, and Cr are among the most commonly found heavy metals in soil. Other heavy metals, such as aluminum (Al), barium (Ba), cobalt (Co), manganese (Mn), selenium (Se), and silver (Ag), can also be present in soil at elevated levels and can pose environmental and health risks. Natural events, such as volcanic emissions, ocean salt sprays, wind-borne soil particles, forest fires, and rock weathering, can contribute to the presence of heavy metals in soil. Biogenic sources, such as the decay of organic matter, can also release heavy metals into soil [5].
Anthropogenic activities, such as industrial processes, mining, and agriculture, can significantly increase the presence of heavy metals in soil beyond natural levels, leading to potential environmental and health hazards. Hazardous materials, such as As, Cd, Cr, Cu, Hg, Pb, and others, can be found in various sources, including sewage, paints, alloys, electronic products, and wastewater from mines. These materials can easily leach into soil and accumulate over time, contaminating soil [6]. Heavy metal contamination can sometimes result from accidental spills or leaks from industrial sites or transportation. The origins of heavy metal pollution in soils vary and can be attributed to natural and human activities [7]. For instance, the E-waste incinerator site in East Jerusalem was studied on soil samples taken from 29 different locations specified varying mobility of heavy metals [8]. These activities can release heavy metals into the air, water, and soil, leading to contamination and potential health hazards for humans and wildlife. Therefore, effective management and control of anthropogenic sources are necessary to reduce environmental heavy metal pollution.

2. Recent Developments in Heavy Metal Remediation Strategies

Soil contamination by heavy metals has become a growing concern due to rapid urbanization and industrialization. Heavy metals, such as lead, arsenic, cadmium, and mercury, are persistent and toxic in the environment, and they can accumulate in the soil over time. This contamination can seriously affect the environment and human health [9]. Soil remediation (Figure 2) is thus a critical process to help protect the environment and human health. Soil can become contaminated with harmful substances, such as heavy metals, pesticides, and petroleum products, through industrial and agricultural practices, waste disposal, and accidental spills [10].
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Figure 2. Remediation techniques for heavy metal removal.
A soil remediation technique known as soil substitution reduces the concentration of pollutants in to a permissible natural limit. Soil spading and soil substitution are two methods used in soil remediation to mitigate the effects of soil contamination by heavy metals or other pollutants. Soil spading, also known as soil turning or soil tilling, involves digging and mixing the polluted soil with pure soil to reduce contaminant concentrations. This method is often used for large areas of contaminated soil, where removing and replacing the entire contaminated soil layer is impractical. Soil spading helps to aerate the soil and promotes microbial activity, which can accelerate the natural breakdown of contaminants in the ground. Soil substitution, also known as excavation and disposal, is a method of soil remediation that involves removing contaminated soil and replacing it with pure soil. This approach is often used for small, localized areas of contamination, such as around underground storage tanks or industrial sites. Soil substitution can effectively reduce the risk of exposure to the contaminant and restore the soil to a healthy state. Both ground spading and soil substitution can be effective methods for soil remediation, but they each have advantages and disadvantages.
The choice of method will depend on the nature and extent of the contamination and other factors, such as cost and accessibility. It is essential to carefully assess the situation and consult with experts to determine the best approach for remediation [4]. This method calls for treating the replaced soil to stop further contamination [11]. Another process of making the contaminated soil less potent is adding new ground and covering the old. This technique effectively reduces the climate-damaging effects of toxic emissions, but it is costly, necessitates a sizable working area, and is only suitable for treating soil that is locally severely contaminated. 
Thermal desorption is used in soil remediation to volatilize heavy metals and metalloids, such as mercury and arsenic, from contaminated soil. While thermal desorption is a method of soil remediation that involves heating contaminated soil to release the contaminants, it does not necessarily involve the use of microwaves, steam, or infrared radiation. Once the heavy metals have been volatilized, a negative vacuum tension is applied, or a transporter gas is used to collect and remove the volatile heavy metals from the contaminated soil. Two types of thermal desorption methods exist: high-temperature desorption and low-temperature desorption. High-temperature desorption is typically performed at temperatures between 320 and 560 °C and is used for heavily contaminated soils. On the other hand, low-temperature desorption is performed at temperatures between 90 and 320 °C and is used for less contaminated soils [4][11]. This innovation has the advantage of being a simple technique for soil remediation. However, the equipment needed to complete thermal desorption is expensive and the process takes a long time [12].
Soil washing typically involves mechanical agitation of the soil using water or aqueous solutions containing chelating agents and/or surfactants. The chelating agents and surfactants help to solubilize and mobilize contaminants, such as heavy metals, pesticides, and petroleum hydrocarbons. The washing process generates a wastewater stream or leachate that contains the dissolved contaminants. The wastewater is then treated using a range of technologies, such as chemical precipitation or biological treatment, to remove or immobilize the contaminants before discharge into the environment [13]. Soil washing typically involves several stages of physical and chemical processes to remove contaminants from soil.
Electrokinetic remediation is another method used for soil remediation to clean up contaminated soil. It involves using an electric field gradient to remove heavy metals and other contaminants from the soil. This method involves placing electrodes in the soil and passing a direct current through the soil between the electrodes. This creates an electric field gradient that drives the movement of heavy metals and other contaminants from the soil toward the electrodes [14]. The contaminants are then removed from the soil by a process known as electroosmosis, where a liquid solution is drawn through the soil by the electric field, carrying the contaminants with it. Electrokinetic remediation has some advantages over other soil remediation methods. It is particularly effective for heavy metals and other ionizable contaminants and can be used for various soil types [15]. 
Phytoremediation is a promising soil remediation technique that has gained attention from various experts due to its efficiency, cost-effectiveness, and eco-friendly nature. It involves using plants to remove or degrade contaminants from the soil [15]. The advantages of phytoremediation techniques are shown in Figure 3.
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Figure 3. Advantages of phytoremediation techniques.

3. Heavy Metal Removal from Contaminated Soil by Phytoremediation

Phytoremediation uses metal-aggregating plants to reestablish debased natural resources, namely, soil and water [16]. The uptake of heavy metals from contaminated soil can occur over the course of several distinct cycles during phytoremediation. The specific system depends on the type of toxin, the plant species used, and other ecological factors. In a process known as phytostabilization, plants are used to immobilize pollutants in soil and prevent their spread to new areas. Plant roots release proteins and organic acids into the soil during the rhizodegradation cycle, which separates soil impurities. Phytoextraction involves the uptake of contaminants by plant roots and their accumulation in the above-ground plant tissues [5]. Phytodegradation is the process by which plants break down contaminants in their tissues through metabolic processes [15]. Phytoaccumulation is when plants take up contaminants and store them in their tissues without breaking them down. Phytovolatilization is when plants release contaminants into the air through transpiration or other mechanisms [5].
The removal of heavy metals from soil and water and the selection of suitable plant species can both be accomplished through phytoremediation [17]. Plants are viable options for phytoremediation due to their physiological capacity to withstand and accumulate heavy metals as well as their adaptability to various environmental conditions. Furthermore, the use of specific plant species for phytoremediation can be tailored to the type of heavy metal pollution, as different plant species have varying abilities to accumulate specific heavy metals [18]. There are various techniques that have been developed for the removal of heavy metals through phytoremediation processes.
However, compared to physiological strategies, they are less viable and more expensive [19]. Standard techniques, such as physicochemical cycles, are typically used to remove contaminants from soil. Due to their more notable effectiveness and lower costs, physiological strategies are generally recognized as additional promising options for soil remediation [3]. Bioremediation can also involve using microorganisms to break down or transform contaminants into less toxic forms. Microorganisms can degrade organic pollutants or transform heavy metals into less harmful substances.
Due to its unique ability to eliminate dangerous synthetic substances through plant underground root growth, bioaccumulation, impurity debasement, or movement [20], the phytoremediation approach has many advantages in ecological clean-up. Various techniques for phytoremediation are shown in Figure 4.
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Figure 4. Techniques for phytoremediation.

4.1. Phytoextraction

This process involves using the natural ability of plants to absorb and accumulate pollutants through their roots and above-ground parts and transform or degrade them into less harmful substances. The plants uptake these pollutants through their root systems and then transport them to their above-ground biomass, accumulating them in various plant parts, such as leaves, stems, and fruits. In some cases, the pollutants can be removed from a site by harvesting the plants and disposing of them elsewhere. The plants can be used for various purposes, such as biofuel production or livestock feed, provided the accumulated toxins are safe. This process is referred to as phytoextraction [21]. Metal exchange to shoots is a significant physiological interaction because projections are much easier to collect than roots—the most effective phytoremediation method for removing heavy metals and metalloids. The main idea behind phytoextraction is to grow appropriate plant species on site, collect the metal-enriched biomass, and then treat it to reduce its mass and size [17].

4.2. Phytostabilization

Phytostabilization is a phytoremediation technique that uses metal-tolerant plant species to immobilize heavy metals in soil and reduce their bioavailability. This is achieved using plants with deep root systems that can penetrate and stabilize the soil, preventing heavy metals from leaching into the environment [22]. This can occur through various mechanisms, including precipitation or complexation of heavy metals in the rhizosphere, uptake, and accumulation of heavy metals in root tissues, and adsorption onto root cell walls. The immobilized heavy metals become less mobile and bioavailable, reducing the potential for human and environmental exposure [23]. Phytostabilization is a technique that helps preserve soil health at heavy-metal-contaminated sites. It involves using plants to immobilize heavy metals in the soil and prevent their dispersion by wind or runoff. This technique is advantageous because it does not require the removal of contaminated biomass, unlike phytoextraction [12].

4.3. Phytovolatilization

This technique eliminates poisons from soil without requiring the land to be taken away or dealt with. Nonetheless, the viability of phytovolatilization relies upon the toxins present, the plant species utilized, and natural conditions. For example, in the phytovolatilization of Hg, the vaporized Hg can be recondensed and redeposited in the environment, resulting in water and soil pollution. Therefore, phytovolatilization must be utilized cautiously, and ecological conditions, for example, wind speed and direction, must be assessed to limit potential ecological harm [24]. Phytovolatilization is viable in controlling certain environmental pollutants, yet it is not broadly utilized as it has certain limitations. The fundamental disadvantage is the likelihood of airborne toxins causing pollution in surrounding areas. Hence, it is necessary to use this strategy cautiously and only in areas with low population densities or air contamination restrictions exist [15].

4.4. Rhizofiltration

Rhizofiltration is a promising approach for removing contaminants from water and liquid waste, and several plant species have been identified as effective in this process. Plants with fibrous root systems and large surface areas are well-suited for rhizofiltration [1]. For example, Typha latifolia effectively removes methyl parathion from hydromorphic soils, while bean species (Phaseolus vulgaris) have been found to extract uranium and cesium from groundwater efficiently.

4.5. Rhizodegradation

Rhizodegradation is a natural and cost-effective method for the remediation of contaminated soils. It is a complex process involving interaction between plant roots, microorganisms, and contaminants [19]. Rhizodegradation is a type of phytoremediation that consists in using plants and their associated root-zone microorganisms to degrade pollutants in soil. The rhizosphere is the zone of soil surrounding the roots of plants, where there is a high concentration of microorganisms that can interact with the plant and the contaminants. The selection of plant species also plays a crucial role in rhizodegradation, as different plants release different types and quantities of exudates, which can influence the microbial community and their ability to degrade contaminants. Rhizodegradation has several advantages over traditional remediation methods, including its low cost, reduced environmental impact, and potential for long-term effectiveness [10].

4.6. Phytodesalination

Phytoremediation has been widely studied and accepted to remove salt from impacted soils using halophytic plants [25]. Halophytes are plants that are adapted to grow in highly saline environments, and they are more effective in heavy metal conditions than glycophytic plants, which grow in non-saline environments [26].

5. Potential Biotechnological Approaches for Phytoremediation

Several aids or techniques can enhance phytoremediation, depending on the specific contaminants and environmental conditions. Some of these aids include: Bioaugmentation: This involves adding beneficial microorganisms to the soil, which can help to break down contaminants and improve plant growth [27]. Phytoextraction: Utilizing plants that can accumulate large concentrations of pollutants in their tissues allows for secure collection and disposal. Rhizofiltration: This technique uses the roots of plants to filter contaminants from water. The roots absorb the contaminants and then release them into the plant tissue, where they can be broken down or stored [3]. Hyperaccumulation: This method makes use of plants that can store exceptionally large concentrations of specific pollutants in their tissues. These plants typically remove metals, such as nickel or lead. Soil amendments: Adding certain substances to soil, such as activated carbon or organic matter, can help to improve the soil structure and increase the availability of nutrients for the plants. Genetic engineering: Researchers can modify plant characteristics to increase their ability to remove specific pollutants, as heavy metals, in the case [14].
Plant biotechnology techniques undoubtedly contributed to the development of transgenic crops, and researchers have been working toward the development of efficient, ethical, and cost-effective bioremediation techniques; however, there are still some challenges. Since they differ from physical–synthetic remediation techniques, these biotechnologies have emerged as alternative options aiming for natural rehabilitation. Other intrusive techniques include high-temperature vitrification, corrosive washing, and the removal of soil from an area, all of which have higher associated costs and have an impact on soil productivity and biodiversity [28].

6. Factors Affecting Phytoremediation Potential

The accessible part of metals is the fraction plants can take up and is influenced by soil pH, redox potential, and the presence of chelating agents or competing ions, as shown in Figure 5. The inaccessible part of metals is firmly bound to soil minerals and cannot be extracted by plant roots. Hence, it is essential to select appropriate plant species and optimize soil conditions to enhance the bioavailability of metals for effective phytoremediation [15][20]. In addition, chelating agents, such as EDTA or citric acid, can enhance the uptake of metals by plant roots, but they may also increase the risk of metal leaching and contamination of groundwater [15]. The use of chelating agents to alter the bioavailability of strong metals may be harmful to plants and influence their behavior. Along these lines, it is essential to consider the advantages and disadvantages of chelating agents to guarantee that they are safe for the environment and climate. 
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Figure 5. Factors affecting phytoremediation potential.

This entry is adapted from the peer-reviewed paper 10.3390/toxics11050422

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