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Review

Research Progress in the Joint Remediation of Plants–Microbes–Soil for Heavy Metal-Contaminated Soil in Mining Areas: A Review

by
Hong Li
1,
Tao Wang
2,
Hongxia Du
3,
Pan Guo
2,
Shufeng Wang
1,2,* and
Ming Ma
1,2
1
Key Laboratory of the Three Gorges Reservoir Area of the Ministry of Education, College of Resources and Environment, Southwest University, Chongqing 400715, China
2
Center of Molecular Ecophysiology (CMEP), College of Resources and Environment, Southwest University, Chongqing 400715, China
3
Chongqing Key Laboratory of Bio-Resource for Bioenergy, College of Resources and Environment, Southwest University, Chongqing 400715, China
*
Author to whom correspondence should be addressed.
Sustainability 2024, 16(19), 8464; https://doi.org/10.3390/su16198464 (registering DOI)
Submission received: 21 June 2024 / Revised: 17 September 2024 / Accepted: 18 September 2024 / Published: 29 September 2024
(This article belongs to the Section Environmental Sustainability and Applications)
Browse Figures
Versions Notes

Abstract

:
Plants growing in heavy metal (HM)-contaminated soil have evolved a special detoxification mechanism. The rhizosphere gathers many living substances and their secretions at the center of plant roots, which has a unique ecological remediation effect. It is of great significance to thoroughly understand the ecological process of rhizosphere pollution under heavy metals (HMs) stress and develop biotechnology for joint remediation using plants and their coexisting microbial systems according to the mechanism of rhizosphere stress. Microbes can weaken the toxicity of HM pollutants by transforming the existing forms or reducing the bioavailability in the rhizosphere. Microbes survive in the HM-polluted soils through the production of stress-resistant substances, the participation of proteins, and the expression of heavy metal resistance genes, which strengthens the resistance of plants. Moreover, microbes can improve the nutritional status of plants to improve plant resistance to HMs. Plants, in turn, provide a habitat for microbes to survive and reproduce, which greatly accelerates the process of bioremediation. Briefly, the combined remediation of soil HMs pollution by plants and microbes is a promising, green, and sustainable strategy. Here, we mainly elucidate the joint remediation mechanism of plant–microbe symbiosis and introduce the coping characteristics of plants, microbes, and their symbiotic system, hoping to provide a scientific basis for the remediation of HM-contaminated soil in mining areas and the sustainable development of the ecological environment.

1. Introduction

Under the background of industrial globalization, human activities such as mining production, industrial emissions, and transportation have caused varying degrees of soil heavy metal accumulation in many countries [1]. Among these activities, the most severe impacts come from tailings ponds and dams, exhaust gases, and wastewater generated in the mining, smelting, and processing of mineral resources, especially tailings ponds and dams. Under the influence of surface biogeochemistry, HMs with high bioavailability and fluidity accumulate in the soil and migrate to other areas, even releasing into rivers, groundwater, and farmland [2,3,4]. This increases the risk of HM exposure in the soil, crops, well water, and fish around the mining area [5,6,7]. Furthermore, particulate emissions of some HMs settle in areas far from mining sites with atmospheric motion and rainfall [8] (Figure 1). Therefore, mining areas have become key targets for soil HM remediation [9].
Soil HM pollution caused by metal mining not only inhibits the growth and reproduction of microorganisms, changes the structure of the soil microbial community, and reduces soil quality but also affects the growth and development of plants. HMs can easily accumulate in plants, especially in edible parts [10], and they bioaccumulate in animals and humans through the food chain, leading to cancer or other diseases and posing great ecological hazards [11]. For example, chromium (Cr), and copper (Cu) are easily absorbed in the intestine, zinc (Zn) is easily absorbed in the stomach, and lead (Pb) can be inhaled into the lungs. These HMs can negatively affect the nervous system, hematopoietic system, and digestive system. Additionally, cadmium (Cd) can cause bone pain disease [11]. In the human health risk assessment of wheat consumption, the bioavailability of Cd and Zn in simulated colon was 53% and 64% of that in the simulated small intestine, respectively. However, the bioaccessibility of Pb showed an obvious escalating trend, being 2.4 times higher than that of intestinal incubation [12]. Moreover, HM pollution can damage the blood lymphocytes and kidneys of organisms [13]. Pb concentrations in the blood and liver of carnivorous fish close to the main pollution source are the highest and decrease with distance from the mining area. In polluted areas affected by mining activities, the overall disease incidence rate of local residents has increased, with a significant increase in chronic diseases and vascular system dysfunction in children, which in turn increases the risk of cancer [14,15]. It is evident that HM pollution caused by mining activities is threatening the sustainable development of the natural ecological environment and human health in mining areas and their surroundings. Therefore, the remediation and treatment of HM pollution in mining areas is imperative.
Phytoremediation is regarded as one of the potential remediation methods for HM-contaminated soil due to its low cost, significant effect, and environmental friendliness [16,17]. However, in practical applications, the slow growth and small biomass of hyperaccumulator, along with the long remediation cycles, low efficiency, and lack of economic benefits, have restricted the development of this technology [18]. The combined remediation of plants–microbes can effectively address these problems. Microorganisms can improve soil nutrients in mining areas, promote plant growth, and enhance the resistance of plants, thus making it possible for plants to adsorb and fix various HMs in mine soil, thereby improving remediation efficiency [19,20,21]. Moreover, due to the long-term exposure to soil environments containing high concentrations of HMs, microorganisms have developed resistance and high tolerance to these HMs. They can also cooperate with plants to remove HMs from polluted soil [22,23]. The joint remediation of plants–microbes has become one of the research hotspots. However, there are no effective measures for the treatment of enriched biomass after restoration, and plants containing HMs pose a risk of returning them to the soil. Therefore, perennial woody plants are considered a good choice.
The interaction between microorganisms and plants not only enhances the resistance of plants to HMs but also provides an activity space for microorganisms, thereby improving the necessary carbon source for microbial growth. This mutualistic symbiosis system greatly accelerates the process of phytoremediation [24]. In recent years, extensive research has been conducted on the joint remediation of plants–microbes in HM-contaminated soil. However, this is still in the development stage and requires further exploration before it can be widely applied in practical production. Here, we provide a detailed description of the characteristics of the plants, microbes, and their symbiont that play key roles in the plants–microbes system and elucidate the common forms and existing problems of joint remediation of plants–microbes, as well as future research considerations. By exploring the joint remediation mechanism of the plants–microbes system, we hope to provide a contribution for the remediation of HM-contaminated soil in mining areas.

2. References Retrieval

For database search strategies, the method described by Li was used [25]. All articles were retrieved using specific topic keywords (heavy metals, mining areas, heavy metal accumulation, tolerance, oxidative stress, transporter proteins, phytoremediation, and bioremediation) by four search engines, namely ScienceDirect, Springer, ProQuest, and Web of Science. The retrieval period of publication was set from 2000 to 2024. For the selection of articles, research or review articles on the same topic as this article were first excluded. For articles with similar themes or conclusions, representative articles that were published more recently were chosen.

3. Characteristics of Heavy Metal Pollution in the Soil of Mining Areas

Soil HM pollution in mining areas primarily comes from mining activities. In various types of mineral deposits, HMs generally exist in the form of sulfides. During the mining and smelting processes, large amounts of tailings containing HM sulfides, such as Pb, Cd, As, Cu, Zn, are generated, which are easily oxidized. On the one hand, the production of acidic wastewater accelerates the dissolution of minerals. On the other hand, HMs are activated, causing them to migrate to the surrounding farmland soil as ions in surface water [26,27]. Due to the long-term accumulation of HMs, their concentrations in the soil of mining areas are significantly higher than that of the surrounding soil [28]. Soil HM pollution in mining areas is often caused by a combination of multiple HMs. Due to the presence of various chemical elements such as As, Pb, Zn, Hg, Cd, Cu, Co, and Ni in mining waste rock, many types of HMs cause soil pollution in mining areas, most of which involve composite contamination by several or even more HMs (Table 1). Globally, due to the various environmental liabilities that are left by abandoned mining areas and the exploitation of mineral resources, large areas of mining soil have been contaminated with HMs [29]. The ecological hazards of HM pollution in mining soil are significant. Currently, the mining and smelting of metal ores, as well as the abandonment of mining sites, are major contributors to soil HM pollution, excessive HM content in grains, and increased ecological risks [4,30].

4. The Role of Plants in the Remediation of Heavy Metal Pollution in Mining Areas and Its Response Mechanism

While ceasing mining activities and implementing source control measures such as wastewater purification can reduce the concentration of HMs in the atmosphere and surface water, phytoremediation of HMs in mining soil can also significantly reduce the concentration of HMs. It is widely accepted that HM accumulation capacities vary with plants, with about 20.6% of plants (growing in China that span 22 provinces) having strong phytoremediation capacities [47]. In the study of indigenous plants suitable for phytoremediation, the most representative families are Gramineae, Leguminosae, Asteraceae, Apiaceae, and some Phanerophytes [48]. However, due to their strong adaptability and hyperaccumulation ability, invasive plant species are also considered potential candidates for phytoremediation in industrial mining areas [49].

4.1. The Role of Plants in the Remediation of HM-Polluted Sites

Current research has found several HM hyperaccumulator plant species, including Noccaea caerulescens, Pteris vittate L., Berkheya coddii, Commelina communs Linn, Sedum alfredii Hance, Sedum plumbizincicola, and Solanum nigrum L. [50]. This suggests that herbaceous plants may be the pioneer species for HM remediation in mining areas. Moreover, the same plant has significantly different enrichment capacities for various HMs. For example, Plantago lanceolata had the highest bioaccumulation factor (BAF, the ratio of HM content in a certain part of a plant to the corresponding HM content in the soil) for Pb, which was five times higher than other HMs. Additionally, the concentration of As in the aboveground of Bouteloua gracilis reached 1053 mg/kg, with the highest bioconcentration factor (BCF, the ratio of the concentration of HM in biological tissues to the concentration dissolved in water), which was close to one [51]. Among 24 native plant species, Jatropha curcas and Capsicum annuum had strong accumulation capacities for Hg, with BCFs of 0.99 and 0.83, respectively [52]. Further research of HM accumulation by plants in mining areas should focus on hyperaccumulator species in heavily polluted sites. The success of phytoremediation depends on both the tolerance of plants to HMs and their biomass. High tolerance to HMs ensures the survival of the plants, while large biomass facilitates the accumulation of HMs within them [53,54,55]. However, herbaceous plants have less biomass and limited capacity, leading to a growing interest in woody plants with larger biomass. It is widely accepted that woody plants have larger biomass and strong tolerance to various HMs. Under HM stress, Cytisus scoparius can reduce the mobility of metals and prevent their diffusion into other ecosystems [56], offering potential for the remediation of tailings ponds in China. In order to identify suitable woody plant species for future vegetation restoration, Li et al. [57] conducted a field survey on the effects of vegetation restoration in mining areas. The results showed that Amorpha fruticosa, Populus tomentosa, and Salix babylonica had the most effective ecological restoration. The quality of the surface soil under the forest was significantly improved (p < 0.05), with the soil under the forest of leguminous plants showing the best quality. Scholars compared the extraction abilities of two woody plants, Robinia pseudoacacia and black poplar, and found that Robinia pseudoacacia had a better extraction ability for iron (Fe), manganese (Mn), and Zn but weaker ability for Cu, Ni, Cr, and cobalt (Co). In contrast, black poplar showed a greater ability to extract Fe, Zn, and Mn [58]. Cd accumulation in the shoots of Fraxinus rotundifolia and Robinia pseudoacacia was significantly higher than that in Platanus orientalis. R. pseudoacacia showed a higher metal accumulation index (MAI, the overall ability of plants to accumulate multiple metals) for the leaves (2.21), while Fraxinus rotundifolia had a higher MAI for the shoots (2.4) [59]. The study also found that HM content was highest in plant roots, followed by trunks and branches, with leaves having the lowest content [58]. Overall, many of the investigated plant species are capable of both absorbing and tolerating HMs.
Additionally, factors such as reasonable community succession, vegetation density, species selection, and planting methods can promote the stability of the internal environment of plants. The succession of the vegetation community can increase the mobility of HMs, thereby affecting the stability of the soil–plant system. Due to the different light requirements of plants growing on the tailings, nitrogen-fixing species are more abundant there than in natural forests, with 47% of plants possessing mycorrhizal symbiosis [60]. In terms of HM extraction, the intercropping effect of three indigenous herbaceous plant species in mining areas is better than that of two plants, while a single plant is the least effective [61]. This suggests that multiple plant species intercropping can improve the phytoremediation efficiency of HMs.

4.2. The Mechanism of Plant Response to HMs

In higher plants, metal ions can be absorbed not only by roots but also through subclasses of aquaporins and then be transported to the vacuolar for compartmentalized storage or aboveground redistribution. Therefore, transporters are very important in responding to HM stress. Currently, the transporters involved in these processes include multiple gene families, including plant cadmium resistance (PCR), cation diffusion facility (CDF), heavy metal ATPase (HMA/P1B), ATP-binding cassette transporter (ABC transporter), multidrug and toxic compound extrusion (MATE), natural resistance-associated macrophage protein (NRAMP), Zrt/Irt-like protein (ZIP), and yellow stripe protein (YSL) [25,62,63,64]. Under high concentrations of HMs, plants develop a series of resistance mechanisms to counteract the toxicity of HMs.

4.2.1. The Absorption and Transportation of HMs by Plants

The root is the most important site for HMs absorption in plants. HM ions mainly enter the root cells through two pathways: the apoplastic pathway and the symplastic pathway, after being activated in the rhizosphere of plants [65] (Figure 2). In the apoplastic pathway, HMs are transported laterally to the xylem through cell walls and extracellular spaces. Cd2+ enters hyperaccumulator Sedum alfredii roots through the root tips and lateral root gaps, with up to 37% of Cd2+ in the xylem originating from the apoplastic pathway [66]. Due to the selective permeability of the cell membrane, HM ions usually enter the cytoplasm through the transport system for essential nutrients after they reach the cell membrane. Ca2+ transporters are key carriers for plants to absorb HMs. Cd2+, Mg2+, and Zn2+ are absorbed by Amaranthus mangostanus L. root cells through calcium ion channels [67]. Zn and Fe transporters such as ZIP1, ZIP2, and IRT1 have a strong affinity for Cd and are important transporters for HM absorption in plant roots [68]. In addition, HMs can also be transported into root cells in chelated form by peptide transporter families such as YSL [69]. After entering the root cells, HM ions need to be transported to the vessels from the xylem parenchyma cells and subsequently to the aboveground areas. Due to the obstruction of the Casparian strip, metal ions can only enter the xylem vessels through the symplastic pathway. In studies of Cd-accumulating plants, Cd was absorbed via the symplastic pathway and Cd concentrations in the xylem sap in high-Cd-accumulating sweet sorghum were higher than those in low-Cd-accumulating sweet sorghum. Root anatomy results showed that the thick barrier of endodermal apoplasmic in the low-Cd-accumulation type might restrict Cd from entering xylem [70]. Therefore, higher accumulation of Cd depends on the effective absorption of root and xylem loading. Xylem loading plays an important role in the process of HMs entering the shoots of plants [71]. There are many important ion transporters or channel proteins in plants that promote the loading of HMs into the xylem, such as heavy metal ATPases (HMAs) and zinc/iron regulatory proteins (ZIPs). The transportation of Cd and Zn from rice roots to aboveground mainly relies on the heavy metal ATPase OsHMA2 [72]. In addition, the NtZIP5A/B, a zinc deficiency-induced transporter in Nicotiana tabacum, controls the vertical distribution and transport rate of Zn and Cd in plants, achieving the transport of Zn to aboveground under Cd stress [73]. The expression of OsHIPP42 improved rice elongation, biomass, and chlorophyll accumulation, thereby enhancing the resistance to and accumulation of Cd [74].

4.2.2. The Allocation and Isolation of HMs

High concentrations of stored HMs can significantly impact plant organelles (Figure 2). Studies have shown that high concentrations of Cu alter the ultrastructure of chloroplast, plastid, mitochondria, and other organelles of jute [53]. During the process of absorbing HMs, plant roots develop mechanisms to resist the toxicity of HMs, as shown in Figure 2. The cell wall serves as the first barrier preventing HMs from entering cells, as pectin and cellulose within the cell wall can bind to some HM ions [75,76]. Zn is mainly stored in the root cortex, while Cd is mainly stored in the extracellular matrix, especially in the cell wall in Sedum plumbizincola [77]. Most of the HMs entering plants are stored in the roots, where they form insoluble complexes with amino acids, organic acids, phytochelatins (PCs), metallothioneins (MTs), and glutathione (GSH), thereby reducing the toxicity of HMs. For example, most Cu is chelated in the roots of plants, initially forming Cu alginate-like substances on the root surface. Cu (I)–glutathione complexes are mainly formed from the root epidermis to the cortex and vascular bundle, while Cu–histidine complexes are formed in the cell layer of root [78]. Meanwhile, these complexes are transported to vacuoles for sequestration through proton/cation exchange transporters, HMA transporters, and ABC transporters, reducing the free cytoplasmic concentration of metal ions [79,80,81] and avoiding damaging important physiological processes in cells. For most plants, cell wall fixation, selective cell membrane permeation, and vacuole sequestration are important parts of the detoxification mechanism of Cd in plants [82].

4.2.3. The Resistance of Plants to HMs

The photosynthesis and antioxidant capacities of plants are closely related to HM resistance, as shown in Figure 3. Titanium (Ti) affects the photosynthetic hypercomplex and PSII reaction center in plants, reducing the net assimilation rate and stomatal conductance by 80% and 90%, respectively, leading to severe toxicity in plants [83]. Under Cd stress, NADPH oxidase, the most important source of ROS (reactive oxygen species), not only regulates the production of H2O2 but also influences the coupling of SOD (superoxide dismutase) and glutathione with some redox reactions and the GSH/GSSG ratio [84]. Other compounds, such as PCs and MTs, can prevent oxidative stress by chelating metal ions in the cytoplasm [85]. PCs are derived from GSH through the catalysis of phytochelatin synthase (PCS), and the synthesis of PC–HM (heavy metal) complexes depletes reduced GSH and alters the oxidative state in plant cells [86]. MTs increase plant tolerance to HMs by regulating the level of ROS [87]. In order to resist the toxicity of HMs, most plants exhibit similar stress response. Under high concentrations of Cd, the biomass, chlorophyll, and gas exchange parameters of plants continued to decline. However, the ability of antioxidant stress and the regulation of ROS were strengthened, and the activities of SOD, POD, CAT, and APX, as well as the expression levels of stress-related genes, were enhanced [88].
Moreover, high concentrations of HMs have a great impact on plant growth, but this can be alleviated by adding plant hormones. Exogenous hormones such as ABA, GA, and ethylene can improve plant growth by inducing cell division and expansion, enhancing nutrient absorption and transport [89], reducing MDA and ROS content, improving antioxidant enzyme activity, and promoting photosynthesis to enhance the tolerance of plants to HMs [90,91]. The ABA signaling pathway regulates specific gene expression through the participation of transcription factors, maintains osmotic balance, induces stress signals transduction, and promotes organic acid and amino acid production, thereby ensuring that plants can adapt to HM stress and maintain homeostasis [92,93]. Previous research has found that ABA signaling molecules interact with MYB49, a previously unknown R2R3-type MYB transcription factor, which directly binds to promoters to actively regulate the expression of the basic helix loop transcription factors bHLH38 and bHLH101, thus activating the genes encoding transporters involved in Cd uptake [94]. Cd-induced ABA acts as a feedback mechanism to control Cd absorption and accumulation in plant cells, preventing the binding of transcription factors with downstream promoters [94]. The expression of WRKY13 directly binds to its promoter to activate the transcription of PDR8, promoting both the accumulation and tolerance of Cd in plants. WRKY13 also acts upstream of PDR8 and positively regulates Cd tolerance [95].

4.2.4. Response of Other Proteins to HMs

In general, plants activate various signaling pathways and defense mechanisms, synthesizing stress-related proteins in response to HMs, which reflects their tolerance to HM stress. Overexpression of MerT increased the tolerance of transgenic Arabidopsis to Hg and reduced the production of ROS, thereby protecting plants from oxidative damage [96]. However, as main components of living cells, toxic metal ions interfere with the process of polypeptide folding to form natural proteins and affect the stability of proteins in cells, resulting in the gradual inactivation of cells [97]. Plants can fight against excessive metals in the environment by regulating complex intracellular signal networks, mediating the synthesis of metal-binding proteins and the expression of transporters and promoting the accumulation of HMs in vacuoles, chloroplasts, and the Golgi apparatus [98,99]. For example, Cd stress induces the activation of calcium-dependent protein kinase (CDPK), calmodulin kinase (CaMK), calmodulin B-like protein kinase (CBLPK), and mitogen-activated protein kinase (MAPK) signaling pathways, leading to an increase in the expression of PC and MT and the accumulation of Cd in chloroplasts [85,100]. The production of organic acids, amino acids, and other metabolites can also rapidly repair proteins damaged by stress and eliminate or degrade proteins with non-natural conformation.

5. Joint Remediation of Plants–Microbes

5.1. Response of Microorganisms in Plants–Microbes Joint Remediation

The efficiency of phytoremediation can be enhanced by inoculating rhizobia, which can form symbiotic relationships with leguminous plants and develop root nodules [92,101]. Rhizobia can tolerate high concentrations of HMs. For example, horse gram rhizobia were able to tolerate 1000 µg/g Co supplemented in culture media and 100 µg/g in Co-supplemented soil [102]. Therefore, with the inoculation of rhizobia, the tolerance of the host plant to HMs can be increased. In addition, inoculation with rhizobia can reduce the absorption of HMs by plant roots, thereby reducing the toxicity of HMs to plants [103]. Some studies have also found that inoculating rhizobium can promote the uptake, transportation, and accumulation of HMs [104,105].
AMFs (Arbuscular mycorrhizal fungi) are also widely present in HM-polluted soil and can establish a good symbiotic relationship with host plants, affecting plant growth metabolism, absorption, and accumulation of HMs. Therefore, AMFs are considered the most significant symbiotic fungi in promoting plant remediation [106]. Although the spore density and root colonization rate of AMF decreased with the increase of soil pollution, arbuscular mycorrhiza with higher tolerance to HMs can be isolated from soil and sediment that is contaminated by high concentrations of HMs. Studies have shown that AMF grown in areas with high concentrations of HMs have the ability to reduce the concentration of HMs in the soil, thus reducing the toxicity of HMs [107].
The colonization of endophytic bacteria in plants is also very common in HM-polluted environments. Endophytic bacteria in plants refer to bacteria isolated from surface-disinfected plant tissues or obtained from within plants, which can colonize various tissues and organs of healthy plants without changing their phenotypic characteristics or functions. Plant endophytes include endophytic fungi, endophytic bacteria, and endophytic actinomycetes, with endophytic bacteria being distributed in the cells or intercellular spaces of roots, stems, leaves, flowers, fruits, and seeds of plants. The endophytic bacteria isolated from Typha latifolia that are Pb-tolerant (Pseudomonas azotoformans JEP3, P. fluorescens JEP8, and P. gessardii JEP33) and Cd-tolerant (P. veronii JEC8, JEC9, and JEC11) have great potential for promoting plant growth, which contributes to T. latifolia adaptation to HM-polluted sites [108]. Cheng [109] found that all four endophytic bacteria treatments activated soil Cd, promoted the growth of S. plumbizincicola, increased its Cd content, and enhanced the phytoremediation of Cd-contaminated farmland soil.
In addition, different rhizospheric strains have different effects, and the HM resistance of strains is partly due to the extensive physiological and biochemical diversity among them. When plants are exposed to high concentrations of HMs, combined inoculation with multiple strains can improve plant biomass and nutrition and their tolerance to HMs. Under HM stress, double inoculation (simultaneous inoculation with two strains) improves plant growth and increases nodule number and nitrogen content, thereby improving the aboveground biomass and stability of plants [19,110,111]. At present, organic amendments (compost, peat moss) are being used in the joint remediation of plants and microbes to improve the efficiency of plant remediation of HMs [112].

5.2. The Mechanism of Plants–Microbes Joint Remediation

Microbe-assisted HM remediation is a sustainable strategy [113]. Microbes’ symbiotic relationship with plants can obtain the necessary nutrients for growth from plants, while microbes can reduce the biological toxicity of HMs to plants, promote nutrient absorption and growth, enhance resistance, and improve the extraction ability of plants for HMs by changing the form and effectiveness of mineral elements [114] (Table 2 and Figure 4).

5.2.1. Promotion of Plant Growth

Plant growth directly affects the accumulation of and tolerance to HMs. Microbes can enhance the survival ability of host plants by enhancing their nutrient acquisition ability, metal tolerance, and stability [132]. The colonization of AMF not only increases the surface area of plant roots but also allows mycelium to extend into spaces that cannot be reached by plant roots, thus promoting the absorption of water, N, P, and K by the plant, thereby promoting plant growth and increasing plant biomass [133]. In addition, the colonization of AMF (Glomus versiform) increases the uptake of nutrients by plants by increasing the activity of soil enzymes (acid phosphatase) [134]. However, the combination of organic amendments and microbes indicates that soil enzyme activity is enhanced by affecting soil nutrient dynamics [135]. Microbes can also promote plant growth by secreting plant hormones such as auxin (IAA), cytokinin, and gibberellin or through nitrogen fixation in HM-contaminated soil. Due to the nitrogen fixation effect of rhizobia, the nitrogen content in the soil increased, the secretion of hormones and metabolites increased, and the availability of phosphorus in the soil and the content of phosphorus in the tissue increased, which improved plant biomass and the phytostabilization of HMs [136,137].

5.2.2. Enhanced Resistance to HMs

In the remediation of HM-contaminated soil, the resistance to HMs comes from the defense mechanisms of symbiotic microbes themselves. Microbes can produce chelating agents, iron carriers, organic acids, and proteins that form complexes with HMs, changing their bioavailability and reducing their phytotoxicity, thereby enhancing the resistance of plants to HMs [22,138]. Research has found that mycorrhizal fungi can secrete a glycoprotein called Glomalin, which reduces the toxicity of HMs to plants by forming glycoprotein–metal complexes [139]. The carboxyl, hydroxyl, amide, and glucuronic acid of extracellular polysaccharides produced by the Rhizobium radiobacter strain VBCK1062 can chelate a large amount of arsenates, increasing plant resistance to As [119]. In the presence of Cd, rhizobia are able to increase the synthesis of glutathione, which determines their tolerance level to Cd [117]. Vaccination with AMF significantly increases the content of total soil protein associated with glomalin and soil aggregates, reduces HM concentrations in interflow and dissolved HM leaching, and thus reduces the toxicity of HMs to plants [140]. AMF can also fix HMs on mycorrhizae through the adsorption of hyphae, inhibit the movement of HMs, prevent excessive entry of HMs into plants, and reduce the toxic effect of HMs on plants [141], which has a positive impact on heavy metal phytostabilization with inoculated plants.
The combination of plants–microbes can repair the damage caused by ROS and ABA induced by HMs. The regulation and expression of related genes produce a series of organic acids, amino acids, and other antioxidant metabolites, which alleviate membrane lipid peroxidation damage and DNA damage caused by HMs, diminish the accumulation of ROS in plants, enhance the photosynthetic capacity, and thus greatly strengthen the resistance of plants [126]. The content of chlorophyll and carotene in inoculated plants increased, while the activity of NADPH oxidase and the production of H2O2 decreased. Additionally, the contents of malondialdehyde (MDA) and proline changed significantly [142,143]. The transcripts of RNA, cell wall, and amino acid metabolism are up-regulated, which increases the synthesis of PCs and proteins [144]. The genes coding for cytokinins are up-regulated, which increases aboveground biomass, while the genes involved in light harvesting are down-regulated, which helps avoid light damage [145]. The cDNA encoding for metallothionein (MTL4) and phytochelatin synthase (AtPCS) are transferred into subspecies of rhizobia to form nodules, with Cd accumulation in roots and nodules being increased, implying that exogenous gene expression can improve the effect of plant metallothionein [146]. As for the microbes in the symbiotic system, they can segregate excess metals in some spores, which increases the tolerance of plants to HMs [141].

5.2.3. Increase in HM Accumulation

Microbes can improve the availability of HMs to reduce their content in the soil by secreting low-molecular weight organic acids, which leads to an increase in the accumulation of HMs in shoots [147]. After inoculating SaSR13 on the Sedum alfredii, the release of root exudates is promoted, especially malic acid and oxalic acid, which promote the absorption of Cd by plants [148]. The inoculation of Pseudomonas sp. Lk9 improved the mineral nutrient supply of soil iron and phosphorus, affected the secretion of host-mediated low-molecular weight organic acids, and increased the effectiveness of soil HMs, resulting in an increase in Cd, Zn, and Cu accumulation in the shoot of black spike grassland by 46.6%, 16.4%, and 16.0%, respectively [149]. Furthermore, Sphingomonas sp. ZYG-4 inoculation enhanced Pb accumulation in the shoots and roots by 268.9% and 1187.3% for A. adenophora and by 163.1% and 343.8% for D. ambrosioides, respectively, compared with the treatment without bacterial inoculation [20].
Microbe–Plant symbiosis can up-regulate the expression of transporter genes, thereby increasing plant uptake and the accumulation of HMs [120]. Research has shown that the expression of ATP-binding cassette transporter gene in the rhizosphere of Robinia pseudoacacia was up-regulated under Cu and Zn stress, which was probably related to the up-regulation of genes encoding CueO, Omp, YeDYZ, and three hypothetical proteins (CUSA protein, fish protein, and unknown protein) [123]. AMF regulates the plant uptake of Cd by stimulating the expression of Cd transporters. In its mycelium, AMF contains a polypeptide-encoding ATP that encodes 1513 amino acids by binding to the ABC transporter GintABC1, which is up-regulated by Cd and Cu [123].

6. Advantages, Limitations, and Prospects of Plants–Microbes Joint Remediation

Microbes can enhance the phytoremediation ability of plants by promoting the nutrient absorption and growth of plants under HM stress, enhancing plant resistance, increasing the content of HMs in roots of plants, and promoting the extraction or fixation of HMs in soil, thus strengthening phytoremediation. Moreover, plants–microbes combined remediation is performed in situ, is environmentally friendly, is free from secondary soil pollution, and has high remediation efficiency, which shows a broad application prospect in the treatment of HM-contaminated soil.
However, the plants–microbes joint remediation is still in its early stages, and the scheme of plants–microbes joint remediation that can be applied on a large scale in actual polluted soil has not yet been discovered. In practical applications, there are some problems, which are as follows: (1) the current inoculation strains are mainly single species or consist of 2–3 types and are cultivated in laboratories, which cannot adapt to the complex microbial communities in natural conditions; (2) in the current research, the sources of soil pollution are single and controllable. It is not yet clear whether the plants –microbes combination can adapt to the combined pollution of various HMs and even organic matter in the natural soil environment; (3) the joint remediation of plants–microbes is greatly affected by environmental conditions (nutrients levels, soil types, climate). The application effects of strains that are obtained through laboratory methods in these complex environments are not ideal. Therefore, future research should focus on the following: (1) continuing to screen and cultivate microbes with strong resistance to HMs and the ability to absorb multiple HMs and studying their adsorption characteristics and detoxification mechanisms; (2) exploring the comprehensive application mechanisms of amendments and plants–microbes joint remediation; (3) using genetic engineering to cultivate organisms with high biomass, rapid growth, and strong adaptability. Combining theory with practice to improve the efficiency of plants–microbes joint remediation.

7. Conclusions

In recent years, the application of plants–microbes combined technologies in the remediation of soil HM pollution has become a research hotspot and has made some progress. The response of plants and microbes to HMs is crucial for plants–microbes joint remediation. The common forms of plants–microbes joint remediation include plant–rhizobia, plant–AMF, plant–endophytic bacteria, and modifiers to assist in plants–microbes joint remediation. Microbes mainly enhance the ability of plants to remediate HMs by promoting the nutrient absorption and growth, enhancing plant resistance and promoting the extraction or fixation of HMs in soil. This provides a theoretical basis for soil remediation in mining areas, and it is hoped that the application of this system will be greatly accelerated.

Author Contributions

H.L., T.W., S.W. and P.G. prepared the manuscript. H.D., S.W. and M.M. revised the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by the National Natural Science Foundation of China (grant number 42177198) and Fundamental Research Funds for the Central Universities (grant number SWU019019).

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Exposure routes of heavy metals in mining areas. The arrows represent the migration pathways of HMs.
Figure 1. Exposure routes of heavy metals in mining areas. The arrows represent the migration pathways of HMs.
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Figure 2. Structural diagram of plant root resistance to heavy metal stress. HMs: heavy metals; HMA2/4: heavy metal ATPases 2 and 4; HMA3: heavy metal ATPases 3; NRAMP1/5: natural resistance-associated macrophage protein 1 and 5; IRT1: iron-regulated transporter 1; YSL: yellow stripe protein; ABCC1/2: ATP-binding cassette subfamily C member 1 and 2.
Figure 2. Structural diagram of plant root resistance to heavy metal stress. HMs: heavy metals; HMA2/4: heavy metal ATPases 2 and 4; HMA3: heavy metal ATPases 3; NRAMP1/5: natural resistance-associated macrophage protein 1 and 5; IRT1: iron-regulated transporter 1; YSL: yellow stripe protein; ABCC1/2: ATP-binding cassette subfamily C member 1 and 2.
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Figure 3. Physiological response mechanisms of plants to heavy metal stress. Abscisic acid (ABA); reactive oxygen species (ROS); superoxide dismutase (SOD); catalase (CAT); glutathione peroxidase (GPX); ascorbate peroxidase (APX); dehydroascorbic acid (DHA); dehydroascorbic acid reductase (DHAR); monodehydroascorbic acid (MDHA); reduced ascorbic acid (ASA); reduced glutathione (GSH); oxidized glutathione (GSSH); reduced coenzyme II (NADPH); coenzyme II (NADP+); phytochelatins (PCs); metallothioneins (MTs).
Figure 3. Physiological response mechanisms of plants to heavy metal stress. Abscisic acid (ABA); reactive oxygen species (ROS); superoxide dismutase (SOD); catalase (CAT); glutathione peroxidase (GPX); ascorbate peroxidase (APX); dehydroascorbic acid (DHA); dehydroascorbic acid reductase (DHAR); monodehydroascorbic acid (MDHA); reduced ascorbic acid (ASA); reduced glutathione (GSH); oxidized glutathione (GSSH); reduced coenzyme II (NADPH); coenzyme II (NADP+); phytochelatins (PCs); metallothioneins (MTs).
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Figure 4. The mechanism of microbial-assisted plant remediation. The dashed arrows represent indirect action, while the solid arrows represent direct action. ABC: ATP-binding cassette transporter; HMA: heavy metal ATPases; PCs: phytochelatins; MT: metallothionein.
Figure 4. The mechanism of microbial-assisted plant remediation. The dashed arrows represent indirect action, while the solid arrows represent direct action. ABC: ATP-binding cassette transporter; HMA: heavy metal ATPases; PCs: phytochelatins; MT: metallothionein.
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Table 1. HM pollution in soil of some mining areas around the world.
Table 1. HM pollution in soil of some mining areas around the world.
Mining AreaCountryMain OresHMsMean Concentration mg/kgReferences
Tonglushan mine, Daye, HubeiChinaCuCd1.46[31]
As43.25
Pb102.35
Cr90.51
Cu355.72
Ni32.31
Zn260.87
Lead (Pb)–zinc (Zn) mine, GuangdongChinaPb, ZnCr30.91[32]
Ni20.25
Cd7.14
Cu57.8
Pb1093.03
Zn867.08
Mn358.77
Fe34,281.45
Xikuangshan antimony (Sb) mine, HunanChina SbSb356.58[33]
Cu45.69
Zn486.42
As53.13
Cd9.98
Pb77.32
Les Malines mining district, Montpellier FrancePb, ZnZn39,364[34]
Pb34,289
Cd225
As338
Ti3.5
Cartagena mining district, La UnionSpainAg, Pb, Zn, Cu, FeCd49[35]
Cu274
Fe94,659
Mn8107
Pb4194
Zn23,361
Co Dinh mine, Thanh HoaVietnam Cr4353[36]
Co341
Ni4440
Cu20.3
Zn106.6
Pb17.6
Touro mine, Galicia SpainCuCr118[37]
Cu911
Ni15.3
Pb19.3
Zn78.2
Jebel Ressas mining site, TunisTunisiaPb and ZnCu14.25[38]
Mn306
Zn42,400
Pb14,500
Cd184
Limni mine, CyprusCyprusCuZn4132[39]
Cu1534
Ni121.7
Cd6.4
Pb28.6
Rongxi Mn mine, Xiushan chongqingChinaMnMn48,383[40]
Cd3.9
Cu80
Pb80.7
Zn131.2
Ait Ammar iron mine, KhouribgaMoroccoFeCd2.12[41]
Cr134.6
Cu35
Zn90.8
Pb9.1
Fe156,461.5
Tungsten molybdenum ore mine, Zakamensk, Baikal regionThe Buryat RepublicTungsten (W)Al70,500[42]
Mn2300
Fe55,000
As4.9
Cr47.8
Cu81
Ni31.7
Pb31.7
Zn133.5
Tongguan gold mine, ShaanxiChinaGold (Au)Hg2.91[43]
Cd2.45
Pb252
Cu46.4
Zn286
As16
Gumuskoy mining area, KutahyaTurkeyAgAs4771[44]
Ag37.78
Pb4320
The gold mining regions situated in the Ife–Ijesha axis, Osun StateNigeriaGold (Au)Fe196.78[45]
Cd0.36
Cu3.78
Cr65.74
Pb6.12
Ni19.56
Zn10.78
Tamesguida abandoned copper mine area, MédéaAlgeriaCuCu599.59[46]
Zn390.02
Cr93.05
As127.07
Pb70.04
Ni58.01
Fe74.3
The maximum permissible limits for HMs in agricultural soils by the WHO and FAO: Fe 150 mg/kg, Mn 437 mg/kg, Cu 6 mg/kg, Zn 50 mg/kg, Cr 65 mg/kg, Pb 10 mg/kg, Ni 75 mg/kg, Cd 0.07 mg/kg, Co 10 mg/kg, and As 0.5 mg/kg.
Table 2. Mechanisms of microbial response to heavy metal stress.
Table 2. Mechanisms of microbial response to heavy metal stress.
MicroorganismsHMsConcentrationResistance MechanismTransporters or Resistance GenesReferences
AgrobacteriumCd16.8 mg/LReactive oxygen species (ROS)Metallothioneins[115]
Rhizobia
R. phaseoli strain B3		Al0–5.4 mg/LRepair and stabilize the membraneABC-transporters and novel proteins, extracellular exopolysaccharide[116]
RhizobiaCd0–33.6 mg/LExtracellular immobilization, periplasmic allocation, cytoplasmic sequestration, and biotransformation of toxic productsGSH[117]
RhizobiaZn54–340 mg/kgPlasmid transfer [118]
RhizobiaAs375–1500 mg/LChanges extracellular polysaccharide compositionCarbohydrates, proteins, and uronic acids were significantly enhanced[119]
Arbuscular mycorrhizal fungiCd1.12 mg/LChanges the expression of Cd transporters and soil bacterial communityExpression of genes Nramp5 and HMA3 in root was up-regulated[120]
Arbuscular mycorrhizal fungiCd81 mg/kg Expression of PtMT2b was up-regulated[121]
Zn300 mg/kg
Arbuscular mycorrhizal fungiCd0–20 mg/kgEnhance P nutrition, promote growthUp-regulated expression of AMF-inducible GmPTs and GmHMA19[122]
Arbuscular mycorrhizal fungiCd50.5 mg/LChanges the redox Up- regulated expression of an ATP-binding cassette (ABC) transporter (GintABC1)[123]
Cu32 mg/L
Arbuscular mycorrhizal fungiCd Decreased the transfer factorImprove the HMA3 gene expression in rice root[124]
Arbuscular mycorrhizal fungiCd2 mg/kgA metabolic shiftThe glycolysis-mediated mobilization of defense mechanisms[125]
Bacillus cereusPb
Zn
Ni
Cu
Cd		150 mg/L
400 mg/L
50 mg/L
200 mg/L
10 mg/L		Plant-beneficial metabolites, modulating the antioxidants [126]
Bacillus sp. MN3-4Pb50–1500 mg/LExtracellular sequestration and intracellular accumulation [127]
Azospirillum brasilenseAs1.88 mg/LIndole
Acetic acid		 [110]
Azospirillum brasilenseAs1.88–37.5 mg/LAs resistance genes mediate the redox As transformation and extrusion outside the cellars operon[128]
Pseudomonas and EnterobacterCu, Ni, Zn and Cd5–500 mg/LRegulating the production of indole-3-acetic acid, phosphate solubilization, iron carrier, and hydrogen cyanide [129]
Pseudomonas fluorescensCd2.8 mg/LPromote photosynthesis, carbon fixationPhotosynthetic genes and C4-pathway carbon fixation-related genes were significantly up-regulated[130]
Paenibacillus sp.
Bacillus sp.		Cd
Ni		18.98 mg/kg
108.12 mg/kg		Surface functional groups (-OH, -NH2, -COO, etc.) reduce the bioavailability of heavy metals [131]
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Li, H.; Wang, T.; Du, H.; Guo, P.; Wang, S.; Ma, M. Research Progress in the Joint Remediation of Plants–Microbes–Soil for Heavy Metal-Contaminated Soil in Mining Areas: A Review. Sustainability 2024, 16, 8464. https://doi.org/10.3390/su16198464

AMA Style

Li H, Wang T, Du H, Guo P, Wang S, Ma M. Research Progress in the Joint Remediation of Plants–Microbes–Soil for Heavy Metal-Contaminated Soil in Mining Areas: A Review. Sustainability. 2024; 16(19):8464. https://doi.org/10.3390/su16198464

Chicago/Turabian Style

Li, Hong, Tao Wang, Hongxia Du, Pan Guo, Shufeng Wang, and Ming Ma. 2024. "Research Progress in the Joint Remediation of Plants–Microbes–Soil for Heavy Metal-Contaminated Soil in Mining Areas: A Review" Sustainability 16, no. 19: 8464. https://doi.org/10.3390/su16198464

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