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Communication

Heavy Metal Remediation Using Phosphate-Solubilizing Fungi: From Bioprocess to Application

by
Da Tian
1,2,†,
Shuo Zhang
1,2,†,
Dechao Wang
1,2,
Liangliang Zhang
1,2,
Haoming Chen
3 and
Xinxin Ye
1,2,*
1
Anhui Province Key Lab of Farmland Ecological Conservation and Nutrient Utilization, Anhui Province Engineering and Technology Research Center of Intelligent Manufacture and Efficient Utilization of Green Phosphorus Fertilizer, College of Resources and Environment, Anhui Agricultural University, Hefei 230036, China
2
Key Laboratory of JiangHuai Arable Land Resources Protection and Eco-Restoration, Ministry of Natural Resources, Anhui Agricultural University, Hefei 230036, China
3
School of Environmental and Biological Engineering, Nanjing University of Science and Technology, Nanjing 210094, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2024, 14(11), 2638; https://doi.org/10.3390/agronomy14112638
Submission received: 7 October 2024 / Revised: 27 October 2024 / Accepted: 7 November 2024 / Published: 8 November 2024
(This article belongs to the Special Issue Environmental Ecological Remediation and Farming Sustainability—3rd Edition)
Browse Figure
Versions Notes

Abstract

:
Heavy metal pollution has been a major environmental issue in recent years, seriously threatening land, water sources, agriculture, and human health. The remediation of heavy metal pollution has been a continuously vital issue for current research. Bioremediation is an effective and cost-efficient approach to reduce heavy metal toxicity. Phosphate-solubilizing fungi (PSF) have shown promise in heavy metal bioremediation due to their high tolerance and activity levels. However, the full potential of PSF in bioremediation needs further exploration. PSF activity, metabolite production, and environmental conditions can influence their efficiency in remediating heavy metals. These factors play a critical role in the practical application of PSF and necessitate improvement pathways. This article reviews potential strategies to enhance heavy metal remediation using PSF and optimizing bioprocesses and applications.

1. Introduction

Heavy metal pollution is a pervasive global environmental issue, significantly impacting human health and ecosystems [1]. This contamination poses severe risks to land, water sources, agriculture, and human well-being. In response to this pressing concern, bioremediation technology has emerged as a frontline approach for addressing environmental heavy metal remediation [1]. This technique utilizes animals, plants, or microorganisms to break down or neutralize pollutants, offering a sustainable solution to the problem. Compared to traditional physical/chemical technologies, bioremediation improves efficiency, cost-effectiveness, and environmental protection, particularly at low metal concentrations [2,3]. Among the various bioremediation methods, phosphate-solubilizing fungi (PSF) microorganisms have garnered significant attention and extensively utilized in heavy metal bioremediation. This is attributed to their remarkable environmental activity and metabolism, such as their ability to secrete organic acids [4]. These metabolites are crucial in transforming heavy metal cations from active to inactive forms, mitigating heavy metal toxicity and facilitating the removal process from contaminated areas [4,5]. Moreover, PSF possess a unique capacity to resist heavy metal toxicity through rapid mutation and evolution, allowing them to adapt to harsh environmental pressures [6,7]. However, environmental factors would affect the production of metabolism, influencing the resistance process and heavy metal remediation capacity using PSF (Figure 1). Therefore, understanding the relationship between metabolic pathways and remediation abilities is essential for PSF application in heavy metal bioremediation. In addition, clarifying the mechanisms, bioprocess, and influencing factors is also needed to improve the efficiency and range in heavy metal bioremediation using PSF.

2. Heavy Metal Remediation Using PSF

2.1. Heavy Metal Toxicity-Resistant Capacity of Phosphate-Solubilizing Fungi

Phosphate-solubilizing fungi (PSF) demonstrate remarkable resilience against high concentrations of heavy metals, thriving in environments contaminated with single or multiple metals. These fungi possess unique mechanisms that allow them to withstand and detoxify heavy metals, making them valuable candidates for bioremediation (Figure 1). For example, Aspergillus niger (A. niger) can tolerate 3477 mg/L of lead (Pb) concentration in an aqueous solution [4]. Furthermore, A. niger can survive in contaminated soils with an arsenic (As) concentration of 95.64 mg/kg and a Pb concentration of 301.83 mg/kg [4]. This robust tolerance highlights the potential of A. niger for bioremediation efforts in areas contaminated with Pb and As. In addition, fungi of Trichoderma asperellum RM-28 showed simultaneous resistance to multiple heavy metals at concentrations as high as 400 mg/L, including aluminum (Al), arsenic (As), cadmium (Cd), copper (Cu), manganese (Mn), and nickel (Ni) [10]. This versatility makes Trichoderma asperellum RM-28 a highly promising candidate for bioremediation in environments contaminated with complex mixtures of heavy metals. Meanwhile, the different species of fungi exhibit varying resistance levels to the same heavy metals. For example, Colletotrichum sp. ALE15 and ALE18 have different maximum tolerance concentrations to cadmium, i.e., 1000 mg/L and 750 mg/L, respectively [11]. In addition, the heavy metal resistance displayed by PSF is not limited to just a few species. Different PSF exhibit varying levels of resistance to the same heavy metal, reflecting the diversity and adaptability of these fungi. For instance, PSF Penicillium oxalicum and Aspergillus AHBB-CT196 show a high Pb and As tolerance in soil bioremediation, respectively [12,13]. This species-specific resistance can be attributed to differences in their metabolic pathways and biochemical mechanisms.

2.2. Mechanism of Heavy Metal Tolerance in PSF

PSF can utilize various strategies to resist heavy metal toxicity, including extracellular remediation and intracellular accumulation (Figure 1). The extracellular pathway for PSF in heavy metal toxicity resistance primarily includes the production of extracellular polymeric substances (EPS), organic acid, etc. [14,15]. These products can combine with heavy metal cations to form insoluble Pb minerals (e.g., lead oxalate and EPS-Pb) and reduce toxicity in the extracellular space [16]. Meanwhile, PSF can also resist heavy metal toxicity via the defense system of the cell wall [17]. The cell wall’s cationic and anionic functional groups can prevent heavy metal cations from entering the cells [17]. Especially under high heavy metal concentrations (e.g., 1000 mg/L Pb), PSF can also form a new cell wall to prevent the entry of heavy metal cations [16]. The intracellular pathway in heavy metal toxicity is resistant to PSF primarily through the metalloproteins that accumulate in the vacuoles [16,18,19]. For example, PSF can maintain activity at elevated Pb levels through intracellular accumulation [16]. However, the excessive heavy metal concentration would also cause the death of PSF.

2.3. Mechanism of Heavy Metal Remediation by PSF

The heavy metal-resistant pathway of PSF can also contribute to the remediation of heavy metal cations. Secondary metabolites such as organic acid (e.g., oxalic acid) and EPS by PSF dominate the remediation of heavy metals [14]. For example, oxalic acid can react with heavy metal cations to form insoluble minerals around cell walls and external medium during bioremediation [16]. Especially for Pb remediation, PSF can secrete large amounts of oxalic acid and significantly reduce the Pb cations by forming lead oxalate minerals [20,21]. In addition, the extracellular polymeric substances (EPS) produced by PSF can also contribute to heavy metal remediation [22]. The EPS contains various organic components with a highly branched chemical structure and functional groups, such as hydroxyl and carboxyl groups [23,24]. For example, the EPS can remove about 1000 mg/L Pb cations via the formation of EPS-Pb [25]. Generally, PSF can remove heavy metals by extracellular precipitation and active uptake [26,27].

3. Factors That Influence Heavy Metal Remediation When Using PSF

3.1. pH

pH is one of the most critical factors in heavy metal remediation when using PSF. At a low pH value, specifically when the pH value is below 3, PSF can reduce the Pb concentration from the medium to 0.52 mg/L [4]. The acidic environment enhances the solubility of heavy metals, facilitating their interaction with PSF. Notably, the immobilizing process of binding heavy metals and reducing heavy metal mobility by PSF can also decrease the surrounding pH value [28]. In addition, the higher pH can increase the adsorption capacity of heavy metals by PSF, e.g., the adsorbed Pb using PSF increased from ~2.5 to 20.7 mg/g Pb when the pH increased from 2 to 5 [29]. This pH-dependent adsorption behavior underscores the importance of fine-tuning the pH conditions to optimize heavy metal remediation by PSF.

3.2. Nutrient Supply

Nutrients such as carbon and nitrogen sources can significantly affect the remediation of heavy metals by PSF. The availability of different carbon sources, such as dextrose and glucose, can elicit varied Pb removal efficiencies. The supply of 20 mg/L dextrose and 2% glucose would cause different Pb removal ratios (99.20% and 99.30% vs. 98.90% and 96%) for Aspergillus fumigatus and Aspergillus flavus [30]. These variations indicate that the type and concentration of carbon sources can significantly impact the metabolic activities of PSF and, consequently, their ability to sequester heavy metals.
Nitrogen is another essential nutrient that plays a crucial role in heavy metal remediation by influencing the metabolic pathways of PSF such as Aspergillus niger and aiding in the dissolution of phosphate rock [14]. Compared with ammonium and urea, nitrate significantly enhances the secretion of oxalate by A. niger, which in turn reduces the Pb concentration during Pb remediation with calcium phosphate (Ca-P) [31]. Additionally, the provision of phosphorus in the form of calcium phosphate can stimulate A. niger to secrete more organic acids, hence contributing to the effective Pb remediation by the combination of PSF and phosphate [32].

3.3. Metal Cations

The presence of other metal cations can significantly interfere with the bioremediation capacity of PSF [30]. Some metal cations, such as potassium, sodium, and magnesium, interfere with the adsorption of heavy metals by competing for binding sites on the cell wall of PSF [33]. This competition reduces the efficiency of PSF in absorbing and immobilizing target heavy metals. Furthermore, cations with the same valence as the target heavy metal exhibit a stronger competitive effect compared to cations with different valences [34]. For example, in a system where Pb2+ and Cd2+ coexist, they compete for oxalic acid species (C2O42−) secreted by PSF to solubilize heavy metals, thereby decreasing the overall remediation efficiency [34]. This competition highlights the need to consider the complex interplay of different metal ions in designing effective heavy metal remediation strategies utilizing PSF.

4. Improvement of PSF in Heavy Metal Remediation

4.1. PSF Combined with Materials

Although PSF exhibits remarkable potential in the bioremediation of heavy metals, the integration of specific materials such as hydroxyapatite and bioapatite further amplifies its effectiveness [35,36,37]. This combination utilizes the unique properties of both PSF and the materials to create a more efficient system for metal immobilization. For example, PSF-A. niger combined with fluorapatite can immobilize Pb to form highly insoluble pyromorphite [4]. Meanwhile, Aspergillus ustus combined with silica nano-powders can be used as a biosorbent to immobilize Cd (II) in aqueous solutions [38]. Mucor plumbeus combined with alum composites can be used as a bioabsorption material to remove Pb (II) cations from contaminated solutions under different conditions [39]. In addition, fungal Fe3O4 nanocomposites can be synthesized and characterized for their remediation potential [40].
These nanocomposites combine the magnetic properties of Fe3O4 with the bioremediation capabilities of PSF, creating a versatile tool for the treatment of heavy metal-contaminated soils and waters.

4.2. Collaboration Between PSF and Other Organisms

PSF can enhance soil remediation of heavy metals by interacting with plants and other microorganisms. For example, A. niger and fenugreek plants can significantly reduce 61% Pb concentration in soil and increase 36% potassium concentration in grain [41]. This symbiotic relationship not only mitigates Pb contamination but also promotes plant growth and nutrient acquisition. PSF can also decrease the lead extractability from soil and plant lead content when inoculated with Acaulospora sp., Funneliformis mosseae, or Gigaspora gigantea [42]. Furthermore, PSF can decrease the soil bioavailability of Ni, Mn, and Cr by 40–100% under the influence of bacteria and fungi [43]. This reduction in bioavailability minimizes the risk of metal accumulation in plants and animals, thereby protecting ecosystems from the deleterious effects of heavy metal contamination.

4.3. The Application of PSF as a Phosphate-Based Biofertilizer

PSF in combination with phosphate complexes has been utilized to develop phosphate-based biofertilizers that not only enrich soil phosphorus levels but also enhance Pb remediation [44]. The application of PSF biofertilizers significantly increases crop yields and soil available P content, allowing for a reduction in phosphate fertilizer usage by up to 50% [45]. This not only reduces agricultural costs but also promotes environmentally sustainable farming practices. In addition, the application of PSF biofertilizer and phosphate can also reduce the Pb concentrations in soil. For example, the combination of phosphogypsum (PG) and biofertilizer containing A. niger can reduce soil Pb concentration from 365 mg/kg to 302 mg/kg [46]. PG not only provides a sufficient P source for the growth of A. niger in highly contaminated soils but also strengthens the formation of insoluble Pb minerals. Thus, the incorporation of phosphate and PSF as fertilizers represents a practical and sustainable approach to long-term Pb remediation, balancing agricultural productivity with environmental stewardship.

5. Conclusions

Phosphate-solubilizing fungi (PSF) have great potential in heavy metal bioremediation due to their high toxicity tolerance and ability to survive in contaminated environments, making them invaluable candidates for heavy metal bioremediation. Their ability to secrete metabolites such as organic acids and extracellular polymeric substances (EPS) is crucial in transforming active heavy metal cations into inactive forms. Furthermore, PSF’s rapid mutation and evolution allow them to adapt to harsh environmental pressures, enhancing their practical application in bioremediation. However, the efficiency of PSF in heavy metal remediation is influenced by various environmental factors, including pH, nutrient supply, etc. Additionally, the presence of other metal cations can interfere with the adsorption of heavy metals by competing for binding sites on the cell wall of PSF. Therefore, the improvement pathway for PSF from bioprocess to application in heavy metal remediation is necessary.
Improving pathways for PSF in heavy metal bioremediation applications should be employed in the future. The potential directions include fungal strain screening, materials construction, biological collaboration, and biofertilization. Firstly, screening effective PSF strains or modifying functional genes to obtain higher heavy metal tolerance and metabolic activity in the secretion of organic acids and EPS, thereby improving the conversion efficiency of heavy metals. Secondly, investigate the optimal combinations and ratios of materials (phosphate, biochar, etc.) to maximize heavy metal immobilization by PSF and reduce the influence of environmental factors. Thirdly, establish the collaboration between PSF and other organisms, such as plants and other microorganisms, to synergistically enhance soil remediation. Furthermore, applying PSF as a phosphate-based biofertilizer improves heavy metal remediation, making it a practical attempt at long-term soil restoration, especially in phosphorus-deficient areas. In summary, PSF offers a sustainable and cost-effective solution to the pervasive problem of heavy metal pollution. By understanding their bioprocess and the factors that influence their remediation abilities, we can develop more efficient and practical applications of PSF in heavy metal bioremediation. Future research should focus on optimizing these factors to maximize the effectiveness of PSF in mitigating heavy metal contamination and protecting human health and ecosystems.

Author Contributions

D.T. and S.Z. wrote the manuscript. D.W. and L.Z. assisted in the data collection. H.C. and X.Y. conceived the idea, revised the manuscript, and led the project. All authors contributed to the article and approved the submitted version. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Natural Science Foundation of Anhui Educational Committee (No. 2024AH040076), the Program at the Department of Natural Resources of Anhui Province (No. 2021-K-4 and 2021-K-11).

Data Availability Statement

The original contributions presented in the study are included in the article, further inquiries can be directed to the corresponding author.

Conflicts of Interest

The authors declare no conflicts of interest.

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Agronomy 14 02638 g001
Figure 1. Heavy metal bioremediation using phosphate-solubilizing fungi [8,9].
Figure 1. Heavy metal bioremediation using phosphate-solubilizing fungi [8,9].
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Tian, D.; Zhang, S.; Wang, D.; Zhang, L.; Chen, H.; Ye, X. Heavy Metal Remediation Using Phosphate-Solubilizing Fungi: From Bioprocess to Application. Agronomy 2024, 14, 2638. https://doi.org/10.3390/agronomy14112638

AMA Style

Tian D, Zhang S, Wang D, Zhang L, Chen H, Ye X. Heavy Metal Remediation Using Phosphate-Solubilizing Fungi: From Bioprocess to Application. Agronomy. 2024; 14(11):2638. https://doi.org/10.3390/agronomy14112638

Chicago/Turabian Style

Tian, Da, Shuo Zhang, Dechao Wang, Liangliang Zhang, Haoming Chen, and Xinxin Ye. 2024. "Heavy Metal Remediation Using Phosphate-Solubilizing Fungi: From Bioprocess to Application" Agronomy 14, no. 11: 2638. https://doi.org/10.3390/agronomy14112638

APA Style

Tian, D., Zhang, S., Wang, D., Zhang, L., Chen, H., & Ye, X. (2024). Heavy Metal Remediation Using Phosphate-Solubilizing Fungi: From Bioprocess to Application. Agronomy, 14(11), 2638. https://doi.org/10.3390/agronomy14112638

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