Abstract
Soil contamination by uranium presents a burgeoning global environmental concern, exerting detrimental effects on both agricultural production and soil health. Biochar, a carbonaceous material derived from biomass pyrolysis, exhibits considerable potential for remediating uranium-contaminated soils. However, a comprehensive review of the effects of biochar on the fate and accumulation of uranium in soil–plant systems remains conspicuously absent. In this paper, uranium sources and contamination are reviewed, and the impact of biochar on uranium immobilization and detoxification in soil–plant systems is analyzed. We reviewed the status of uranium contamination in soils globally and found that mining activities are currently the main sources. Further meta-analysis revealed that biochar addition significantly reduced the soil uranium bioavailability and shoot uranium accumulation, and their effect value is 58.9% (40.8–76.8%) and 39.7% (15.7–63.8%), respectively. Additionally, biochar enhances the soil microenvironment, providing favourable conditions for promoting plant growth and reducing uranium mobility. We focused on the mechanisms governing the interaction between biochar and uranium, emphasising the considerable roles played by surface complexation, reduction, ion exchange, and physical adsorption. The modification of biochar by intensifying these mechanisms can promote uranium immobilisation in soils. Finally, biochar alleviates oxidative stress and reduces uranium accumulation in plant tissues, thereby mitigating the adverse effects of uranium on plant growth and development. Overall, our review highlights the capacity of biochar to remediate uranium contamination in soil–plant systems through diverse mechanisms, providing valuable insights for sustainable environmental remediation.
Highlights
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Biochar reduces uranium mobility through a variety of mechanisms, including surface complexation, reduction, ion exchange, and physical adsorption.
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Biochar significantly reduces uranium bioavailability in soil and limits its accumulation in plants.
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Modified biochar has been shown to enhance its effectiveness in immobilising uranium.
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Biochar application to soil not only promotes uranium remediation but also improves soil quality.
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1 Introduction
Uranium, an element with an atomic number of 92 and an atomic weight of 238.03, was first discovered in 1789 by German chemist Martin Heinrich Klaproth as a component of pitchblende (Monreal and Diaconescu 2010; Yang 2023). This naturally occurring radioactive element is crucial for electricity generation in nuclear reactors. It is primarily found in trace amounts in the Earth's crust, at approximately 2.5 parts per million (Malaviya and Singh 2012; Akash et al. 2022). However, anthropogenic activities such as mining, nuclear power generation, nuclear accidents (e.g., Chernobyl and Fukushima), and phosphate fertiliser application have markedly elevated uranium levels in soil, resulting in radiological and chemical toxicity risks (Rani et al. 2023). The widespread accumulation of uranium, extending beyond localized regions, can be attributed to a multitude of factors. These include geochemical processes, anthropogenic activities, and natural weathering, all of which significantly impact soil–plant systems over considerable distances (Pérez-Sánchez and Thorne 2014). Given its chemical and radiological toxicity, uranium poses significant risks to plant growth, agricultural productivity, and food safety (Srivastava et al. 2020). Furthermore, uranium accumulation by plants leads to its transfer along the food chain, ultimately affecting human health, with potential implications for cancer development at levels exceeding 0.05 mg kg−1 body mass d−1 (Gao et al. 2019). Thus, there is an urgent need to develop effective and sustainable strategies to mitigate the adverse effects of uranium contamination.
Biochar, a carbonaceous material derived from biomass pyrolysis, has garnered considerable attention for its potential role in techniques aimed at remediating uranium-contaminated soil (Fahad et al. 2023; Li et al. 2024). The unique properties of biochar, including its high surface area, high porosity, and ability to retain water and nutrients, strongly mitigate uranium contamination in soil (Azeem et al. 2022). For instance, Liu et al. (2022c) demonstrated that the addition of biochar to uranium-containing tailings resulted in uranium adsorption onto the porous surface of the biochar through chemical reactions involving oxygen-rich organic groups. This led to a 40% reduction in uranium concentration in the pore water of the tailing soil. The immobilisation of uranium by biochar is a complex process that involves various mechanisms such as surface complexation, reduction, ion exchange, and physical adsorption (Qiu et al. 2021). The high porosity and extensive surface area of biochar, as explained by Guilhen et al. (2021), make it an efficient platform for the physical adsorption of uranium, significantly limiting its mobility in soil. Physical adsorption not only contributes to uranium immobilisation but also plays a pivotal role in preventing further dispersion (Ahmed et al. 2021d). As uranium associates with biochar, various mechanisms are activated, and surface complexation is particularly prominent (Liao et al. 2022b; Lingamdinne et al. 2022). This process involves a sequence of chemical reactions with the oxygen-rich organic groups present in biochar. Furthermore, ion exchange and physical adsorption ensure the immobilisation of uranium (Liao et al. 2023). Simultaneously, the interaction between biochar and microorganisms in soil promotes the microbial reduction of uranium(VI) to uranium(IV), the uranium shifts from a more soluble and mobile form to a less soluble and more stable form (Ouyang et al. 2023). This reduction leads to the precipitation or adsorption of uranium onto soil particles or biochar, reducing its mobility in the soil (Hilpmann et al. 2023). These multifaceted mechanisms significantly expand the interactions between uranium and biochar, providing a potent strategy for the remediation of uranium-contaminated soils. Furthermore, researchers have investigated the potential of enhancing the efficacy of biochar in uranium remediation through modification (Chen et al. 2023b; Guo et al. 2023). This modification aims to alter the inherent characteristics of biochar, including its microstructure and surface functional group composition, thereby enhancing its potential as an effective tool for uranium immobilisation.
Plants acquire uranium primarily through passive diffusion, facilitated transport, or active uptake mechanisms, which predominantly occur through the root system (Chen et al. 2021; Lai et al. 2021). Once absorbed, uranium can be transported to the aerial plant parts, potentially inducing toxicity and adverse effects on growth and development (Cui et al. 2023). Biochar plays a crucial role in preventing the migration of uranium in soil–plant systems, thereby detoxifying uranium and mitigating its toxicity to plants (Qi et al. 2021; Yin et al. 2022). Detoxification protects plants from uranium-induced damage and mitigates the potential transfer of uranium along the food chain. Recent evidence has demonstrated the effectiveness of biochar in preventing uranium migration and detoxifying soil–plant systems (Qi et al. 2021; Liu et al. 2022c). For instance, biochar application to uranium-contaminated land has led to a remarkable increase in plant production, highlighting the ability of biochar to alleviate uranium toxicity and enhance plant growth (Qi et al. 2022). The application of biochar provides the additional advantage of improving soil quality and fertility by improving its physical, chemical, and biological properties, thereby facilitating healthy plant growth (Khan et al. 2022; Mousavi et al. 2023). Biochar is produced from sustainable biomass sources, which enhances its environmental benefits. These combined strengths confirm that biochar is a promising and versatile solution for the remediation of uranium-contaminated soils.
A large number of studies have demonstrated that biochar can effectively immobilise uranium in soil, reduce plant uranium uptake, and alleviate its toxic effects on plants. Recent reviews have highlighted the role of biochar in uranium removal from aqueous medium, but they have overlook the effects of biochar on uranium immobilisation in soils (Fahad et al. 2023; Shen et al. 2023). Moreover, meta-analysis, a powerful analytical method in environmental studies, can provide a comprehensive analysis of the effects of biochar on uranium-contaminated soil and plant uranium accumulation (Chen et al. 2023a; Huang et al. 2023, 2024). Despite its potential, this specific area of research remains unexplored. This review, therefore, combines meta-analysis to provide significant insights into the impact of biochar on uranium immobilisation, uptake, and detoxification in soil–plant systems. In this paper, we analyze sources of uranium pollution and uranium contamination status globally. We illustrate effects of biochar application on uranium immobilisation in soil. We also review the inner mechanisms for uranium immobilisation by biochar including surface complexation, reduction, ion exchange, and physical adsorption. Lastly, we summarize the effects of biochar application on uranium accumulation and toxicity in plants. This comprehensive analysis highlights the crucial role of biochar in mitigating uranium contamination, and provides a promising pathway for sustainable environmental management and agricultural practices.
2 Global status of uranium contaminations
2.1 Occurrence, existing forms, and sources
Uranium, a vital element for electricity generation in nuclear reactors, has garnered increasing attention globally due to its pivotal role in nuclear power production (Cui et al. 2023). It is naturally and widely distributed in the Earth's crust, surpassing the abundance of silver, mercury, and cadmium (Peng and Cao 2021). The reserves of uranium in oceans alone exceed the quantity found in the Earth's crust by over a thousand times, amounting to approximately 4.5 billion tons (Endrizzi et al. 2016). Naturally occurring uranium comprises three isotopes: uranium-234, uranium-235, and uranium-238. Uranium-238 is the most abundant, accounting for approximately 99.3% of natural uranium, while uranium-235, although less abundant, has the ability to sustain a nuclear chain reaction (Adebiyi et al. 2021). All these isotopes have half-lives exceeding 105 years, posing long-term environmental and health risks (Sharma et al. 2022).
Uranium exists in diverse chemical and physical forms in the environment, and its occurrence and behaviour are influenced by various factors. These factors include the geological composition of the soil and rocks, pH, redox conditions, organic matter content, and interactions with other elements and minerals (Ganguly and Bhan 2023; Kumar et al. 2023). In terms of chemical form, uranium can exist in different oxidation states, with uranium(VI) and uranium(IV) being the most common forms (John et al. 2022). Uranium(VI) is typically present in oxidised environments and can form soluble complexes such as uranyl ions (UO22+) and various carbonate complexes. Uranium (IV), on the other hand, tends to be found in reduced environments and may be associated with minerals or solid phases (Ganguly and Bhan 2023). The oxidation state of uranium in the environment is not fixed but can change in response to shifts in environmental factors, leading to a dynamic equilibrium between the two forms. Such factors include the presence of certain bacteria, the composition of the surrounding material (soil, rock, etc.), and the availability of oxygen or other electron acceptors/donors (Ganguly and Bhan 2023). Physically, uranium can be present in soluble, sorbed, or precipitated forms in soil (Satpathy et al. 2023). Therefore, a BCR extraction method was developed to assess the bioavailability and mobility of uranium in the environment (Thorgersen et al. 2023). The BCR extraction method typically includes four fractions: exchangeable, reducible, oxidisable, and residual (HongE et al. 2022; Liu et al. 2023a). The exchangeable phase of uranium is commonly used to assess its bioavailability in soil–plant systems. The exchangeable fraction refers to the portion of uranium that is loosely bound and readily available for uptake by plants and other organisms (Zhang et al. 2014). In contrast, the residual fraction represents a relatively stable form of uranium that is tightly bound and is less accessible to plants or other organisms (Huang et al. 2022; Wang et al. 2023). The residual fraction is typically composed of insoluble compounds, such as metal oxides or minerals, where uranium ions are strongly bound and less mobile. The reducible fraction of uranium, associated with iron and manganese oxides, typically remains stable. However, it can become mobile if these oxides dissolve in reducing environments such as waterlogged or anaerobic areas (Gao et al. 2021). Similarly, the oxidizable fraction of uranium, bound to organic matter and sulfide minerals, is ordinarily immobile. Nevertheless, its availability may increase due to the decomposition of organic matter or the oxidation of sulfide minerals (Peña et al. 2020). The uranium forms in the soil near a uranium mine in southeastern China are primarily in the residual fraction, whereas the soils in Oak Ridge are dominated by carbonate-bound fractions, and the soils surrounding abandoned uranium mines in Brazil are primarily in the oxidised fraction (Zhou and Gu 2005; Ouyang et al. 2019; Galhardi et al. 2020). The complex interactions between uranium and the surrounding matrix result in the mutual transformation of different uranium fractions through various reactions, including adsorption, desorption, precipitation, redox reaction and complex formation (Florez-Vargas et al. 2023).
Uranium originates from both natural and anthropogenic sources (Fig. 1). Natural sources include the geological distribution of uranium in rocks, soils, and minerals as well as atmospheric deposition and volcanic eruptions (Chen et al. 2021). Anthropogenic sources, on the other hand, arise from human activities, including mining and milling operations, fertilizer use, nuclear fuel cycle activities, industrial processes, and accidents related to nuclear power plants (Ma et al. 2020). Notably, uranium mining and milling, which account for 41.14% of contamination, are significant contributors to uranium contamination and represent the primary sources (Ramadan et al. 2022). These activities involve the extraction and processing of uranium ore, resulting in the release of uranium and its associated contaminants into the soil, water, and air (Morereau et al. 2022). Groundwater accounts for 39.67% of contamination, primarily due to the leaching of uranium from soils and deposits, which poses a significant risk to the integrity of drinking water (Ma et al. 2020). Furthermore, uranium contamination is intensified by various other anthropogenic activities, including the use of phosphate fertilisers, nuclear facilities, and military operations, which can accelerate the release of uranium into the environment (Ma et al. 2020). Nuclear accidents, such as the Chernobyl and Fukushima nuclear accidents, can also result in local pollution and environmental issues (Schilz et al. 2022).
2.2 Degree of pollution and the phenomenon of compound pollution
Because the sources of uranium contamination can vary significantly, the concentration of uranium in soil also exhibits considerable variation in background levels (Table 1). For example, the average concentrations of uranium in soils in Chile and Germany are 0.79 mg kg−1 and 1.9 mg kg−1, respectively (Table 1) (Utermann and Fuchs 2008; Cabral Pinto et al. 2014). The soil around uranium mining areas typically has a high uranium content. In abandoned uranium mining areas in central Portugal, the uranium concentration in sampled soil ranged from 17.3 to 271 mg kg−1 (Antunes et al. 2011). Surface sediments from sampling sites downstream of uranium mining and milling areas in Guangdong province, China, exhibited a high uranium content ranging from 17.4 to 3935.0 mg kg−1 (Liu et al. 2015).
Moreover, the phenomenon of compound pollution should be taken into account. Uranium often coexists with other heavy metals. For example, Skipperud et al. (2013) reported that large quantities of tailings containing Cd, Pb, and As are generated from U mining. Furthermore, a global meta-analysis indicated that most of the soil near uranium mines is heavily polluted by uranium and Cd (Chen et al. 2022a). A global meta-analysis reported that the average contents of U, Cd, Cr, Pb, Cu, Zn, As, Mn, and Ni in soils from uranium mining areas were 39.88-, 55.33-, 0.88-, 3.81-, 3.12-, 3.07-, 9.26-, 1.83-, and 1.17-fold greater, respectively, than those in the upper continental crust (Chen et al. 2022a). The combined pollution of uranium with other metals in soils can induce synergistic or co-cumulative effects, increasing environmental and health risks.
3 Effects of biochar application on uranium immobilisation in soils
The presence of exchangeable uranium in soils is a considerable concern because it can be readily absorbed by plants, posing risks to human health (Nduka et al. 2022). The application of biochar to uranium-contaminated soils is a promising strategy. The sorptive capacity of biochar acts as a barrier that both physically and chemically interacts with uranium, thereby effectively inhibiting its migration in the soil (Lyu et al. 2021a; Li et al. 2024). This review collected the existing literature on the remediation of uranium-contaminated soil using biochar and conducted a meta-analysis. This comprehensive analysis encompasses the impact of biochar on exchangeable uranium in the soil and the subsequent uptake of uranium by plants (Fig. 2). We observed that biochar addition had a significant negative effect on the available soil uranium concentration, with a mean decrease of 58.9% (ranging from 40.8% to 76.8%) (Fig. 2a). Furthermore, biochar significantly inhibited shoot uranium accumulation, with a mean decrease of 39.7% (ranging from 15.7% to 63.8%) (Fig. 2b). These results provide solid evidence for the considerable impact of biochar on immobilising uranium in soil, thereby reducing its uptake by the aerial parts of plants. For instance, a recent study observed that the application of 10% biochar to uranium-contaminated soils notably decreased uranium leaching, from 26.37% to 3.18%, highlighting the potential of biochar in mitigating uranium migration and protecting the surrounding environment (Fu et al. 2022).
Additionally, our meta-analysis revealed that the modified biochar possesses an enhanced potential for uranium remediation. The modified biochar exhibited a greater capacity to reduce exchangeable uranium in soil (67.2%) compared to the original biochar (51.6%). This effect arises from the surface modification of the biochar, which enhances its adsorption capacity and interaction with uranium in the soil (Xia et al. 2022). The modification of biochar involves physical, chemical, and biological methods to improve its structure and properties (Liu et al. 2022d). Specifically, physical methods include thermal treatment and grinding to alter the surface area and porosity (Sun et al. 2022; Stasi et al. 2022). These processes significantly increase the surface area of the biochar, providing more sites for uranium adsorption and interaction. Similarly, chemical methods involve acid/base treatment or impregnation with metals or other compounds to enhance adsorption and catalytic properties (Jin et al. 2018; Hu et al. 2020; Lingamdinne et al. 2022). This not only introduces additional functional groups onto the biochar surface, such as hydroxyl, carboxyl, and amine groups, but also optimizes its overall charge distribution, enhancing its ability to interact with uranium. Moreover, biological methods may include the use of microorganisms to modify the biochar’s surface properties, further increasing its functionality and specificity towards uranium (Qi et al. 2022). These modifications expand the biochar's adsorption capacity, ion exchange ability, and interaction with uranium, thus contributing to the observed improvement in remediation (Yin et al. 2022). It was discovered that the addition of phosphorus-modified bamboo biochar (PBC) cross-linked with magnesium–aluminium layered double-hydroxide (LDH) composite ("PBC@LDH") resulted in a 54% reduction in the uranium leaching efficiency (Lyu et al. 2021a). The PBC@LDH composite exhibited strong affinity for uranium, effectively minimising uranium leaching and safeguarding groundwater quality. The scanning electron microscopy images before and after biochar modification are shown in Fig. 3. We have observed that most of the stomates on the surface of the unmodified (Fig. 3a) biochar were blocked by its flaky structure, whereas the surface of the modified (Fig. 3b, c) biochar appeared rough and uneven, with increased pores and rougher pore channels, indicating the successful modification of biochar with phosphorous and LDH (Lyu et al. 2021a). These modifications increased the functional groups and contributed to the increased effectiveness of biochar in repairing uranium-contaminated soils (Chen et al. 2023b).
Besides its direct uranium immobilisation capabilities, biochar has been shown to enhance soil health and fertility by improving soil pH, organic matter content, and cation exchange capacity (Singh et al. 2022; Li et al. 2023b; Yang et al. 2023c). Moreover, biochar positively influences soil microbial communities, creating conditions conducive to the growth of beneficial microorganisms (Yang et al. 2023b). This, in turn, enhances soil nutrient cycling and plays a crucial role in uranium immobilisation (Dai et al. 2021b). Biochar improves soil pH because of its alkaline nature, which reduces uranium availability in soils (Yang et al. 2023a). Organic matter in the soil has a high capacity to adsorb uranium owing to the presence of functional groups. Therefore, an increased organic matter content in soil is beneficial for uranium immobilisation. In a recent study, it was discovered that the mixed bacteria-loaded biochar application to soil altered the microenvironment by increasing the soil organic matter, cation exchange capacity, fluorescein diacetate hydrolysis activity, and dehydrogenase activity (Qi et al. 2022). The mixed bacteria-loaded biochar significantly decreased the availability of uranium and Cd in soil by 67.4% and 54.2%, respectively, reducing their accumulation in vegetables and promoting celery growth. In addition, the mixed bacteria-loaded biochar alters the structure and function of rhizosphere soil microbial communities by increasing the abundance of beneficial bacteria, while reducing plant pathogenic fungi, which may play an indirect role in inhibiting uranium uptake by celery (Qi et al. 2022). Similarly, Li et al. (2024) found that the pH, cation exchange capacity, enzyme activities, nutritional level of the rhizosphere soil, and abundance and diversity of the bacterial community significantly improved after biochar application. The improvement in soil quality was mainly due to increased microbial activity and organic matter content in the soil after biochar application (Li et al. 2024).
Although biochar has significant potential as a remediation technique for uranium-contaminated soils, several limitations and challenges must be considered. Firstly, the effectiveness of biochar in immobilising uranium may vary depending on its properties such as the type of feedstock, pyrolysis conditions, and post-treatment processes (Qiu et al. 2022). A previous study investigated the impact of biochar produced from five different materials—corn stover, herbal residue, cow manure, distiller's grains, and sugarcane bagasse—on uranium availability in soil. It was found that biochar derived from corn stover significantly reduced uranium availability, with a 36.2% decrease compared to the control. In contrast, soil amended with biochar derived from herbal residues demonstrated the least reduction in uranium availability, with a decrease of only 10% compared to the control (Qi et al. 2021). Furthermore, it has been observed that the preparation of biochar at different pyrolysis temperatures influenced its uranium adsorption capacity, with biochar produced at 500 °C exhibiting the highest efficiency, attributable to the abundance of active sites (Liao et al. 2022c). Therefore, the selection of the feedstock type and production method is crucial for optimising uranium immobilisation. Secondly, the efficacy of biochar application for uranium remediation may depend on site-specific conditions, including soil properties, uranium speciation, and local environmental factors (Kanwar et al. 2023). Taskin et al. (2019) demonstrated that biochar amendments had no effect on uranium concentration in maize grown in calcareous soil. Thus, a comprehensive understanding of site-specific characteristics is essential to determine the appropriate biochar type, application rate, and method for optimal uranium immobilisation. Finally, there is limited research available regarding the long-term effects of biochar on soil–plant systems and the potential accumulation of uranium in biochar-amended soils. Indeed, this is a critical area of study that warrants further exploration to fully understand and responsibly harness the benefits of biochar.
4 Inner mechanisms of uranium immobilisation by biochar
A comprehensive understanding of the complex mechanisms that govern uranium immobilisation through biochar is essential for the development of effective soil remediation strategies. In this section, we present a thorough description of the mechanisms that enable biochar to effectively immobilise uranium and elucidate the interactions involving surface complexation, reduction reactions, ion exchange, and physical adsorption (Fig. 4). Table 2 provides a comprehensive summary of the primary mechanisms governing uranium immobilisation for various types of biochar.
4.1 Surface complexation
Surface complexation, a crucial mechanism for uranium immobilisation by biochar, involves the creation of coordination bonds between the surface functional groups of biochar (primarily oxygen-, sulphur-, nitrogen-, and phosphorus-containing groups such as carboxyl, hydroxyl, and phosphate) and uranium ions in soil (Leng et al. 2020; Dai et al. 2021a; Tan et al. 2021). Inner- and outer-sphere complexation are the two ways in which surface complexation occurs (Xue et al. 2023). Inner-sphere complexation involves direct covalent bonding between uranium ions and the functional groups on the biochar surface. Inner-sphere complexation typically leads to strong bonds, often resulting in permanent attachment of ions to the biochar surface. In contrast, outer-sphere complexation is characterised by electrostatic interactions between the adsorbate and mineral surface (Yi et al. 2023). This adsorption mechanism, also known as physisorption, involves the hydration shells of water molecules forming a barrier between the adsorbate and adsorbent. Outer-sphere complexes are generally weak and reversible. Therefore, surface complexation typically refers to inner-sphere complexation (Alam et al. 2018; Li et al. 2018). In theoretical research, the effect of ionic strength on the adsorption efficiency is often used to distinguish between inner- and outer-sphere complexation (Liu et al. 2022a). Outer-sphere complexes are generally formed by non-specific, often Coulombic or Van der Waals forces, which can be largely influenced by the ionic strength of the solution (Lepore et al. 2022). However, inner-sphere complexes, which involve direct coordination between the adsorbate and the surface, are less influenced by changes in ionic strength, which explains the minor variations in the adsorption efficiency (Philippou et al. 2022).
The surface functional groups on biochar, specifically the carboxylic and hydroxyl groups, play a critical role in the formation of strong and stabilising complexes with uranyl ions (Dai et al. 2021a; Wu et al. 2022a; Gan et al. 2023; Li et al. 2023a). Ahmed et al (2021a) demonstrated the importance of –COOH and –OH groups in the sorption of uranyl ions onto biochar surface, indicating the presence of these groups significantly influences the sorption capacity. Similarly, Fu et al (2022) confirmed the important role of –COOH and –OH groups in the formation of complex surface bonds, effectively which effectively reduces the mobility and bioavailability of uranium in the soil. Additionally, though the literature is limited, some reports indicated the involvement of aromatic groups in the complexation process through the formation of π–π bonds (Liu et al. 2021a). It is common for biochar to possess aromatic functional groups, containing π-electrons within their aromatic rings. Uranium ions interact with these π-electrons because of their empty d orbitals, forming stable complexes that significantly immobilise uranium ions in soil.
However, the abundance and reactivity of the surface functional groups in biochar are determined by several factors, including the pyrolysis temperature, type of feedstock, and modification (Janu et al. 2021). Research showed that biochar produced at low temperatures (500 °C) tended to have a high concentration of oxygen-rich functional groups, which enhanced its capacity to adsorb uranium. Conversely, biochar produced at high temperatures (750 °C) tended to have reduced adsorption capabilities due to high-temperature metamorphism and obscured pores (Guilhen et al. 2019). Furthermore, the type of feedstock has significant effects on the quantity of surface oxygen-carrying functional groups, thereby profoundly impacting uranium adsorption performance. Jin et al. (2018) indicated this variation in a study, demonstrating that uranium adsorption capacities of wheat-straw-derived biochar and cow-manure-derived biochar were found to be 8.7 mg g−1 and 64.0 mg g−1, respectively (Table 2). This significant variation in adsorption capacity has led to increased research on innovative biochar modification techniques aimed at enhancing the abundance of functional groups. An example of such success is demonstrated in the work of Liao et al. (2022b), where the functionalization of biochar with KMnO4 and H2O2 led to a drama tic increase in the quantity of –OH groups on the surface of the biochar, thereby considerably improving the uranium immobilisation efficiency.
The details of surface complexation and uranium adsorption on biochar were elucidated through the application of advanced analytical techniques. Spectroscopic methods such as Fourier Transform Infrared spectroscopy (FT-IR), X-ray absorption spectroscopy (XAS), and X-ray photoelectron spectroscopy (XPS), have provided crucial insights into the structural and chemical intricacies at the biochar–uranyl interface (Liu et al. 2023b). A comprehensive investigation using these methods determined that uranium mainly adhered to the biochar surface via carboxyl and phenolic hydroxyl groups that were reactive to protons, suggesting the presence of both inner- and outer-sphere complexation (Alam et al. 2018). These methodologies provide important evidence that highlights the crucial role of surface functional groups in uranium immobilisation (Hu et al. 2018b).
4.2 Reduction reactions
Uranium, which is found in various valence states, significantly influences its behaviour and mobility in soil. Hexavalent uranium(VI), primarily in the form of uranyl ions (UO22+), is highly soluble and mobile in soil solutions, whereas tetravalent uranium(IV) is relatively insoluble and less mobile (John et al. 2022). To mitigate the risks posed by highly soluble uranium(VI), researchers have focused on modifying biochar properties to facilitate the reduction of uranium(VI) into its more stable and less soluble form, uranium(IV) (Chen et al. 2021). Previous research has indicated that biochar lacks the capability to directly reduce uranium(VI) to uranium(IV), and this process can only be facilitated indirectly through specific modifications (Yuan et al. 2017). Two primary methods for modifying biochar have been found to effectively reduce uranium (VI) to uranium (IV): Fe modification and microbial modification (Fig. 4) (Ouyang et al. 2023; Ren et al. 2023).
Investigations showed that biochar functionalized with Fe possesses potent electron donor properties (Pang et al. 2022). Through their interaction with UO22+ in soil, these active metals contribute electrons from the biochar surface, consequently promoting the reduction of uranium(VI) to a more stable state, uranium(IV). This approach has great potential for enhancing the remediation efficiency of uranium-contaminated land. For instance, Yin et al. (2022) conducted a study on phosphorus-modified bamboo biochar cross-linked with a magnesium–aluminium-layered double-hydroxide composite. Their investigation revealed the compound's effectiveness in catalysing the reduction of uranium(VI) to uranium(IV) in uranium-contaminated soil, accompanied by a significant reduction in available uranium by up to 55.97% compared with the control (Yin et al. 2022).
Microbe-modified biochar is another important method used for uranium(VI) reduction. Metal-reducing bacteria in the environment, such as Bacillus sp. dwc-2, Shewanella, and Geobacter, which have unique metabolic capabilities, act as electron acceptors and actively participate in reduction reactions, ultimately reducing uranium (VI) to uranium (IV) (Li et al. 2017; Lovley et al. 1991). Numerous studies have demonstrated that biochar application can enhance microbial reduction ability (Rushimisha et al. 2022; Wu et al. 2022b; Dong et al. 2023). The interaction between microorganisms and biochar for uranium reduction is influenced by various factors: (i) biochar as a microbial shelter: biochar plays a crucial role in complex soil, functioning as a shelter for microbes, thus considerably contributing to uranium reduction (Zheng et al. 2022). The porous structure of biochar facilitates both microbial colonisation and growth by providing an extensive surface area and an interconnected pore network, creating an optimal environment for microbial habitation (Li et al. 2022). Frankel et al. (2016) demonstrated that biochar application substantially increased microbial biomass and activity, providing evidence for the role of biochar as a microbial shelter. This shelter not only provides a suitable habitat for microbes but also catalyses their remediation activities, ultimately leading to the reduction and immobilisation of uranium (Arshad et al. 2017); (ii) Biochar-mediated soil improvement: biochar application enhances the inherent soil properties, building a favourable environment for microbial activity (Wei et al. 2023). This was accomplished by enriching the soil with essential nutrients, such as potassium and phosphorus, thus stimulating the growth of microorganisms (Limwikran et al. 2018). Furthermore, biochar improved soil cation exchange capacity and water retention, creating a favourable environment for microbes, thereby considerably contributing to uranium reduction and immobilisation (Tan et al. 2022). (iii) Biochar as an Electron Shuttle: Enriched with carbon, biochar exhibits characteristics similar to those of electron shuttles. A previous study suggested two unique electron shuttle pathways related to biochar, namely “geo-battery” and “geo-conductor” (Sun et al. 2017). The former relies on the surface functionality of the biochar, which can store and release electrons, thereby facilitating redox reactions in the soil (Hou et al. 2022). One gram of biochar can store and utilise as much as 2 mM of electrons for redox reactions in soil (Klüpfel et al. 2014). The geo-conductor pathway is attributed to the high conductivity of biochar due to its carbon structure, which supports direct electron transfer (Sun et al. 2017). These unique characteristics contribute to the role of biochar as an electron shuttle during a wide range of biogeochemical processes. The interaction of biochar with reducing microorganisms establishes an ongoing electron exchange between microorganisms and metal ions, encouraging redox reactions, and ultimately resulting in uranium immobilisation (Yu et al. 2023). Ren et al. (2023) revealed that the oxido-reductively active segment of biochar, predominantly the component containing oxygen, serves as a potent electron shuttle agent in microbial reduction processes, effectively facilitating chromium (Cr) reduction in soil. Notably, chromium is similar to the polyvalent metal ions in uranium, which suggests potential analogous processes. Ding et al. (2018) supported this perspective by showing that biochar-supported microorganisms accelerate the reduction of uranium from U(VI) to U(IV), accompanied by mineral coprecipitation. Overall, microbial modification of biochar provides an effective approach for uranium(VI) reduction, with promising prospects for remediating U-contaminated environments.
4.3 Ion exchange
The ion exchange properties of biochar also contribute to the immobilisation of uranium (Fig. 4) (Liao et al. 2022d). Biochar, which contains exchangeable cations such as Ca2+ and K+, actively participates in these ion exchange reactions, thereby immobilising positively charged uranium ions on its surface (Lingamdinne et al. 2022). For example, cattle-bone biochar had a large number of phosphate groups, and the results showed that UO22+ takes the place of Ca2+ and is incorporated into phosphate groups, effectively immobilising uranium(VI) on the biochar surface (Ashry et al. 2016). Similarly, metal ions (such as Ca2+, Mg2+, Na + , and K+) in anaerobic granular sludge biochar act as effective adsorption sites and actively engage in ion exchange processes which contribute to the removal of uranium(VI) (Zeng et al. 2020).
The efficiency of uranium immobilisation through ion exchange depends on the cation content of biochar and the environment conditions (Kumar et al. 2023). The adsorption and immobilisation capacity of biochar for uranium generally increases with its cation content (Thakur et al. 2022). The impact of different treatment methods on the cationic content of biochar is quite significant (Lingamdinne et al. 2022). For instance, biochar produced from municipal waste typically exhibits higher levels of cationic content compared to those derived from plant materials (Zhao et al. 2015). The content of exchangeable cations in the biochar decreases with increasing pyrolysis temperature (Li et al. 2019c). Additionally, the immobilisation process of uranium is further affected by the presence of competing ions in the soil. High concentrations of common cations, such as Ca2+ and Al3+, can reduce the uranium binding capacity of biochar (Liao et al. 2022d). This is attributed to these ions occupying the binding sites on the biochar, thereby limiting the availability of sites for uranium immobilisation (Mishra et al. 2017).
4.4 Physical adsorption
Physical adsorption is governed by nonchemical interactions between molecules, including electrostatic and van der Waals forces (Fig. 4) (Wen et al. 2018; Ji et al. 2020). Although the van der Waals forces are relatively weak, they form a common adsorption mechanism (Yang et al. 2019). The strength of van der Waals forces depends on the specific surface area, pore volume, and pore radius of the material (An et al. 2022). Biochar, which is notable for its extensive specific surface area and proliferous pore structure, enables the initial adsorption of uranium ions through van der Waals forces (Zhang et al. 2023). The pore structure of biochar is substantially influenced by the feedstock, pyrolysis temperature, and modification processes. For example, biochar derived from crop residues and wood typically has a larger specific surface area than that derived from animal manure and solid waste (Tomczyk et al. 2020).
The adsorption of uranium on biochar is also influenced by electrostatic interactions, which are determined by the surface potential of the biochar, known as the point of zero charge (Pzc), in combination with the environmental pH (Mukherjee et al. 2011). When the environmental pH decreased below the Pzc of biochar, the biochar surface became positively charged. This positive charge weakens the electrostatic attraction between the biochar and positively charged uranium, leading to a reduced adsorption efficiency (Kumar et al. 2011). Conversely, when the environmental pH exceeds the Pzc of the biochar, the biochar surface becomes negatively charged, enhancing electrostatic attraction and facilitating the interaction between the biochar and positively charged uranium ions (Kasera et al. 2022). Understanding the surface potential of biochar and its interaction with the environmental pH is crucial for optimising the application of biochar in uranium pollution remediation.
However, physical adsorption is not the dominant mechanism of uranium immobilisation by biochar. Li et al. (2019b) examined the effects of biochar modified with potassium permanganate on its performance in uranium immobilisation. They observed a significant decrease in the specific surface area of the biochar, reducing it to one-third of its original value. Despite that the surface area decreased, the introduction of functional groups significantly increased the uranium adsorption capacity. These results highlight that the interaction between the functional groups and uranyl ions through complexation is more significant than that through physical interactions. The modification of biochar with potassium permanganate increased the presence of O–H groups and introduced Mn–O groups, improving its ability to form complexes with uranium.
4.5 Other mechanisms
It is noteworthy that biochar enriched with phosphorus groups not only aids in uranium immobilisation through surface complexation but also engages in a distinct precipitation reaction (Liao et al. 2022d). In these biochar, phosphate ions can chemically react with uranyl ions adsorbed on their surfaces (Ruan et al. 2022). Such reactions lead to the formation of uranium phosphate minerals, notably autunite (Ca[(UO2)(PO4)]2·11H2O), characterized by their extremely low solubility (Lyu et al. 2021b). Unlike surface complexation, this precipitation process results in the emergence of new mineral phases, transforming uranium ions into forms that are not bioavailable (Lyu et al. 2021b). Consequently, the formation of these insoluble minerals substantially improves the stability of uranium in the environment, thereby reducing its migration in soil.
Overall, uranium immobilisation by biochar in soil is a complex process involving four primary mechanisms: surface complexation, reduction, ion exchange, and physical adsorption. Although their relative contributions vary, these mechanisms often function simultaneously. These mechanisms vary based on factors such as the biochar properties, soil conditions, and concentrations and chemical forms of uranium ions. It is crucial to comprehensively understand the complex mechanisms of uranium interaction with biochar for practical applications.
5 Effect of biochar application on uranium accumulation and toxicity in plants
5.1 Biochar reduced uranium uptake by plants
The accumulation of uranium in plants poses significant environmental and public health risks, particularly in uranium-contaminated areas (Liu et al. 2022c). Thus, investigating the transfer of uranium from soil to plants has become a priority for soil remediation (Chen et al. 2021; Ao et al. 2022). Plants generally absorb UO22+ through epidermal root cells, utilising carriers and ion channels similar to essential elements such as calcium, iron, and magnesium. Anionic uranium species such as UO2(CO3)22− and UO2PO42− may traverse cell membranes via anionic channels resembling bicarbonate or phosphate (Duquène et al. 2010; Chen et al. 2021; Lai et al. 2021). As reviewed above, biochar application has shown significant potential for decreasing uranium accumulation in plants. Biochar effectively immobilises uranium, reducing its bioavailability and consequently limiting uranium uptake by plant roots, thereby preventing uranium translocation to the aboveground parts of plants (Fig. 5). Indeed, the rhizosphere—the area of soil influenced by root secretions and associated soil microorganisms—plays a vital role in uranium remediation (Wu et al. 2022a, b). The Red Flinders grass has been found to exude acetic acid, citric acid, oxalic acid, formic acid, and lactic acid in roots (Liu et al. 2022c). These low-molar-weight organic acids can facilitate the dissolution of Fe (oxyhydr)oxides, including goethite and magnetite, in Fe-rich matrices, promoting the transformation of Fe-bearing minerals from magnetite to ferrihydrite (Liu et al. 2022c). This process leads to the formation of amorphous ferrihydrite-like minerals, which typically exhibits extensive surface area, facilitating uranium immobilization via co-precipitation or inner-sphere surface complexation. Biochar could facilitate the association between uranium and iron, thereby contributing to the effective immobilization of uranium (Liu et al. 2022c).
However, it is important to note that the effectiveness of biochar in reducing uranium accumulation in plants varies depending on various factors. As previously stated, key determinants of biochar efficacy are its type and properties, including the feedstock used in its production, pyrolysis temperature, and modification method. The inherent properties of the soil in which biochar is applied also influence its functionality (Boghi et al. 2018). Taskin et al. (2019) found that the addition of biochar to calcareous soil did not reduce the uranium content in soybeans. This observation may be attributed to the formation of highly mobile anionic complexes between UO22+ and carbonate in calcareous soil, leading to increased absorption of uranium by plants compared to that in natural soil (Shahandeh and Hossner 2002). Another factor affecting the effectiveness of biochar is the plant species to which it is applied (Gao et al. 2019; Cui et al. 2023). Different plant species have unique physiological and metabolic responses to uranium and biochar. Tomatoes and kohlrabi may exclude uranium, whereas cucumbers and radishes may accumulate uranium in their tissues, thereby posing a risk to the food chain (Hou et al. 2018). Subsequent research explored the effect of biochar on reducing uranium accumulation in vegetables and found that its effectiveness was species-dependent (Qi et al. 2022). The finding indicated that the order of enrichment in the above-ground parts was Brassica chinensis L. > Apium graveolens L. > Lycopersicon esculentum Mill in biochar-treated contaminated soil. Overall, the application of biochar can be regarded as a promising and environmentally friendly approach for mitigating uranium accumulation in plants and promoting safe agricultural production on uranium-contaminated lands. However, a more comprehensive assessment of their potential and limitations is necessary to improve our understanding of their efficacy in environmental remediation.
5.2 Biochar inhibited root-shoot transport of uranium
The translocation of uranium from plant roots to shoots forms a critical connection in the relationship between plants and uranium, substantially influencing the accumulation and distribution of uranium in plant tissues, and is usually measured using transfer factors (TFs) (Dhir 2021). Upon entry into the roots, uranium ions complex with endogenous phosphate residues, resulting in precipitation and fixation within plant organs, thereby preventing their translocation from the roots to the leaves (Laurette et al. 2012). This regulation can significantly minimise the potential phytotoxic effects associated with uranium accumulation, thereby promoting the survival and well-being of plants in uranium-contaminated environments (Wang et al. 2019b). This transportation is modulated by various parameters, including soluble uranium concentrations in the soil (Vandenhove et al. 2007), expression levels of transporter genes in plants (John et al. 2022), and external environmental conditions (Mertens et al. 2022). In the presence of uranium, transporter genes (IRT1, FRO2, and FIT1) and calcium transporter CAX7 in Arabidopsis thaliana, for instance, have been observed to be affected, and external calcium inhibits uranium accumulation in roots (Doustaly et al. 2014; Mertens et al. 2022; Sarthou et al. 2022). The addition of biochar to the soil has a significant influence on this transport process. Yin et al. (2022), for instance, discovered that the TF of uranium for phosphorus-modified bamboo biochar treatments decreased by 11.9% compared with the control treatment, suggesting a positive effect in limiting the migration of uranium from roots to shoots in Indian mustard. A recent study found that biochar application to rice plants under heavy metal stress significantly upregulated the expression of OsMTP11 and CATa, with OsMTP11 showing a 3.2-fold increase and CATa exhibiting a 5.1-fold increase (Pehlivan et al. 2023). These results indicated that the presence of biochar induced a transcriptional response, aiding plant growth under the stress imposed by heavy metals.
5.3 Biochar alleviated uranium phytotoxicity
Biochar alleviates uranium phytotoxicity by reducing uranium availability in soil and improving soil quality (Qi et al. 2022). Physiological indicators, such as chlorophyll levels, nutrition, and photosynthetic performance are essential metrics for quantifying crop health and productivity under stressful conditions (Sapre et al. 2022). The application of biochar significantly enhanced nutrient uptake and synthesis of photosynthetic pigments, leading to a significant improvement in plant performance under stress (Fig. 5) (Majeed et al. 2022). Moreover, uranium induces the overproduction of reactive oxygen species (ROS) in plant cells, which damages membrane integrity and increases the accumulation of oxidative markers, including malondialdehyde (MDA), hydrogen peroxide, and electrolyte leakage (Khan et al. 2022). Biochar has significant potential for mitigating uranium-induced oxidative damage in plants. The application of biochar has been shown to effectively decrease MDA concentrations in ryegrass experiencing uranium stress, thereby indicating its potential in alleviating such stress-induced damage (Zhang et al. 2019b). Plants have a defence system to cope with ROS, which includes various antioxidant enzymes that mitigate the deleterious effects of oxidative stress (Han et al. 2023). Biochar application improves plant tolerance to abiotic stress by increasing antioxidant activity (Irshad et al. 2020). Biochar application enhances antioxidant activities in plants by increasing the content of antioxidant enzymes such as superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), and ascorbate peroxidase (APX) (Rizwan et al. 2018). SOD mitigates superoxide radicals, whereas POD and CAT catalyse the breakdown of hydrogen peroxide, thereby reducing potential oxidative damage. APX utilises ascorbate to detoxify peroxides (Zhu et al. 2023a). By significantly increasing antioxidant activity, biochar improves plant tolerance to abiotic stress and promotes overall plant health and productivity.
6 Concluding remarks and future perspectives
This review comprehensively describes the potential of biochar as a remediation solution for uranium-contaminated soils and its beneficial effects on plant productivity. The global challenge of uranium contamination, primarily from industrial activities, results in soil toxicity, which has detrimental effects on plant growth. Biochar is a promising remediation agent owing to its unique properties. Biochar not only reduces the mobility and bioavailability of uranium in soil through surface complexation, reduction, ion exchange, and physical adsorption processes but also enhances soil nutrition. Notably, the modification of biochar to enhance its surface complexation effect as well as the synergistic reduction mechanism in interactions with microorganisms is recognised as a promising direction for further research. Additionally, biochar substantially decreases uranium uptake by plants, transport and related toxicity, and its effectiveness depends on multiple factors, including the biochar type, soil characteristics, and plant species.
Based on published papers and our review, future research should explore the following four points. Firstly, an examination of the relationships among various factors influencing the remediation efficacy of biochar in the soil–plant system, including soil properties, levels of uranium contamination, plant species, and biochar characteristics, is imperative because of the existing limitations in our understanding of this complex system. Secondly, exploring the potential of biochar to improve soil quality and crop growth is critical. This involves assessing the impact of biochar on soil nutrient cycling, water retention, and crop growth, providing insights for sustainable agricultural practices. However, related investigations have been limited to date. Thirdly, the effects of biochar application on plant responses to uranium exposure should be investigated using molecular techniques such as transcriptomics or proteomics. In particular, the mechanisms and expression of transporter genes in plant cells are poorly understood. Last but not least, long-term field trials and sustained investigations are necessary to track the performance and effect of biochar on different soil compositions and environmental conditions. Emphasis should be placed on the intricate interactions between biochar, soil microbiota, and plant physiology (Additional file 1).
Availability of data and materials
The datasets used or analyzed during the current study are available from the corresponding author on reasonable request.
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Acknowledgements
We would like to thank the College of Environment and Resource, Xichang University, China.
Funding
This study was supported by the National Natural Science Foundation of China (U21A20237, 41977031, 41402248); the Key R&D Projects of Liangshan Prefecture Science and Technology Plan (22ZDYF0162, 22ZDYF0171); the Ministry of Science and Technology of the People’s Republic of China (2019YFC1803500, 2019YFC1803504); the Key R&D Projects of Sichuan Provincial Science and Technology Department (2018SZ0298, 2023YFS0390); the Bureau of Science and Technology Aba Qiang Tibetan Autonomous Prefecture (R22YYJSYJ0004, R23YYJSYJ0010).
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FH: data curation, investigation, visualization, writing- original draft. FD: writing-review and editing. LC: conceptualization, writing—review and editing. YZ: writing-review and editing. LZ: writing—review and editing. SS: writing-review and editing. ZW: writing-review and editing. JL: writing-review and editing. LF: conceptualization, supervision, writing-review and editing. All authors read and approved the final manuscript.
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The authors have no competing interests to declare that are relevant to the content of this article.
Additional information
Handling editor: Xing Yang
Supplementary Information
Additional file 1: Text S1.
Literature search. Text S2. Methods of meta-analysis. Table S1. Basic information of the publications extracted for this meta-analysis.
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Huang, F., Dong, F., Chen, L. et al. Biochar-mediated remediation of uranium-contaminated soils: evidence, mechanisms, and perspectives. Biochar 6, 16 (2024). https://doi.org/10.1007/s42773-024-00308-3
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DOI: https://doi.org/10.1007/s42773-024-00308-3