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Article

Effects of Rare Earth Element-Rich Biochar on Soil Quality and Microbial Community Dynamics of Citrus grandis (L.) Osbeck. cv. Guanximiyou

by
Zhiqi Chen
1,
Liujun Feng
1,
Zhiqiang Chen
1,*,
Zhibiao Chen
1,
Jie Wu
1 and
Qiang Lin
2
1
School of Geographical Sciences, Fujian Normal University, Fuzhou 350117, China
2
Soil and Water Conservation Station of Fujian Province, Fuzhou 350003, China
*
Author to whom correspondence should be addressed.
Agriculture 2025, 15(8), 895; https://doi.org/10.3390/agriculture15080895
Submission received: 15 March 2025 / Revised: 10 April 2025 / Accepted: 17 April 2025 / Published: 20 April 2025
(This article belongs to the Section Agricultural Soils)
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Abstract

:
Rare earth elements (REEs) are key resources of strategic importance, but pollution has increased due to uncontrolled mining. Although heavy metal hyperaccumulating plants are environmentally friendly, they require strict control during post-treatment, or they may cause secondary pollution. Therefore, their safe disposal plays a key role in the ecological restoration of REE mines. In this study, rare earth element (REE)-rich biochar was produced by pyrolyzing the REE hyperaccumulator Dicranopteris pedata. This biochar was then applied to the Citrus grandis (L.) Osbeck. cv. Guanximiyou soil amendment experiment to evaluate its effects on soil physicochemical properties and microbial indicators. Four treatments were established: CK (0% REE-rich biochar), BC1 (1% REE-rich biochar), BC3 (3% REE-rich biochar), and BC5 (5% REE-rich biochar). The BC5 treatment decreased soil REE bioavailability, thereby preventing REE pollution. The BC5 treatment also demonstrated the highest efficacy in improving soil total organic carbon (229.11%), total nitrogen (53.92%), total phosphorus (55.61%), total potassium (55.50%), available nitrogen (14.76%), available phosphorus (46.79%), and available potassium (159.42%) contents compared to CK. Furthermore, soil enzyme activities were significantly increased by BC5 treatment (p < 0.05). At the bacterial phylum level of classification, the bacterial diversity index (Chao1 and Shannon) exhibited elevated levels under BC5 conditions. Furthermore, the Chao1 index of fungal diversity exhibited a substantial augmentation of 55.67% (p < 0.05) in the BC5 treatment in comparison to the CK, and also significantly higher than the other treatments (p < 0.05). Our study showed that the composition of soil microorganisms was altered by REE-rich biochar. Proteobacteria, Acidobacteria, Actinobacteriota, and Chloroflexi are dominant among bacteria, while Ascomycota is dominant among fungi. Mantel and redundancy analyses showed that the most important environmental factor affecting the structure of soil microbial communities was pH, especially in the case of bacteria. In summary, this study showed that the application of 5% REE-rich biochar provided the best improvement in soil physicochemical properties and microbial diversity. These findings highlight its potential for soil remediation and provide new ideas for recycling heavy metal hyperaccumulating plant waste.

1. Introduction

Rare earth elements (REEs) are a group of heavy metals recognized for their unique physicochemical properties, which have attracted significant attention for their application in new materials and energy. Currently, rare earths can be divided into LREEs (La, Ce, Pr, Nd, Sm, and Eu), which have a small relative atomic mass, and HREEs (Y, Gd, Tb, Dy, Ho, Er, Tm, Yb, and Lu), which have a large atomic mass, based on the atomic number and chemical properties of the element. Additionally, they have become a special and important strategic resource in China because of their complete range of elemental species and distribution forms [1,2]. As the demand for resources and mining efforts continue to increase, an increasing number of REEs are being released into the environment, causing varying degrees of damage and pollution. Therefore, heavy metal pollution caused by the production of REEs needs to be addressed urgently [3]. Environmental remediation is a multifaceted process that may involve many remediation methods. These approaches encompass the replacement of soil, chemical stabilization, and phytostabilization, among other methods [4,5]. Among these methods, phytoremediation is widely used due to its high environmental benefits and sustainability [6]. Plants have been shown to accumulate and stabilize heavy metals in the soil through the root system and other physiological functions, but they also produce a large amount of heavy metal-rich biomass. Subsequent to the decomposition of plants, the heavy metals remaining in the plants will re-enter the ecosystem, causing secondary contamination of soil and water, and ultimately harming humans and animals through the food chain [7]. Therefore, the proper disposal of phytoremediation residues from mine sites is critical.
Pyrolysis has garnered significant interest for its ability to reduce the mass and volume of waste biomass while concurrently generating substantial energy and heavy metal-stabilized biochar products. In comparison with conventional waste management methodologies, such as landfill disposal, composting, and incineration, pyrolysis has been demonstrated to offer substantial advantages in terms of environmental impact and resource utilization [8,9]. This study also offers a novel approach to managing waste biomass from heavy-metal-hyperaccumulator plants. As an emerging functional material, biochar has great potential for soil improvement and sustainable agricultural development due to its unique properties (e.g., strong adsorption capacity, rich pore structure, etc.). [10]. Compared to traditional raw materials, metal-loaded biochar produced by the pyrolysis of heavy metal-enriched plants not only retains the advantages of ordinary biochar, but the metal elements within the plants can also regulate the structure and adsorption properties of the biochar [11,12].
Pinghe County, situated within the province of Fujian, has the distinction of containing China’s most extensive area dedicated to the cultivation of ‘Guanximiyou’ pomelo (Citrus grandis (L.) Osbeck. cv. Guanximiyou) [13]. Its cultivation area has reached 4×104 hm2, with an annual production of over 120 × 104 t. Recent years have seen a rapid development of the pomelo industry in Pinghe County, a process which has had deleterious effects on the environment. Serious environmental problems have arisen due to over-exploitation, uncontrolled fertilization, and other problems [14]. Relevant studies have shown that irrational application of fertilizers causes soil acidification, affects soil properties, reduces soil fertility, inhibits beneficial flora and related enzyme activities, results in a decline in soil quality, and ultimately affects crop yield and quality [15]. Therefore, implementing reasonable and effective measures to improve the soil quality in pomelo orchards is crucial to the local pomelo industry.
D. pedata is a perennial herbaceous plant regarded as an important pioneer species in the ecological restoration of mining areas because of its advantages in the ecological restoration of ionic REEs in the South, such as high adaptability, vigorous growth, and tolerance to heavy metals [16,17]. At the same time, D. pedata is also one of the prominent hyperaccumulators of REEs (leaf REE content of up to 3000 μg g−1 or more, compared to about 10−4–10−2 μg g−1 for common plants). However, there are few reports on the preparation of biochar from D. pedata for soil improvement in rare-earth mining areas. Based on this, we used pyrolysis to prepare biochar to treat D. pedata after the completion of phytoremediation in mining areas.
Currently, there are fewer studies on the application of carbonization materials from rare earth-enriched plants to soil remediation, and it is not clear whether the application of such carbonization materials to the soil will have beneficial or detrimental effects on soil physicochemical properties and microorganisms. We applied the prepared REE-rich biochar as an experimental soil amendment in pomelo pots and hoped to achieve both effective treatment and safe application of this biochar. Therefore, our study aimed to observe the effects on soil quality and microbial indicators of adding REE-rich biochar to the soil in the ‘Guanximiyou’ pomelo production area. Specifically, it included the following aspects: (1) investigating the influence of applying different amounts of REE-rich biochar on the content and chemical speciation of REE in soil; (2) elucidating the influence of different levels of REE-rich biochar application on soil nutrient and enzyme activities; (3) investigating the effects of REE-rich biochar on soil microbial communities under different application conditions; and (4) assessing the risk of environmental transport of REE-rich biochar. This study will provide a new research idea for resource recovery and secondary use of ecological remediation residues in rare earth mining areas.

2. Materials and Methods

2.1. REE-Rich Biochar Production

In this experiment, D. pedata cultivated under uniform growth conditions (the plant height was 30 cm, and the ground diameter was 0.1 cm) was selected as test materials from a rare earth mining area in Hetian Town (Fujian, China; 25°36′ N, 116°26′ E). After the D. pedata was harvested, it was dried in an oven at 65 °C for 72 h, then ground and passed through a 100 mm sieve. D. pedata powder was placed in a tube furnace, heated to a target temperature of 800 °C at a N2 flow rate of 0.1 L min−1 and a heating rate of 5 °C min−1 and held at a constant temperature for 2 h. Subsequently, the material was allowed to cool naturally, after which it was retrieved to obtain the REE-enriched biochar.

2.2. Physicochemical Properties and Characterization of REE-Rich Biochar

The specific surface area and pore size of the biochar samples were determined using a specific surface area meter (Micromeritics ASAP 2460, Norcross, GA, USA). An elemental analyzer (Model Vario EL cube, Frankfurt, Germany) was used to determine the elemental composition of the biochar. The microscopic surface of the biochar was observed using a scanning electron microscope (ZEISS Sigma 300, Oberkochen, Germany) for elemental composition analysis. The investigation of the crystal structure and constituent elements of the biochar sample was undertaken using the technique of X-ray diffraction (Rigaku SmartLab SE, Tokyo, Japan). The structure of the biochar functional groups was analyzed using a Fourier transform infrared spectrometer (Thermo Fisher Scientific Nicoleti S20, Billerica, MA, USA). Furthermore, a zeta potential analyzer (Malvern Zetasizer Nano ZS90, Malvern, UK) was also used to determine the zeta potential of the biochar samples. The REE contents of the raw D. pedata before preparation and the REE-rich biochar after preparation are shown in Table 1.

2.3. Pot Plant Experiment

We chose to conduct our potting experiments in the year 2022 in Changting Village (Fujian, China; 24°38′ N, 117°20′ E). The soil utilized in the experiment was obtained from local pomelo plantation areas. The climate of the region is humid subtropical, with a frost-free period of 310 days, an average annual temperature of 21.3 °C, an annual rainfall of 1654.3 mm, and an average annual sunshine of 1905.4 h. The predominant soil type is red loam, whose parent material is classified as ferruginous or oxidized sand, according to the FAO [18]. The background values of the topsoil (0–20 cm) in the pomelo plantation area are shown in Table 2.
In the present study, we conducted an outdoor culture test. Before the commencement of the experiment, topsoil (0–20 cm) was collected from the pomelo plantation areas using an “S” sampling method. Mix the soil samples thoroughly and store them indoors in a cool place to dry naturally. After air-drying, impurities, as well as plant and animal residues, were carefully removed from the soil, and then the soil was sifted through a 2 mm sieve. To prevent contamination of the soil with other microorganisms during the sieving process, the sieves were sterilized by autoclaving (121 °C, 30 min) prior to use. The experiment involved the implementation of four distinct treatments, each with a specific biochar application rate. The biochar application rates were expressed as percentages of the air-dried soil mass. The control treatment, designated as CK, did not receive biochar application. The biochar application treatments included BC1 (1% REE-rich biochar), BC3 (3% REE-rich biochar), and BC5 (5% REE-rich biochar). Each treatment was replicated four times, resulting in 16 potted plants. Before the start of the potting experiment, soil mixed with biochar was packed into pots (the diameter was 35 cm, the height was 24 cm) with a weight of 5 kg per pot (5 kg of soil was added directly to the CK treatment group), followed by random selection of uniform and robust pomelo seedlings (the plant height was 60 cm, the ground diameter was 2 cm) from the pomelo plantation area and planting them in pots equipped with the substrate (one plant per pot) for 90 days.
After the experiment, three pots were randomly selected for soil sampling in each treatment pot at a sampling depth of 0–20 cm. The collected soil was then sieved through a 2 mm sieve after removing debris such as residual roots. A portion of the soil samples underwent natural desiccation and was subsequently utilized for the assessment of soil pH, total nutrients, and REEs. Following the extraction of soil samples intended for soil column leaching experiments, the remainder was stored in a refrigerator at 4 °C for the determination of rapid soil nutrients, enzyme activities, and microbial indices.

2.4. Soil Column Experiment

A 200 g soil sample was meticulously weighed and thoroughly mixed with 0%, 1%, 3%, and 5% REE-rich biochar, then incubated at room temperature for 60 days. During the incubation period, the water content was maintained at 60% by performing daily weight measurements. A transparent polyvinyl chloride (PVC) pipe with a 35 cm column length and an inner diameter of 5 cm was selected as the lysimetric column. To avoid contamination of the soil with other microorganisms, PVC pipes were sterilized with 75% ethanol. The bottom of the column was meticulously sealed with gauze to ensure the soil specimens remained firmly in place and did not fall during the process, and the inner wall of the PVC pipe was uniformly coated with petroleum jelly to prevent the lysimetric solution from flowing out of the inner wall, which would affect the experimental results. The quartz sand was approximately 2 cm thick. Then, the soil sample was loaded with a soil thickness of 20 cm, and the top of the soil was covered with quartz sand of approximately 2 cm thickness to prevent the drenching solution from destroying the surface structure of the soil sample and ensure that the drenching solution seeps down uniformly. The simulation of a one-year drenching volume in Pinghe County was conducted based on the county’s average annual rainfall, evaporation, and water-bearing area of the soil column. The simulation yielded a result of approximately 1.7 L. The drenching solution was modeled using Fujian acid rain with a 1:1 ratio of HNO3:H2SO4 (volume volume). A total of 5 drenching events were simulated for 5 years. Five replicates were performed for each treatment. All leachates were collected post-completion of the test and stored in a refrigerator at 4 °C for subsequent analysis. The collected leachate was filtered through a 0.22 μm membrane and then used to determine the concentration of REE. At the end of the soil column leaching experiments, the soil column was carefully divided into four groups of 5 cm-thick sections (depths: 0–5 cm, 5–10 cm, 10–15 cm, and 15–20 cm). Subsequently, the four sets of soil samples obtained were analyzed for REE content.

2.5. Analysis of Indicators

2.5.1. Analysis of Soil REE Content and Chemical Speciation

Soil REE content was determined using a method previously documented by Luo [19]. First, soil samples were subjected to a series of pretreatment procedures. Specifically, the air-dried soil was ground and passed through a 0.075 mm sieve, then sealed and stored. The acid digestion method (HNO3-HF-HClO4) was used to digest the soil samples. Soil samples (0.5 g) were placed on a graphite digester (SH220F, China) and eliminated with hydrochloric acid (10 mL) at elevated temperatures (120 °C) for a duration of 8 h. Subsequently, the samples were digested with 10 mL of nitric acid, 10 mL of hydrofluoric acid, and 5 mL of perchloric acid. Finally, an inductively coupled plasma mass spectrometer (ICP-MS, Thermo Fisher Scientific, USA) was used to determine the REE content.
In addition, the chemical speciation of REEs in soil was analyzed using the BCR continuous extraction method (Bureau Communautaire de Référence) [20], which is noted for its simplicity and reproducibility. Rare earth elements are classified into weak acid exchange, reduced, oxidized, and residual states, and these states are designated by F1, F2, F3, and F4, respectively. F1 and F2 are more likely to be released into the soil than F3 and F4, with high mobility and bioefficacy. F3 is easily released under oxidizing conditions but remains relatively stable under reducing conditions. F4 is extremely stable in soil and is not easily released. The steps in the BCR extraction method are listed in Table 3.

2.5.2. Analysis of Soil Chemical Properties and Enzyme Activities

The soil pH and the TN content were determined by pulverizing the air-dried soil and passing it through a 0.25 mm sieve. The method of determination was based on the experimental method of Bao [21]. Soil pH is measured using a pH meter (water–soil ratio 1:2.5). Potassium dichromate–sulfuric acid oxidation was used to assess TOC. The Kjeldahl method was used to determine TN. The soil was subjected to H2SO4–HClO4 digestion, followed by a colorimetric method to estimate TP. Before the determination of TK, the soil was subjected to digestion with hydrofluoric, nitric, and perchloric acids, and subsequently, its content was determined using a Profile DV Inductively Coupled Plasma Atomic Emission Spectrometer (ICP-AES, Teledyne Leeman Laboratories, Hudson, NH, USA).
Fresh soil samples stored at 4 °C were sieved through 1 mm and used for the soil’s quick-acting nutrients and enzyme activity indexes. Fast-acting nutrients were determined using Olsen’s method [22]. The extraction and determination of soil AN was conducted using the alkaline hydrolysis digestion method. The determination of available phosphorous (AP) was executed by the NaHCO3-H2SO4 leaching-molybdenum-antimony colorimetric method, the AK determination was performed using the NH4OAc leaching-flame photometer method. The enzyme activity was determined using the method described by Saiya-Cork [23]. A standard 96-microliter fluorescence assay was used to determine hydrolytic enzyme activity. We selected five enzymes related to soil carbon and nitrogen cycling for our study, including soil β-glucosidase (BG), cellobiose hydrolase (CBH), β-N-acetylaminoglucosidase (NAG), leucine aminopeptidase (LAP), and alkaline phosphatase activity (ALP).

2.5.3. Analysis of Soil Microbial Diversity and Community Composition

The extraction of genomic deoxyribonucleic acid (DNA) from soil samples was carried out utilizing the AxyPrep DNA gel recovery kit (AXYGEN Corporation). The extracted DNA was then detected by 1% agarose gel electrophoresis. Polymerase chain reaction (PCR) amplification was conducted on designated sequencing regions (soil bacterial 16S V4-V5 and fungal ITS1 regions) using synchronized specific primers with barcodes or fusion primers containing base mismatches. Polymerase chain reaction (PCR) amplification was performed using TransGen AP221-02, and three replicates were set up for each sample. PCR products from the same sample were then mixed and electrophoresed on a 2% agarose gel to recover the target bands. After library construction, up-sequencing was performed using the NovaSeq6000. The FASTQ data obtained from the sequencing process were subjected to a quality control procedure using Pear software (v0.9.11). This procedure entailed the removal of ambiguous base-containing and primer mismatched sequences, the trimming of the sequences to remove bases with quality values lower than Q20, and splicing the two ends of the sequences according to the overlapping relationship of paired-end reads. The minimum overlap was set to 10 base pairs (bp), and the p-value was set to 0.0001 to obtain the FASTA sequence. The noise-reduced data were then compared with the database for species annotation using the classification sklearn module in QIIME2 software (v1.8.0). This process was managed by the Beijing Ovison Gene Technology Co., Ltd. (Beijing, China) (https://www.crunchbase.com/organization/allwegene-tech, accessed on 27 February 2024).

2.6. Data Analysis

Preliminary data organization and table plotting were carried out using Microsoft Excel 2021. Species annotation of bacteria and fungi and the calculation of alpha diversity indices were performed using QIIME2 software with Silva 138.1 and Unite v9.0 databases, respectively. IBM SPSS 26 was used for analysis of variance (ANOVA) and significance testing. Pearson correlation analysis was performed using the R 4.4.1 software vegan and ggplot2 packages. Redundancy analysis (RDA) was performed on microbial gate levels, REE content, and soil physicochemical factors using Canoco 5.0 software. Using Origin 2024, the following figures were created: biochar characterization, soil REE content and morphology, soil physicochemical properties, dilution curves, microbial community Wayne plots, and microbial phylum-level relative abundance.

3. Results

3.1. Characterization of REE-Rich Biochar Biochar

As demonstrated in Table 4, the specific surface area, pore diameter, and pore volume of REE-rich biochar produced at 800 °C were 439.48 m2 g−1, 0.19 cm3 g−1, and 1.71 nm, respectively.
The SEM image at 10.00 μm scale shows that the ash on the surface of REE-rich biochar was effectively removed, and the pores were smooth. The EDS results showed that the REE-rich biochar was enriched with the rare earth element Y in addition to common elements such as C, N, and O. The elemental weight percentage and atomic mass percentage of Y in the REE-rich biochar were 0.41% and 7.71%, respectively (Figure 1).
FTIR (Fourier transform infrared) characterization revealed that the REE biochar exhibited pronounced absorption peaks at 3430 cm−1 (-OH), 3127 cm−1 (N-H), 1400 cm−1 (C-H), and 1039 cm−1 (C-O). Diffraction peaks at 21.51° and 43.12° were identified by XRD analysis. The zeta potential declined with increasing pH, and equipotential was observed at approximately pH 5.7 (Figure 2).

3.2. Changes in REE Content and Chemical Speciation of the Soil After Application of REE-Rich Biochar

A substantial alteration (p < 0.05) in soil REE content and morphology was observed after the application of REE-rich biochar. The LREE content was significantly higher than that of the HREE under different treatments (Figure 3) (p < 0.001). In the BC5 treatment, the LREE and HREE contents were significantly increased by 140.30% and 81.77%, respectively, compared with those of the CK (p < 0.001), and were also higher than those of the other treatments in both cases. As the concentration of applied biochar increased, the percentages of F1 and F2 REEs in the soil gradually decreased, whereas the percentages of F3 and F4 increased concomitantly. Furthermore, the combined percentage of F3 + F4 was highest in the BC5 treatments.

3.3. Changes in Physicochemical Properties and Enzyme Activities of the Soil After Application of REE-Rich Biochar

According to Figure 4, the application of REE-rich biochar improved soil acidification and nutrients. Soil pH, TOC, TP, AP, and AK under the application of REE-rich biochar treatment were elevated by 4.18–6.42%, 13.15–229.11%, 12.02–55.61%, 3.67–46.79%, and 6.40–159.42%, respectively, compared to those of the CK treatment, whereas the soil TN, TK, and AN showed a decreasing trend, followed by an increase with an increase in biochar application. Decreasing and then increasing trends were observed with an increase in biochar application, in which the BC5 treatment significantly increased the soil pH, total nitrogen, total potassium, and quick-acting nitrogen content by 6.42%, 53.92%, 55.50%, and 14.76%, respectively, compared with CK (p < 0.05), and were also higher than the other treatments where biochar was applied.
The application of REE-rich biochar altered soil enzyme activities to varying degrees (Figure 5). As the amount of biochar used increases, the activities of three enzymes, BG, CBH, and NAG, showed a general trend of increasing, while the activity of LAP showed a downward and then upward trend. Among them, the activities of the five enzymes were significantly increased by 14.23%, 15.77%, 19.89%, 10.13% and 31.21% under BC5 treatment compared to the CK treatment (p < 0.05).In addition, all of them were higher than the other biochar treatments.

3.4. Changes in Soil Microbial Diversity After Application of REE-Rich Biochar

3.4.1. OTU Analysis of Soil Microorganisms

The total number of bacterial OTUs was 5787, while the number of fungal OTUs was 2081. The number of bacterial OTUs per treatment was: 106 (CK), 103 (BC1), 112 (BC3), and 155 (BC5). For fungal OTUs, the counts were as follows: 122 (CK), 138 (BC1), 229 (BC3), and 273 (BC5). A clear distinction in community species was observed between the treatments for both bacteria and fungi. The number of bacterial cooccurrences varied from 21 to 32 times the number of uniquely amplified sequences, while the number of fungal occurrences ranged from 1 to 4. These results suggest that the application of REE-rich biochar enhances the number of shared species in the microbial communities in the soils from the pomelo plantation area (Figure 6).

3.4.2. Analysis of Alpha Diversity of Soil Microorganisms

As shown in Table 5, the implementation of REE-rich biochar resulted in various effects on soil microbial diversity. For fungi, the Chao1 index was significantly increased by 52.67% (p < 0.05) under the BC5 treatment compared to the CK treatment and was also significantly higher (p < 0.05) than the other treatments. The highest Shannon index was recorded under the BC3 treatment, which increased significantly by 17.59% and 19.36% (p < 0.05) compared to CK and BC1 treatments, respectively.

3.4.3. Analysis of Soil Microbial Community Structure

The top ten microbial communities with the highest relative abundance in the four treatments, categorized by phylum, were as follows (Figure 7). Among the bacterial phyla with a relative abundance > 10%, Proteobacteria, Acidobacteria, Actinobacteriota, and Chloroflexi were the dominant phyla in all treatments. The relative abundance of Proteobacteria showed an increasing and then decreasing trend with the increase of REE-rich biochar dosage. Conversely, the relative abundance of Acidobacteria exhibited a declining trend, followed by an ascending trend, in response to the augmentation of REE-rich biochar application. In terms of the fungal community composition, Ascomycota was the dominant phylum in all treatments. With the increasing application of REE-rich biochar, the relative abundance of Ascomycetes exhibited a decreasing-then-increasing trend. The fungi species with undetermined taxonomic affiliation accounted for 11.09% to 21.20%. These results indicate that at the phylum level, the dominant soil flora showed a high degree of similarity among treatments. However, there are large differences in relative abundance.

3.5. Migration Risk of REE-Rich Biochar

Figure 8 shows the mobility characteristics of the REE content in REE-rich biochar. During the leaching of the soil column, the concentrations of REEs in the biochar-added treatment showed a decreasing trend and leveling-off trend with time, indicating that the REEs in biochar were released at a slow and low rate. In general, the REE content in the leaching solution of the soil column in all experimental groups showed a trend of increasing and then decreasing with soil depth. In addition, there was a significant difference in the REE content of the soil column drench solution among the four treatment groups at different soil column depths; the CK and BC1 treatment groups had the highest REE content in the drench solution in the 5–10 cm soil layer, whereas the BC3 and BC5 treatments had the highest REE content in the drench solution in the 10–15 cm soil layer.

3.6. Coupling of Soil Environmental Factors with Microbial Community Structure

To analyze the interactions between soil quality factors and their relationships with the indicators of microbial community richness and diversity, Mantel analyses of soil environmental factors and indicators of microbial richness and diversity were performed (Figure 9). The results showed that soil LREEs and HREE contents were positively correlated (Pearson’s r > 0.5) with soil TOC, TN, TP, TK, AK, BG, and NAG, indicating a close relationship between soil REEs and soil nutrient content. The bacterial Chao1 index was significantly positively correlated with soil TOC, TP, AP, AK, NAG, LREEs, and HREEs, whereas the Shannon index was significantly and positively correlated with soil pH. Furthermore, there was also a significant positive correlation between the fungus Shannon index and soil LAP.
Figure 10 shows the redundancy analysis (RDA) of the top ten microbial phyla in terms of their abundance and soil quality factors. The Proteobacteria phylum was positively correlated with AP and CBH. Acidobacteriota, Actinobacteriota, Chloroflexi, Gemmatimonadota, Bacteroidota, Firmicutes, Cyanobacteria, Myxococcota, and Verrucomicrobiota were positively correlated with pH, TOC, TN, TP, TK, AN, AP, AK, BG, CBH, NAG, LAP, ALP, LREEs, and HREEs. Ascomycota was positively correlated with pH and AN. The Basidiomycota, Chytridiomycota, Rozellomycota, Mortierellomycota, Aphelidiomycota, Glomeromycota, Zoopagomycota, and Kickxellomycota were positively correlated with TOC, TN, TP, TK, AN, AP, AK, BG, CBH, NAG, LAP, ALP, LREEs, and HREEs. From the RDA, it can be seen that pH has the greatest influence on bacteria in the environment and a greater influence on the presence of fungi in the environment. In summary, the dominant populations of soil microorganisms are significantly correlated with soil chemical properties, and changes in the microbial community structure drive changes in soil chemical properties.

4. Discussion

4.1. Effects of REE-Rich Biochar Application on REE Content and Chemical Speciation of the Soil

In this study, it was found that the morphology of REEs in the soil changed significantly with increasing biochar application. When the concentration of biochar application was gradually increased, the proportion of acidizable (F1) + reducible (F2) states of REEs in soil gradually decreased, while the proportion of oxidizable (F3) + residual (F4) states showed the opposite trend, which was similar to the results reported by Li et al. [24]. This may be because biochar ash contains potassium, calcium, magnesium, and other mineral elements, as well as hydroxides and carbonates which, when applied to soil, can improve soil acidity and increase soil pH [25]. As the amount of applied biochar increased, the soil pH also increased, the negative charge carried on the surface of soil particles increased, and the adsorption and immobilization of cations were enhanced [26]. REEs, as soil cations, are more easily immobilized by soil particles in alkaline soils, which convert the REEs from a more active form to a more stable form. Furthermore, because the surface of biochar is rich in functional groups and active sites [27], it can chemically react with REEs after being applied to the soil to form stable compounds that are not easily broken down and released into the soil, thereby reducing the activity of REEs [28].

4.2. Effect of REE-Rich Biochar Application on Physicochemical Properties of the Soil

The present study demonstrated that REE-rich biochar fortified can enhance soil physicochemical properties. Soil pH, TN, and AN content were highest in the BC5 treatment, suggesting that the addition of high concentrations of REE-rich biochar is more suitable for improving the soil environment than the addition of low concentrations of REE-rich biochar, which is in line with the results reported by Liu et al. [29]. The reason for this may be that biochar itself is rich in organic matter and mineral elements, which can directly increase soil nutrient levels when applied to the soil [30]. Simultaneously, because it has a complex void structure and strong adsorption capacity [27], biochar can help reduce soil nutrient loss and effectively conserve nutrients. Notably, the soil TN, TK, and AN content tended to decrease and then increase with increasing biochar application, similar to the findings reported by Xie et al. [31]. This phenomenon may be associated with the impact of biochar on soil microbial activity. In the early stages of biochar implementation, soil microorganisms may need to adapt to new environmental conditions [32], resulting in a temporary decrease in microbial activity, which in turn affects the conversion and release of soil nutrients. As microorganisms gradually adapt to and utilize the nutrients provided by biochar, their activities gradually recover and increase, promoting the process of nutrient transformation and release in the soil [33]. Soil enzymes are important biocatalysts in soil ecosystems and are involved in a variety of biogeochemical cycling processes, including microbial decomposition of organic matter, nutrient cycling, and the transformation of organic/inorganic compounds [34]. Our study found that the application of REE-rich biochar altered the soil enzyme activity to varying degrees. In this study, the activities of β-glucosidase, cellobiose hydrolase, β-N-acetylaminoglucosidase, leucine aminopeptidase, and other enzymes, in general, showed a gradual increase with increasing biochar application concentration compared to the CK treatment. All enzymes showed their highest activity in the BC5 treatment, indicating that a higher concentration of biochar addition was more conducive to increasing soil enzyme activities, which is consistent with the research results reported by Jin et al. [35]. This may be because biochar provides more habitats and reaction substrates for soil microbial metabolism and activities [36], which promotes microbial growth and reproduction, leading to an increase in microbial biomass and, thus, higher enzyme activities, which are closely related to microbial activity.

4.3. Effects of REE-Rich Biochar Application on the Soil Microbial Community

In this study, there were significant differences in the species richness and diversity of soil bacterial communities in response to the addition of REE-rich biochar, with the bacterial Chao1 and Shannon indices being higher under the BC5 treatment than under the other treatments. Wang et al. [37] suggested that the diversity of microbial communities can directly influence the stability of soil ecosystems, and a decrease in microbial community diversity due to a decrease in soil quality and vice versa, which is similar to the results of this study. This may be because higher concentrations of biochar amendment can provide richer nutrients for microorganisms and sufficient energy for microbial growth [38], resulting in higher numbers of specific bacterial taxa in the soil compared to other treatments. In addition, the results of the Mantel analysis in this study showed that the nutrient contents of soil TOC, TP, AP, and AK, as well as the enzyme activities of BG and NAG, were significantly and positively correlated with the bacterial Chao1 index (Pearson’s r > 0.5), soil pH was significantly and positively correlated with the bacterial Shannon index (Pearson’s r > 0.5), and soil LAP activity was significantly and positively correlated with the fungal Chao1 index (Pearson’s r > 0.5), similar to those of Liu et al. [39]. This may be because rare earth element-rich biochar improves microbial growth by improving soil properties that are critical for microbial growth, which enhances positive interactions among soil microorganisms, improves the response of the soil microbial network to adverse external conditions, and increases microbial adaptability to the environment [40].
In this study, we also found that Proteobacteria, Acidobacteria, and Actinobacteriota were the dominant phyla in the bacterial community at the phylum classification level in all treatments; however, their relative abundances showed different trends with increasing biochar application, which was similar to the results reported by Chen et al. [41], indicating that these bacterial taxa have a strong ability to survive and adapt to environmental changes. In addition, the highest relative abundance of Ascomycetes was found in the BC3 treatment, followed by the BC5 treatment, suggesting that Ascomycetes prefer to live in eutrophic environments. Notably, the relative abundance of the Actinobacteria phylum was higher under all CK treatments compared to the other biochar treatments, which is consistent with the findings of Yao et al. [42]. The reason for this may be because biochar application increased the abundance of Ascomycetes and Acidobacteria phylum in the soil. Meanwhile, there is an interaction between Actinobacteria phylum and other phylum competing for resources [43], and the increased abundance of Ascomycetes and Acidobacteria phylum occupies more resources and limits the growth and reproduction of other taxa [44]. For fungi, Ascomycota was the dominant taxon in all the treatments; however, its relative abundance was higher in the CK treatment compared to the other biochar-amended treatments. Biochar application has been shown to significantly reduce the relative abundance of ascomycetes in soil [45], which may be due to the high levels of minerals (K+, Ca2+, Mg2+, etc.) in biochar, or the ability of specific organic compounds in biochar to chemically react with the soil, which can inhibit the growth of certain fungi [46]. Furthermore, the findings of the redundancy analysis indicated that the environmental factor exerting the most significant influence on the proliferation of bacterial and fungal communities was pH. It has been shown that soil physicochemical factors, such as pH, can alter the structure of soil microbial communities by affecting the physiological metabolism of soil microorganisms, altering the competitive relationship between microbial communities, or inhibiting the growth of non-adapted microorganisms [47]. Bacterial and fungal groups that are more adapted to, or prefer, this type of environment may become more competitive for survival in the soil, being able to grow and reproduce better. Simultaneously, the ecological niche width of microbial taxa that are not well adapted to changes in the soil environment shrinks, and the abundance of taxa gradually decreases or even declines [48].

4.4. REE-Rich Biochar Migration Risk and Environmental Applicability

Although REEs have important effects on plant growth and soil ecosystems, their excessive accumulation poses potential risks to the environment and human health [49]. Therefore, when using REE-rich biochar for agricultural production, changes in the content and form of REEs and their potential impacts on the environment and human health must be considered. In our experiments, the average levels of REEs in the soil column leachate at 1%, 3%, and 5% REE-rich biochar additions were 0.21 mg kg−1, 0.39 mg kg−1, and 0.52 mg kg−1, respectively, all of which are well below the clinically harmful intake of REEs in adults (6.0–6.7 mg kg−1) [50] and would not pose a risk to human health. After leaching, the leachate from the BC3 treatment had the highest REE content in the 10–15 cm layer, reaching 199.96 mg kg−1. A comparison of the rare earth content with the background value in Fujian Province (223.47 mg kg−1) reveals a disparity [51], indicating that the application of REE-rich biochar would not cause soil REE pollution. Furthermore, the total REE (LREE+HREE) content in soil was found to be greatest in the BC5 treatment, at 66.48 mg kg−1. This value was also found to be lower than the background value of soil REE content in Fujian Province. These results show that the application of REE-rich biochar to the environment does not result in REE contamination in the soil, although it can increase the levels of REEs in the environment. This study also found that with the increase in biochar application, the soil REE form gradually changed from a form that could be easily absorbed by the environment (F1 + F2) to a stable form that could not be easily moved in the environment (F3 + F4), which confirms the safety of the REE-rich biochar.
As a new type of functional biochar material, REE-rich biochar has broad application prospects in agricultural production [24]. This study found that REE-rich biochar could significantly improve soil quality, increase soil enzyme activity, and promote the diversity and stability of soil microbial communities, thus providing a more favorable soil environment for the growth of pomelo. These results strongly support the use of REE-rich biochar in agricultural production. However, the application of REE-rich biochar in agricultural production faces several challenges. For example, biochar is relatively expensive to produce, and feedstock sources are limited. This limits large-scale production and the widespread use of biochar. In the future, there is a need to develop more economical and efficient methods for biochar preparation and feedstock sources to reduce production costs and expand its range of applications. This study has some limitations. First, this study preliminarily investigated the improvement of soil in the pomelo plantation after the addition of REE-rich biochar but did not address the growth and quality of pomelo trees. Second, this study was carried out at the pot experiment stage and was not conducted in a field. To this end, we conducted field experiments with REE-rich biochar. We monitored and measured the key growth parameters and quality indicators of pomelo to further enhance the utility of REE-rich biochar for ecological restoration.

5. Conclusions

We analyzed the effects of applying different concentrations of biochar enriched with rare earth elements on soil quality and soil microbial community characteristics of the ‘Guanximiyou’ pomelo plantation through a 90-day experiment. The results showed that the application of 5% REE-rich biochar significantly increased the REE content in the soil, altered the chemical speciation of REEs from weakly acid-soluble and reducible states to oxidizable and residual states, and reduced the bioavailability of REEs in the environment, which would not cause REE pollution. In addition, the soil physicochemical properties, nutrient content, and enzyme activity improved after the application of 5% REE-rich biochar. In terms of the microbial community, the application of 5% REE-rich biochar significantly increased the community richness and diversity and changed the dominant populations of bacteria and fungi. Mantel and RDA analyses showed that the soil microbial community structure was significantly correlated with physicochemical properties, suggesting that biochar indirectly influences microbial communities by regulating the soil environment. These results demonstrate that REE-rich biochar can be used as a soil amendment without negative environmental impacts. Our study offers a novel approach for avoiding secondary environmental pollution from the REEs in the waste D. pedata biomass but also facilitates the reuse of REEs and biochar resources. At the same time, this study also provides a new idea for future resource recycling in the mine reclamation industry.

Author Contributions

Conceptualization: Z.C. (Zhiqiang Chen) and Z.C. (Zhibiao Chen); methodology: Z.C. (Zhiqi Chen), L.F. and Z.C. (Zhiqiang Chen); formal analysis: Z.C. (Zhiqi Chen), L.F., and Z.C. (Zhiqiang Chen); investigation: Z.C. (Zhiqi Chen), L.F., Z.C. (Zhiqiang Chen), and J.W.; resources: Z.C. (Zhiqiang Chen) and Z.C. (Zhibiao Chen); data curation: Z.C. (Zhiqi Chen), L.F., Z.C. (Zhiqiang Chen), and J.W.; writing—original draft preparation: Z.C. (Zhiqi Chen) and L.F.; writing—review and editing: Z.C. (Zhiqiang Chen) and Z.C. (Zhibiao Chen); supervision: Z.C. (Zhiqiang Chen), Z.C. (Zhibiao Chen), and Q.L.; project administration: J.W. and Q.L.; funding acquisition: Z.C. (Zhiqiang Chen) and Z.C. (Zhibiao Chen). All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Water Conservancy Science and Technology Project of Fujian (grant number MSK202435, grant number MSK202433, grant number MSK202208) and the Soil and Water Conservation Experiment Station Horizontal Fund of Fujian (grant name: Construction of a SWAT Model and Evaluation of the Effectiveness of Soil Erosion Management in Typical Ecologically Clean Subwatersheds in Red Soil Erosion Areas).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The original contributions presented in this 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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Figure 1. SEM-EDS analysis of biochar: (A) SEM image showing the surface morphology, (B) EDS spectrum displaying the elemental composition.
Figure 1. SEM-EDS analysis of biochar: (A) SEM image showing the surface morphology, (B) EDS spectrum displaying the elemental composition.
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Figure 2. Biochar characterization: (A) FTIR spectrum showing functional groups, (B) XRD pattern indicating crystalline structure, and (C) zeta potential as a function of pH.
Figure 2. Biochar characterization: (A) FTIR spectrum showing functional groups, (B) XRD pattern indicating crystalline structure, and (C) zeta potential as a function of pH.
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Figure 3. Soil REE content and forms under different treatments: (A) light/heavy REE content; (B) REE form. Note: error bars indicate standard deviations (n = 3); the asterisk denotes statistically significant differences, *** p < 0.001. A similar pattern is observed below.
Figure 3. Soil REE content and forms under different treatments: (A) light/heavy REE content; (B) REE form. Note: error bars indicate standard deviations (n = 3); the asterisk denotes statistically significant differences, *** p < 0.001. A similar pattern is observed below.
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Figure 4. (A) pH; (B) TOC; (C) TN; (D) TP; (E) TK; (F) AN; (G) A; and (H) AK under different treatments. Note: the asterisk denotes statistically significant differences, * p < 0.05; ** p < 0.01; *** p < 0.001.
Figure 4. (A) pH; (B) TOC; (C) TN; (D) TP; (E) TK; (F) AN; (G) A; and (H) AK under different treatments. Note: the asterisk denotes statistically significant differences, * p < 0.05; ** p < 0.01; *** p < 0.001.
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Figure 5. Soil enzyme activity under different treatments: (A) BG; (B) CBH; (C) NAG; (D) LAP; and (E) ALP. Note: the asterisk denotes statistically significant differences, * p < 0.05; ** p < 0.01.
Figure 5. Soil enzyme activity under different treatments: (A) BG; (B) CBH; (C) NAG; (D) LAP; and (E) ALP. Note: the asterisk denotes statistically significant differences, * p < 0.05; ** p < 0.01.
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Figure 6. Petal diagram of soil microbial operational taxonomic units (OTUs) of (A) bacteria and (B) fungi.
Figure 6. Petal diagram of soil microbial operational taxonomic units (OTUs) of (A) bacteria and (B) fungi.
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Figure 7. (A) Bacterial and (B) fungal microbial communities at the phylum level under the different treatments.
Figure 7. (A) Bacterial and (B) fungal microbial communities at the phylum level under the different treatments.
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Figure 8. Variation in REE content over time in the soil column leaching solution under different biochar addition treatments (A) and variation in REE content in soil column depth after leaching (B).
Figure 8. Variation in REE content over time in the soil column leaching solution under different biochar addition treatments (A) and variation in REE content in soil column depth after leaching (B).
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Figure 9. The Mantel test revealed the relationship between the richness and diversity of (A) bacteria and (B) fungi and the measurement parameters. Note: the asterisk denotes statistically significant differences, * p < 0.05; ** p < 0.01; *** p < 0.001.
Figure 9. The Mantel test revealed the relationship between the richness and diversity of (A) bacteria and (B) fungi and the measurement parameters. Note: the asterisk denotes statistically significant differences, * p < 0.05; ** p < 0.01; *** p < 0.001.
Agriculture 15 00895 g009
Agriculture 15 00895 g010
Figure 10. RDA analysis of (A) bacteria and (B) fungi at phylum level abundance and environmental variables. Note: E1, pH; E2, TOC; E3, TN; E4, TP; E5, TK; E6, AN; E7, AP; E8, AK; E9, BG; E10, CBH; E11, NAG; E12, LAP; E13, ALP; E14, LREEs; E15, HREEs. BP1, Proteobacteria; BP2, Acidobacteriota; BP3, Actinobacteriota; BP4, Chloroflexi; BP5, Gemmatimonadota; BP6, Bacteroidota; BP7, Firmicutes; BP8, Cyanobacteria; BP9, Myxococcota; BP10, Verrucomicrobiota. FP1, Ascomycota; FP2, unidentified; FP3, Basidiomycota; FP4, Chytridiomycota; FP5, Rozellomycota; FP6, Mortierellomycota; FP7, Aphelidiomycota; FP8, Glomeromycota; FP9, Zoopagomycota; FP10, Kickxellomycota.
Figure 10. RDA analysis of (A) bacteria and (B) fungi at phylum level abundance and environmental variables. Note: E1, pH; E2, TOC; E3, TN; E4, TP; E5, TK; E6, AN; E7, AP; E8, AK; E9, BG; E10, CBH; E11, NAG; E12, LAP; E13, ALP; E14, LREEs; E15, HREEs. BP1, Proteobacteria; BP2, Acidobacteriota; BP3, Actinobacteriota; BP4, Chloroflexi; BP5, Gemmatimonadota; BP6, Bacteroidota; BP7, Firmicutes; BP8, Cyanobacteria; BP9, Myxococcota; BP10, Verrucomicrobiota. FP1, Ascomycota; FP2, unidentified; FP3, Basidiomycota; FP4, Chytridiomycota; FP5, Rozellomycota; FP6, Mortierellomycota; FP7, Aphelidiomycota; FP8, Glomeromycota; FP9, Zoopagomycota; FP10, Kickxellomycota.
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Table 1. Rare earth element content before and after preparation.
Table 1. Rare earth element content before and after preparation.
REE Content of D. pedata and Carbonized MaterialIndexContent
REEs (mg kg−1)D. pedataLight REEs3232.42
Heavy REEs136.41
Total REEs3368.83
REE-rich biocharLight REEs4419.53
Heavy REEs173.78
Total REEs4593.31
Table 2. Basic chemical properties of the soil in the pomelo plantation area.
Table 2. Basic chemical properties of the soil in the pomelo plantation area.
Basic Chemical Properties of SoilIndexContent
Chemical propertiespH5.61
Total organic carbon (TOC, g kg−1)23.14
Total nitrogen (TN, g kg−1)1.13
Total phosphorus (TP, g kg−1)0.97
Total potassium (TK, g kg−1)197.81
Available nitrogen (AN, g kg−1)0.24
Available potassium (AK, g kg−1)375.84
REEsLight REEs(LREEs, mg kg−1)17.54
Heavy REEs(HREEs, mg kg−1)14.37
Total REEs(TREEs, mg kg−1)31.91
Table 3. BCR sequential extraction procedure.
Table 3. BCR sequential extraction procedure.
FractionExtraction Method
F10.5 g soil sample + 20 mL CH3COOH (0.11 mol L−1), shaken for 16 h (25 °C, 180 rpm) and filtration.
F2F1 residue + 20 mL NH2OH HCl (0.5 M, pH 1.5), shaken for 16 h (25 °C, 180 rpm) and filtration.
F3F2 residue + 5 mL H2O2 (30%, pH 2–3), shaken for 1 h (25 °C) and placed in a water bath for 1 h (85 °C). When the solution was reduced to 1–2 mL, 5 mL of H2O2 was added again and heated at 85 °C to near dryness. After cooling, 25 mL of 1 mol L−1 NH4Ac (pH 2) was added and shaken for 16 h (25 °C, 180 rpm), followed by filtration.
F4F3 residue was dried and digested with HF-HCl-HNO3 (v/v/v = 1:3:1).
Table 4. Basic physicochemical properties of biochar.
Table 4. Basic physicochemical properties of biochar.
BiocharMass percentage of elements/(%)Surface area
/(m2 g−1)		Pore size
/(nm)		Pore volume
/(cm3 g−1)
CHN
72.870.740.61439.481.710.19
Table 5. α-diversity indexes of bacteria and fungi for different treatments of biochar.
Table 5. α-diversity indexes of bacteria and fungi for different treatments of biochar.
MicroorganismTreatmentsChao1 IndexShannon Index
BacteriaCK4571.63 ± 34.94 a10.21 ± 0.11 a
BC14623.78 ± 123.19 a9.92 ± 0.27 a
BC34531.01 ± 70.13 a9.90 ± 0.07 a
BC54788.11 ± 80.11 a10.35 ± 0.05 a
FungiCK784.62 ± 25.01 b5.40 ± 0.20 bc
BC1776.94 ± 50.85 b5.32 ± 0.35 c
BC3774.10 ± 21.75 b6.35 ± 0.28 a
BC51197.87 ± 60.30 a6.01 ± 0.40 ab
Note: Different lowercase letters indicate the significant differences (p < 0.05).
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Chen, Z.; Feng, L.; Chen, Z.; Chen, Z.; Wu, J.; Lin, Q. Effects of Rare Earth Element-Rich Biochar on Soil Quality and Microbial Community Dynamics of Citrus grandis (L.) Osbeck. cv. Guanximiyou. Agriculture 2025, 15, 895. https://doi.org/10.3390/agriculture15080895

AMA Style

Chen Z, Feng L, Chen Z, Chen Z, Wu J, Lin Q. Effects of Rare Earth Element-Rich Biochar on Soil Quality and Microbial Community Dynamics of Citrus grandis (L.) Osbeck. cv. Guanximiyou. Agriculture. 2025; 15(8):895. https://doi.org/10.3390/agriculture15080895

Chicago/Turabian Style

Chen, Zhiqi, Liujun Feng, Zhiqiang Chen, Zhibiao Chen, Jie Wu, and Qiang Lin. 2025. "Effects of Rare Earth Element-Rich Biochar on Soil Quality and Microbial Community Dynamics of Citrus grandis (L.) Osbeck. cv. Guanximiyou" Agriculture 15, no. 8: 895. https://doi.org/10.3390/agriculture15080895

APA Style

Chen, Z., Feng, L., Chen, Z., Chen, Z., Wu, J., & Lin, Q. (2025). Effects of Rare Earth Element-Rich Biochar on Soil Quality and Microbial Community Dynamics of Citrus grandis (L.) Osbeck. cv. Guanximiyou. Agriculture, 15(8), 895. https://doi.org/10.3390/agriculture15080895

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