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Article

Asynchronous Synergetic Remediation Strategy for Cd-Contaminated Soil via Passivation and Phytoremediation Technology

by
Jian Cao
1,2,
Chenyang Lv
1,2,
Chenxu Zhang
1,2,
Fengxiang Yin
1,2,
Zhengbo Gao
3,
Long Wei
4 and
Lichang Wang
4,*
1
School of Minerals Processing and Bioengineering, Central South University, Changsha 410083, China
2
Key Laboratory of Hunan Province for Clean and Efficient Utilization of Strategic Calcium-Containing Mineral Resources, Central South University, Changsha 410083, China
3
School of Marxism, Central South University, Changsha 410083, China
4
School of Geosciences and Info-Physics, Central South University, Changsha 410083, China
*
Author to whom correspondence should be addressed.
Agronomy 2024, 14(9), 1913; https://doi.org/10.3390/agronomy14091913
Submission received: 13 July 2024 / Revised: 21 August 2024 / Accepted: 23 August 2024 / Published: 26 August 2024
(This article belongs to the Section Agroecology Innovation: Achieving System Resilience)
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Abstract

:
Cadmium (Cd) contamination in soil has emerged as a significant challenge for agricultural production. Phytoremediation and passivation are key techniques for remediating Cd-contaminated soil. However, few studies have focused on the synergistic effects of these two techniques. In this work, the effectiveness of synergetic remediation strategies, both synchronous and asynchronous, utilizing passivation and phytoremediation techniques, was explored. The results of pot experiments and field experiments indicated that optimal remediation effects were obtained by asynchronous synergetic remediation, removing over 80% of bioavailable Cd within 14 days. Mechanistic studies conducted using XPS analysis, soil property analysis, and microbial diversity analysis confirmed that the chelation effect of SDD and soil pH value are the primary factors contributing to the effectiveness of both remediation strategies. In contrast, the variations in microbial populations are identified as the crucial factors influencing the varying outcomes of the two sequential remediation approaches. This research demonstrates that asynchronous synergistic remediation is a promising strategy for mitigating Cd contamination in soil.

1. Introduction

In recent years, the rapid development of industrial activities has exacerbated heavy metal contamination in soil [1,2]. Cadmium, a highly toxic and mobile heavy metal, poses a serious threat to both human health and the ecological environment [2,3]. Hunan Province is the “Land of Nonferrous Metals” in China, while the agricultural region adjoining Dongting Lake in Hunan Province is renowned as the “Land of Fish and Rice”. However, the “Land of Fish and Rice” faces severe heavy metal pollution due to mining, beneficiation, and metallurgical activities. As a result, the Cd levels in crops such as rice and vegetables surpass safety standards [4,5]. At present, an effective and environmentally friendly remediation technique is urgently required to support the agricultural production of the “Land of Fish and Rice”.
Among various soil remediation strategies, phytoremediation is a promising technology developed in the past thirty years [6]. The main process of phytoextraction contains five steps: metal mobilization in the rhizosphere, metal ion uptake by plant roots, translocation towards aerial plant parts, metal sequestration in plant tissues, and heavy metal tolerance [7]. Admittedly, phytoremediation technology has the advantages of remediation cost, ecological safety, and environmental friendliness. However, the imperfections of phytoremediation technology are also obvious: a lengthy remediation cycle and limited effectiveness [8].
Currently, the synergetic remediation strategy exhibits superiority in the field of soil remediation. Through integrating multiple remediation technologies and optimizing synergistic effects, synergetic remediation enhances the stability and effectiveness of remediation effects [9,10]. For a better development of phytoremediation, the synergy of phytoremediation with passivation technology has emerged as a feasible approach. The addition of a passivator could rapidly decrease the bioavailable Cd content in soil and promote plant growth [11]. Therefore, utilization of synergistic interactions between passivators and plants can further elevate the remediation of Cd [10,12].
Until now, a considerable number of studies have focused on the remediation of Cd-contaminated soils by using the synergy of passivation and phytoremediation technology, but there has been no general agreement on the sequence of passivation and phytoremediation technology. Gasco proved that remediation of Cd-contaminated soil could be improved by using passivation and phytoremediation technology synchronously. The critical point lay in the fact that the extraction ability of plant roots (Brassica napus) towards Cd was enhanced by the synergistic effect of biochar [12]. On the other hand, remediation effects could also be improved by using passivation and phytoremediation technology asynchronously. Wang Yale et al. reported that employing an asynchronous synergetic remediation technology could significantly decrease bioavailable Cd levels and toxicity leaching rates [13]. In this case, phytoremediation (Tagetes patula L.) was conducted prior to the use of passivation technology (mercapto-palygorskite was used as the optimized passivator). Although both synchronous and asynchronous synergetic remediation have been studied, there is limited research targeting the different remediation effects caused by different sequences.
This study specifically focuses on the synergetic remediation effect of an optimized passivator and native plants in two different sequences (synchronous and asynchronous). The optimized synergetic remediation strategy was applied in the agricultural region adjoining Dongting Lake in Hunan Province, and a significant reduction in bioavailable Cd confirmed the potential application value of the synergetic remediation strategy.

2. Materials and Methods

2.1. Materials and Medicines

Hydroxyapatite (80 μm, Shanghai, China), 18-Crown-6 (≥99% purity, Shanghai, China), calcium phosphate monobasic (≥95% purity, Shanghai, China), ammonium dihydrogen phosphate (analytical grade, Shanghai, China), sodium dimethyldithiocarbamate (SDD) (≥95% purity, Shanghai, China), and Cd chloride hemi (pentahydrate) (≥98% purity, Shanghai, China) were purchased from Shanghai Maclin Biochemical Co., Ltd., Shanghai, China. The required plants (Tagetes patula L., Cynodon dactylon, and Bidenspilosa L.) were obtained by germinating seeds of uniform size and fullness and raising seedlings in a greenhouse with natural light, day and night temperatures of 28/21 °C, and humidity of 73/86%. The seeds were germinated and grown in a clean sand bed for two weeks. Then, ten seedlings of similar size were transplanted into a flowerpot. Deionized water was used to prepare samples and solutions.

2.2. Soil Sample Preparation

The uncontaminated soil used in the experiments was sourced from a vegetable greenhouse in Changsha City, Hunan Province, China (28°04′41.2″ N, 112°57′02.0″ E), air-dried, and sieved to below 20 mesh for further use. The physicochemical properties of the manually contaminated soil used in this study are summarized in Table 1.
The preparation method for the Cd-contaminated soil samples was as follows: the air-dried soil was mixed with a corresponding volume of Cd chloride hemi(pentahydrate) solution to prepare the Cd-contaminated soil samples, which were then sealed at room temperature for 10 days. The bioavailable Cd content in the soil was determined to be 2.54 mg/kg. According to the agricultural soil pollution risk control standards, the soil heavy metal content indicator (Cd) exceeded the national soil safety standard. The soil was used to simulate the cadmium-contaminated soil in the farming area of Dongting Lake, Hunan Province, China.

2.3. Experimental Design

2.3.1. Plant Screening Experiment

In this study, a plant screening experiment was initially conducted using Cd-contaminated soil (2.54 mg/kg). Tagetes patula L., Cynodon dactylon, and Bidenspilosa L. were planted in 10 cm × 10 cm pots (each containing 400 g of soil) for 45 days to select the most bioavailable Cd-accumulating plants. The soil was preserved, and the experiment was repeated three times. All the following pot experiments were carried out in a greenhouse with natural light, day and night temperatures of 28/21 °C, and humidity of 73/86%. At the same time, the soil water content was maintained at about 5 % of the field capacity by regularly weighing the flowerpots and adding deionized water when necessary.

2.3.2. Passivator Screening Experiment and Dosage Conditions Experiment

In the simulated contaminated soil, 18-Crown-6, hydroxyapatite, calcium dihydrogen phosphate, ammonium dihydrogen phosphate, and SDD were applied at a concentration of 0.5%. The CK received no passivator. Soil samples were collected on days 14, 28, and 32, with each experimental setup replicated three times to identify the most effective passivator. Subsequently, a dosage experiment was conducted using the optimal passivator. A series of passivator dosage gradients (0%, 1%, 2%, 3%, 4%, and 5 %) were set with the simulated contaminated soil to determine the optimal passivator dosage. The soil was preserved, and the experiment was repeated three times.

2.3.3. Impact of Passivators on Plant Growth in Cd-Contaminated Soil

To the simulated contaminated soil, according to the previous passivator experiments, varying dosages of 0%, 1%, 2%, 3%, 4%, and 5% of SDD were added prior to the placement of selected Tagetes patula L. seedlings into pots for cultivation. The experiments were replicated three times. On the 42nd day, the Tagetes patula L. plants were harvested for subsequent analysis.

2.3.4. Synergetic Remediation Experiment

In Cd-contaminated soil with a concentration of 2.54 mg/kg, the optimal dosage of passivator (1%) and transplanted Cd-accumulating plants were added for synchronous and asynchronous synergetic remediation strategies. Sampling and analysis were performed on days 0, 14, 28, and 42 to compare the remediation effectiveness of the two strategies. Each experiment was conducted in triplicate to ensure reliability.

2.3.5. Field Remediation

The remediation area is located in the Zhongzhou Levee region along the banks of Dongting Lake in Yueyang County, Hunan Province, China, at 112°48′ east longitude and 29°25′ north latitude (Figure 1). This area experiences a subtropical monsoon climate characterized by hot summers, mild winters, and abundant, concentrated rainfall. Soil sampling revealed severe Cd contamination, with a bioavailable Cd concentration of 2.56 mg/kg. Synchronous and asynchronous synergetic remediation strategies were implemented in this area to evaluate their effectiveness in reducing bioavailable cadmium levels over time.

2.4. Analysis of Soil Samples

2.4.1. Determination of Bioavailable Cd

To determine the content of bioavailable Cd in the soil, 10 g of the soil sample was uniformly taken, air-dried, ground to particles smaller than 2.0 mm, and then added to a solution of diethylene triamine pentaacetic acid–calcium chloride–triethanolamine (DTPA-CaCl-TEA) buffer. The mixture was shaken at a constant temperature (25 °C, 250 r/min) for 2 h, centrifuged at 4000 r/min for 20 min, filtered through a 0.45 μm membrane into a 10 mL centrifuge tube, and stored at 4 °C until further analysis using ICP-MS (NEXION 2000, Parkin Elmer Healthy Technology Co., Ltd., Beijing, China) (HJ 804-2016) [15].

2.4.2. Determination of Cd Forms in Soil

To determine the forms of Cd in the soil, samples were uniformly collected and pre-dried at 60 °C for 2 h, then ground to a particle size of 100 μm. Following the sequential extraction procedure of speciation of 13 trace elements in soil and sediment (GB/T 25282-2010, China) [16], Cd forms, including weak acid-extractable, reducible, oxidizable, and residual fractions, were sequentially extracted [17,18]. The contents were measured by ICP-MS (NEXION 2000, Parkin Elmer Health Technology Co., Ltd., Beijing, China).

2.4.3. Soil Humus Content Measurement

To measure the humus content in soil, air-dried soil (10 g) was uniformly sampled and 0.1000 g to 0.5000 g (accurate to 0.0001 g) was weighed using a reduction method. The soil samples, sieved through a 0.149 mm mesh, were placed into a hard glass tube. Next, silver sulfate (0.1 g) was added, followed by 5.00 mL of 0.8000 mol/L potassium dichromate standard solution. Using a syringe, sulfuric acid (5 mL) was carefully added, and the mixture was gently swirled to ensure thorough mixing. Then, 3–4 drops of o-phenanthroline indicator were added. The mixture was titrated with 0.2 mol/L ammonium ferrous sulfate standard solution until the color of the solution changed from orange-yellow to blue-green and finally to reddish brown. The humus content was calculated based on the volume of the standard solution added. This procedure was performed according to standard operating procedure F-HZ-DZ-TR-0046 [19].

2.4.4. Soil Electrical Conductivity Measurement

The soil electrical conductivity was measured using the electrode method (HJ802-2016) [20]. A soil-to-water (m/V) ratio of 1:5 was employed. Specifically, soil was weighed and placed into a 250 mL oscillation bottle, to which water at 20 ± 1 °C was added. The bottle was tightly sealed and placed on a horizontal constant-temperature shaker and shaken for 30 min. After shaking, the bottle was allowed to stand for 30 min, then the mixture was filtered, and the filtrate was collected in a 100 mL beaker. The electrical conductivity of the filtrate was then measured using a conductivity meter (DDS-307, Qiwei Instrument Co., Ltd., Hangzhou, China).
For the determination of soil moisture content, aluminum sample boxes with lids were dried in an oven (202-00S, LICHEN, Shanghai, China) at 105 ± 5 °C, then cooled to room temperature in a desiccator and weighed (m0), accurate to 10 mg. Fresh soil samples weighing between 30 and 40 g were transferred to the aluminum boxes, and the combined weight of the covered box and soil was measured (m1), accurate to 10 mg. The boxes with the lids removed were placed in an oven at 105 ± 5 °C. After drying, the boxes were cooled in a desiccator to room temperature and weighed. This process was repeated (drying for an additional 2 h, cooling, and weighing) until a constant weight (m2) was achieved, accurate to 10 mg. The soil moisture content (%) was calculated using the following formula [21]:
Soil   Moisture   Content   ( % ) = m 1 − m 2 m 1 − m 0 × 100
For the determination of soil pH value, soil samples (10 g) were uniformly taken, air-dried, ground to a particle size smaller than 2.0 mm, and placed in a suitable container with 25 mL of potassium chloride solution. The container was sealed and shaken for 5 min, left to stand for 1 h, and soil pH was measured using the potentiometric method [22] (standard method: NY/T 1377-20, China) [23].

2.4.5. Soil X-ray Photoelectron Spectroscopy (XPS)

To investigate the mechanism of interaction between passivators and Cd, X-ray photoelectron spectroscopy (XPS; Thermo Fisher Scientific K-Alpha, Waltham, MA, USA) analysis was conducted to study the changes in the binding energy of Cd on the surface. The standard peak with a binding energy of 284.8 eV in the C1s spectrum was used for charge correction [24].

2.4.6. Analysis of Microbial Diversity in Soil

To investigate the microbial community composition under various co-remediation treatments, a UV spectrophotometer (NanoDrop NC2000, Thermo Fisher Scientific, Waltham, MA, USA) was used to sequence 16S rDNA amplicons to evaluate microbial diversity. The DNA samples were quantified using Nanodrop, and their quality was evaluated through 1.2% agarose gel electrophoresis [25]. PCR amplification was carried out using Pfu high-fidelity DNA polymerase from All-Style Gold, with a minimal number of cycles to maintain consistency across all samples [26]. The fluorescence of the PCR amplification products was quantified using the Quant-iT PicoGreen dsDNA Assay Kit and a microplate reader (BioTek, FLx800, Waltham, MA, USA), with the Quant-iT PicoGreen dsDNA Assay Kit (Thermo Fisher Scientific K-Alpha, Waltham, MA, USA) serving as the fluorescence reagent. Based on the fluorescence quantification results, the samples were mixed in the appropriate proportions required for sequencing. Sequencing libraries were prepared using Illumina’s TruSeq Nano DNA LT Library Prep Kit (Illumina, Beijing, China).

2.4.7. Data Analysis

In this study, all tests were carried out in triplicate to ensure reliable data. Statistical analysis of the data was performed using IBM SPSS Statistics 26 software. One-way analysis of variance (ANOVA) was used to compare the intergroup differences of different parameters, with significance set at p < 0.05. Post hoc analysis was conducted using Duncan’s test, and the results are indicated in figures and tables using letter notations.

3. Results and Discussion

3.1. Screening of Optimized Plants for Synergetic Remediation

Figure 2 illustrates the enrichment effect of different plants on the bioavailable Cd in soil. From the results, compared with CK, Tagetes patula L. and Bidenspilosa L. reduced the bioavailable Cd concentration in soil by 1.27 and 0.73 mg/kg, respectively, both exhibiting certain levels of bioavailable Cd uptake capacity from the soil. Nevertheless, the enrichment capability of Cynodon dactylon was almost negligible, which may be attributed to the inhibitory effect of the phytoextraction process caused by high Cd concentrations. Among three screened plants, Tagetes patula L. showed the best adsorption capacity for bioavailable Cd, leading to an obvious reduction rate of 50.4% (the bioavailable Cd concentration = 1.27 mg/kg). Moreover, due to its adaptability to various soil types, ease of cultivation, fast growth rate, early maturation, low nutrient requirements, tolerance to heavy metal stress, interactions with microorganisms, well-developed root system capable of secreting various root exudates, and ability to promote the biological transformation of Cd [27,28], Tagetes patula L. was chosen as the optimized plant for subsequent synergetic remediation processes.

3.2. Screening of Optimized Passivators for Combined Remediation

Figure 3 illustrates the passivation effects of five passivators (dosage = 0.5%) on bioavailable Cd in contaminated soil. It can be observed that at a 0.5% dosage, all five passivators exhibited enhanced passivation effects with increasing passivation time, leading to a reduction in bioavailable Cd concentration in the soil by 0.29–2.19 mg/kg. After 42 days of passivation, 18-Crown-6 was able to effectively reduce the bioavailable Cd content in the soil (0.29 mg/kg), possibly due to the formation of large chelate complexes with Cd ions facilitated by multiple ether bonds (-O-) in its structure [29]. On the 42nd day, hydroxyapatite, calcium phosphate monobasic, and ammonium dihydrogen phosphate successively decreased the bioavailable Cd content in the soil (the reduction rates were 31.75%, 47.62%, and 34.52%).
The key mechanisms include the following: 1. The substitution of Ca2+ in hydroxyapatite (HAP) with Cd2+ ions through exchange reactions, facilitating effective adsorption of divalent cations [30]. 2. The P-O/P=O groups in their structure can precipitate with Cd2+ ions, resulting in stable precipitation and decreased mobility [31,32,33,34,35]. Among five passivators, SDD exhibited the best passivation effect, showing a significant passivation effect after 14 days of remediation. On the 42nd day, SDD reduced the bioavailable Cd content in the soil by 2.19 mg/kg. This may be attributed to the chelating group dithiocarbamate (S=C-S-) in the SDD molecular structure, which can efficiently chelate Cd ions in the soil [36,37,38,39]. In order to facilitate subsequent synergetic remediation, SDD was screened as the optimized candidate passivator for synergetic remediation. Additionally, the effects of the dosage and passivation time of SDD on passivation efficacy were investigated.

3.2.1. Effect of SDD Dosage on Passivation Effect

The effect of SDD concentration (0%, 1%, 2%, 3%, 4%, and 5%) on the bioavailable Cd content in the soil over time is shown in Figure 3. It can be observed from Figure 4 that during the passivation process, the bioavailable Cd content in the soil significantly decreased with increasing SDD concentration. Additionally, with the increase in passivation time, the bioavailable Cd content in the soil decreased, especially at concentrations of 1%, 2%, and 3%, while at concentrations of 4% and 5%, the difference in the bioavailable Cd reduction rates between the two dosages (4% and 5%) was not significant (p < 0.05).
This may be due to the higher concentration of dithiocarbamate (S=C-S-) in the soil at higher concentrations, which provides more chelation sites for Cd2+ binding, leading to saturation. Furthermore, it can be observed from Figure 3 that after 14 days of passivation, a significant portion of Cd2+ in the soil was effectively passivated (bioavailable Cd content: 0.899–0.205 mg/kg). Currently, some common passivators (such as calcium magnesium phosphate and biochar) have been shown to effectively reduce the bioavailable Cd content in soil by 15.5% to 61.1% [40,41,42,43,44]. In comparison, SDD demonstrated a higher passivation efficiency, ranging from 64.3% to 91.9%. The high passivation efficiency of SDD in the remediation may be attributed to several factors: 1. The presence of the soft dithiocarbamate and the hard thioureide resonance forms (the latter resonance form is the outcome of delocalization of the nitrogen lone pairs onto the sulfur atom), which can stabilize Cd2+. 2. The presence of small bite angles in the dithiocarbamate moiety contributes to the stability of the chelating ligand [45].

3.2.2. Effect of SDD Dosage on the Fraction of Cd in Soil

Heavy metals in the soil are mainly categorized into four forms: exchangeable forms (EFs), reducible forms (RFs), oxidizable forms (OFs), and residual forms (ResFs). Each form plays a different role in the toxicity, migration, and natural circulation of metals in the environment [17,18]. When the external environment changes (such as the pH value, redox potential value, etc.), the exchangeable and reducible forms become more readily bioavailable for plant uptake. On the contrary, the oxidizable and residual forms behave oppositely [46]. Therefore, it is essential to evaluate the impact of passivators on the distribution of Cd forms in the soil.
Figure 5 displays the influence of different dosages of SDD (0, 1, 2, 3, 4, and 5 mg/kg) at various dosage on the form distribution of Cd. From Figure 5, it can be observed that at a dosage of 0, the EF, RF, OF, and ResF forms of Cd in the soil account for 3.66%, 49.31%, 45.41%, and 1.89% of the total Cd, respectively, on day 14. Under the same passivation time, upon the addition of SDD, there is a shift of Cd from EF and RF forms towards OF and ResF forms in the soil. With an increase in dosage, the content of OF and ResF forms is maintained at approximately 90% or above. This phenomenon may be attributed to the stable complex formation between the dithiocarbamate (S=C-S-) functional group in SDD and Cd [38]. In addition, the pH value of contaminated soil plays a significant role in the transformation of soil metal forms, which could be one of the contributing factors to this change [43]. It is noteworthy that the content of the ResF form in the soil initially increased and then decreased with an increase in passivator dosage. This trend may be due to a decrease in the abundance of soil microorganisms at high concentrations, as microorganisms possess functional groups (hydroxyl, carboxyl, amino, and thiol groups) on their cell walls that play a role in the passivation of metals [47,48]. Furthermore, with an increase in passivation time, the overall variation in the content of OF and ResF forms remains relatively stable, also above 90%. These results indicate that SDD exhibits a good passivation effect on Cd in soil.

3.2.3. The Effect of SDD Dosage on Plant Biomass

Figure 6 depicts the biomass of Tagetes patula L. after 42 days of planting in response to varying dosages of SDD. The results indicate that at a low dosage (1 mg/kg), there was no significant difference in the biomass of shoots and roots compared to the control group (p < 0.05). However, when the dosage exceeded 1 mg/kg, both shoot and root biomass showed a significant decrease. The reduction in biomass could be attributed to the phytotoxic effects of SDD at higher dosages, which inhibited plant growth [49]. The findings suggest that the addition of an appropriate dosage of SDD can mitigate the impact on plant growth.

3.3. Comparison of Passivation Effects in Synergetic Remediation Strategies

In order to investigate the impact of different synergetic remediation strategies on the reduction in bioavailable Cd in soil, two groups were established: asynchronous application of phytoremediation followed by passivator (Scheme 1) and synchronous application of plant and passivator (Scheme 2). Additionally, considering the experimental results from previous sections and cost-effectiveness, a 1% dosage was selected for the passivator treatment.
Figure 7 illustrates the impact of different synergetic remediation strategies on the bioavailable Cd in soil, and the initial content of bioavailable Cd in the soil was 2.54 mg/kg. Upon conducting Scheme 1 and Scheme 2, it was evident that both remediation approaches exhibited significant remediation efficiency after a 14-day remediation period, resulting in the obvious bioavailable Cd reduction rates of 2.237 mg/kg and 1.48 mg/kg, respectively. Scheme 1 demonstrated more significant reduction in bioavailable Cd in the soil compared with Scheme 2 (more than 1.5 times).
This difference may be attributed to the passivation effect of SDD and the phytoextraction process. The reasons for this phenomenon may lie in the following aspects: 1. microbes in the rhizosphere soil play a role in promoting Cd accumulation in plants [50,51]. However, when employing Scheme 2, while SDD passivates Cd, it may inhibit the normal activity of soil microbes, thereby reducing their abundance. Certain bacteria or fungi possess functional groups on their cell surfaces, such as carboxyl, hydroxyl, and thiol groups, that exhibit strong chelation capabilities towards heavy metal ions, leading to the immobilization of metals on cell surfaces and reducing their bioavailability [43,47]. 2. The acidic organic compounds secreted by plant roots can trigger reactivation and dissolution of passivated heavy metals through acidification or chelation reactions [52,53]. Applying Scheme 1 (asynchronous) can help mitigate these effects.

3.4. Remediation Mechanism

3.4.1. Effect of SDD Dosage on Soil Humus Content

The primary product of soil humification is humus, whose surface-active functional groups, including carboxyl, phenolic hydroxyl, and alcoholic hydroxyl groups, play a significant role in enhancing the soil environment and improving soil fertility [54,55]. Figure 8 illustrates the impact of SDD dosage on the humus content in soil. When the SDD dosage ranges from 1% to 3%, a notable increase in soil humus content can be observed compared to the 0% dosage. However, further augmentation of SDD dosage leads to a substantial decrease in humus content. This finding aligns with the trend observed in plant growth dynamics presented in Section 3.2.3, suggesting that excessive SDD usage may inhibit plant growth by degrading the soil environment and reducing soil fertility.

3.4.2. Effect of SDD on Soil pH Value

Soil pH value is a key factor influencing the stability of heavy metals in soil [56,57]. In acidic soils, significant competition for adsorption occurs between a large amount of H+ ions and heavy metal ions with the OH− ions on the surfaces of soil particles. However, as soil pH value increases, the competitive interaction between H+ and heavy metals diminishes, reducing the mobility of water-soluble heavy metals and converting them into insoluble compounds for stabilization [58].
Figure 9 depicts the variation in soil pH values at 14, 28, and 42 days with the addition of different dosages of SDD. It is evident that as the dosage of passivator increases, there is a significant rise in soil pH value. This aligns with the results observed in the previous dosages and passivation effectiveness experiments [59]. SDD, possessing dithiocarbamate (-CS2) functionality, can alleviate the competitive adsorption between H+ and Cd2+, facilitating the formation of more stable precipitates of Cd2+ with OH− [56,60]. Additionally, it can be observed from Figure 9 that with increased passivation time, there is a certain degree of decline in soil pH value. This could possibly be attributed to the organic nature of SDD, leading to microbial degradation in the soil, causing the release of H+ back into the soil [61].

3.4.3. Impact of SDD Dosage on Soil Electrical Conductivity and Moisture Content

Soil electrical conductivity (EC) and moisture content play crucial roles in altering heavy metal bioavailability and plant growth [51]. Figure 10 illustrates the changes in soil EC and moisture content after 14 days of remediation with varying dosages of SDD. It is evident that soil EC decreases with increasing SDD dosages, which may be attributed to the chelation of Cd in the soil with SDD, forming insoluble precipitates. This trend aligns with the observations in Section 3.2.1 regarding the effect of SDD dosage on the available cadmium content in the soil, further corroborating the high remediation efficiency of SDD.
Conversely, soil moisture content shows an increasing trend with higher SDD dosages, suggesting that SDD may improve soil structure at these concentrations, thereby enhancing soil water retention capacity. However, it is important to note that excessively high moisture contents might restrict soil aeration, posing a potential threat to root health. This could be one of the reasons for the observed phytotoxic effects of high SDD concentrations on Tagetes patula L.

3.4.4. X-ray Photoelectron Spectroscopy (XPS) Analysis

X-ray photoelectron spectroscopy (XPS) is a commonly used microscopic characterization technique [62]. It was employed to detect the chemical states of metal ions before and after passivator treatment, providing further insights into the underlying mechanisms.
Figure 11 presents the high-resolution Cd3d XPS spectra of the control group A (0% SDD) and treatment group B (1% SDD) after 14 days of passivation. In the CK group, the Cd3d XPS spectrum exhibited two main peaks at binding energies around 406.1 eV (Cd3d5/2) and 412.8 eV (Cd3d3/2), resembling the characteristic peaks of Cd2+ [63]. Upon peak fitting of the Cd3d XPS spectrum in the experimental group, two new peaks emerged at binding energies of approximately 411.8 eV and 405.1 eV. This indicates a change in the chemical form of Cd, with these two peaks resembling characteristic peaks of Cd-O and Cd-S bonds, as reported in previous studies [63]. The formation of Cd-O bonds is primarily associated with minerals in the soil, where the surfaces of layered silicate minerals, crystalline oxides, and amorphous oxides adsorb Cd2+ to some extent [43,64]. The formation of Cd-S bonds, on the other hand, is mainly attributed to the chelation between the dithiocarbamate group (S=C-S-) in SDD and Cd2+ [65]. Additionally, the binding energies of the Cd2+ characteristic peaks at 406.1 eV (Cd3d5/2) and 412.8 eV (Cd3d3/2) decreased to 406.0 eV and 412.6 eV, respectively, serving as crucial evidence of the interaction between Cd2+ ions and SDD. The decrease in binding energies indicates that Cd2+ ions receive electrons from SDD, leading to an increase in the electron density of Cd and a reduction in the binding energy.

3.4.5. Microbial Diversity Analysis in Soil

In soil, a diverse and abundant microbial community plays a crucial role in the detoxification and transformation of heavy metals through adsorption and conversion process [10,66]. A more in-depth understanding of the changes in the microbial community can help elucidate the mechanisms behind the two remediation sequences. Therefore, high-throughput sequencing analysis was conducted on microbial DNA extracted from the soil (16S V3V4) to investigate the changes in microbial population diversity before and after remediation.
Figure 12 illustrates the relative abundance of phyla in the soil after 14 days of treatment in the CK, Scheme 1 (asynchronous application of phytoremediation followed by passivator; 14 d, 1%), and Scheme 2 (synchronous application of plant and passivator; 14 d, 1%) groups. At the phylum level, distinct bacterial community structures were observed in CK, Scheme 1, and Scheme 2. Proteobacteria and Chloroflexi showed relatively significant variations, as depicted in the Figure 12. Following Scheme 1, the relative abundance of Proteobacteria increased by 14.72% compared to CK. However, Scheme 2 resulted in a decrease of 5.03%. Previous studies have reported that Proteobacteria play a crucial role in the symbiotic relationship between plants and microorganisms in remediation processes by fixing nitrogen (N) and secreting substances such as ethylene, gibberellic acids, cytokinin, and auxins [67,68]. This highlights the promoting effect of phytoremediation on the growth of Proteobacteria compared to synchronous remediation with a passivator, enhancing the synergistic effect of synergistic remediation and leading to a more substantial reduction in the bioavailable Cd content in the soil. On the other hand, the relative abundance of Chloroflexi decreased by 5.18% and increased by 6.89% after Scheme 1 and Scheme 2, respectively. It is worth noting that the relative abundance of Chloroflexi is negatively correlated with soil pH [69]. As discussed earlier, higher pH values result in more OH- ions in the soil, which favors the passivation of heavy metals. Therefore, it can be inferred that the differences in microbial populations may be a crucial factor leading to the distinctions between the two remediation approaches.

4. Application of Two Remediation Strategies in the Field

To evaluate the effectiveness of two remediation strategies in practical applications, a field experiment was conducted in the Dongting Lake farming area. As indicated in Table 2, Scheme 1 demonstrated high efficiency in practical use, with the bioavailable Cd content reduced by 2.17 mg/kg by the 14th day of remediation and further decreased to 2.34 mg/kg by the 70th day. In contrast, Scheme 2 showed consistently lower effectiveness throughout the entire period. Additionally, in the later stages, an increase in the bioavailable cadmium content was observed in the soil treated with Scheme 2, indicating a degree of instability.
These results indicate that the asynchronous application of phytoremediation followed by passivators not only significantly reduces bioavailable Cd under laboratory conditions but also maintains high remediation efficiency and stability in field applications.

5. Conclusions

This study provides a comprehensive evaluation of two remediation strategies: asynchronous application of phytoremediation followed by passivators (Scheme 1) and synchronous application of plants and passivators (Scheme 2). The following conclusions are drawn:
  • Screening experiments on enrichment plants and six passivators revealed that SDD and Tagetes patula L. exhibited the most effective remediation results.
  • Synergetic remediation experiments showed that both sequential combined methods significantly reduced the effective Cd content in the soil. The remediation effectiveness was ranked as asynchronous application > synchronous application.
  • Mechanistic studies fully confirmed that the strong chelation of the dithiocarbamate group (S=C-S-) in SDD with Cd2+ in the soil, coupled with the increase in soil pH, were the primary factors contributing to the observed excellent remediation effects in the two sequential synergetic remediation strategies. Furthermore, variations in microbial populations, specifically Proteobacteria and Chloroflexi, were identified as crucial factors influencing the effectiveness of the two sequential remediation approaches.
In conclusion, asynchronous synergetic remediation strategy (phytoremediation followed by passivation remediation) showed significant efficacy in laboratory experiments. The application of an asynchronous synergetic remediation strategy in the Dongting Lake agricultural area in Hunan Province, China, successfully reduced the available Cd content in local soil by over 90%. These results suggest promising potential for the field of soil heavy metal remediation.

Author Contributions

J.C.: experiment design and paper modification. C.L.: synergetic remediation experiment. C.Z.: pollutant extraction and analysis. F.Y.: data processing. Z.G.: field experiment. L.W. (Long Wei): research supervise. L.W. (Lichang Wang): funding support. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Science and Technology Innovation Program of Hunan Province [2022RC1039]; the International and Regional Science and Technology Cooperation and Exchange Program of the Hunan Association for Science and Technology [2024SKX-KJ-06]; the Natural Science Foundation of China [52274287]; the Science and Technology Innovation Program of Hunan Province of China (Grant No. 2023RC3051); the Science and Technology Program of Changsha of China (Grant No. kh2401026); the Research Foundation of the Department of Natural Resources of Hunan Province (Grant No. HBZ20240153); and the Research Foundation of the Department of Natural Resources of Hunan Province [HBZ20240148].

Data Availability Statement

The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Actual remediation site (a heavy metal-contaminated Dongting Lake farming area).
Figure 1. Actual remediation site (a heavy metal-contaminated Dongting Lake farming area).
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Figure 2. Screening of optimized plants for synergetic remediation after 45 days of growth. (Different letters above the bars in the bar chart indicate significant differences at the p < 0.05 level between different treatments. Error bars represent the standard deviations of the means, n = 3).
Figure 2. Screening of optimized plants for synergetic remediation after 45 days of growth. (Different letters above the bars in the bar chart indicate significant differences at the p < 0.05 level between different treatments. Error bars represent the standard deviations of the means, n = 3).
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Figure 3. Screening of optimized passivators for combined remediation (concentration = 0.5%). (Different letters above the bars in the bar chart indicate significant differences at the p < 0.05 level between different treatments. Error bars represent the standard deviations of the means, n = 3).
Figure 3. Screening of optimized passivators for combined remediation (concentration = 0.5%). (Different letters above the bars in the bar chart indicate significant differences at the p < 0.05 level between different treatments. Error bars represent the standard deviations of the means, n = 3).
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Figure 4. Impact of SDD dosage on the bioavailable Cd content in contaminated soil under varying passivation durations. (Error bars represent the standard deviations of the means, n = 3).
Figure 4. Impact of SDD dosage on the bioavailable Cd content in contaminated soil under varying passivation durations. (Error bars represent the standard deviations of the means, n = 3).
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Figure 5. Influence of SDD dosage on Cd forms under varied passivation durations (14 d, 28 d, and 42 d).
Figure 5. Influence of SDD dosage on Cd forms under varied passivation durations (14 d, 28 d, and 42 d).
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Figure 6. The effect of SDD dosage on the biomass of Tagetes patula L. roots and shoots. (Different letters above the bars in the bar chart indicate significant differences at the p < 0.05 level between different treatments. Error bars represent the standard deviations of the means, n = 3).
Figure 6. The effect of SDD dosage on the biomass of Tagetes patula L. roots and shoots. (Different letters above the bars in the bar chart indicate significant differences at the p < 0.05 level between different treatments. Error bars represent the standard deviations of the means, n = 3).
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Figure 7. Impact of various synergetic remediation strategies on the bioavailable Cd content. (Different letters above the bars in the bar chart indicate significant differences at the p < 0.05 level between different treatments. Error bars represent the standard deviations of the means, n = 3).
Figure 7. Impact of various synergetic remediation strategies on the bioavailable Cd content. (Different letters above the bars in the bar chart indicate significant differences at the p < 0.05 level between different treatments. Error bars represent the standard deviations of the means, n = 3).
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Figure 8. Influence of SDD dosage on soil humus content. (Different letters above the bars in the bar chart indicate significant differences at the p < 0.05 level between different treatments. Error bars represent the standard deviations of the means, n = 3).
Figure 8. Influence of SDD dosage on soil humus content. (Different letters above the bars in the bar chart indicate significant differences at the p < 0.05 level between different treatments. Error bars represent the standard deviations of the means, n = 3).
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Figure 9. Influence of SDD dosage on soil pH value under varied passivation durations. (Error bars represent the standard deviations of the means, n = 3).
Figure 9. Influence of SDD dosage on soil pH value under varied passivation durations. (Error bars represent the standard deviations of the means, n = 3).
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Figure 10. Impact of SDD dosage on soil electrical conductivity and moisture content after 14 days of remediation.
Figure 10. Impact of SDD dosage on soil electrical conductivity and moisture content after 14 days of remediation.
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Agronomy 14 01913 g011
Figure 11. (A) Remediation of cadmium-contaminated soil with 0% SDD dosage for 14 days. (B) Remediation of cadmium-contaminated soil with 1% SDD dosage for 14 days.
Figure 11. (A) Remediation of cadmium-contaminated soil with 0% SDD dosage for 14 days. (B) Remediation of cadmium-contaminated soil with 1% SDD dosage for 14 days.
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Agronomy 14 01913 g012
Figure 12. The relative abundance of soil bacteria at the phylum level. (CK: no treatment, Scheme 1: asynchronous application of phytoremediation followed by passivator, Scheme 2: synchronous application of plant and passivator).
Figure 12. The relative abundance of soil bacteria at the phylum level. (CK: no treatment, Scheme 1: asynchronous application of phytoremediation followed by passivator, Scheme 2: synchronous application of plant and passivator).
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Table 1. The physicochemical properties of the soil sample.
Table 1. The physicochemical properties of the soil sample.
PropertiespHSoil Organic Matter
(g/kg)		Available Nitrogen
(mg/kg)		Bioavailable Cd
(mg/kg)		Available Phosphorus
(mg/kg)
Soil7.7046.8341.90.08109
The Physical Properties of the Soil Sample
Composition (%)Sand45.5
Silt35.4
Clay19.1
Texture [14]Loam
Table 2. Comparison of the actual remediation effects of Scheme 1 (asynchronous) and Scheme 2 (synchronous) in the Dongting Lake farming area.
Table 2. Comparison of the actual remediation effects of Scheme 1 (asynchronous) and Scheme 2 (synchronous) in the Dongting Lake farming area.
Time/dayBioavailable Cd Concentration (mg/kg)
Scheme 1Scheme 2
02.562.56
140.390.65
280.360.60
420.290.90
560.230.93
700.220.94
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Cao, J.; Lv, C.; Zhang, C.; Yin, F.; Gao, Z.; Wei, L.; Wang, L. Asynchronous Synergetic Remediation Strategy for Cd-Contaminated Soil via Passivation and Phytoremediation Technology. Agronomy 2024, 14, 1913. https://doi.org/10.3390/agronomy14091913

AMA Style

Cao J, Lv C, Zhang C, Yin F, Gao Z, Wei L, Wang L. Asynchronous Synergetic Remediation Strategy for Cd-Contaminated Soil via Passivation and Phytoremediation Technology. Agronomy. 2024; 14(9):1913. https://doi.org/10.3390/agronomy14091913

Chicago/Turabian Style

Cao, Jian, Chenyang Lv, Chenxu Zhang, Fengxiang Yin, Zhengbo Gao, Long Wei, and Lichang Wang. 2024. "Asynchronous Synergetic Remediation Strategy for Cd-Contaminated Soil via Passivation and Phytoremediation Technology" Agronomy 14, no. 9: 1913. https://doi.org/10.3390/agronomy14091913

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