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Article

Effect of Microplastics on the Bioavailability of (Semi-)Metals in the Soil Earthworm Eisenia fetida

by
Xue Xiao
1,2,
Jia-Ling Li
1,
Wan-Li Rao
1,
Chun-Mei Zhao
1,*,
Er-Kai He
3,
Ye-Tao Tang
1,
Hua-Yi Chen
4 and
Rong-Liang Qiu
1
1
Guangdong Provincial Key Laboratory of Environmental Pollution Control and Remediation Technology, School of Environmental Science and Engineering, Sun Yat-sen University, Guangzhou 518107, China
2
State Environmental Protection Key Laboratory of Environmental Pollution Health Risk Assessment, South China Institute of Environmental Sciences, Ministry of Ecology and Environment, Guangzhou 510655, China
3
School of Geographic Sciences, East China Normal University, Shanghai 200241, China
4
School of Tropical Agriculture and Forestry, Hainan University, Haikou 570228, China
*
Author to whom correspondence should be addressed.
Agronomy 2025, 15(5), 1052; https://doi.org/10.3390/agronomy15051052 (registering DOI)
Submission received: 21 March 2025 / Revised: 17 April 2025 / Accepted: 22 April 2025 / Published: 27 April 2025
(This article belongs to the Special Issue Risk and Management of Organic Contaminants in the Agricultural Environment)
Browse Figures
Versions Notes

Abstract

:
Microplastics have a large surface area and hydrophobic characteristics, which helps them to easily adsorb organic matter and trace metals in soil. This interaction has the potential to alter soil physicochemical properties, affect the bioavailability of metals, and finally influence the toxicity of organisms. In the present study, we exposed Cd or As (Cd/As) to the earthworm Eisenia fetida (Savigny, 1826) in uncontaminated paddy soil, both in the presence and absence of polystyrene (PS) MPs (100~300 μm). The results show that MPs exhibit a significant influence on the physicochemical properties of As-contaminated soil, notably reducing the pH while increasing the electrical conductivity (EC), redox potential (Eh), and dissolved organic carbon (DOC), relative to single As treatment. At a Cd concentration of 40 mg·kg−1, the addition of MPs substantially altered the soil properties, decreasing the pH while increasing the EC and DOC. The effect of MPs on the bioavailable Cd content in soil was associated with Cd concentration. Specifically, MPs significantly increased the content of DGT (diffusion gradient technology)-Cd at a Cd concentration of 60 mg·kg−1. Regarding the bioavailable As content in the soil, MPs led to an increase at a high As concentration (40 mg·kg−1). Moreover, the addition of MPs amplified the uptake rate constants (ku) of DGT-Cd/As at various exposure concentrations, expediting the uptake of Cd/As by earthworms. In addition, compared to Cd treatment, the growth inhibition of earthworms in the As-treatment group was more significant due to microplastics. The results show that MPs in terrestrial environments magnify the negative effects of (semi-)metals, a phenomenon intricately tied to the degree of contamination by (semi-)metals. The interaction between MPs and metals may induce higher ecological risks for organisms.

Graphical Abstract

1. Introduction

In recent decades, the widespread use of plastics in various sectors, such as industry, agriculture, daily necessities, and medicine, has been driven by their durability, stable performance, and cost-effectiveness [1]. Plastic residues have been detected in soil samples from 19 provinces in China, with levels in the range of 0.1–324.5 kg·ha−1 [2]. However, the low recovery rate of plastics results in a significant portion being either landfilled or discarded in the environment, particularly in agroecosystems [3]. Over time, these plastics undergo gradual degradation into microplastics (<5 mm, MPs) through natural weathering, exposure to ultraviolet (UV) radiation, and biodegradation [4]. MPs enter agroecosystems through various pathways, including agricultural plastic-film usage, sewage sludge application, atmospheric deposition, and the use of organic fertilizers [5,6,7,8]. Once introduced, MPs are highly prone to interacting with soil aggregates, which may destabilize soil structure and consequently influence the physicochemical properties of soil [9].
Metal contamination in agricultural soils is a prevalent issue in China, posing a threat to the safe production of food crops. While certain metals are natural trace elements, human activities, like metal mineral smelting, coal and oil combustion, and the application of metal pesticides, can elevate their concentrations, leading to soil contamination [10,11]. The statistics reveal that approximately one-fifth of China’s farmland is contaminated, with the situation being particularly severe in southern China regarding Cd and As pollution. Some southern provinces exceeded the recommended limit of 0.3 mg·kg−1 of Cd, with values ranging from 0.15 to 0.87 mg·kg−1 [12]. According to the Bulletin on National Soil Pollution Status Survey published in China in 2014, the proportion of sampling sites with arsenic content in soil exceeding the national standard of 20 mg kg−1 reached 2.7% of the total number of sampling sites [13].
Given their substantial specific surface area and pronounced hydrophobicity, MPs exhibit strong adsorption capabilities for a broad spectrum of pollutants [14,15]. Although some studies focus on the interaction between MPs and trace metals, the influence of this interaction toward terrestrial organisms still remains unclear [16]. Some studies suggest that MPs may induce the desorption of trace metals from the soil. For instance, Zhang et al. [17] demonstrated that polyethylene MPs promote the desorption of Cd from soil because of the binding capacity of MPs. However, as the interaction between MPs and Cd adsorbed onto them is weak, the addition of MPs into the soil will eventually increase the mobility of Cd. This finding raises concerns about the heightened risk of Cd in agroecosystems due to the presence of MPs.
MPs possess organic characteristics and are small enough to be easily ingested or dermally absorbed by soil organisms (such as earthworms and wireworms), therefore they can act as carriers that may enhance the bioavailability of adsorbed substances. Some studies have reported that polypropylene increased the bioavailability of trace metals in the soil, promoting their accumulation in earthworms, particularly in organs like the liver and intestine [18]. Conversely, Wang et al. [19] found that MPs decreased the bioavailability of As and reduced the accumulation of total As, thereby diminishing toxicity to earthworms. However, the mechanism by which MPs affect the bioavailability of Cd or As in earthworms, particularly the dynamic process of bioaccumulation, remains unclear.
Hence, there is an immediate need to elucidate the correlation between the changes in soil physicochemical properties induced by MPs and the bioavailability of metals in soil. Moreover, it is also crucial to determine whether the compound toxicity of MPs and trace metals can be explained through an understanding of the dynamic process of metal bioaccumulation in organisms. In addition, PS particles are one of the most common polymers (PS, PP, PE, PVC, etc.) found in the natural environment [20] and are widely distributed in soils [21]. In this study, Eisenia fetida served as the test organism, uncontaminated paddy soil as the exposure media to better control the exposure condition, and polystyrene (PS) particles (100~300 μm), along with Cd and As, as the study metals(loids). The investigation into the effects of MPs on the bioavailability and toxicity of trace metals in the soil environment was conducted through exposure experiments and creating a toxicokinetic model (TK).

2. Materials and Methods

2.1. Test Microplastics

Polystyrene microplastics (PS-MPs) with particle sizes ranging from 100 to 300 μm were obtained from BaseLine ChromTech Research Center (Tianjin, China) in April 2022. Before use, suspensions of PS-MPs (10% w/w) were prepared using deionized water and subjected to sonication for 30 s to prevent particle agglomeration. The morphology of MPs was captured using field emission scanning electron microscopy (FESEM) (Zeiss Gemini 500, Jena, Germany) (Figure S1).

2.2. Test Organism

The exposed paddy soil obtained from farmland at South China Agriculture University in Guangzhou, China, did not receive a mulching film for the past five years and was free from Cd or As contamination (Table S1). In comparison to the concentrations of metal(loid)s added in this study, the background levels of Cd or As in the paddy soil were considered negligible. The earthworms Eisenia fetida were provided by the Guang He breeding farm in Hui Zhou, Guangdong Province, China. They were maintained under controlled laboratory conditions at 20 ± 2 °C, with a light:dark cycle of 8 h:16 h and a relative humidity of 75%. Before the experiments, the earthworms were acclimated to clean soil with a maximum water-holding capacity of 35% (w/w) for a minimum of one week. Healthy adult earthworms exhibiting well-developed clitellum and body weights between 300 and 600 mg/ind. were chosen for further testing.

2.3. Soil Incubation Experiment

After being air-dried for one week, the uncontaminated paddy soil was finely ground to pass through a 5 mm sieve. The Cd and As solutions were prepared with CdCl2 (GR) (Sigma, Livonia, MI, USA) and Na3AsO4 (GR) (Sigma), respectively. For alternating wet and dry soil incubation experiments, every 48 h, 70 mL deionized water was added to 250 g of grounded soil and mixed thoroughly. The experiment period was set for 60 d with an 8 h:16 h light:dark cycle. In this experiment, a single Cd/As contamination treatment and mixed Cd/As with MP treatment were set up. The physicochemical characteristics of clean paddy soil are detailed in Table S1. The concentrations of metal(loid) were established at 20, 40, and 60 mg·kg−1 for Cd, and 10, 20, and 40 mg·kg−1 for As, respectively. The percentage of MPs in the soil was 3% w/w. No MPs were added after the 60 d incubation period.

2.4. Exposure Experiment on the Earthworms

The soil after incubation was used as the media to expose Eisenia fetida for the toxicity tests, adhering to the guidelines of the OECD (2016) [22]. Before exposure, the earthworms were subjected to depuration for 24 h, and their body weights were measured and documented. Subsequently, eight earthworms were introduced into each container for one replicate, with triplicates conducted for each treatment. We did not feed the earthworms during the exposure in order to prevent the potential contaminants from the food. All the conditions for the exposure were the same to those of the culture. At the designated timepoints of 1, 3, 4, and 7 d, the surviving earthworms were rinsed with deionized water, weighed using scales, and the total number for each replicate was recorded. They were then stored at −80 °C for further analyses.

2.5. Physicochemical Properties and Metal(Loid) Concentration of Soil and Organisms

The physicochemical properties of the soil in this study, including pH, electrical conductivity (EC), redox potential (Eh), and dissolved organic matter (DOC), were measured after a 60 d incubation period. Soil pH was measured with a pH meter (soil/water ratio: 1:5, Metrohm 913, Herisau, Switzerland). Soil EC was measured using a conductivity meter (Sanxin MP551, Shanghai, China). The Eh of soil was determined by the potentiometric method. DOC was quantified using a TOC organic carbon analyzer (soil/water ratio: 1:2). The bioavailable Cd and As in the soil were extracted using the thin-film diffusion gradient (DGT) technique, and their concentrations were analyzed by Inductively Coupled Plasma Mass Spectrometry (ICP-MS, PerkinElmer NexIon 350D, Waltham, MA, USA) [23].
The DGT devices employed in this research were obtained from Nanjing Vision Environmental Science & Technology Co., Ltd. (Nanjing, China). We used incubated soil for earthworm cultivation. Before deploying the DGT, a weight of 60 g of air-dried soil was measured, transferred into a 250 mL beaker, adjusted to 60% of the maximum water-holding capacity (MWHC) using ultrapure water, and equilibrated for 48 h. Subsequently, the soil was moistened in the range of 80–100% maximum water-holding capacity for 24 h at indoor ambient temperature. The soil slurry was subsequently divided into three equal portions, with each portion transferred into a 60 mm diameter Petri dish. Each dish was equipped with a DGT device, and the dishes were incubated at 25 °C for 24 h. After retrieving the DGT devices, the binding gels were extracted and eluted with 1 mL of 1 M HNO3 for a minimum of 24 h before analysis. Using the equation described by Wang et al. [12], the time-averaged concentration of Cd and As measured by DGT (DGT-Cd, DGT-As) was calculated.
At the designated timepoints of 1, 3, 4, and 7 d of exposure, three earthworms were taken from each container. The earthworms were depurated for 24 h. Subsequently, 5 mL of 65% p.a HNO3 (GR) was added to the organisms, and the mixtures were homogenized for 30 s. The earthworms were then digested using a heating block at 120 °C for 3 h. The digested samples underwent dilution with 2% HNO3 to a final volume of 10 mL, and the concentrations of Cd/As in the digests were analyzed by ICP-OES.

2.6. Modeling Toxicokinetic Processes

Assuming the exposure concentrations of Cd and As remained constant during the exposure period, the relationship between Cd/As accumulation in Eisenia fetida and the exposure time was modeled using a one-compartment model to characterize the dynamic accumulation process of Cd/As in E. fetida.
C ( t ) = k u × C s k e × ( 1 − e − k e × t )
where C(t) is the body concentration of Cd/As in earthworms measured under different exposure times (mg·kg−1); Cs is the bioavailable concentration of Cd/As (mg·L−1) quantified by DGT in the soil. By minimizing the residual sum of squares in Equation (1), the relationship between Cd/As body concentration in earthworms and the exposure time was fitted, and the uptake rate constants (ku, L·kg−1·d−1) and elimination rate constants (ke, d−1) of Cd and As were determined.

2.7. Statistical Analysis

All data were statistically analyzed by SPSS V26 2019 (IBM, Armonk, NY, USA) and expressed as means and standard deviations (n = 3). Variations between treatments were evaluated using one-way or two-way analyses of variance (ANOVA, p < 0.05), with subsequent Duncan’s pairwise comparisons applied to identify significant differences. Model fitting was performed using MATLAB R2019a with the curve fitting tool in the software. All experiments were conducted in triplicate, and the figures were generated using Origin 9.0. The entire experiment was conducted between April and September 2022.

3. Results

3.1. The Influence of PS-MPs on the Properties of Cd/As Contaminated Soil

To investigate the impact of MPs on the physicochemical properties of soils contaminated with Cd or As (Cd/As), we conducted a 60 d exposure study and measured soil parameters, including pH, EC, Eh, and DOC. The results demonstrate that coexposure to Cd/As with MPs significantly reduces soil pH, EC, and Eh compared to the control group, while concurrently increasing the soil DOC (Figure 1). Specifically, when Cd/As was added without MPs, a reduction in soil pH was observed; however, a significant elevation occurred with increasing Cd concentrations (20~60 mg·kg−1) and As concentrations (10~40 mg·kg−1) (Figure 1A,E). In the presence of MPs, the soil pH generally decreased under Cd/As exposure, except at the 20 mg·kg−1 Cd level. The trend of soil EC showed an inverse correlation with pH, as increasing Cd/As concentrations resulted in a reduction in soil EC. Interestingly, MPs significantly enhanced soil EC under Cd/As treatments compared to exposure without MPs (Figure 1B,F). The soil Eh decreased with increasing Cd/As concentrations without MPs; however, the presence of MPs induced distinct patterns in soil Eh under Cd/As exposure. No significant changes in Eh were observed under the coexposure of Cd and MPs in comparison to Cd exposure alone. Nevertheless, the addition of MPs markedly increased Eh with As exposure (Figure 1C,G). Regarding soil DOC, an increase was observed with rising Cd/As concentrations, both in the presence and absence of MPs (Figure 1D,H). These findings indicate that the impact of MPs on the physicochemical characteristics of Cd/As-contaminated soils is influenced by the elemental characteristics of the metals and their contamination levels.

3.2. The Available Fraction of Cd/As in Soil

To investigate the influence of MPs on the bioavailability of Cd/As in soil, the bioavailable fraction of Cd/As was evaluated using DGT, and the concentrations of DGT-extracted Cd/As are presented in Figure 2. In comparison to soil solely contaminated with Cd, the introduction of MPs exhibited no significant influence on DGT-Cd levels at lower Cd concentrations (20 and 40 mg·kg−1). However, at the elevated Cd concentration (60 mg·kg−1), MPs significantly increased the DGT-Cd concentration. A parallel trend was observed for DGT-As concentrations when As concentrations were increased in the presence of MPs. MPs did not elevate DGT-As concentrations at lower As levels (10 and 20 mg·kg−1), but they significantly increased DGT-As at a higher As concentration (40 mg·kg−1) in comparison to As exposure alone. Consequently, these results indicate that the effect of MPs on the bioavailability of Cd/As in soil is closely associated with their contamination levels. MPs may induce a greater bioavailability of Cd/As at higher Cd/As concentrations.

3.3. Dynamic Bioaccumulation of Cd

Figure 3 illustrates the changes in the Cd concentration of earthworms over the 7 d exposure period. In general, with prolonged exposure time and higher exposure concentrations, the accumulation of Cd in earthworms showed a significant increase. However, this accumulation trend decelerated with prolonged exposure. In comparison to exposure to Cd alone, MPs had no significant impact on the Cd concentrations of earthworms during the initial stages of exposure (1 d exposure). Notably, a significant increase in Cd concentration in earthworms was observed from 3 d exposure onward in the presence of MPs, especially for 40 mg·kg−1 Cd. In contrast, at a higher Cd level (60 mg·kg−1), MPs did not exert a substantial influence on the accumulation of Cd in earthworms throughout the exposure period. Consequently, the most pronounced enhancement in Cd accumulation in earthworms by MPs occurred at a Cd exposure concentration of 40 mg·kg−1.
Based on one-compartment model fitting, the uptake (ku) and elimination rate constants (ke) of Cd/As by earthworms under different concentrations are presented in Table 1. Relative to singular Cd pollution, the presence of MPs elevated the ku of Cd. The significant increase in Cd ku was observed at 20 and 40 mg·kg−1 exposure concentrations in the presence and absence of MPs. With increasing exposure concentrations of Cd in earthworms, ke showed a decrease both in the presence and absence of MPs. However, the introduction of MPs did not markedly alter the ke values compared to those observed in treatments with only Cd exposure (p < 0.05, except 20 mg·kg−1 Cd).

3.4. Dynamic Bioaccumulation of As

The changes in As bioaccumulation in earthworms over the exposure period are depicted in Figure 4. The bioaccumulation of As in earthworms increased over time, and the rate of As concentration increase slowed after 3 d of exposure. Notably, the As body concentration had a 3-fold increase within the exposure concentration range from 10 to 40 mg·kg−1. In comparison to exposure solely to As, the introduction of MPs did not significantly increase As bioaccumulation in earthworms at low As concentrations, except at the high As exposure level (40 mg·kg−1).
The ku of As modestly increased at low As exposure concentrations in the presence of MPs (Table 1), but significantly increased at 40 mg·kg−1 As with MPs. This suggested that MPs can facilitate the absorption of As by earthworms. A reduction in ke was also noted with increasing As exposure concentrations, both with and without MPs. However, compared to exposure to As alone, the presence of MPs did not significantly change As ke in earthworms (p < 0.05).

3.5. PS-MPs Affect the Growth Inhibition of Eisenia fetida in Cd/As-Contaminated Soil

No mortality of E. fetida was observed in any of the treatments during the earthworm toxicity experiments. Figure 5 demonstrates the effect of MPs on the percentage of growth inhibition of earthworms in Cd- or As-contaminated soils. Generally, the growth inhibition of earthworms increased with the duration of Cd/As exposure. MPs showed varying effects on the growth of earthworms in Cd/As-contaminated soil. In comparison to exposure to Cd alone, the introduction of MPs did not markedly impede the growth of E. fetida at the termination of the 7 d Cd exposure period. However, the growth inhibition induced by As was statistically increased under As concentrations ranging from 10 to 40 mg·kg−1 with the existence of MPs after a 7 d exposure period.

4. Discussion

4.1. Effects of PS-MPs on Soil Properties

In the present study, the addition of MPs significantly affected the physicochemical properties of both uncontaminated and Cd/As-contaminated soil. MPs significantly decreased the pH of soil, especially at the highest concentration of Cd/As, compared with those of the control or Cd/As alone, which was similar to the results of Feng et al. [24]. This is because, as the MPs aged in the soil, the functional groups carried by the MPs entered the soil, and organic acids were also produced during the aging process, leading to changes in soil pH from 6.74 to 6.69. Such a decrease in pH due to the presence of MPs can lead to the bioavailable Cd/As-concentration increase in the soil, which was proved by the result for the DGT experiment (Figure 2). In addition, due to surface charges, MPs selectively adsorb positively or negatively charged substances and undergo ion exchange with ions in soil solutions, which can finally change the soil pH [24,25]. MPs may also affect the diversity and structure of soil microorganisms, resulting in changes in the pH of soil [24].
The trend in EC mirrored that of pH, as increasing Cd/As concentrations led to a decrease in soil electrical conductivity. However, the introduction of MPs significantly enhanced electrical conductivity under Cd/As treatments compared to scenarios without MPs. This suggests that MPs can exacerbate the impact of trace metal contamination on soil conductivity, potentially influencing nutrient availability and microbial activity [26,27]. The Eh of the soil decreased with increasing Cd or As concentrations. Interestingly, the presence of MPs induced distinct patterns in soil Eh between Cd and As exposure. Coexposure of Cd and MPs showed no significant change in Eh compared to Cd exposure alone, while the addition of MPs significantly increased Eh in the presence of As. This indicates that MPs may modulate the redox conditions of soil in a metal-specific manner, possibly influencing metal speciation and bioavailability [28].
MPs readily agglomerate with soil components, such as microbial secretions and organic matter [29], and impact soil DOC by stimulating enzyme activity or indirectly altering the decomposition and transformation of organic matter by changing the structure and activity of microbial communities [30]. Similar to the present study, Wang, Wang [28] showed that the addition of MPs increased the content of soil DOC, which may be due to intermediate products resulting from their degradation during aging in the soil. However, Chamas et al. [31] found that MPs have half-lives ranging from 0.035 to 9000 years, so they tend to be stable and persistent in the soil for long periods and are not easily degraded to produce large amounts of dissolved organic matter.

4.2. Effects of PS-MPs on Available Cd/As

In the present study, the influence of MPs on the concentration of DGT-Cd in soil was found to be associated with the degree of Cd contamination. No significant effect was observed at low Cd contamination levels, potentially due to a substantial amount of Cd2+ adsorbed by soil colloids during the soil incubation process, resulting in a low concentration of free Cd2+ in the soil solution. Consequently, the addition of MPs did not exert a notable impact on the DGT-Cd concentration within the soil. Conversely, at a high level of Cd contamination (60 mg·kg−1), the presence of MPs significantly increased the DGT-Cd concentration. This phenomenon may be attributed to the lower pH induced by MPs at a high Cd concentration (Figure 1E), which causes more Cd to be potentially bioavailable [32].
The impact of MPs on the bioavailability of As in soil also depended on the As contamination level. At low As contamination levels, MPs slightly but not significantly decreased the concentrations of DGT-As in the soil. Conversely, at high As contamination levels, MPs significantly increased DGT-As concentration. This observed variability may be attributed to the influence of MPs on the physicochemical properties of the contaminated soil. In our study, the addition of MPs led to a decrease in the pH of highly Cd/As-contaminated soil but an improvement in soil DOC, and finally increased the content of bioavailable Cd/As in the soil. Although we observed similar trends of DGT-Cd/As in the presence of MPs, the underlying interaction among Cd/As, MPs, and soil at the soil solid–liquid interface would be different due to their distinct properties [33]. Yu, Zhang [11] revealed different responses in metal speciation to the addition of MPs. The effect of MPs on the Fe-Mn oxide-bound fraction of As surpassed that on the carbonate-bound fraction and organic-bound fraction. In contrast, the effect on the organic-bound fraction of Cd outweighed the impact on the other two fractions. This discrepancy can arise from the different modes of action of MPs on metals: primarily adsorption or co-precipitation with Fe-Mn oxides for As, and potentially the formation of complex organically bound fractions for Cd. Consequently, MPs interact with Cd/As through diverse mechanisms, leading to consequential effects on their bioavailability [15].

4.3. Effects of PS-MPs on the Toxicokinetic Process of Cd/As in Eisenia fetida

Our findings indicate that the addition of MPs facilitates the accumulation of Cd in earthworms at a concentration of 40 mg·kg−1. Similarly, in soils highly contaminated with As at 40 mg·kg−1, MPs also significantly promoted the accumulation of As in earthworms. This aligns with the previous research, which demonstrated that MPs enhanced the accumulation of metals, specifically Cu2+ or Ni2+, in earthworms after 21 d exposure [34]. Similar observations have been reported in aquatic studies, which revealed an increased concentration of Cd in the liver, guts, and gills of zebrafish when exposed to a combination of Cd and MPs [35]. This phenomenon may be attributed to the ability of heavy metal ions to adhere to the surface of MPs, undergo internalization, and subsequently release through internal digestion processes in organisms [36]. Consequently, this process leads to the elevated bioaccumulation of heavy metals in organisms at the presence of MPs.
The results from the one-compartment model fitting unveile a decreasing trend in the ku of Cd and As with increasing concentrations. Interestingly, the presence of MPs augmented the ku of Cd/As. This suggests that MPs promoted the uptake of Cd/As by earthworms. The bioaccumulation of metals is acknowledged to be concentration-dependent, with exposure time playing a crucial role [37,38]. Numerous studies focus on the dynamic accumulation of different concentrations of metals in organisms. For instance, Huang et al. [39] estimated the ku and ke values for rare earth elements in Enchytraeus crypticus at varying exposure concentrations, demonstrating that the ku value of certain elements decreased after reaching a peak with increasing exposure concentration. This decline may stem from limitations imposed by carriers responsible for transporting metal ions or increased cellular mortality at high metal-exposure concentrations, resulting in the reduced uptake capacity of the organism for the toxicant [40].
Studies have shown that ku can be influenced by the characteristics of test species, contaminants, and environmental factors [41]. On the other hand, ke is primarily determined by the characteristics of the test organisms and is less affected by factors such as contaminant concentration [42]. Our study demonstrated that MPs increased the bioavailability of Cd/As in the soil solution, leading to elevated ku values in Eisenia fetida, providing evidence that microplastics promote the uptake of Cd/As in the earthworms.

4.4. Effects of PS-MPs on the Toxicity of Cd/As in Eisenia fetida

It is worth noting that the accumulation of Cd in earthworms exceeded that of arsenic As at equivalent levels of Cd and As contamination. This discrepancy suggests a higher likelihood of Cd enrichment in E. fetida compared to As. Metals accumulated in organisms exert toxicity through binding to specific action sites, inducing the production of reactive oxygen species, such as hydrogen peroxide and free radicals, in the organisms. This accumulation results in the production of lipid peroxidation products, damaging cell membranes, causing DNA damage, and interfering with antioxidant defense systems [43]. However, the results from the growth inhibition rate of earthworms in Cd/As-contaminated soil by MPs (Figure 5) reveal that earthworms in the As-treated group experienced a more pronounced growth inhibition than those in the Cd-treated group. This observation indicates that As is more toxic to earthworms than Cd. The different toxic effects of Cd and As may stem from their distinct uptake pathways and mechanisms of toxic action. Arsenic enters cells through the phosphate transport system, and arsenate potentially interferes with the electron transport chain or phosphorylation reactions in glucose metabolism. This interference hampers glucose metabolism and energy production [44,45,46].
Given the similarity between the ionic forms of Cd2+ and Ca2+, they can compete for the same type of ligand, allowing Cd2+ to be transported at the cellular basement membrane level by means of Ca2+-ATPase or Na+/Ca2+ exchange. This disruption ultimately affects intracellular Ca transport and metabolism. Moreover, the entry of Cd into organisms may induce the production of metallothionein, a crucial detoxifying substance. Wallace et al. [47] demonstrated that a 5-fold increase in dietary Cd exposure in grass shrimp led to a 32-fold increase in Cd storage in its cytosol due to MT induction, emphasizing the significance of MT in mitigating the toxic effects of Cd. The distinction in the toxicity of Cd and As accounts for the varying co-toxicity of Cd/As with MPs. The combination of As and MPs resulted in a more pronounced toxic effect on earthworms, highlighting the intricate interplay between metal toxicity and emerging contaminants MPs.

5. Conclusions

The present study revealed that MPs affect the effectiveness and toxicity of (semi-)metals on E. fetida in the terrestrial environment. MPs had a significant effect on the physicochemical characteristics of As-contaminated soil, significantly reduced pH, and increased EC, Eh, and DOC. The effect of MPs on the physicochemical properties of Cd-contaminated soil was associated with the level of Cd contamination, where a Cd dose higher than 20 mg·kg−1 led to a notable decrease in pH and an increase in the EC and DOC of soil upon the addition of MPs. MPs markedly increased the content of DGT-Cd at the Cd concentration of 60 mg·kg−1. The effect of MPs on the content of bioavailable As in soil showed an increase in DGT-As content at a high As concentration (40 mg·kg−1). The addition of MPs increased the uptake rate constants (ku) of DGT-Cd/As at various exposure concentrations and accelerated the uptake of Cd/As by earthworms. It further demonstrated that MPs in the terrestrial environment accelerate the accumulation of heavy metals in Eisenia fetida. The results reveal that the effects of microplastics in soil on the bioavailability of heavy metals are closely related to the types, concentrations, and exposure times of metal elements. The results of this study can provide a theoretical basis for accurately assessing the ecological risks of combined pollution by microplastics and heavy metals in soil.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy15051052/s1, Figure S1: The morphological characteristics of the polystyrene microplastics observed under Scanning electron microscope; Table S1: The physicochemical properties and metal backgrounds of clean paddy soil utilized in the present study.

Author Contributions

X.X. proposed the research ideas; designed the research schemes; conducted the experiments; analyzed the data; wrote, revised, and finalized the first draft of this paper. J.-L.L. conducted the experiments and analyzed the data. W.-L.R. conducted the experiments and analyzed the data. Y.-T.T. designed the research schemes and analyzed the data. E.-K.H. designed the research schemes and analyzed the data. H.-Y.C. designed the research schemes and analyzed the data. R.-L.Q. designed the research schemes and analyzed the data. C.-M.Z. proposed the research ideas; designed the research schemes; revised and finalized the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the National Natural Science Foundation of China (42077362), and the Research Fund Program of Guangdong Provincial Key Laboratory of Environmental Pollution Control and Remediation Technology (2023B1212060016).

Data Availability Statement

The original contributions presented in this study are included in the article/Supplementary Materials. Further inquiries can be directed to the corresponding author(s).

Conflicts of Interest

The authors declare no conflicts of interest.

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Agronomy 15 01052 g001aAgronomy 15 01052 g001b
Figure 1. Effects of PS-MPs on pH (A,E), electrical conductivity (EC) (B,F), redox potential (Eh) (C,G), and dissolved organic carbon (DOC) (D,H) of Cd/As contaminated soil after 60 d incubation. The exposure concentrations of Cd were 20, 40, and 60 mg·kg−1, and those of As were 10, 20, and 40 mg·kg−1, respectively. Data represent the mean values of each treatment (±SD, n = 3). Different letters indicate significant difference among treatments (p < 0.05).
Figure 1. Effects of PS-MPs on pH (A,E), electrical conductivity (EC) (B,F), redox potential (Eh) (C,G), and dissolved organic carbon (DOC) (D,H) of Cd/As contaminated soil after 60 d incubation. The exposure concentrations of Cd were 20, 40, and 60 mg·kg−1, and those of As were 10, 20, and 40 mg·kg−1, respectively. Data represent the mean values of each treatment (±SD, n = 3). Different letters indicate significant difference among treatments (p < 0.05).
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Figure 2. Effects of PS-MPs on the concentrations of Cd/As extracted by the thin-film diffusion gradient (DGT) in Cd/As-contaminated soil after 60 d incubation. (A) DGT-Cd; (B) DGT-As. Data represent the mean values of each treatment (±SD, n = 3). Different letters indicate significant difference among treatments (p < 0.05).
Figure 2. Effects of PS-MPs on the concentrations of Cd/As extracted by the thin-film diffusion gradient (DGT) in Cd/As-contaminated soil after 60 d incubation. (A) DGT-Cd; (B) DGT-As. Data represent the mean values of each treatment (±SD, n = 3). Different letters indicate significant difference among treatments (p < 0.05).
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Figure 3. The bioaccumulation (with standard error) of Cd in earthworms during 7 -d Cd exposure period under (A) 20 mg·kg−1, (B) 40 mg·kg−1, and (C) 60 mg·kg−1. Data represent the mean values of each treatment (±SD, n = 6).
Figure 3. The bioaccumulation (with standard error) of Cd in earthworms during 7 -d Cd exposure period under (A) 20 mg·kg−1, (B) 40 mg·kg−1, and (C) 60 mg·kg−1. Data represent the mean values of each treatment (±SD, n = 6).
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Figure 4. The bioaccumulation (with standard error) of As in earthworms during 7 d As exposure at (A) 10 mg·kg−1, (B) 20 mg·kg−1, and (C) 40 mg·kg−1. Data represent the mean values of each treatment (±SD, n = 6).
Figure 4. The bioaccumulation (with standard error) of As in earthworms during 7 d As exposure at (A) 10 mg·kg−1, (B) 20 mg·kg−1, and (C) 40 mg·kg−1. Data represent the mean values of each treatment (±SD, n = 6).
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Figure 5. Effects of PS-MPs on the percentage of growth inhibition of earthworms exposed to: (A) 20 mg·kg−1 Cd; (B) 40 mg·kg−1 Cd; (C) 60 mg·kg−1 Cd; (D) 10 mg·kg−1 As; (E) 20 mg·kg−1 As; (F) 40 mg·kg−1 As-contaminated soil. Data represent the mean values of each treatment (±SD, n = 3). Different letters indicate significant differences among treatments (p < 0.05).
Figure 5. Effects of PS-MPs on the percentage of growth inhibition of earthworms exposed to: (A) 20 mg·kg−1 Cd; (B) 40 mg·kg−1 Cd; (C) 60 mg·kg−1 Cd; (D) 10 mg·kg−1 As; (E) 20 mg·kg−1 As; (F) 40 mg·kg−1 As-contaminated soil. Data represent the mean values of each treatment (±SD, n = 3). Different letters indicate significant differences among treatments (p < 0.05).
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Table 1. Cd/As uptake rate constants (ku) and elimination rate constants (ke) of earthworms based on one-compartment model fitting under different levels of Cd/As contamination (mg·kg−1) in the presence and absence microplastics (MPs). The asterisk (*) stands for the significant difference among the treatments (one-way ANOVA, p < 0.05).
Table 1. Cd/As uptake rate constants (ku) and elimination rate constants (ke) of earthworms based on one-compartment model fitting under different levels of Cd/As contamination (mg·kg−1) in the presence and absence microplastics (MPs). The asterisk (*) stands for the significant difference among the treatments (one-way ANOVA, p < 0.05).
Treatmentku (L·kg−1·d−1)ke (d−1)
CdCd-2031.1 (±4.0)0.57 (±0.043) *
Cd-20+MPs48.7 (±3.5) *0.49 (±0.037)
Cd-4028.2 (±8.3)0.26 (±0.062)
Cd-40+MPs44.2 (±6.3) *0.34 (±0.14)
Cd-6023.5 (±6.2)0.20 (±0.094)
Cd-60+MPs25.5 (±3.0)0.26 (±0.075)
AsAs-1014.2 (±0.7)0.44 (±0.19)
As-10+MPs15.1 (±2.1)0.49 (±0.17)
As-208.9 (±5.3)0.23 (±0.33)
As-20+MPs9.7 (±0.056)0.088 (±0.003)
As-4016.0 (±1.3)0.21 (±0.024)
As-40+MPs19.3 (±1.5) *0.27 (±0.061)
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Xiao, X.; Li, J.-L.; Rao, W.-L.; Zhao, C.-M.; He, E.-K.; Tang, Y.-T.; Chen, H.-Y.; Qiu, R.-L. Effect of Microplastics on the Bioavailability of (Semi-)Metals in the Soil Earthworm Eisenia fetida. Agronomy 2025, 15, 1052. https://doi.org/10.3390/agronomy15051052

AMA Style

Xiao X, Li J-L, Rao W-L, Zhao C-M, He E-K, Tang Y-T, Chen H-Y, Qiu R-L. Effect of Microplastics on the Bioavailability of (Semi-)Metals in the Soil Earthworm Eisenia fetida. Agronomy. 2025; 15(5):1052. https://doi.org/10.3390/agronomy15051052

Chicago/Turabian Style

Xiao, Xue, Jia-Ling Li, Wan-Li Rao, Chun-Mei Zhao, Er-Kai He, Ye-Tao Tang, Hua-Yi Chen, and Rong-Liang Qiu. 2025. "Effect of Microplastics on the Bioavailability of (Semi-)Metals in the Soil Earthworm Eisenia fetida" Agronomy 15, no. 5: 1052. https://doi.org/10.3390/agronomy15051052

APA Style

Xiao, X., Li, J.-L., Rao, W.-L., Zhao, C.-M., He, E.-K., Tang, Y.-T., Chen, H.-Y., & Qiu, R.-L. (2025). Effect of Microplastics on the Bioavailability of (Semi-)Metals in the Soil Earthworm Eisenia fetida. Agronomy, 15(5), 1052. https://doi.org/10.3390/agronomy15051052

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