Introduction

The contamination of arsenic (As) and cadmium (Cd) in agricultural soil has emerged as a persistent environmental challenge, especially in China1. Neither As nor Cd are essential for plants; however, they can accumulate in the human body through the food chain1,2 and have been designated as Group 1 non-threshold carcinogens for humans3,4. As a result, both As and Cd are prioritized as significant pollutants in soil. Rice, a fundamental cereal grain that supports half of the global populace with an estimated cultivation area of approximately 160 million hectares5,6. These elements subsequently accumulate in the plant’s roots, shoots, leaves, and grains more than other cereal crops3,7. The main pathway for the transfer of Cd into rice is primarily through root absorption, leaf absorption, and epidermal penetration, ultimately concentrating in rice grain8. Rice inherently exhibits high ability to take up and transfer As (III) under the anoxic environment, and rice plant has the higher ability to reduce As (V) in root to As (III) then uploading it to xylem sap, which results in high grain As9. Hence, delineating effective methods to curtail the transfer of As and Cd from tainted paddy soil to rice grain becomes paramount for both agroecology and public health1,10.

Rice’s absorption of Cd and As doesn’t correspond directly to their cumulative quantities in the soil but is closely tied to their speciation and bioavailability1,11. Nonetheless, due to their distinct chemical properties, As and Cd often exhibit contrasting bioavailability responses to variations in soil pH and Eh2,12. For instance, under inundated conditions, As solubility notably escalates mainly because of the reductive dissolution of soil iron (Fe) (oxy)hydroxides and the conversion of As(V) to As (III)13. In contrast, Cd solubility tends to markedly diminish due to manganese (Mn) and Fe(oxy)hydroxide adsorption and the formation of CdS precipitation5,11. Conversely, in drained oxidative conditions, As remains relatively stable with As(V) being the predominant species that firmly adheres to mineral soil components such as Fe and Al (hydr)oxides14. Simultaneously, an aerobic environment can promote the assimilation and mobilization of Cd15,16. Consequently, strategizing to concurrently reduce the enrichment of As and Cd by rice from contaminated paddies is a formidable endeavor17.

Agronomic management practices, such as irrigation schemes and fertilizer application, significantly influence soil pH, Eh, and soil organic matter (SOM)11,17,18. These factors subsequently dictate the transformation, mobility of trace elements in the soil, and their assimilation by the rice plant19,20. Studies have indicated that organic fertilizers can markedly reduce Cd enrichment in rice grain21,22. Specifically, upon applying a high dosage of organic fertilizer (22,500 kg/hm2), the available Cd content in soil and Cd in rice grains decreased by 52.1% and 68.2%, respectively21. Organic fertilizers such as compost promote the practice of organic agriculture, helps maintain soil macro and microporosity, slows the release of nutrients, thereby improving soil fertility and health, providing adequate plant nutrition, and supporting crop productivity23. Compost organic molecules can bind to soil heavy metals and pesticides, reducing the concentration of these harmful substances in the soil24. However, relying solely on organic compost may not satisfy the nutrient demand for optimal crop yields due to its limited concentration of plant-accessible nutrients and its gradual nutrient release25,26. Thus, a balanced application of chemical fertilizer alongside organic compost may present an efficient strategy for nutrient management26. Additionally, studies have shown that combining organic and inorganic fertilizers significantly reduces the heavy metal content in rice compared to using inorganic fertilizers alone27,28.

Rice is renowned for its ability to develop iron and manganese plaques on its root surfaces. These plaques, amorphous and/or crystalline layers of Fe/Mn (hydr)oxides, have the capacity to adsorb and co-precipitate metal(loid)s in the rhizosphere, thus influencing metal uptake in rice29,30. Numerous studies have demonstrated that the Fe plaque on the root surface of rice acts as both an adsorbent and a barrier to metals, including As, Cr and Cd, thereby preventing these metals from entering the rice plant31,32,33. Organic fertilizers can potentially promote the formation of Fe plaques and subsequently decrease Cd enrichment in rice22,34. Yet, the interplay between organic fertilizer and its synergistic application with chemical fertilizers in shaping Fe-plaque formation and the enrichment of As and Cd within these plaques remains underexplored, particularly in As and Cd co-contaminated paddy soil.

The aim of this study is to delineate the effects of varying proportions of pig manure compost and chemical fertilizers on As and Cd absorption and translocation in rice and the underlying mechanisms. We postulate that: the application of pig manure compost and chemical fertilizers will elevate soil pH and SOM across all treatments; this will subsequently alter the soil bioavailability of Cd and As; and the development of Fe/Mn plaques on root surfaces will immobilize As and Cd, ultimately curbing their uptake, transportation, and accumulation in rice grain. Should these hypotheses be validated, this study could pave the way for an eco-friendly and cost-effective method to concurrently recycle pig manure and ameliorate As/Cd contamination in rice grains.

Materials and methods

Soil and organic compost characteristics

The soil sample under investigation, characteristic of the limestone yellow loamy paddy soil, was procured from a rice paddy field in Guiyang, China, from a depth of 0–20 cm. This region is known for its elevated background concentrations of As and Cd35. Prior to analysis, the soil was subjected to air-drying, meticulously cleared of stones and coarse roots, sieved to a granularity of 2.0 mm, and subsequently homogenized for consistency. The basic properties of the tested soil were shown in Table 1. The concentrations of soil Cd and As were approximately 1.6 and 2.1 times higher than as the regulatory limitations of soil pollution risk control by the Chinese Soil Environmental Quality Standard for agricultural soil (GB 15618 -2018).

Table 1 Basic properties of the test soils and organic compost.
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We used pig manure compost (PM) as the organic fertilizer in which was prepared by aerobic composting the pig manure with rice straw in a greenhouse for 77 days, and the ratio of raw material and straw was 4:1 mixed. A self-made composting reflecting device made of thermal insulation material was used in the experiment. Its top was a perforated foam board with a cushion height, and the bottom was open, which is convenient for the ventilation and leachate removal. The composting device is 40 cm× 40 cm× 90 cm in size, and the ventilation mode is intermittent. The fan was turned on every 60 min for 10 min, and the ventilation rate is 0.2 L/kg·min. The properties of the compost were shown in Table 1. The concentrations of Cd and As were much lower than the limitation requirements of toxic and harmful substance in fertilizers in China (GB 38400 -2019).

Pot experiments

The pot experiment was conducted in a greenhouse of Southwest University, Chongqing, China, from May 15 to September 23 in 2019. PM was applied with chemical fertilizer in different proportions listed as follows: (1) NPK (all N is supplied by urea); (2) 25PM (25% of N by PM and 75% of N by urea); (3) 50PM (50% of N by PM and 50% of N by urea); (4) 75PM (75% of N by PM and 25% of N by urea); and (5) 100PM (all N by PM), each treatment was treated with 3 replications. The rates of N, P and K applied to soil were 0.15 g N kg−1, 0.15 g P2O5 kg−1 and 0.24 g K2O kg−1 soil, respectively. Chemical regents of urea, K2HPO4 and KCl were used to supply N, P and K in chemical fertilizers. No fertilizer addition was set up as the control (CK). The fertilizers were mixed thoroughly with 4 kg of soil at the rate of the experiment design before transferring into polyvinyl pots (24 cm in height and 22 cm in diameter). After pots were submerged with tap water for 15 days, one rice seedling (Oryza sativa L.var. Fengyou 210) was transplanted to each pot and tap water was added to maintain at 3–5 cm water level above the soil surface throughout the rice growing period. Pots were rearranged randomly every week until one week before harvest when the surface water had been dried naturally22,36.

Rice plants were harvested after 130 days of cultivation. The intact plant was carefully dug out from the pot, and the remaining soil was divided into two parts, one part was for soil available Fe and Mn determination while the other part was for physiochemical parameter measurements. Rice plants were collected and washed with tap water first and then deionized water. After the removal of Fe/Mn plaque, roots were washed with deionized water again and then dried at 105 ℃ for 30 min, followed by at 70 ℃ to constant weight. The plants were dried then crushed into powder for further analysis.

Analytical methods

Soil property analyses

Soil pH was measured using a pH electrode with the soil and water ratio of 1:2.5 and soil organic matter was determined by using potassium dichromate oxidation outer heating37. Soil available Fe and Mn were extracted with solution containing 0.005 M diethylenetriaminepentaacetic acid (DTPA) −0.1 M triethanolamine (TEA) −0.01 M CaCl238. Soil available Cd and As were extracted by 0.01 M CaCl239 and 0.5 M NaHCO340, respectively. The fractions of soil As and Cd were sequentially extracted according to the modified European Union Bureau of Reference (BCR)41; including the acid extractable fraction (F1, extracted by 0.11 M acetic acid (HOAc)), reducible fraction (F2, extracted by 0.5 M hydroxylamine hydrochloride (NH2OH), pH 2), oxidized fraction (F3, extracted by 30% H2O2 (pH 2–3) and 1 M NH4OAc (pH 2)) and the residual fraction (F4, digested with HNO3-HCl (3:1, v/v)).

Iron and management plaque extraction and analyses

The Fe/Mn plaques on fresh root surfaces were extracted using dithionite-citrate-bicarbonate (DCB) solution as described by Liu et al.42. Each excised fresh root sample was incubated in 50 mL of 0.03 M sodium citrate (Na3C6H5O7·2H2O) and 0.125 M sodium bicarbonate (NaHCO3) for 10 min, and then added 1.0 g of sodium dithionite (Na2S2O4) at room temperature. After 1 h, each sample was washed three times with deionized water, the liquid fraction was collected and added back to the DCB extract, and then reconstituted to 100 mL of the final volume using deionized water for further analysis. The concentrations of As and Cd in extraction solution were determined by an atomic fluorescence spectrometer (PF 52, China) and a graphite furnace atomic absorption spectrometer (AA-6880 AFG, Japan), respectively, while Fe and Mn were determined by an atomic absorption spectrophotometer (TAS-990, China).

Rice sample analyses

Cd and As concentrations in rice samples were quantified using methods described by Bashir et al.43 and Islam et al.5 respectively, with minor modifications. In brief, approximately 0.5 g of plant sample was digested with concentrated HNO3-HClO4 (2:1, v/v) for Cd and HNO3-HCl (3:1, v/v) for As in an electric furnace until a clear solution was obtained. Cd and As concentrations in the digestion liquid were determined using graphite furnace atomic absorption spectrometer (AA-6880 AFG, Japan) and atomic fluorescence spectrometer (PF 52, China), respectively.

Quality assurance (QA) and quality control (QC)

The QA/QC for the total As and Cd determinations were conducted using reagent blanks, duplicates, and analyzing the certified standard reference samples for plants (GBW (E) 100353) and soil (GBW07387) obtained from the China Standard Materials Research Center. The recovery rates of total Cd and As in soil and plant samples were 96–103% and 97–104% for Cd, and 95–105% and 94–103% for As, respectively.

Data proceeding and statistical analyses

The translocation factors (TFs) of Cd and As within rice plant were calculated using Eqs. (1)–(3)44:

$${\text{TF}}_{stem/root} = {\text{C}}_{stem}/{\text{C}}_{root}$$
(1)
$${\text{TF}}_{leaf/stem} = {\text{C}}_{leaf}/{\text{C}}_{stem}$$
(2)
$${\text{TF}}_{grain/stem} = {\text{C}}_{grain}/{\text{C}}_{stem}$$
(3)

Where TFstem/root, TFleaf/stem, and TFgrain/stem represent the transfer coefficients of Cd/As transfer from root to stem, from stem to leaf and from stem to grain, respectively. Croot, Cstem, Cleaf and Cgrain represent the Cd/As concentrations in root, stem, leaf and grain of rice (mg·kg−1), respectively.

All statistical analyses were performed using SPSS 26 for windows. Data (expressed as means ± standard error, n = 3) were subjected by one-way analysis of variance (ANOVA), and significant differences among treatments were determined by the Duncan’s multiple range test at P < 0.05. The correlation analyses were based on the Pearson’s correlation coefficients at the P < 0.01 or P < 0.05 level. All figures were made in Origin 8.5 software.

Results

Soil pH, SOM, and available Fe and Mn

The soil pH, SOM, and available Fe and Mn showed no significant variances between the CK and NPK treatments. However, when contrasting with CK, co-application treatments comprising varying proportions of PM and chemical fertilizer exhibited notable differences in these parameters (Table 2). Specifically, co-application treatments led to an elevation in soil pH and SOM by 0.14–0.52 units (P < 0.05) and 3.2–13.4% (P < 0.05), respectively. Moreover, these treatments resulted in a significant decline in available Fe and Mn concentrations by 13.9–31.2% (P < 0.05) and 13.6–40.4% (P < 0.05), respectively.

Table 2 Effects of co-application of organic and chemical fertilizers on soil pH, SOM, DTPA-Fe and DTPA-Mn under different treatments.
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The fractions and availability of Cd/As in soil

The distribution patterns of Cd and As fractions in the soil are depicted in Fig. 1a, b. Predominantly, irrespective of treatments, the residual fractions (F4) dominated both Cd and As content in the soil, constituting 35.1–50.2% (Fig. 1a) and 71.6–78.3% (Fig. 1b) of the total Cd and As concentrations, respectively. Examination of data from Fig. 1a, b indicates that fertilization differentially affected the distribution of As and Cd fractions in the studied paddy soil. In the case of Cd, fertilization treatments led to reductions in the percentages of F1 and F2 by 20.1–30.6% (P < 0.05) and 26.4–52.6% (P < 0.05), respectively. Simultaneously, there was a surge in the percentages of F3 and F4 by 14.9–37.4% (P < 0.05) and 28.7–42.8% (P < 0.05), respectively (Fig. 1a). Conversely, for As, increasing the share of PM initially led to a decrease followed by an uptick in the percentages of F1 and F2. Specifically, there were significant reductions under NPK and 25PM treatments (P < 0.05), while notable increases were observed with 75PM and PM treatments (P < 0.05). Notably, the percentages of As in F3 and F4 fractions remained relatively stable despite changes in PM proportions (Fig. 1b).

Fig. 1
figure 1

The percentages of (a) Cd and (b) As fractions in the total Cd and total As and the concentrations of available (c) Cd and (d) As in soil under different treatments. Cd and As fractions: F1 (acid extractable fraction), F2 (reducible fraction), F3 (oxidizable fraction) and F4 (residual fraction). The error bars indicated standard deviation of three replicates. The different lower-case letters in the same figure indicated significant differences (ANOVA, P < 0.05) among different treatments. CK: control, NPK: all N is supplied by urea, 25PM: 25% of N by pig manure compost and 75% of N by urea, 50PM: 50% of N by pig manure compost and 50% of N by urea, 75PM: 75% of N by pig manure compost and 25% of N by urea, PM: all N is supplied by pig manure compost.

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Bioavailable Cd concentrations, represented as CaCl2-Cd in the soil, saw significant declines ranging from 0.03 to 0.09 mg·kg−1 in fertilizer treatments when contrasted with the control (P < 0.05). A pattern emerged where the extent of decrease first rose and subsequently waned as PM proportions increased, with the lowest CaCl2-Cd observed under the 75PM treatment (Fig. 1c). In contrast, for As, concentrations of its bioavailable form, denoted as NaHCO3-As, underwent significant augmentation when PM proportions surpassed 50% (Fig. 1d) (P < 0.05). These observations underscore that the combined application of varied PM proportions and chemical fertilizers influences the bioavailability of As and Cd in the soil differently.

The biomass of rice

Table 3 shows that the biomass of rice root, stem, leaf, and grain in fertilization treatments raised significantly by 51.5–107.6%, 42.4–93.7%, 19.6–114.1%, and 30.7–70.9% (P < 0.05), respectively, comparing to control. The biomass of rice grain in the combination fertilization treatments was significantly higher than that of NPK treatment, and the highest grain yield was obtained in the 75PM treatment, suggesting that rice grain yields were significantly increased by the co-application the organic and chemical fertilizers.

Table 3 Biomass (g·pot−1 DW) of rice various parts for different treatments at harvest.
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Fe/Mn and Cd/As concentrations in the Fe/Mn plaques on root surface

The Fe concentrations within the Fe/Mn plaques on the rice root surface were notably dominant, being approximately 55.4–69.4 times higher than Mn concentrations. This observation underlines that the Fe plaque predominantly constitutes the Fe/Mn plaques, corroborating the findings presented by Zhang et al.29 All fertilization strategies significantly augmented the concentrations of both Fe and Mn plaques (Fig. 2a, b) (P < 0.05). When juxtaposed with the NPK treatment, the co-application approach bolstered the concentrations of Fe and Mn plaques by 34.9–86.2% and 16.3–48.5%, respectively. As the PM proportions increased, there was a subsequent rise in the formation of Fe/Mn plaques, but this trend did not extend beyond the 75PM treatment.

Fig. 2
figure 2

Concentrations of (a) Fe, (b) Mn, (c) Cd and (d) As in the Fe/Mn plaque on the surface of roots of rice. Significant differences are indicated by different letters (P < 0.05). Fe, Mn, and Cd concentrations in the Fe/Mn plaque were measured using the DCB method. CK: control, NPK: all N is supplied by urea, 25PM: 25% of N by pig manure compost and 75% of N by urea, 50PM: 50% of N by pig manure compost and 50% of N by urea, 75PM: 75% of N by pig manure compost and 25% of N by urea, PM: all N is supplied by pig manure compost.

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Relative to the control (CK), all fertilization methods led to substantial increments in the concentrations of Cd and As within the Fe/Mn plaque. Notably, the NPK treatment specifically amplified As concentrations within the Fe/Mn plaques (P < 0.05). In contrast to the NPK treatment, co-application notably elevated the concentrations of DCB-Cd and DCB-As by 28.9–101.5% and 16.5–58.1% (P < 0.05), respectively. This escalation followed the sequence: 75PM > 100PM > 50PM > 25PM > NPK > CK (Fig. 2c, d). These findings underscore that the synergistic use of organic and inorganic fertilizers can significantly amplify the sequestration of Cd and As in Fe/Mn plaques, especially when higher PM proportions (namely 75PM and 100PM treatments) are employed.

Cd and As concentrations in rice tissues

As shown in Fig. 3, the concentrations of Cd and As in different parts of rice followed the order of root > stem > leaf > grain. The concentrations of As and Cd in rice followed the same order of CK > NPK > 25PM > 50PM > 100PM > 75PM, which exhibits the lowest accumulation of As and Cd in 75PM. NPK treatment alone had no effect on Cd concentrations in rice leaf and grain, but it significantly reduced the concentrations of Cd in root and stem. Compared with those of NPK treatment, co-application of PM treatments decreased Cd concentrations in roots, stems, leaves and grains by 4.4–15.4%, 17.8–49.8%, 35.5–62.4% and 28.9–70.4%, respectively (P < 0.05). Regardless of the proportions of PM, the concentrations of Cd in grains (0.03–0.09 mg·kg−1) were significantly below the maximum level recommended by National Food Safety Standard for Maximum Levels of Contaminants in Foods (0.2 mg·kg−1, GB 2762-2017). The NPK treatment significantly decreased the concentrations of As in all rice tissues and the co-application with PM resulted in further decrease in the concentrations of As in roots, stems, leaves and grains by 11.7–33.8%, 8.1–28.1%, 7.4–26.8% and 33.8–67.4%, respectively (P < 0.05).

Fig. 3
figure 3

Concentrations of Cd (a–d) and As (e–h) in different parts of rice plants under different organic compost dosage treatments. Significant differences were indicated by different lower-case letters (ANOVA, P < 0 0.05). NPK: all N is supplied by urea, 25PM: 25% of N by pig manure compost and 75% of N by urea, 50PM: 50% of N by pig manure compost and 50% of N by urea, 75PM: 75% of N by pig manure compost and 25% of N by urea, PM: all N is supplied by pig manure compost.

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The translocation of Cd and As in rice

The translocation factor (TF) has been considered as the key factor in evaluating the ability of plants to transfer heavy metals within rice45. The TFstem/root and TFgrain/stem of Cd were 17.69–33.60 and 1.61–2.71 time higher than those of As, respectively, but the TFleaf/stem were much lower than that of As, suggesting that rice has a lower ability to transfer As from roots to stems and from stems to grains, but had a higher ability to transfer As from stems to leaves than that of Cd (Table 4). Compared with CK, the TFs of Cd within rice were not influenced by NPK treatment but were significantly decreased by the co-application of PM treatments (P < 0.05), suggesting that PM could inhibit the translocation of Cd from roots to stems and from stems to grains. In terms of As, co-application had no obvious influence on TF from stems to leaves, heightened TF from roots to stems slightly, but significantly decreased the TF from stems to grains (P < 0.05).

Table 4 Transportation coefficients of Cd and As in rice tissues under different treatments.
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Discussion

Increasing PM proportion passivated Cd but activated As in soils by raising soil pH and SOM

Soil pH and SOM are pivotal factors influencing the solubility, availability, and fate of soil heavy metal(loids)11,44. In our investigation, this pH surge can be attributed to the microbial decomposition of organic anions18 and the inherently higher pH of PM. Given that compost is laden with organic matter, the rise in SOM can be attributed to the augmented organic matter input as the proportion of PM increased. This is in line with findings by Tang et al.46 who posited that pig manure compost, being alkaline, aids in countering soil acidity while concurrently elevating SOM.

To understand the influence of alterations in soil pH and SOM due to varied fertilizer applications on the availability of these elements, we conducted a correlation analysis. The results displayed a significant inverse relationship between pH value and CaCl2-extractable Cd (r = −0.790, P < 0.01), whereas a direct correlation existed between pH and NaHCO3-extractable As (r = 0.634, P < 0.01). Generally, amelioration of soil pH augments the negative charge on soil colloids, intensifying the adsorption of the positively charged ion, Cd2+, and facilitating the desorption of negatively charged anions, As3+ and As5+, from soil colloids. This process consequently diminishes the bioavailability of soil Cd, while increasing that of soil As1,47. Notably, our data revealed that co-application of PM elevates soil pH, thereby reducing the CaCl2-extractable Cd and intensifying the NaHCO3-extractable As in the soil (Fig. 4). Cao et al.48 made similar observations, indicating that an upswing in soil pH positively impacts the availability of As, while negatively affecting that of Cd. The relationship between soil SOM and CaCl2-extractable Cd was found to be significantly negative (r = −0.723, P < 0.01), while it was significantly positive with NaHCO3-extractable As (r = 0.653, P < 0.01). Concerning SOM, it possesses the capacity to immobilize soil Cd by adsorbing Cd from the soil solution owing to its functional groups, like hydroxyl, carboxyl, and phenolic groups49. In contrast, it enhances the mobility of As due to the pronounced competition between As(V) and As(III) for active adsorption sites on mineral surfaces50. This underscores the premise that the downturn in CaCl2-extractable Cd and the upswing in NaHCO3-extractable As can be linked to the augmented SOM resulting from the combined application of PM and chemical fertilizer.

Fig. 4
figure 4

A partial least squares path model describing the effects of the key factors on Cd (a) and As (b) concentrations in rice grain. The red and blue line indicate positive and negative correlations, respectively (***P < 0.001,**P < 0.01, *P < 0.05).

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A study by Li et al.51 posited that organic matter can facilitate the transition of soluble and exchangeable Cd to more stable Cd forms, including Fe/Mn oxide-bound, organic-bound, and residual Cd. In our research, relative to the control and NPK treatments, there was a discernible rise in SOM when PM was co-applied with chemical fertilizers. This shift caused a stark reduction in mobile Cd factions (F1 and F2) and a noticeable increment in immobile Cd factions (F3 and F4). These observations intimate that the combined application of PM and chemical fertilizers fosters the transition of Cd from mobile to stable fractions. Furthermore, this co-application markedly reduced oxidizable As concentrations. A higher PM content notably augmented the concentration of acid extractable and reducible As, suggesting that elevated SOM post PM application can intensify As release. This finding is congruent with Norton et al.52 who concluded that organic matter application can bolster As release into soil pore water.

Attenuating the accumulation and translocation of Cd and As in grains by co-application of PM and chemical fertilizer

The PLS-PM quantified the relationship among related parameters (e.g., soil pH, SOM, Available Cd and As, Fe/Mn and Cd/As concentrations in Fe/Mn plaque) and Cd and As concentrations in rice (Fig. 4). The evaluation parameters goodness of fit (GOF) were 0.6154 and 0.6437, respectively, showing a reasonable fit. According to the path coefficient, the Fe/Mn contents in the Fe/Mn plaque were positively affected by soil pH and SOM and had positive effects on the Cd contents in the Fe/Mn plaque but negative effects on the grain Cd (Fig. 4a), indicating that the adsorption of Cd from the environment by Fe and Mn oxides on the Fe/Mn plaque may restrain grain Cd accumulation. Furthermore, soil pH and SOM had significant negative effects on the effective available Cd concentration, the available Cd concentration had significant indirect effects on grain Cd content via its impact on root Cd and TFgrain (Fig. 4a). For As, different from Cd, the changes of soil pH and SOM mainly directly positively affecting the formation of Fe/Mn plaque on the root surface to directly or indirectly affect the As content in roots and the TFgrain, and then had a significant negative effect on the accumulation of As in grains. The total effect of soil available As on grain As accumulation was relatively small (Fig. 4b).

Compared with CK and NPK, the contents of Fe and Mn in Fe/Mn plaques increased after PM application, especially at 75PM, this could be attributed to that PM employment increased soil pH and SOM and promoted the formation of Fe/Mn plaques to a certain extent. Elevated soil pH can cause more Fe and Mn to precipitate with OH−, bolstering the formation of the Fe/Mn plaque33. A rise in SOM has been linked to an increase in Fe release into the solution due to SOM complexation, which in turn boosts the formation of the Fe plaque when organic amendments are introduced22,53. Interestingly, the quantities of Fe/Mn plaques in the 75PM treatment surpassed those in the 100PM treatment (Fig. 2a, b). This might be attributed to the higher levels of dissolved organic matter (DOM) in the 100PM treatment. Elevated DOM can enhance the acid and/or reductive dissolution of the Fe/Mn plaque, instigating Fe/Mn release from the plaques back into the soil solution54. This might also be due to an elevated Eh when SOM levels were excessively high, leading to a reduction of Fe concentration in soil and subsequently attenuating the formation of Fe plaques55,56. As depicted in Fig. S1, there exists a pronounced positive correlation between the concentrations of Cd and As and those of Fe and Mn in the plaques. This signifies that these plaques are efficient reservoirs for soil-derived As and Cd. The prominent amounts of Fe/Mn plaques in the 75PM treatment, as well as the associated DCB-Cd and DCB-As levels, highlight this capability. Thus, the escalation in DCB-Cd/As (Fig. 2c, d) can be linked to the amplified formation of Fe/Mn plaques on rice roots induced by PM introduction. Such findings resonate with the work of other researchers57,58.

The formation of Fe/Mn plaques on rice roots, this would bolster the potential to sequester heavy metal(loid)s within these plaques, thereby mitigating the uptake of these metals by plants59,60. Figure 4a shows that Cd content in Fe/Mn plaques on rice root surface significantly restrained root Cd and TFgrain, and thus reduces Cd accumulation in grain. Zeng et al.4 determined that Fe plaques, formed under flooding conditions, depress the transfer of Cd from soil to roots. In addition, the increase of soil pH and SOM will decrease the soil available Cd content, and thus diminish the Cd concentration in rice roots and TFgrain, so as to relieve the Cd accumulation in grain. Liu et al.22 found that CaCl2-Cd in the rhizosphere was significantly and positively correlated with Cd content in roots and shoots, emphasizing the role of CaCl2-Cd in Cd accumulation in rice. These results indicated that the decrease of available Cd in soil and the enhancement of Fe/Mn plaques on rice root surface could prevent the uptake of Cd from soil to rice root and the transport of Cd in plants, thus reducing the concentration of Cd in grain. For As, the abatement of As accumulation in grains was mainly due to the formation of Fe/Mn plaques, which whittled the uptake and transport of As in roots (Fig. 4b). Wu et al.61 posited that these plaques act as barriers, impeding As uptake and subsequent accumulation in rice. Given the minute transfer coefficient of As from root to stem, the primary site of As deposition from the soil appears to be the rice root (Table 2; Fig. 3h). This suggests that the root effectively retains As, resulting in minimal As transport to stems and grains. Thus, co-application of PM and chemical fertilizer alters soil properties, fostering an environment conducive to Fe/Mn plaque formation. This augments the immobilization of As on the rice root surface, mitigating its transport to the plant’s aerial parts.

Environmental implications of PM application

In view of the pressure on natural resources and environmental degradation, it is necessary to move towards a more sustainable economic model. The new policy of the European Union aims to optimize the use of resources and energy, and to recycle a wide variety of waste, turning it into valuable products62. Aerobic composting is currently the most reasonable way of resourceful and harmless treatment of swine manure due to its advantages of low cost and ease of operation. Furthermore, it exhibits multifaceted capabilities in enhancing soil quality, promoting soil fertility, and regulating the activities of heavy metals23,24.

This study demonstrated the applicability of utilizing pig manure compost in conjunction with chemical fertilizer to diminish the accessibility of Cd and facilitate the development of Fe plaque on the surface of plant roots and the enrichment of As/Cd. This is achieved through the elevation of soil pH and SOM levels. The presence of Fe plaque on the root surface effectively impedes the uptake and translocation of As and Cd by rice plants, consequently mitigating the accumulation of these toxic heavy metals in rice grains. Pig manure compost is a form of aerobic compost that combines pig manure and rice straw, representing a method of waste resource utilization in which fulfills the mandate issued by The Ministry of Agriculture and Rural Affairs of China that calls for reducing the use of chemical fertilizer by 2025. This plan emphasizes the importance of decreasing the quantity of agricultural chemical fertilizer and enhancing the utilization of organic fertilizer resources. Our research not only has the benefits of waste resourcing and circular economy, but also provides a low-cost and environmentally friendly technology for remediation of heavy metal contamination in soil. Further inquiry is needed to explore the utility and potential for replication of this methodology in the field practice.

Conclusion

This research illustrates the combined application of varying proportions of PM and NPK in curtailing the uptake of Cd and As by rice grains. This decrement is proportionally correlated with the ratios of PM to NPK until a 75% PM composition (75PM) is achieved at which point the reduction of Cd and As in the grains maximizes. The underlying reasons for this phenomenon can be attributed to the increase in soil pH and SOM facilitated by the combined application of PM and NPK, coupled with the formation of Fe/Mn plaques. The joint application of PM and NPK emerges as a viable and practical strategy in the remediation of Cd and As contaminated paddy fields. The proportion of pig manure compost and chemical fertilizer should be properly considered in which 75% of PM mixed with 25% of chemical fertilizer was found to be the most effective ratio for the purpose of attenuated accumulation of Cd and As in rice grain.