Abstract
Fe-modified biochar (FB) and co-using Chinese milk vetch and rice straw (MR) are two effective ways for mitigating the cadmium (Cd) contamination in paddy fields in southern China. Nevertheless, the effects of FB combined with MR on Cd passivation mechanism remain unclear. In the current study, the strengthening effects of FB induced by MR were found and the mechanisms of the extracted dissolved organic matter (DOM) from the co-decomposition of MR on Cd alleviation were investigated through pot experiment and adsorption experiment. Pot experiment demonstrated that co-incorporating FB and MR decreased available Cd by 23.1% and increased iron plaque concentration by 11.8%, resulting in a 34.7% reduction in Cd concentrations in brown rice compared with addition of FB. Furthermore, co-using FB and MR improved available nutrients in the soil. The molecular characteristics of DOM derived from the decomposition of MR (DOM-MR) were analyzed by fluorescence excitation emission matrix spectroscopy-parallel factor analysis (EEM-PARAFAC) and Fourier transform-ion cyclotron resonance mass spectrometry (FT-ICR MS). Results showed that lignin/carboxylic-rich alicyclic molecules and protein/amino sugar were the main compounds, potentially involved in the Cd binding. Adsorption experiments revealed that the addition of DOM-MR improved the functional groups, specific surface area, and negative charges of FB, inducing the strengthening of both physisorption and chemisorption of Cd(II). The maximum adsorption capacity of Fe-modified biochar after adding DOM-MR was 634 mg g−1, 1.30 times that without the addition of DOM-MR. This study suggested that co-incorporating MR, and FB could serve as an innovative practice for simultaneous Cd remediation and soil fertilization in Cd-polluted paddy fields. It also provided valuable insights and basis that DOM-MR could optimize the performances of Fe-modified biochar and enhance its potential for Cd immobilization.
Graphical Abstract
Highlights
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Chinese milk vetch and rice straw strengthened the Cd remediation by biochar.
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Soil DOM was the key influencing factor on soil Cd immobilization.
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DOM optimized the properties of biochar and produced richer functional groups.
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The combination of DOM and biochar had a higher specific surface area than biochar alone.
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DOM strengthened the physisorption and chemisorption capacities of Cd(II) on biochar.
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1 Introduction
Cadmium (Cd) is among the serious health risks to humans through the food chain (Wang et al. 2019; Zou et al. 2021). Various soil Cd amendments have been developed for soil Cd passivation over the last years, of which, biochar is the promising material for in-situ passivation methods with various advantages (Arabi et al. 2021; Ok et al. 2020; Palansooriya et al. 2020). Former study has verified the function of biochar to mitigate Cd contamination in water and soil through mechanisms such as adsorption, complexation, and precipitation (Abbas et al. 2017; Yin et al. 2016). Nevertheless, due to the limited stabilization performance of pristine biochar on heavy metals (Shaheen et al. 2022), modified or functionalized biochar is gradually emerging as the novel amendment with outstanding immobilization effect on Cd (Qu et al. 2022a; Shi et al. 2022). Fe-modified biochar (FB) could enhance the sorption sites for Cd due to its rich mesoporous structure and abundant functional groups (Irshad et al. 2022; Zhu et al. 2020). At present, FB is widely applied in paddy fields and exhibited the strong potential on inhibiting Cd availability (Wan et al. 2020).
Chinese milk vetch (MV) is a winter-growing legume green manure that can balance the soil fertility, enhance rice productivity, and improve environmental quality (Gao et al. 2023). Previous studies revealed that co-incorporating MV and rice straw (RS) played a more remarkable role in reducing Cd availability through promoting the conversion of Cd fractions and the increase of iron plaque (IP), leading to the reduction of Cd content in rice (Zhang et al. 2020a, b). However, the effect is limited, for which the team's recent field experiment was optimized and found that the joint use of MV, RS, and biochar could enhance the reduction of available Cd (Liang et al. 2022). Nevertheless, the explanation for the enhancement mechanism and the role played by MV and RS is unclear and therefore needs to be demonstrated by pot experiments and batch adsorption experiments.
Dissolved organic matter (DOM) is complex, containing components of different molecular weights, and its effect on heavy metals is multifaceted (Min et al. 2021). Previous study discovered that planting perennial green manure ryegrass and straw mulch in orchards improved soil DOM content and composition (Zhang et al. 2019a, b, c). And the DOM obtained from organic material is rich in functional groups, which might complex with heavy metals, thus affecting their morphological structure, mobility, and bioavailability (Plaza et al. 2006). Researchers found that DOM from rice straw promoted iron oxide particle agglomeration and precipitation, immobilizing Cr(III) and enhancing its removal, with carboxyl groups being pivotal (** mulch on the content and composition of soil dissolved organic matter in apple orchard on the loess plateau. J Environ Manage 250:109531" href="/article/10.1007/s42773-024-00313-6#ref-CR84" id="ref-link-section-d14012937e1177">c; Zhang et al. 2018). Numerous studies observed that the adding of biochar and green manure could increase soil pH and reduce Eh, thereby facilitating IP formation on roots (Irshad et al. 2022). This finding aligns with the results obtained in our study indicating that obvious positive correlations appeared between pH and DCB-Fe as well as DCB-Cd (P < 0.01). Another finding was that the increasing rice biomass in MRFB-S may help to increase root activity and thus increase ROL (Additional file 1: Fig. S5). Some research also evidenced that the addition of MV-S or RS-S could promote greater microbial iron reduction via soil reducing-bacteria (Zheng et al. 2022), and result in a larger increase in soil pH following submergence, thus facilitating the formation of IP.
The Cd levels observed in the different parts of rice plant were ranked as follows: the highest in root, followed by shoot, and the lowest in brown rice (Fig. 3). The root is the primary gateway for Cd to enter the rice from the soil and is the main tissue of Cd accumulation, which is significantly and positively correlated with effective Cd (Additional file 1: Fig. S3). The Cd absorbed by rice roots and transported to the above-ground part was mainly distributed in rice straw, while the proportion of Cd in the rice grain was small, which also reduced the risk of Cd entering the food chain from another perspective (Chen et al. 2021a, b). Compared with CK-S, MR-S, and FB-S treatments, MRFB-S treatment greatly lowered the Cd concentrations of brown rice by 86.2%, 82.5%, and 34.7%, respectively. Among these treatments, Cd level in brown rice treated with MRFB-S did not surpass the Cd safety threshold (0.2 mg kg−1). For the shoot and root, MRFB-S also showed the lowest Cd concentration, significantly decreased by 77.7% and 58.8% compared to MR-S, 29.1% and 22.1% compared to FB-S, respectively (P < 0.05). Moreover, MRFB-S not only reduced the Cd level in the rice plant, but also greatly improved the biomass of the rice grain and shoot by 71.9% and 58.2%, respectively, compared with CK-S (Additional file 1: Fig. S5). A previous study has found that Fe-modified biochar greatly reduced the Cd level in rice plants, mainly due to the passivation of Cd, the generation of stable Cd complexes, and the dilution effect induced by the increase of crop biomass (Sun et al. 2021). Some researchers also evidenced that co-using milk vetch and rice straw promoted the transformation from active Cd to a steady form (Wang et al. 2022a, b, c). In the present study, MRFB-S greatly reduced the Cd availability and boosted the conversion of the Cd species in soil to more stable residual states, thereby blocking the Cd uptake by the rice plant. Additionally, MRFB-S treatment facilitated the formation of IP, hindering or decreasing the movement of Cd into rice root system, further inhibiting the Cd adsorption by rice (Yin et al. 2017). These findings were favored by the current result that there was a greatly negative correlation between DCB-Fe and total Cd in different tissues of rice plant (P < 0.001) (Additional file 1: Fig. S3). Overall, the co-incorporation of MV, RS, and FB was an effective measure that could take into account both soil fertilization and cadmium pollution control.
3.2 Effects of key factors on Cd bioavailability
In addition to the environmental variables (e.g., Cd fraction) directly related to Avail-Cd, there are multiple indirect factors (soil physiochemical properties) affecting the Cd bioavailability. To assess the importance of physiochemical properties on Avail-Cd levels as shown in Additional file 1: Table S6, we performed the random forest regression model (Fig. 4A). Among the soil physiochemical properties, DOM had the highest Inc MSE value, suggesting that DOM played an extremely critical role in regulating the Cd availability. The combination of Cd with DOM has been widely reported to constrict mobility of Cd (Borggaard et al. 2019). In the present study, DOM was negatively associated with Avail-Cd (Additional file 1: Fig. S3), suggesting that higher DOM helped reduce the Cd availability. Nevertheless, researchers found that the DOM from air-dried cotton stalk and farmyard manure reduced the exchangeable Cd due to its more components with low molecular weight, low aromaticity, and high hydrophilicity (Min et al. 2021). We speculated that the composition of DOM generated from fresh samples and decomposition differed. DOM produced from the co-decomposition of milk vetch and rice straw predominantly consisted of high molecular weight compounds, which might contribute to the reduction of Cd activity. pH was another imperative factor and highly negatived related to Avail-Cd (El-Naggar et al. 2022), and this agreed with the results of the current study (Additional file 1: Fig. S3).
Partial least squares path model (PLS–PM) further discerned the relationships and influences of related parameters on brown rice Cd levels (Fig. 4B). Therein, the goodness of fit (GOF) statistic (GOF = 0.796) evaluated the model well. Soil pH was significantly positively correlated with DOM (0.63) (P < 0.001) and Fe2+ (0.58) (P < 0.01). DOM (−0.44) and pH (−0.53) strongly and negatively affected the Avail-Cd (P < 0.01), indicating that higher pH and DOM levels favored the reduction of Avail-Cd. The latent variables (IP) represent DCB-Fe and DCB-Cd. Fe2+ showed a significant and positive correlated with IP (0.79) (P < 0.01). Moreover, Avail-Cd was directly and positively related to brown rice Cd (0.39) (P < 0.05), suggesting that the decrease in Avail-Cd benefited the mitigation of Cd uptake by brown rice. IP had a negative effect on it ( −0.49) (P < 0.05). This result could be supported by the finding of Zhou et al. (2018), who found that Cd content in IP was significantly or highly significantly correlated with Cd in whole rice plants. In summary, DOM plays a crucial role in regulating the bioavailability of Cd.
3.3 Characterization of DMR, FB, and DMRFB
The SEM graphs and EDS spectra showed the surface morphology and main element composition of FB and DMRFB, both of which had visible loose structure and multi-element characteristics (Additional file 1: Fig. S6). DMRFB exhibited uneven surfaces with more particles and highly porous structure compared with FB. Elemental analysis indicated that DMRFB increased oxygen element concentration by 12.5% relative to FB (Table 1), implying that the presence of DOM generated from MR decomposition increased the abundance of oxygenated functional groups in FB (Lyu et al. 2022a). Unsurprisingly, compared with DMR and FB, DMRFB contained richer functional groups (carboxyl, hydroxyl, carbonyl, and esters) (Additional file 1: Fig. S7A). Moreover, DMRFB had higher oxygen-to-carbon ratio, implying DMRFB was highly aromatic.
The N2 adsorption–desorption characteristics of FB and DMRFB as well as the volume and size of the pores were analyzed. DMRFB showed larger pore volume and smaller average pore sizes than those of FB, which were more conducive to the pore adsorption for Cd (Table 1). Besides, the curve was a typical IV type with H3 hysteresis loop characteristic of mesoporous materials, according to the IUPAC classification (Additional file 1: Fig. S8C) (Qu et al. 2022a). The above results of BJH analysis and adsorption curve features for DMRFB and FB indicated that mesoporous structures predominated its morphological feature in line with the result of pore-size distributions (Additional file 1: Fig. S8D). Additionally, the SBET is a vital indicator of the sorption ability of adsorbent. The SBET of DMRFB (49.4 m2 g−1) was significantly higher compared to that of FB (24.9 m2 g−1) (Table 1), 1.99 times that of FB, indicating that DMRFB has the potential to offer a larger quantity of active adsorption points for Cd(II) (He et al. 2018).
The XRD patterns of DMR, FB, and DMRFB reflected their excellent crystalline nature and contained numerous minerals. In XRD profiles of FB and DMRFB (Additional file 1: Fig. S7E), the peaks at 18.05° and 47.13° belonged to (001) and (102) planes of Ca(OH)2 (JCPDS PDF 81-2040), respectively. Correspondingly, the other diffraction peaks at 29.37°, 43.12°, and 47.45° were assigned to the (104), (202), and (018) planes of CaCO3 (JCPDS PDF 72-1937), respectively. The characteristic peak of all materials at 39.38° represented FeO(OH), and the peaks at 50.70° and 34.08° corresponded to (211) planes of α-FeO(OH) (JCPDS PDF 17-0536) and (200) planes of FeSO4 (JCPDS PDF 12-0068). KCl was found at 28.59°. In XRD profiles of DMR, KCl (JCPDS PDF 75-0296) and KHCO3 (JCPDS PDF 12-0292) were the major phases (Additional file 1: Fig. S7B).
3.4 Cd(II) adsorption performance of FB and DMRFB
3.4.1 Adsorption isotherm and kinetic analysis
At a certain concentration of Cd solution, the Cd(II) equilibrium concentrations observed with DMR and FB treatments were higher than that found in DMRFB treatment. Additionally, as the DOM extraction time prolonged, the influence of DMRFB on Qe stabilized gradually (Additional file 1: Fig. S9). The linear correlation analysis indicated that Cd(II) equilibrium concentration was negatively correlated with pH (Additional file 1: Fig. S10). It was also found that DMRFB with the lowest Cd(II) equilibrium concentration had a higher pH value than FB, which was more conducive to the acquisition of precipitation (e.g., Cd(OH)2) (Yin et al. c). Additional file 1: Fig. S13C and D present the number and relative abundance of four main subgroups (CHO, CHNO, CHOS, CHNOS) in the DOMs of the three samples. The recalcitrant DOM formulas, particularly those belonging to the CHO and CHNO subgroups, were specifically plotted in the lignins/CRAM-like structural region highlighted in the VK diagram (Additional file 1: Fig. S14). Although lignins and CRAM compounds have similar O/C and H/C molar ratios, molecular weights, and DBE, they also exhibit different structural characteristics. In conclusion, the molecular diversity and complexity of DOM can be enhanced by the DMR, which may consequently impact the Cd binding process.
3.6 Overall findings and proposed mechanism
This study provided the basis for the observed extreme decrease in Cd concentration in rice plants under MRFB-S treatment, which can be largely attributed to the strengthening effect on stabilizing Cd by MR-S. MRFB-S transformed the Cd from active state to stable state and the increased Res-Cd might be CdCO3 and Cd(OH)2 supported by above results (Fig. 6, and Additional file 1: Fig. S8E). Large amounts of DOM released by MR had a positive influence on the Cd immobilization, as evidenced by the negative correlation between Avail-Cd and DOM in the correlation heat map and PLS-PM analysis (Additional file 1: Fig. S3 and Fig. 4B). A previous study has shown that DOM could interact with Cd through coordination, chelation, or complexation and decreased the Cd mobility, and further decreased Cd concentration in rice (Khan et al. 2017). In this process, the DOM with variable properties in complex soil environments played a significant role in controlling the migration and transformation of Cd (Zhang et al. 2022a, b, c). The complex biological processes between DOM and microbial metabolism are considered to be the primary driving force behind DOM characteristics (Xu and Guo 2018). Therefore, higher microbial activity in paddy soils may influence the protein-like components in DOM, thereby affecting the interaction between Cd and DOM. Herein, the current study further provided the sufficient evidence that DOM was the key factor influencing the Cd availability (Fig. 4A). Wang et al (2022a, b, c) found that co-incorporation of Fe and DOM can form the Fe-OM complexes, which could stabilize bioavailable amorphous Fe and indirectly reduce Cd accumulation in brown rice. Similarly, co-using FB and MR in this study exhibited higher levels of Fe(II) in soil, resulting in promoting the Cd immobilization (Additional file 1: Fig. S4).
From another perspective, on the one hand, more available Fe (Fe(II)) in MRFB-S treatment could be absorbed by rice, thus suppressing the Cd uptake by brown rice through competition. The fact that more more Fe(II) of DMRFB was retained in the reaction system supported the above inference (Fig. 6E). On the other hand, more Fe(II) derived from the addition of MR contributed to the formation of more IP, and then prevented the Cd uptake by the rice plant. Meanwhile, a previous study showed that MV significantly increased the relative abundance of soil reducing-bacteria, further improving the formation of IP (Zheng et al. 2022), which is consistent with the present result about Fe plaque. Similarly, RS application could promote the greater microbial iron reduction (Yuan et al. 2019). In addition, FB could provide the Fe source for the IP formation and further controlled the Cd adsorption by rice (Sui et al. 2021). Consequently, co-incorporation of MR and FB exhibited the stronger capacity on decreasing Cd bioavailability. Furthermore, the dilution effect induced by the enhancement of rice biomass also helped to decrease the Cd contents in rice plants (Gasco et al. 2019; Han et al. 2006). Therefore, the above results indicated that the co-using MV, RS, and FB is excellent strategy that shows promise for remediation of Cd-contamination paddy soil.
The adsorption experiments manifested that DMRFB could improve the sorption performance of Cd(II) and the adsorption occurred mainly through chemisorption of monolayers. The chemical adsorption capacity of DMRFB was higher than that of FB primarily due to the increase in functional groups (including oxygen and aromatic functional groups) and the enhancement of negative charge both brought about by the presence of DOM. Four chemisorption mechanisms were proposed to explain why the DMRFB produced high Cd(II) adsorption capacity. (i) More oxygenated functional groups of DMRFB participated in the surface complexation, thus providing the possible of forming intricate compounds containing Cd (Qu et al. 2022b; Zheng et al. 2023), long-term application of biochar may have adverse effects on the soil environment. This is primarily due to its non-specific adsorption characteristics, which can lead to issues like salinization. Ultimately, these adverse effects can hinder crop growth (Wang et al. 2020). Thus, it was essential to seek the path of simultaneous soil Cd pollution treatment and fertilization.
Substantial crop straws are harvested in China, yet the overall utilization efficiency is low and the phenomenon of resource wastage is severe (** et al. 2023; Ren et al. 2019). Thus, enhancing the integrated utilization of crop residues is significant. Previous researchers found that returning RS to the field not only reduced air pollution caused by straw burning, but also returned considerable amounts of nutrients to the soil and improved crop production (Yang et al. 2019; Zhou et al. 2023). Meanwhile, co-utilizing MV and RS is an innovative strategy in southern China to enhance their decomposition and consistent release of significant DOM into the soil for agricultural benefits (Zhou et al. 2020a). This study provided the vital evidence that the Cd(II) sorption was largely strengthened through adding the DOM derived from the co-decomposition of MV and RS, which might offer potential for the remediation of Cd-contaminated soil by combined green manure, rice straw, and passivated material in paddy fields. Furthermore, the superior Cd(II) adsorption performance of FB has achieved high adsorption efficiency at lower dosages compared to previous studies, reducing the potential negative effects associated with large-dosage application of biochar (Sui et al. 2021; Sun et al. 2022). From another perspective, the improvement of different physicochemical properties of soil by co-using milk vetch, rice straw, and iron-modified also reflected its adaptability and superiority on soil fertilization.
4 Conclusion
This study showed that co-incorporating milk vetch, rice straw, and Fe-modified biochar improved soil nutrient, elevated the rice grain biomass, and decreased the Cd concentration in brown rice, achieving production without exceeding the safety limit. In addition, the DOM derived from the decomposition of MR exhibited certain diversity and complexity, with its main components (lignin/carboxylic-rich alicyclic molecules and protein/amino sugar) potentially involved in the adsorption of Cd. Correspondingly, Fe-modified biochar attained more negative charges, specific surface area, and functional groups due to the induction of the DOM, which strengthened the physisorption and chemisorption capacities of Cd(II) on Fe-modified biochar. Overall, co-using milk vetch, rice straw, and Fe-modified biochar is a promising practice to remediate Cd-polluted farmland. Nevertheless, dynamic soil conditions (e.g., pH, Eh, and microbial activities) at the field scale may induce interactions between FB and DOM derived from MR and the subsequent effects on the mobility of Cd, and thus deserve further study.
Availability of data and materials
The datasets used or analyzed during the current study are available from the corresponding author on reasonable request.
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Acknowledgements
We thank Dr. **ng **a (Anhui Agricultural University) who provided technical assistance and constructive feedback on this manuscript. Thanks to the XPS support from Shiyanjia Lab (www.shiyanjia.com).
Funding
This research was funded by the National Key Research and Development Program of China (2021YFD1700200), the earmarked fund for CARS‐Green manure (CARS-22), and the Agricultural Science and Technology Innovation Program of Chinese Academy of Agricultural Sciences (ASTIP).
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TL: Data curation, Formal analysis, Methodology, Visualization, and Roles/Writing—original draft; GZ: Methodology, Investigation and Validation, Writing—review and editing; DC: Methodology, Writing—review and editing; ZM: Data curation and Formal analysis; SG: Investigation and Validation; JN: Investigation and Resources; YL: Investigation and Project administration; YL: Investigation and Project administration; HF: Funding acquisition, Investigation and Project administration; Chunqin Zou: Conceptualization and Supervision, Supervision, and Writing—review and editing; Weidong Cao: Conceptualization and Supervision, Funding acquisition, Project administration, Resources, Supervision, and Writing—review and editing.
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file 1: Fig. S1. Adsorption capacity of different biochar. Fig. S2. Effect of Cd(II) equilibrium concentrations under different treatments. Fig. S3. Correlation heat map of Cd bioavailability and soil properties. (Blue and red represent negative and positive correlations, respectively. Darker colors represent higher correlations. *, P<0.05, **, P<0.01, ***, P<0.001). Fig. S4. Fe2+ concentrations in soil (LSD Test, P < 0.05). Fig. S5. Biomass of rice different tissues (LSD Test, P < 0.05). Fig. S6. SEM-EDS map** images of FB and DMRFB before Cd(II) adsorption (A, FB; B, DMRFB). Fig. S7. FT-IR spectrum (A: DMR, FB, and DMRFB) and XRD profile of DMR (B: DMR). Fig. S8. EDS-map** images (A: FB-Cd and B: DMRFB-Cd), N2 adsorption-desorption isothermal curve and pore-size distributions (C and D), and XRD and FT-IR profiles of FB and DMRFB (E and F). Fig. S9. Effect of Cd(II) adsorption at different decomposition time. Fig. S10. The linear correlation between pH and Cd(II) equilibrium concentrations. Fig. S11. Desorption efficiency at different initial Cd(II) concentrations. Fig. S12. Five fluorescent components in DOM identified by EEM-PARAFAC analysis. A, Spectral characteristics of five identified components (The contour lines and colors represent the relative intensity of emission (yellow and navy blue correspond to most and least intense, respectively). B, Excitation and emission loadings of five components from DOM. Fig. S13. Numbers and intensities of the identified DOM formulae by elemental groups (A, number; B, intensity) and biochemical classes (C, number; D, intensity) in the samples of DMR, FB, and DMRFB. Fig. S14. Van Krevelen diagram of the carboxylic-rich alicyclic molecules (CRAM) (A, DMR; B, FB; C, DMRFB). Table S1. The experimental design for pot trial. Note: Chinese milk vetch and rice straw were calculated and applied to the soil using fresh and dry weights, respectively. Table S2. The basic physicochemical properties of studied soil. Table S3. Compound class and boundaries of regions in van Krevelen diagrams. Table S4. Molecular properties of DOM in different samples. Table S5. The resulting information of Shapiro-Wilk analysis. Table S6. Effects of different treatments on soil chemical properties in pot experiments. Table S7. The adsorption isothermal model parameters on FB and DMRFB for Cd(II). Table S8. Summary of for modified biochar adsorption capacity on Cd(II). Table S9. The kinetic model parameters of adsorption. Table S10. Thermodynamic parameters for Cd(II) adsorption by FB and DMRFB. Table S11. The activation energy of FB and DMRFB. Table 12. The concentrations of acidic functional groups. Table S13. The percentages of atomic in XPS. Table S14. Identities and related references for similar components using the OpenFluor database.
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Liang, T., Zhou, G., Chang, D. et al. The dissolved organic matter from the co-decomposition of Chinese milk vetch and rice straw induces the strengthening of Cd remediation by Fe-modified biochar. Biochar 6, 27 (2024). https://doi.org/10.1007/s42773-024-00313-6
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DOI: https://doi.org/10.1007/s42773-024-00313-6