http://orcid.org/0000-0002-9133-7754
Figures
Abstract
Rice plants accumulate cadmium (Cd2+) within the grain, increasing the danger of human exposure. Natural materials have been used in soil remediation, but few studies have examined the risks (based on the bioavailability of these metals to plants) of using these materials, so the practice remains controversial. In the present study, we evaluated the effectiveness of biochar produced from sugarcane bagasse, vermicompost (VC), vermicompost solid residue (VCR) and humin for remediation of Cd2+-contaminated soils. We characterized the interactions between these materials and Cd2+ and evaluated their capacity to alter Cd2+ availability to rice plants. Our results show that under the conditions in this study, biochar and humin were not effective for soil remediation. Although biochar had high Cd2+ retention, it was associated with high Cd2+ bioavailability and increased Cd2+ accumulation in rice plants. VC and VCR had high Cd2+ retention capacity as well as low Cd2+ availability to plants. These characteristics were especially notable for VCR, which was most effective for soil remediation. The results of our study demonstrate that in the tested materials, the bioavailability of Cd2+ to plants is related to their structural characteristics, which in turn determine their retention of Cd2+.
Citation: de O. Pinto T, García AC, Guedes JdN, do A. Sobrinho NMB, Tavares OCH, Berbara RLL (2016) Assessment of the Use of Natural Materials for the Remediation of Cadmium Soil Contamination. PLoS ONE 11(6): e0157547. https://doi.org/10.1371/journal.pone.0157547
Editor: Andrew C. Singer, NERC Centre for Ecology & Hydrology, UNITED KINGDOM
Received: February 9, 2016; Accepted: June 1, 2016; Published: June 24, 2016
Copyright: © 2016 de O. Pinto et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the paper and its Supporting Information files.
Funding: A.C.G. (sisFaperj: 2012028010) thanks FAPERJ (Edital Pós-doutorado Nota 10), FAPERJ APQ1 and a CAPES/CNPq postdoctoral scholarship (Science without Borders-PVE A060/2013). The authors thank Universal/CNPq and CARBIOMA/CNPq.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Remediation of heavy metal (HM)-contaminated soils using materials of natural origin and with low environmental impact has been a viable strategy over the last few years [1–3]. Cadmium (Cd2+) contamination is of particular concern because Cd2+ occurs in almost all environments and is quickly mobilized by human activities such as mining [4]. In plants, Cd2+ uptake occurs through the roots, where its accumulation is high; Cd2+ is then translocated through the xylem via the apoplast or the symplast to the rest of the plant [5]. Cd2+ accumulation in rice plants presents a risk to human health because the metal accumulates within the rice grain [6,7]. Rice accumulates large amounts of Cd2+ in its tissues [8]; therefore, it is the cereal that introduces the most Cd2+ into the human diet through ingestion [7]. In addition, rice’s genetic characteristics permit Cd2+ accumulation and transport from the roots to the shoots and grains [9,10].
Many studies have examined the use of materials such as biochar, vermicompost (VC) and humic fractions for soil remediation with the goal of decreasing the impact of plant Cd2+ accumulation [11–15]. Biochar has been widely used over the past few years as a soil amendment [16,17] that provides plant protection [18,19] and improves crop yields [20,21]. VCs are known to improve soil quality [22] and plant growth [23] and have been used for remediating HM-contaminated soils [24]. Studies have also assessed the use of humic substances (HS) for soil remediation due to their high structural diversity, which favors interaction with HM [25,26]. Specifically, humin has a high HM retention capacity [27] and acts as an indicator of the stability of humified organic matter within the soil [28,29]. Despite these studies, the risks of using biochar, VC and HS for remediation of Cd2+-contaminated soils are not clear, and comparative studies of Cd2+ retention, availability and subsequent assimilation by plants are needed. We tested the hypothesis that the structural characteristics of biochar, VC and humin determine their interaction with Cd2+ and that the nature of this interaction influences Cd2+ uptake by plants.
The goals of the present study were to characterize the nature of Cd2+ retention in biochar, VC, VC solid residue (VCR) and humin and to evaluate the effects of these materials on the availability of Cd2+ to rice plants. The Langmuir and Freundlich adsorption isotherms were determined, and the materials were characterized before and after Cd2+ retention using cross-polarization/magic-angle spinning nuclear magnetic resonance spectroscopy (CP/MAS 13C-NMR) and Fourier transform infrared spectroscopy (FTIR). Multivariate analysis of the resulting data was performed. To study the capacity of the tested materials to decrease Cd2+ availability for plants, rice plants were grown in the presence of the tested materials and the retained Cd2+ and the Cd2+ contents of the plant tissues were quantified.
Materials and Methods
Studied materials (VC, VCR, biochar and humins)
VC produced from plant debris and cow manure was supplied by the Agroecological Farm (Fazenda Agroecológica) of EMBRAPA Agroecology, Seropédica, Brazil. VCR was obtained through HS extraction of the VC, following the methods of Garcia et al. [30]. Biochar was obtained from sugarcane bagasse and as a byproduct of bio-oil production. To obtain the biochar, pyrolysis was carried out at 650°C for 1 h. Scanning electron microscopy shows that the resulting material had the morphological characteristics of biochar (S1 Fig). Humin was obtained from organic soil collected in Santa Cruz, Baixada Fluminense, Rio de Janeiro, Brazil.
Adsorption isotherms modeling of Cd2+ retention by the tested materials
Adsorption isotherms for Cd2+ retention were constructed using data obtained in the following manner. Cadmium chloride (CdCl2) solutions with a final volume of 100 mL and containing various concentrations of Cd2+ (1 mg L-1, 5 mg L-1, 20 mg L-1, 50 mg L-1 and 100 mg L-1) were added to 20 g of each tested material; the solutions were stirred for 240 minutes for biochar (pH = 4.2), 360 minutes for VC (pH = 5.0), 150 minutes for humin (pH = 4.8) and 190 minutes for VCR (pH = 5.0). Following stirring, the suspensions were filtered and supernatant Cd2+ concentrations were determined by atomic absorption spectroscopy (VARIAN 55B Atomic Absorption Spectrometer).
The retention data were fitted to a linear Langmuir isotherm according to the following equation:
where Ce is the equilibrium concentration of the adsorbate (mg L-1), Qe is the amount of metal adsorbed per gram of the absorbent at equilibrium (mg g-1), b is the Langmuir absorption constant at a given temperature (L mg-1), and Qmax is the maximum adsorption capacity (mg g-1).
A linear Freundlich isotherm was used, according to the following equation:
where KF (mg g-1) is the sorption capacity and n is the sorption intensity.
Spectroscopic characterization of materials
Infrared spectra of the materials were obtained in the spectral range from 4000–400 cm-1 using FTIR (Thermo Scientific Nicolet 6700) with KBr plates (5 mg of each material + 200 mg KBr).
CP/MAS 13C-NMR was performed using a Bruker AVANCE II 400 MHz NMR spectrometer equipped with a 4 mm narrow MAS probe and operated at a 13C resonance frequency of 100.163 MHz. Spectrum acquisition and processing was performed using the Bruker Topspin 2.1 software. The free induction decay (FID) was zero filled to 4 k and multiplied by an exponential weighing function corresponding to a line broadening of 70 Hz.
Influence of material structure on Cd2+ retention
Chemometric principal component analyses (PCAs) of the CP/MAS 13C-NMR spectra and FTIR data were performed for all materials using the Unscrambler® X 10.3 software (Camo Software AS Inc., Oslo, Norway). 13C-NMR and FTIR spectra of the materials with and without retained Cd2+ were imported into the software, and their areas were normalized. PCA analyses for each material were performed using the NIPALS algorithm with CROSS VALIDATION.
Cd2+ bioavailability to rice plants
Plant material and experimental conditions.
Cd2+ uptake by rice plants (Oryza sativa L.) was investigated for the Piauí rice variety. Plants were grown in a growth chamber under a 12 h light/12 h dark photoperiod at 28°C/24°C (day/night), 70% relative humidity, and a light intensity of 250 μmol m−2 s−1. Rice seeds were surface-sterilized with 2% sodium hypochlorite for 10 minutes and rinsed with distilled water. The seeds were placed in jars with gauze soaked in distilled water for germination. Four days after germination, the seedlings were transplanted into jars containing washed and autoclaved sand mixed with each of the tested Cd2+ enriched materials (170 mg Cd2+ g-1 material). The Cd2+ values were obtained from the adsorption isotherms (the retained Cd2+ values were confirmed through quantification by atomic absorption spectrometry). Substrates were prepared using ratios selected based on experimental evidence obtained in our laboratories or previously reported. Biochar was applied at 30 g kg-1, a concentration that has been observed to improve soil conditions [31,32]; VC was applied at 200 g kg-1, a concentration that has been observed to increase plant production and improve soil conditions [30]; VCR was applied at 90 g kg-1, a concentration observed to retain heavy metals [30]; and humin was applied at 20 g kg-1, a concentration that is consistent with its natural abundance [33,34]. Following planting, ¼ strength Hoagland solution [35] was added to the substrate on each of the first three days, and ½ strength solution was added daily for the remainder of the experiment (pH 5.8). A completely randomized experimental design was used for all experiments; the experimental design included five plants per pot and ten replicates per treatment. The experiment was run for 28 days after transplantation. All determinations were made from four harvests spaced seven days apart.
Root parameters
Assessments of root parameters were performed using WinRhizo Arabidopsis 2012b and the data were analyzed using XLRhizo (Regent Instruments, Quebec, Canada Inc.). Four root parameters were quantified and analyzed: length (mm), surface area (mm2), average diameter (mm) and the number of roots. Root length (mm) and the number of roots were classified as very fine (0.5–1.5 mm), fine (1.5–3.5 mm) or thick (> 3.5 mm). Roots and shoots were subsequently placed in an oven and dried at 105°C until they reached a constant weight, after which the leaf and root dry weight was determined.
Cd2+ content of plant tissues
The Cd2+ content of the rice plants was quantified by atomic absorption spectrometry using a VARIAN 55B atomic absorption spectrometer (Agilent Technologies, Headquarters 5301 Stevens Creek Blvd, Santa Clara, CA 95051, United States). The roots and leaves were ground and digested using a mixture of concentrated nitric acid and perchloric acid (HNO3/HClO4). Following digestion, the samples were added to 25 mL of distilled water and filtered for Cd2+ determination.
Exchangeable Cd2+ content and bioavailability
At the end of the experiment, the bioavailable Cd2+ was extracted from the substrates using deionized H2O; the exchangeable Cd2+ was extracted using MgCl2 (0.05 mol L-1) [36]. Phytoextraction indices were calculated based on the values for Cd2+ adsorbed by plants and accumulated in plant tissues. The bioconcentration factor (BCF) was calculated using the following equation: BCF = Cd2+ (plant tissue)/ Cd2+ (soil) [37]. The plant’s capacity for translocating Cd2+ from the root to the shoot was determined using the translocation index (TI): TI = Cd2+ (shoot)/ Cd2+ (root)*100 [38].
Results and Discussion
Modeling of Cd2+ retention using the Langmuir and Freundlich isotherms
The four tested materials showed L-type adsorption isotherms, indicating Cd2+ interaction with the surface of the material until saturation of the available binding sites (Fig 1A) [39]. Linear Langmuir isotherms were the best-fitting isotherms for Cd2+ retention on biochar (R2 = 99.18, p<0.001), but these isotherms fit poorly for retention on VC (R2 = 30.80, p<0.001) (Fig 1B). Linear Freundlich isotherms were the best-fitting isotherms for Cd2+ retention on VCR (R2 = 95.51, p<0.001), humin (R2 = 94.32, p<0.001) and VC (R2 = 82.50, p<0.001) (Fig 1C).
From top to bottom: A) general adsorption isotherms, B) linear Langmuir isotherms and C) linear Freundlich isotherms. Retention values were determined through simple linear regression and were significant at p<0.05 (n = 15).
The good fit of the Langmuir model for biochar indicates that retention occurred through monolayer formation, with retention sites presenting equivalent affinities for Cd2+ (Fig 1B) [40]. In contrast, the poor fit of the Langmuir model and the good fit of the Freundlich model for VC indicate that the binding sites had heterogeneous chemical characteristics. However, the good fit of the Freundlich model for VCR and humin indicates that these materials possess higher binding site diversity and heterogeneity than the other materials. Retention on these materials may initially result from chemical bonds and later from electrostatic interactions (Fig 1C) [40]
According to the adsorption parameters obtained from the Langmuir isotherms, VCR had the highest retention capacity, followed by biochar, VC and humin. VC and VCR presented lower b values than the other tested materials. The parameter b is related to the adsorption energy, indicating stronger interactions with Cd2+; in our samples, these may have been chemical interactions [30,41]. The parameter Kf, which can be obtained from the Freundlich isotherms and is related to the sorption relative capacity [30,41,42], was highest for VC and VCR. The value of n, which in our samples ranged from 1 to 10, is related to sorption intensity [30,41,42]; it indicated high retention by the four tested materials and was greatest for biochar (Table 1).
In the PCA, PC1 was observed to explain 99.9% of the total variance and showed that Cd2+ retention in the tested materials had a relationship with higher Cd2+ concentrations (Fig 2A). This result indicates that the differences in retained Cd2+ were more pronounced when the materials interacted with 50 and 100 mg L-1 Cd2+. The PCA for the adsorption isotherm parameters explained 91.31% of the total variance and showed a close relationship between the tested materials and n (PC1 63.12%) (Fig 2B), confirming favorable interactions between the materials and Cd2+.
PCA Showing the Relationship between (A) the Tested Materials (biochar, VC, VCR and humin) and Various Cd2+ Concentrations (1 to 100 mg Cd2+ L-1, in blue) and (B) the Tested Materials (biochar, VC, VCR and Humin) and the Langmuir and Freundlich Isotherm Parameters (Qmax, b, Kf and n, in Blue).
Characterization of Cd2+ retention
Characterization of retention using CP/MAS 13C-NMR.
VC had a higher number of carboxyl groups (10.7%) than VCR (6.4%) and humin (7.1%); and VC and VCR had more aliphatic oxygenated and nitrogenous groups than humin (S1 Table). Biochar had a large number of substituted aromatic structures (Ar-O,N; 62.5%) and a relatively high number of carboxyl (8.6%) and carbonyl (2.8%) groups.
No differences in peak presence in the CP/MAS 13C-NMR spectra were observed among the four materials both with and without retained Cd2+ at any of the five Cd2+ concentrations tested (S2 Fig). In addition, no significant changes in the amounts of the structures detected through integration of spectral regions were observed, and there were no changes in aromaticity or aliphaticity due to Cd2+ retention (S1 Table).
PCA of the pure spectra (Fig 3A, 3B, 3C and 3D) revealed structural differences between the materials with and without retained Cd2+ at the highest Cd2+ concentrations tested. Concentrations of 50 and 100 mg L-1 Cd2+ resulted in the greatest structural differences for VC, indicated by their shifts to negative values for PC1 (78%) (Fig 3A). Structural changes in biochar were observed at Cd2+ concentrations greater than 5 mg L-1 (Fig 3B). Structural changes in humin and VCR were observed at the lowest Cd2+ concentration tested (1 mg L-1).
PCA Analysis of CP/MAS 13C-NMR Pure Spectra (A, B, C, D and E) and the Carbon Type (A1, B1, C1, D1 and E1) of Materials with and without Various Levels of Retained Cd2+.
PCA of the spectra integrated by region showed that the different structures present in the tested materials had implications for the interaction of the materials with Cd2+ (Fig 3A1, 3B1, 3C1 and 3D1). Oxygenated moieties (-COOH, CAr-O, Calk-O and Calk-di-O) were related to VC with an without retained Cd2+ at concentrations of 1–20 mg L-1 but not at the highest Cd2+ concentrations (50–100 mg L-1). Thus, the interaction of VC with Cd2+ at high Cd2+ concentrations seems to result in changes to the more oxygenated side chains; these changes may result from chemical binding of Cd2+ (Fig 3A1). The interactions of biochar with Cd2+ at concentrations greater than 1 mg L-1 resulted in changes to the -COOH and -C = O groups (Fig 3B1). In contrast, in humin, all tested Cd2+ concentrations caused changes due to Cd2+ interactions with -COOH, C = O and Calk-di-O groups (Fig 3C1). In VCR, the Calk-O,N groups may act as available sites for Cd2+ retention at concentrations higher than 1 mg L-1 (Fig 3D1).
Characterization of retention through FTIR.
The four tested materials had similar ionized functional groups, all of which favor interaction with Cd2+ (S3 Fig). Absorption bands at approximately 3,400 cm-1 were observed for all materials tested, consistent with stretching vibrations (ν) of–OH and/or–NH groups (alcohols, carboxylic acids and amides). Bands between approximately 1,620 cm-1 and 1,650 cm-1 indicate ν for C = C aromatic, C = O amide I, and symmetric–COO- groups, and those between approximately 1,035 cm-1 and 1,110 cm-1 belong to ν of–OH groups from aliphatic alcohols and polysaccharides (S3 Fig) [43–47].
PCA was also performed on the spectra of materials with and without retained Cd2+ (Fig 4). This experiment revealed changes in functional groups that were not evident from visual analysis of the FTIR spectra. Differences in functional groups were observed in all materials tested at the highest Cd2+ concentrations and without Cd2+ (Fig 4). These results confirmed the PCA results for the 13C-NMR data.
Previous studies have confirmed the Cd2+ retention capacity of all tested materials except VCR (biochar, humin and VC) [48–53]. However, these studies examined the structural changes and chemical groups involved in Cd2+ retention using chemometric methods. We found that all tested materials had a high Cd2+ retention capacity (Table 1), with VCR and biochar displaying the highest amounts of retained Cd2+. Hydroxyl (-OH), -NH and -COO- groups (Fig 3), all of which are nitrogenated and oxygenated chemical groups (e.g., -COOH and -C = O) (Fig 3A1, 3B1 and 3C1), are directly involved in Cd2+ retention by biochar, VC and humin. Hydroxyl (–OH) and–NH groups in Calk-O,N structures may be the initial sites of Cd2+ retention in VCR (Fig 3, Fig 3D and 3D1).
Cd2+ availability of the tested materials to rice plants
The type of growth substrate affected plant growth. Growth inhibition was observed for plants grown in biochar and humin; this effect was similar to the toxicity produced by available Cd2+ (Fig 5).
Quantification of Cd2+ in the roots and leaves of rice plants showed how much Cd2+ was released by each of the substrate materials (Fig 6A and 6B). Plants growing on substrates containing humin or biochar or with bioavailable Cd2+ had higher Cd2+ accumulation in roots. In contrast, plants growing in substrate containing VC and VCR had lower Cd2+ accumulation in roots, with slightly higher root accumulation than in the control plants. These results indicate that the Cd2+ retained in humin and biochar is readily available for plant uptake, whereas VC and VCR decrease the Cd2+ available for plant uptake. The plant Cd2+ contents suggested that Cd2+ is retained through weaker interactions in humin and biochar or that the Cd2+ binding sites in these materials are structurally more superficial than those in VC and VCR. Either of these conditions would give the plant roots better access to the metal; the interaction of these materials with roots, as well as acid exudation and resulting rhizosphere acidification, could facilitate the release of weakly or superficially retained Cd2+.
Root and Leaf Cd2+ Contents of Rice Plants from the First Harvest until 28 Days after Seedling Transfer (DAT) (A and B); on the x axis, 1st, 2nd, 3rd and 4th indicate, respectively, the first, second, third and fourth harvests from each experiment, conducted at seven-day intervals. Values are reported as averages ± the standard error (n = 30). (C) The translocation index (TI) and (D) the bioconcentration factor (BCF) were calculated at 28 DAT.
Plants grown in the presence of available Cd2+ exhibited greater Cd2+ translocation from roots to leaves (Fig 6B). Greater Cd2+ accumulation in leaves due to translocation was also observed for plants growing in substrates containing humin and biochar. This observation confirms that these materials increase the availability of Cd2+, allowing the Cd2+ to be accumulated by plants. In contrast, plants growing on VC and VCR had low Cd2+ translocation and little accumulation in leaves.The findings were confirmed by comparison of the translocation indices (TIs) of plants grown under different conditions (Fig 6C). The high TIs of plants grown in the presence of Cd2+ indicate that Cd2+ bioavailability strongly affects its accumulation in the shoot. Plants grown in humin and biochar containing Cd2+ had higher TIs than plants grown in VC and VCR, confirming the capacity of humin and biochar to increase the bioavailability of Cd2+. The Cd2+ bioconcentration factor (BCF) for plants grown with Cd2+ was also high due to this Cd2+ bioavailability (Fig 6D). Humin and biochar yielded the highest BCF values, again confirming the bioavailability of the Cd2+ in these substrates.
Assimilation of Cd2+ resulted in varying levels of toxicity in plants grown in substrates containing the tested materials, and this assimilation affected plant growth (Fig 7). Compared with plants in the control treatment, root growth was inhibited in plants grown in all of the tested materials; the experimental plants had decreased root length, smaller root area and a decreased number of roots. These effects were less pronounced for plants grown in VC and VCR and more pronounced for plants grown in biochar and humin.
Values are reported as averages ± the standard error (n = 30).
Root thickening was observed after plant growth in all materials containing Cd2+, confirming the detrimental effects of Cd2+. Increased root diameter (thickening) of the root may be a response to Cd2+ toxicity. Shoot growth did not present the same response as root growth for all tested materials. The leaf length and the area of plants grown in VC and VCR were higher relative to the control plants, and these parameters were lower for plants grown in humin and biochar relative to the control plants.
Biochar and humin release high amounts of Cd2+ during their interaction with roots (Fig 7). This bioavailable Cd2+ accumulates in roots and is translocated into the leaves, resulting in toxicity to the rice plants and inhibition of root and leaf growth and development (Fig 7). VC and VCR release lower amounts of bioavailable Cd2+ to plants than biochar and humins, resulting in lower Cd2+ accumulation in the roots and leaves relative to the other treatments. Thus, plant growth in VC and VCR produced lower Cd2+ toxicity, resulting in decreased root growth and increased shoot growth compared to the control (Fig 7)
Leaf and root biomass were also determined (Fig 8). A pronounced inhibitory effect on leaf and root biomass production was observed for plants grown with biochar and humin containing Cd2+, compared to the control and the other treatments. In contrast, plants grown with VC and VCR had similar root biomass as the control plants, and plants grown with VCR had higher leaf biomass than the control.
Values are reported as averages ± the standard error (n = 30).
The effects on biomass production of growing plants in VC and VCR in the presence of Cd2+ may be attributed to an antioxidative defense response in which the synthesis of defense and transport proteins is increased in order to decrease Cd2+ toxicity [54–56]. Fragments of humic molecules present in humified materials may also have anti-stress effects through antioxidative protection [23,57] or may stimulate growth through hormone action [58,59].
Quantification of the Cd2+ remaining in the substrates after 28 days of plant growth confirmed the Cd2+ retention levels (Fig 9). At the end of the experiment, the VC substrate had high amounts of bioavailable and exchangeable Cd2+. Plants grown in this material had low Cd2+ contents in their tissues, confirming that the Cd2+ in VC was not easily released and thus that VC has a strong Cd2+ retention capacity. The VCR substrate had a higher amount of exchangeable Cd2+ than bioavailable Cd2+ and supplied low amounts of Cd2+ for plant uptake. This finding suggests that the relatively small amount of bioavailable Cd2+ released by VCR either formed weak bonds with the VCR or was complexed at more superficial binding sites. A similar result was observed for biochar; plants grown in this material accumulated large amounts of Cd2+, indicating weak or superficial bonds between the biochar and Cd2+. A large amount of exchangeable Cd2+ remained in the biochar at the end of the experiment, suggesting that Cd2+ retention by biochar occurs primarily through electrostatic bonds or through bonds in the interior of the material. Similar results were observed for humin, which had the lowest exchangeable Cd2+ values of any of the tested materials at the end of the experiment; thus, the Cd2+ released by humin during its interaction with plants was probably adsorbed through weak chemical bonds.
In the present study, we evaluated natural materials that are commonly used for phytoremediation of soils contaminated by heavy metals. Biochar showed a high capacity for Cd2+ retention. However, when all binding sites are occupied, biochar makes large amounts of Cd2+ available to plants via interaction with roots, and this Cd2+ accumulates in plant tissues. This finding indicates that biochar should be used with care for phytoremediation. Other authors have expressed concerns regarding the use of biochar for phytoremediation based on studies conducted under other experimental conditions [60,61]. Humin is not recommended for phytoremediation because, in addition to possessing the lowest Cd2+ retention capacity, it easily made Cd2+ available to plants. In this study, VC and VCR showed the most promising results. VC had high Cd2+ retention and resulted in the lowest plant Cd2+ accumulation. In addition, shoot growth was increased by VC in the presence of retained Cd2+. VCR had both high Cd2+ retention and low Cd2+ bioavailability. The observed capacity of VCR for heavy metal retention is consistent with previous reports [30].
Conclusion
The structural characteristics of the materials tested affect their Cd2+ retention and Cd2+ bioavailability and consequently determine the Cd2+ toxicity to rice plants. The results of this study have practical implications, indicating that rigorous monitoring should be employed when biochar is used for remediation of Cd2+-contaminated soils or to increase crop yields in soils with unknown degrees of heavy metal contamination. In addition, we conclude that humin is not effective for soil remediation due to its low Cd2+ retention and high capacity to release bioavailable Cd2+ to plants. In contrast, VC proved to be a promising material for the remediation of Cd2+-contaminated soils. However, because humic substances may form stable compounds with Cd2+, other environmental concerns that were not evaluated in the present study should be investigated (for example, solubility). The most promising material tested in this study was VCR. This is a novel result that has not been reported in previous studies.
Supporting Information
S1 Fig. Scanning electron microscopy of biochar used in this study.
https://doi.org/10.1371/journal.pone.0157547.s001
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S2 Fig. CP/MAS 13C-NMR spectra of the materials with and without levels of retained Cd2+.
https://doi.org/10.1371/journal.pone.0157547.s002
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S3 Fig. FTIR spectra of the tested materials with and without various levels of retained Cd2+.
https://doi.org/10.1371/journal.pone.0157547.s003
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S1 Table. Amount of type carbon (%) obtained by integrating areas in the CP/MAS 13C-NMR spectra with and without the retained metal.
https://doi.org/10.1371/journal.pone.0157547.s004
(DOCX)
Acknowledgments
A.C.G. (sisFaperj: 2012028010) thanks FAPERJ (Edital Pós-doutorado Nota 10), FAPERJ APQ1 and CAPES/CNPq postdoctoral scholarship (Science without Borders-PVE A060/2013). The authors thank Universal/CNPq and CARBIOMA/CNPq.
Author Contributions
Conceived and designed the experiments: TOP RLB ACG. Performed the experiments: TOP JNG OHT ACG. Analyzed the data: ACG RLB NMS. Contributed reagents/materials/analysis tools: JNG OHT. Wrote the paper: ACG RLB.
References
- 1. Sabir M, Waraich EA, Hakeem KR, Öztürk M, Ahmad HR, Shahid M. Phytoremediation: mechanisms and adaptations. Soil Remediation and Plants: Prospects and Challenges. 2014: 85: 85–105.
- 2.
Perminova IV, Hatfield K, Hertkorn N. Use of Humic substances to remediate polluted environments: from theory to practice. Russia: Springer Netherlands; 2005. p. 285–309.
- 3. Lucchini P, Quilliam RS, DeLuca TH, Vamerali T, Jones DL. Does biochar application alter heavy metal dynamics in agricultural soil? Agric Ecosyst Environ. 2014;184: 149–157.
- 4. Larison JR, Likens GE, Fitzpatrick JW, Crock JG. Cadmium toxicity among wildlife in the Colorado Rocky Mountains. Nature. 2000;406: 181–183. pmid:10910356
- 5. Benavides MP, Gallego SM, Tomaro ML. Cadmium toxicity in plants. Braz J Plant Physiol. 2005;17: 21–34.
- 6. Uraguchi S, Fujiwara T. Cadmium transport and tolerance in rice: perspectives for reducing grain cadmium accumulation. Rice. 2012;5: 1–8.
- 7. Meharg AA, Norton G, Deacon C, Williams P, Adomako EE, Price A, et al. Variation in rice cadmium related to human exposure. Environ Sci Technol. 2013;47: 5613–5618. pmid:23668419
- 8. Jiang S, Shi C, Wu J. Genotypic differences in arsenic, mercury, lead and cadmium in milled rice (Oryza sativa L.). Int J Food Sci Nutr. 2012;63: 468–475. pmid:22106866
- 9. Ueno D, Kono I, Yokosho K, Ando T, Yano M, Ma JF. A major quantitative trait locus controlling cadmium translocation in rice (Oryza sativa). New Phytol. 2009;182: 644–653. pmid:19309445
- 10. Uraguchi S, Mori S, Kuramata M, Kawasaki A, Arao T, Ishikawa S. Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice. J Exp Bot. 2009;60: 2677–2688. pmid:19401409
- 11.
Lehmann J, Joseph S, eds. Biochar for environmental management: science and technology. London: Routledge; 2012.
- 12. Lakhdar A, Achiba WB, Montemurro F, Jedidi N, Abdelly C. Effect of municipal solid waste compost and farmyard manure application on heavy‐metal uptake in wheat. Commun Soil Sci Plant Anal. 2009;40: 3524–3538.
- 13. Tejada M, García-Martínez AM, Parrado J. Effects of a vermicompost composted with beet vinasse on soil properties, soil losses and soil restoration. Catena. 2009;77: 238–247.
- 14. Karami N, Clemente R, Moreno-Jimenez E, Lepp NW, Beesley L. Efficiency of green waste compost and biochar soil amendments for reducing lead and copper mobility and uptake to ryegrass. J Hazard Mater. 2011;191: 41–48. pmid:21565444
- 15. Fellet G, Marmiroli M, Marchiol L. Elements uptake by metal accumulator species grown on mine tailings amended with three types of biochar. Sci Total Environ. 2014;468–469: 598–608. pmid:24056450
- 16. Renner R. Rethinking biochar. Environ Sci Technol. 2007;41: 5932–5933. pmid:17937262
- 17. Xu HJ, Wang XH, Li H, Yao HY, Su JQ, Zhu YG. Biochar impacts soil microbial community composition and nitrogen cycling in an acidic soil planted with rape. Environ Sci Technol. 2014;48: 9391–9399. pmid:25054835
- 18. Elad Y, David DR, Harel YM, Borenshtein M, Kalifa HB, Silber A, et al. Induction of systemic resistance in plants by biochar, a soil-applied carbon sequestering agent. Phytopathology. 2010;100: 913–921. pmid:20701489
- 19. Elad Y, Cytryn E, Harel YM, Lew B, Graber ER. The biochar effect: plant resistance to biotic stresses. Phytopathol Mediterr. 2012;50: 335–349.
- 20. Major J, Rondon M, Molina D, Riha SJ, Lehmann J. Maize yield and nutrition during 4 years after biochar application to a Colombian savanna oxisol. Plant Soil. 2010;333: 117–128.
- 21. Viger M, Hancock RD, Miglietta F, Taylor G. More plant growth but less plant defence? First global gene expression data for plants grown in soil amended with biochar. GCB Bioenergy. 2015;7: 658–672.
- 22. Oo AN, Iwai CB, Saenjan P. Soil properties and maize growth in saline and nonsaline soils using cassava-industrial waste compost and vermicompost with or without earthworms. Land Degradation & Development. 2015;26: 300–310.
- 23. García AC, Santos LA, Izquierdo FG, Rumjanek VM, Castro RN, dos Santos FS, et al. Potentialities of vermicompost humic acids to alleviate water stress in rice plants (Oryza sativa L.). J Geochem Explor. 2014;136: 48–54.
- 24. Jadia CD, Fulekar MH. Phytoremediation: the application of vermicompost to remove zinc, cadmium, copper, nickel and lead by sunflower plant. Environmental Engineering and Management Journal. 2008;7: 547–558.
- 25. Havelcová M, Mizera J, Sýkorová I, Pekař M. Sorption of metal ions on lignite and the derived humic substances. J Hazard Mater. 2009;161: 559–564. pmid:18490104
- 26. Senesi N, Sposito G, Martin JP. Copper (II) and iron (III) complexation by humic acid-like polymers (melanins) from soil fungi. Sci Total Environ. 1987;62: 241–252.
- 27. Zhang J, Wang S, Wang Q, Wang N, Li C, Wang L. First determination of Cu adsorption on soil humin. Environ Chem Lett. 2013;11: 41–46.
- 28. Rice JA. Humin. Soil Sci. 2001;166: 848–857.
- 29. González-Pérez JA, González-Vila FJ, Almendros G, Knicker H. The effect of fire on soil organic matter—a review. Environment International. 2004;30: 855–870. pmid:15120204
- 30. García AC, Izquierdo FG, Sobrinho NMBDA, Castro RN, Santos LA, Souza LGAD, et al. Humified insoluble solid for efficient decontamination of nickel and lead in industrial effluents. J Environ Chem Eng. 2013;1: 916–924.
- 31. Zhao X, Wang JW, Xu HJ, Zhou CJ, Wang SQ, Xing GX. Effects of crop-straw biochar on crop growth and soil fertility over a wheat-millet rotation in soils of China. Soil Use and Management. 2014;30: 311–319.
- 32. Borchard N, Wolf A, Laabs V, Aeckersberg R, Scherer HW, Moeller A, et al. Physical activation of biochar and its meaning for soil fertility and nutrient leaching–a greenhouse experiment. Soil Use and Management. 2012;28: 177–184.
- 33. Fontana A, Pereira MG, Nascimento GD, Anjos LD, Ebeling AG. Matéria orgânica em solos de tabuleiros na região Norte Fluminense-RJ. Floresta e Ambiente [Forest and Environment]. 2001;8: 114–119.
- 34. Guareschi RF, Pereira MG, Perin A. Organic matter fractions in areas Oxisol under different management systems in Cerrado the State of Goiás, Brazil. Semina: Ciências Agrárias (Londrina). 2013;34: 2615–2627.
- 35.
Hoagland DR, Arnon DI. Growing plants without soil by the water-culture method. Committee on Relation of Electricity to Agriculture; 1950.
- 36. Ure AM, Quevauviller P, Muntau H, Griepink B. Speciation of heavy metals in soils and sediments. An account of the improvement and harmonization of extraction techniques undertaken under the auspices of the BCR of the commission of the European communities. Int J Environ Anal Chem. 1993;51: 135–151.
- 37. Zhuang P, Yang QW, Wang HB, Shu WS. Phytoextraction of heavy metals by eight plant species in the field. Water Air Soil Pollut. 2007;184: 235–242.
- 38. Zacchini M, Pietrini F, Mugnozza GS, Iori V, Pietrosanti L, Massacci A. Metal tolerance, accumulation and translocation in poplar and willow clones treated with cadmium in hydroponics. Water Air Soil Pollut. 2009;197: 23–34.
- 39. Giles CH, MacEwan TH, Nakhwa SN, Smith D. 786. Studies in adsorption. Part XI. A system of classification of solution adsorption isotherms, and its use in diagnosis of adsorption mechanisms and in measurement of specific surface areas of solids. Journal of the Chemical Society (Resumed). 1960: 3973–3993.
- 40. Foo KY, Hameed BH. Insights into the modeling of adsorption isotherm systems. Chem Eng J. 2010;156: 2–10.
- 41. Jordao CP, Fernandes RB, Ribeiro KL, Nascimento BS, de Barros PM. Zn(II) adsorption from synthetic solution and kaolin wastewater onto vermicompost. J Hazard Mater. 2009;162: 804–811. pmid:18602752
- 42. Iqbal M, Saeed A, Zafar SI. FTIR spectrophotometry, kinetics and adsorption isotherms modeling, ion exchange, and EDX analysis for understanding the mechanism of Cd(2+) and Pb(2+) removal by mango peel waste. J Hazard Mater. 2009;164: 161–171. pmid:18799258
- 43. Muscolo A, Sidari M, Attinà E, Francioso O, Tugnoli V, Nardi S. Biological activity of humic substances is related to their chemical structure. Soil Sci Soc Am J. 2007;71: 75–85.
- 44. Droussi Z , D'Orazio V, Provenzano MR, Hafidi M, Ouatmane A. Study of the biodegradation and transformation of olive-mill residues during composting using FTIR spectroscopy and differential scanning calorimetry. J Hazard Mater. 2009;164: 1281–1285. pmid:19013021
- 45. Amir S, Jouraiphy A, Meddich A, El Gharous M, Winterton P, Hafidi M. Structural study of humic acids during composting of activated sludge-green waste: elemental analysis, FTIR and 13C NMR. J Hazard Mater. 2010;177: 524–529. pmid:20106591
- 46. Li X, Xing M, Yang J, Huang Z. Compositional and functional features of humic acid-like fractions from vermicomposting of sewage sludge and cow dung. J Hazard Mater. 2011;185: 740–748. pmid:21030148
- 47. Russell L, Stokes AR, Macdonald H, Muscolo A, Nardi S. Stomatal responses to humic substances and auxin are sensitive to inhibitors of phospholipase A2. Plant and Soil. 2006;283: 175–185.
- 48. Matos GD, Arruda MAZ. Vermicompost as natural adsorbent for removing metal ions from laboratory effluents. Process Biochem. 2003;39: 81–88.
- 49. Fine P, Scagnossi A, Chen Y, Mingelgrin U. Practical and mechanistic aspects of the removal of cadmium from aqueous systems using peat. Environ Pollut. 2005;138: 358–367. pmid:15936861
- 50. Beesley L, Marmiroli M. The immobilisation and retention of soluble arsenic, cadmium and zinc by biochar. Environ Pollut. 2011;159: 474–480. pmid:21109337
- 51. Uchimiya M, Chang S, Klasson KT. Screening biochars for heavy metal retention in soil: role of oxygen functional groups. J Hazard Mater. 2011;190: 432–441. pmid:21489689
- 52. Andreas R, Zhang J. Characteristics of adsorption interactions of Cadmium(II) onto humin from peat soil in freshwater and seawater media. Bull Environ Contam Toxicol. 2014;92: 352–357. pmid:24464297
- 53. Park J-H, Ok YS, Kim S-H, Cho J-S, Heo J-S, Delaune RD, et al. Competitive adsorption of heavy metals onto sesame straw biochar in aqueous solutions. Chemosphere. 2015;142: 77–83. pmid:26082184
- 54. Maksimović I, Kastori R, Krstić L, Luković J. Steady presence of cadmium and nickel affects root anatomy, accumulation and distribution of essential ions in maize seedlings. Biologia Plantarum. 2007;51: 589–592.
- 55. Lux A, Martinka M, Vaculik M, White PJ. Root responses to cadmium in the rhizosphere: a review. J Exp Bot. 2011;62: 21–37. pmid:20855455
- 56. Gill SS, Tuteja N. Cadmium stress tolerance in crop plants: probing the role of sulfur. Plant Signal Behav. 2011;6: 215–222. pmid:21330784
- 57. García AC, Santos LA, Izquierdo FG, Sperandio MVL, Castro RN, Berbara RLL. Vermicompost humic acids as an ecological pathway to protect rice plant against oxidative stress. Ecol Eng. 2012;47: 203–208.
- 58. Canellas LP, Olivares FL, Okorokova-Façanha AL, Façanha AR. Humic acids isolated from earthworm compost enhance root elongation, lateral root emergence, and plasma membrane H(+)-ATPase activity in maize roots. Plant Physiol. 2002;130: 1951–1957. pmid:12481077
- 59. Dobbss LB, Canellas LP, Olivares FL, Aguiar NO, Peres LEP, Azevedo M, et al. Bioactivity of chemically transformed humic matter from vermicompost on plant root growth. J Agric Food Chem. 2010;58: 3681–3688. pmid:20232906
- 60. Khan S, Chao C, Waqas M, Arp HP, Zhu YG. Sewage sludge biochar influence upon rice (Oryza sativa L) yield, metal bioaccumulation and greenhouse gas emissions from acidic paddy soil. Environ Sci Technol. 2013;47: 8624–8632. pmid:23796060
- 61. Melo LC, Puga AP, Coscione AR, Beesley L, Abreu CA, Camargo OA. Sorption and desorption of cadmium and zinc in two tropical soils amended with sugarcane-straw-derived biochar. J Soils Sediments. 2015;16: 226–234.