Article pubs.acs.org/JAFC
Use of Fe-Impregnated Biochar To Efficiently Sorb Chlorpyrifos, Reduce Uptake by Allium fistulosum L., and Enhance Microbial Community Diversity Xiao-Yan Tang,†,∥ Wen-Da Huang,†,∥ Jing-Jing Guo,† Yang Yang,*,†,‡ Ran Tao,† and Xu Feng† †
Institute of Hydrobiology, Jinan University, Guangzhou 510632, China Engineering Research Center of Tropical and Subtropical Aquatic Ecological Engineering, Ministry of Education, Guangzhou, China
‡
ABSTRACT: Fe-impregnated biochar was assessed as a method to remove the pesticide pollutant chlorpyrifos, utilizing biochar/FeOx composite synthesized via chemical coprecipitation of Fe3+/Fe2+ onto Cyperus alternifolius biochar. Fe-impregnated biochar exhibited a higher sorption capacity than pristine biochar, resulting in more efficient removal of chlorpyrifos from water. Soil was dosed with pristine or Fe-impregnated biochar at 0.1 or 1.0% w/w, to evaluate chlorpyrifos uptake in Allium fistulosum L. (Welsh onion). The results showed that the average concentration of chlorpyrifos and its degradation product, 3,5,6-trichloro-2pyridinol (TCP), decreased in A. fistulosum L. with increased levels of pristine biochar and Fe-biochar. Fe-biochar was found to be more effective in reducing the uptake of chlorpyrifos by improving the sorption ability and increasing plant root iron plaque. Bioavailability of chlorpyrifos is reduced with both biochar and Fe-biochar soil dosing; however, the greatest persistence of chlorpyrifos residues was observed with 1.0% pristine biochar. Microbial community analysis showed Fe-biochar to have a positive impact on the efficiency of chlorpyrifos degradation in soils, possibly by altering microbial communities. KEYWORDS: chlorpyrifos, Fe-impregnated biochar, adsorption, plant uptake, microbial diversity
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INTRODUCTION Biochar is a stable carbon-rich byproduct of residue pyrolysis in waste biomass treatment, with various potential applications in the remediation of agricultural and environmental contaminants.1 In addition, biochar is a highly efficient and costeffective sorbent, with applications in the removal of various organic contaminants from water and in reducing the bioavailability of contaminants in soils, therefore decreasing their accumulation and toxicity to plants within the ecosystem.2−4 Extensive research has been performed on the use of biochar in the removal of soil pollutants via adsorption; however, it has been observed that the addition of biochar results in significant changes within the composition and diversity of soil microbial communities, so more attention should be paid to the activity and interactions of biochar with soil biota.3,5,6 It has been shown that dosing of soils with biochar can alter nutrient balance, carbon availability, pH, bacterial adhesion, microorganisms from other ecosystems, cation-exchange capacity (CEC), and water-holding capacity (WHC), with all of these aspects influencing the soil microbial community.5 Despite this, currently little is known about the mechanisms through which biochar affects microbial communities. Therefore, for biochar to be utilized effectively as a method to control pesticide residues in soils, it is essential to establish whether the use of biochar poses a direct risk to soil microbial communities or enhances overall soil health. Recently, a magnetic medium (e.g., magnetite, Fe2O3) was introduced to preparations of powdered biochar to enhance their performance in environmental remediation applications.7,8 In addition to biochar, Fe2O3 is an effective sorption agent for various chemical compounds, such as heavy metals, organic dyes, and antibiotics.9−11 Fe3O4/Fe2O3/activated carbon and γ© 2017 American Chemical Society
Fe2O3 nanocomposites have been shown to enhance the degradation of organic contaminants,12,13 whereas in soil systems, ferrous iron (Fe(II)) can increase the rate of organic pollutant transformation by supporting the growth of soil microorganisms with a reductive ability, increasing levels of biogenic Fe(II) formed by these microorganisms.14,15 Chlorpyrifos (O,O-diethyl O-(3,5,6-trichloro-2-pyridyl) phosphorothioate) is a widely used organophosphorus insecticide for the control of a large number of insect crop pests.16 However, large amounts of this pesticide remain in the environment and are commonly found in water and soil,17 leading to toxicity against nontarget organisms18 and humans19 through the food chain. The half-life of chlorpyrifos in soil is usually between 60 and 120 days, with 3,5,6-trichloro-2pyridinol (TCP) being the major degradation product formed.20 Soil contamination can be defined as an excess or persistence of any element or compound that may cause a toxic response in biota or the general public via direct exposure or secondary toxicity routes, resulting in an unacceptable level of environmental risk.21 To reduce the translocation and accumulation of pesticides within plants and to ensure the safety of agricultural products from contaminated soils, remedial actions are required and biochar systems show promise in this field.2 The objectives of this work were (1) to examine and compare the sorption characteristics of chlorpyrifos with pristine and iron (Fe)-impregnated biochar; (2) to assess Received: Revised: Accepted: Published: 5238
March 23, 2017 May 26, 2017 May 31, 2017 May 31, 2017 DOI: 10.1021/acs.jafc.7b01300 J. Agric. Food Chem. 2017, 65, 5238−5243
Article
Journal of Agricultural and Food Chemistry
dithionite). The whole root system per container, composed of three separate plant root systems, was submerged into 40 mL of DCB solution at 25 °C for 60 min and then rinsed three times with deionized water. Rinse water was retained and combined with the DCB extracts and then made up to a final volume of 100 mL using deionized water,22 and the Fe concentration of the suspension was determined using the 1,10-phenanthroline colorimetric method.23 Plant matter and soil samples were freeze-dried, with extraction of chlorpyrifos and TCP performed using the QuEChERS method.2 Both chlorpyrifos and TCP were measured using high-performance liquid chromatography (HPLC) with an Agilent 1100 system fitted with a Symmetry C18 column and gas chromatograph−mass spectrometer (Agilent: autosampler with oven 7694, GC 6890, MS 5973) with an HP-5 column, following the method established by Agudelo et al.24 and Tang et al.25 High-Throughput Sequencing of the Microbial Community. Genomic DNA was extracted from 0.25 g of the soil sample using the E.Z.N.A.Soil DNA Kit (OMEGA, USA) according to the manufacturer’s protocol. Amplicon libraries were constructed for 454 highthroughput sequencing using the bacterial F515 and R806 primers, which target the V4 hypervariable region. PCR sequences were generated following standard and established methods,26 and PCR products were purified using a QIA quick Gel Extraction Kit (Qiagen, Chatsworth, CA, USA), prior to pyrosequencing using a 454 GS-GSFLX titanium sequencer (454 Life Sciences Corp., Branford, CT, USA).27 Raw reads were analyzed using QIIME software to remove the low-quality sequences,28 and OUT richness, Chao 1, and the Shannon index were determined using Mothur v.1.17.0. Data Analysis. Statistical data analysis was performed using SPSS v.13.0 software (Chicago, IL, USA), with one-way ANOVA analyses used to compare plant uptake of pesticides from biochar and Febiochar dosed soil, chlorpyrifos residue persistence in soil, and iron plaque formation on root surface. Dissipation data for chlorpyrifos within soil was analyzed using a first-order reaction kinetics model, with k as the rate constant (h−1),29 whereas chlorpyrifos half-life (DT50) was calculated on the basis of the reaction constant (DT50 = 0.693/k).
various concentrations of pristine and Fe-impregnated biochar, for their potential to reduce the uptake of chlorpyrifos from soils by Allium fistulosum L. (Welsh onion) plants; (3) to investigate changes in soil microbial diversity following soil dosing with pristine and Fe-impregnated biochar.
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MATERIALS AND METHODS
Materials. Chlorpyrifos (98.2%) and 3,5,6-trichloro-2-pyridinol (TCP; 98.0%) were obtained from Dr. Ehrenstorfer (Germany). Graphitized carbon black (GCB) and primary−secondary amine (PSA) were obtained from CNW Technologies GmbH (Düsseldorf, Germany). Ferrous nitrate (Fe (NO3)3·9H2O) was obtained from Guangzhou Chemical Co. (China). Unless specified, all chemicals were used directly as received. Cyperus alternifolius L. strain was collected as wild type from local constructed wetlands in Guangzhou, China. Preparation of Sorbents. Biochar was produced from dried C. alternifolius L. straw matter, using slow pyrolysis at 450 °C for 3 h under limited-oxygen conditions. The obtained biochar samples were washed using deionized water to remove impurities and then dried at 80 °C. Solutions of iron salt (50 g of Fe (NO3)3·9H2O in 400 mL of DI water) were mixed with 100 g of biochar with continuous agitation for 12 h and then dried at 100−120 °C. Biochar material was then washed with deionized water to remove surface iron hydroxide and dried at 80 °C, resulting in Fe-impregnated biochar material.9 The morphology of the biochar materials utilized in these studies was observed using field-emission scanning electron microscopy (SEM; Zeiss Ultra 55), equipped with an energy dispersive X-ray spectrometer (EDS) and X-ray diffractor (XRD, Rigaku, MiniFlex600, Cu Kα, Japan). Chlorpyrifos Sorption and Plant Growth Experiments. Chlorpyrifos is an organophosphate pesticide with low water solubility (2.0 mg L−1 at 25 °C) and high hydrophobicity (log Kow = 4.70).2 To determine adsorption isotherms, a simulated environmental water system was used, where the chlorpyrifos solution was diluted to 0.2, 0.3, 0.4, 0.5, 0.6, 0.8, 1.0, and 1.5 mg L−1 using 0.05 mol L−1 CaCl2 solution, with 100 mg L−1 NaN3 added to inhibit bacterial degradation of chlorpyrifos. Sorbent material (0.01 g) was added to 10 mL of chlorpyrifos, with the mixture sealed in a Teflon-capped glass vial and shaken at 25 ± 1 °C for 24 h to reach the adsorption equilibrium. The final suspension was filtered through a 0.45 μm PTFE filter (Millipore, Bedford, MA, USA), and the filtrate was extracted by liquid−liquid extraction using hexane, collected, and then analyzed immediately. A. fistulosum L. was utilized as a model for plant uptake, with plants maintained in a research greenhouse at Jinan University (Guangzhou, China). Study units were composed of a plastic container forming a closed system, filled with 300 g of soil with three A. fistulosum L. seedlings selected to be in a healthy condition and of 3 cm height. To evaluate the effect of dosing soil with either biochar or Fe-biochar, the following treatments were used: (1) unamended soil; (2) biochardosed soil at 0.1 or 1.0% (w/w); (3) Fe-biochar-dosed soil at 0.1 or 1.0% (w/w), with each treatment performed in triplicate. One and a half milliliters of a 10 mg mL−1 chlorpyrifos solution was added into every test system, resulting in a final exposure concentration of 50 mg kg−1, and containers were agitated continually for 24 h. Following this, the containers were opened and air-dried to allow acetone to evaporate for 48 h. Soil moisture content was adjusted to 50% of soils maximum water-holding capacity (MWHC) before A. fistulosum L. seedlings were planted in triplicate, with watering every 48 h and maintained at a constant grow temperature of 34/27 °C day/night. Soil samples were collected every 7 days, as well as at the end of the study (day 35), when above-ground sections of plants were harvested and weighed to establish fresh weights. The underground portions of plants (root systems) were removed from the soil substrate, and they were then carefully and thoroughly washed with deionized water to remove the substrate from the surface of the roots prior to analysis. Analytical Method. Iron plaques were extracted from fresh root surfaces using a dithionite−citrate−bicarbonate (DCB) solution (0.03 M sodium citrate; 0.125 M sodium bicarbonate; and 0.6 g of sodium
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RESULTS AND DISCUSSION
Characterization of the Samples. To confirm the presence of iron oxide in Fe-biochar, SEM-EDS and XRD analyses of both pristine biochar and Fe-biochar was performed, with results presented in Figure 1. SEM analysis of biochar and Fe-biochar structures shows that the surface of Fe-biochar is more complex, with more roughness than seen on the pristine biochar. This may result from the presence of magnetic iron particles covering the biochar surface, where effectively Febiochar is composed of two phases, iron oxide nanoparticles and biochar. Successful impregnation of Fe onto the Fe-biochar surface was established using EDS analysis, confirming the presence of iron oxide on the surface of both biochar and Febiochar, although showing various atomic proportions of Fe and O, with pristine biochar ranging from 0 to 23.76% and Febiochar ranging from 3.97 to 26.84% (Figure 1A1−2). The XRD patterns for pristine biochar and Fe-biochar are presented in Figure 1B, showing that iron oxide particles mainly correspond to magnetite, with only minimal additional phases observed. Novel peaks appeared in the spectra of Fe-biochar (2θ = 35.4°(Fe3O4) and 62.7° (Fe2O3)),30,31 indicating that iron oxides in matrix with biochar were well crystallized. Batch Sorption of Chlorpyrifos onto Pristine Biochar and Fe-Biochar. Sorption isotherms for chlorpyrifos and pristine biochar or Fe-biochar are shown in Figure 2, with isotherm equilibrium data established and analyzed using the Langmuir isotherm model and the Freundlich isotherm model. 5239
DOI: 10.1021/acs.jafc.7b01300 J. Agric. Food Chem. 2017, 65, 5238−5243
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Figure 2. Sorption isotherms of chlorpyrifos onto pristine biochar and Fe-biochar.
capacity of adsorbents (μg g−1); and KL is the Langmuir adsorption equilibrium constant (L μg−1), where qmax and KL can be determined by the intercept and the slope of the linear plot of Ce/qe versus Ce, respectively. Table 1 shows the coefficient of determination (R2) for biochar (R2 = 0.818) and Fe-biochar (R2 = 0.865), with maximum chlorpyrifos sorption capacities of biochar and Febiochar obtained using the Langmuir model being 724.29 and 769.23 μg g−1, respectively. The Langmuir constant, KL, which denotes sorption energy, was found to be 0.011 L μg−1. The isotherms suggest that high affinity surface sorption mechanisms exist for chlorpyrifos on both biochar and Fe-biochar and as the KL values for biochar and Fe-biochar lie between 0 and 1, an ongoing adsorption process is favorable.33 In comparison to the Langmuir isotherm model, the Freundlich isotherm is an empirical equation employed to describe heterogeneous systems,34 with a linear form of the Freundlich equation being 1 ln qe = ln KF + ln Ce n where qe and Ce are the adsorption equilibrium, KF (μg g−1)(μg L−1)n is the Freundlich affinity coefficient, and n is the Freundlich linearity index. The Freundlich isotherm showed a slightly better overall fit with data generated (R2 = 0.926 for biochar and R2 = 0.910 for Fe-biochar) as compared with the Langmuir model (Table 1). The best-fit Freundlich constants were 48.6 ((μg g−1) (μg L−1)n) KF and 0.46 n for pristine biochar and 61.62 ((μg g−1)(μg L−1)n) KF and 0.40 n for Fe-biochar, confirming the ability of Fe-biochar to adsorb chlorpyrifos more efficiently at room temperature than pristine biochar. We found similar results for the removal of various contaminants by zero-valent iron biochar.35 As the n value is below unity, the adsorption of chlorpyrifos onto the surface of both pristine biochar and Febiochar could be affected by chemisorption mechanisms under the experimental conditions utilized.36 Uptake of Chlorpyrifos from Soil by A. fistulosum L. and the Effect of Soil Dosing with Pristine Biochar and Fe-Biochar. Following 5 weeks of growth in treated soils, A. fistulosum L. were analyzed to determine the concentration of chlorpyrifos residues remaining (Figure 3). The addition of pristine biochar and Fe-biochar into soils significantly (p
0.760), with the half-lives of chlorpyrifos in the soil types ranging from 23.654 to 29.731 days, ranked in the order of persistence of 1.0% biochar > 1.0% Fe-biochar > 0.1% biochar > unamended soil > 0.1% Febiochar. It is of note that the half-life of chlorpyrifos in unamended soil, 0.1% Fe-biochar, and 0.1% biochar showed no significant difference. In addition, the half-life of chlorpyrifos in 1.0% Fe-biochar or 1.0% pristine biochar showed no significant difference, although both of these were significantly longer halflives than were observed in the other systems. As the content of biochar loading increases, the half-life of chlorpyrifos increases, suggesting that pristine biochar and Fe-biochar reduced chlorpyrifos biodegradability, findings that are similar to previous studies.2 However, when the pristine biochar and Fe-biochar contents are the same, the half-life of chlorpyrifos in Fe-biochar-amended soil is shorter than that of pristine biocharamended soil, which suggested that Fe-biochar perhaps can increase chlorpyrifos degradation in the soil. Early reports showed that the redox action of Fe2+/Fe3+ (Fe(II)/Fe(III)), the electron-transfer mediator of the BC oxygen functional groups, and Fe-impregnated biochar had notable influences on the microbial community and promoted the rapid degradation of microorganisms.8,40 High-throughput sequencing was used to analyze microbial community dynamics in soil as a result of pristine biochar and Fe-biochar dosing. The number of operational taxonomic units (OTUs) increased from 2978 to 3651, whereas the Chao 1 index and Shannon diversity index increased from 4739 to 5398 and from 7.16 to 8.80, respectively, when biochar and Fe-biochar were added to the soil. Therefore, the richness and diversity of species were improved with biochar dosing, with overall ranking in the order of 1.0% Fe-biochar > 1.0% biochar > 0.1% Fe-biochar > 0.1% biochar > unamended soil (Figure 4). These findings indicate that the presence of biochar or Fe-biochar can increase the richness and diversity of species in the soil, as supported by the results of previous studies.5 The bioavailability of chlorpyrifos was reduced with both pristine biochar and Fe-biochar soil dosing, reducing plant access to pesticide residues; however, compared with pristine biochar, Fe-biochar was more effective in chlorpyrifos degradation, potentially due to changes in the
Figure 3. Iron plaque formation on root surfaces of A. fistulosum L. under various biochar and Fe-biochar exposures, with detectable concentrations of chlorpyrifos and TCP residues in above-ground parts of A. fistulosum L. Different letters above columns represent statistically significant differences (p < 0.05).
0.05) reduced chlorpyrifos bioaccumulation in A. fistulosum L. by 3−75% and reduced TCP bioaccumulation by 9−57%. The results indicated the extent of the reduction in chlorpyrifos and TCP bioaccumulation with increasing pristine biochar or Febiochar soil loadings. Figure 3 shows that the lowest concentrations for chlorpyrifos and TCP residues were detected in A. fistulosum L. grown in soils containing 1.0% Fe-biochar. The uptake of chlorpyrifos and TCP in A. fistulosum L. can be ranked, from highest to lowest level of uptake, as unamended soil system > 0.1% biochar system > 0.1% Febiochar system > 1.0% biochar system > 1.0% Fe-biochar system. These findings are consistent with previous work on chlorpyrifos uptake in plant species, showing the uptake of the pesticides are lower overall in soil dosed with biochar.2,4 In the present study, Fe-biochar was found to be better than pristine biochar for preventing uptake of chlorpyrifos by A. fistulosum L., with the uptake of chlorpyrifos by A. fistulosum L. found to show no significant difference when grown in unamended soil or soil dosed with only 0.1% pristine biochar. The uptake of pesticides by plant species in the presence of pristine biochar has been found to be dependent on various factors, such as feedstock material, production temperature, and biochar application rate,37,38 which is consistent with the findings of the present study. Iron plaque formation on root surfaces (DCB-Fe) (p < 0.05) was shown to increase due to dosing with both pristine biochar and Fe-biochar, with a maximum increase of 2.3-fold observed in 1.0% Fe-biochar dosed soil systems (Figure 3). These results show that biochar increased iron plaque formation,39 and in comparison with pristine biochar, Fe-biochar may increase iron plaque formation on root surfaces, preventing chlorpyrifos and TCP uptake by A. fistulosum L. 5241
DOI: 10.1021/acs.jafc.7b01300 J. Agric. Food Chem. 2017, 65, 5238−5243
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of China. E-mail:
[email protected],
[email protected]. Phone: 86-20-85222101. Fax: +86-20-85222101. ORCID
Yang Yang: 0000-0002-4123-4888 Author Contributions ∥
X.-Y.T. and W.-D.H. contributed equally to this work.
Funding
We acknowledge the financial support from Special-funds Project for Applied Science and Technology of Guangdong Province (Project 2015B020235008) and the National Natural Science Foundation of China (Fund 51579115). Notes
The authors declare no competing financial interest.
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Figure 4. Microbial species richness and diversity in chlorpyrifoscontaminated soil systems: unamended soil; pristine biochar-dosed soil; and Fe-biochar-dosed soil.
soil microbial communities. Therefore, soil amendment with Fe-biochar may be a promising in situ remediation technique for pollutant sequestration and to minimize pesticide residue accumulation in agricultural stock produced in contaminated soils.
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REFERENCES
AUTHOR INFORMATION
Corresponding Author
*(Y.Y.) Institute of Hydrobiology, Jinan University, 601 Huangpu West Road, Guangzhou 510632, People’s Republic 5242
DOI: 10.1021/acs.jafc.7b01300 J. Agric. Food Chem. 2017, 65, 5238−5243
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