Effects of superabsorbent polymers on the fate of fungicidal carbendazim in soils

Journal of Hazardous Materials 328 (2017) 70–79

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Effects of superabsorbent polymers on the fate of fungicidal carbendazim in soils Yatian Yang, Haiyan Wang ∗ , Lei Huang, Sufen Zhang, Yupeng He, Qi Gao, Qingfu Ye ∗ Institute of Nuclear Agricultural Sciences, Key Laboratory of Nuclear Agricultural Sciences of Ministry of Agriculture and Zhejiang Province, Zhejiang University, Hangzhou 310029, China

h i g h l i g h t s

g r a p h i c a l

a b s t r a c t

• SAPs affected the transformation of MBC in oxic soils.

• MBC mineralization was obviously inhibited in loamy and saline soils with SAPs. • SAPs enhanced the dissipation of MBC in acidic clayey soil. • SAPs increased the bound residue of MBC in soils. • Soil microbial state was changed after treated with MBC and SAPs during incubation.

a r t i c l e

i n f o

Article history: Received 13 September 2016 Received in revised form 27 December 2016 Accepted 28 December 2016 Keywords: Superabsorbent polymers (SAPs) Carbendazim Transformation Metabolites

a b s t r a c t Superabsorbent polymers (SAPs) have been extensively used as soil amendments to retain water, and they often coexist with pesticides in agricultural fields. However, effects of SAPs on the fate of pesticides in soil remain poorly understood. In this study, a laboratory experiment was conducted to evaluate the effects of SAPs on the transformation of 14 C-carbendazim in soils. The results showed that compared to the SAPs-free control, 11.4% relative reduction of 14 C-carbendazim extractable residue was observed in red clayey soil with SAPs amendment after 100 days of incubation (p < 0.05). Carbendazim dissipation was enhanced by 34.7%, while no obvious difference was found in loamy soil and saline soil (p > 0.05). SAPs changed the profiles of major metabolites (2-aminobenzimidazole and 2-hydroxybenzimidazole) to some extent. After 100 days of SAPs treatment, the mineralization of 14 C-carbendazim was significantly reduced by 37.6% and 41.2% in loamy soil and saline soil, respectively, relative to the SAPs-free treatment (p < 0.05). SAPs increased the bound residue of carbendazim by 11.1–19.1% in comparison with SAPsfree controls. These findings suggest SAPs amendments significantly affected the fate of carbendazim and attention should be given to the assessment of environmental and ecological safety of pesticides in SAPs-amended soils. © 2017 Elsevier B.V. All rights reserved.

1. Introduction Abbreviations: SAPs, superabsorbent polymers; MBC, carbendazim; POPOP, 1, 4-bis (5-phenyloxazoly-2-yl)-benzene; PPO, 2, 5-diphenyloxazole; ER, extractable residue; BR, bound residue; St-g-PAM, starch-g-polyacrylamide; MBA, N, N’-methyl bis-acrylamide; 2-AB, 2-aminobenzimidazole; H-AB, 2-hydroxybenzimidazole. ∗ Corresponding authors. E-mail addresses: [email protected] (Q. Ye), [email protected] (H. Wang) . http://dx.doi.org/10.1016/j.jhazmat.2016.12.057 0304-3894/© 2017 Elsevier B.V. All rights reserved.

Superabsorbent polymers (SAPs) can absorb and retain up to several hundred times their weight of water [1]. Due to their excellent water retention abilities, SAPs have been widely utilized in many areas such as medicine, horticulture, sanitary products, and agriculture [2–5]. In particular, SAPs are usually applied as soil con-

Y. Yang et al. / Journal of Hazardous Materials 328 (2017) 70–79

ditioner in agriculture to hold soil moisture, improve soil stability or aeration, and prevent soil erosion [6]. Moreover, SAPs have been employed in combination with pesticides to control their release rates in order to promote the efficiency use of both pesticides and water [7,8]. Therefore, it is common for pesticides and SAPs to coexist in agricultural fields. SAPs are macromolecule polymers, capable of serving as an organic carbon source for soil microorganisms [8]. The presence of SAPs and other organic amendments could alter soil microbial communities, and hence influence the environmental behaviors of pesticides in soils. Marin-Benito et al. [9] demonstrated that amendment with mushroom substrates enhanced microbial activity and promoted the dissipation of fungicides in the vineyard. Achtenhagen et al. [10] found that SAPs amendments could significantly increase the sorption of 14 C-imazalil in soils and stimulate microbial activity. Additionally, SAPs contain certain functional groups, such as carboxylic acid, carboxamide, hydroxyl, amine, and imide groups, which could interact with pesticides or the soil matrix via catalysis with soil enzymes and microorganisms [11]. Thus, SAPs might influence the biological/abiotic degradation behavior of pesticides in soils. The addition of SAPs would generate unpredictable impacts on the fate and ecological effect of pesticides. Thus, the environmental fate, biological effects, and toxicity of commercially available pesticides in SAPs-amended soil must be clarified. Carbendazim, a broad-spectrum benzimidazole fungicide, is widely used to control fungal diseases in crops and vegetables [12]. Carbendazim could adsorb strongly to soils, and is moderately persistent in crops and soils, posing risks to agroecosystem and human health [13]. However, little is known of the effects of the co-existence of SAPs and carbendazim on the environmental fate of carbendazim in soils. Therefore, we used self-synthesized SAPs combined with 14 C-labelled carbendazim to evaluate the transformation of carbendazim, including characterization of dissipation of the parent compound, the kinetic changes of metabolic products and extractable residue (ER), non-extractable/bound residue (BR) and mineralized 14 C-CO2 in soils amended with SAPs during the incubation.

2. Material and methods 2.1. Chemicals 14 C-Carbendazim

(methyl (1H-benzo[d]imidazol-2-yl-2carbamate; radio-chemical and chemical purity >97%; 51 mCi/mmol specific radioactivity) was purchased from ChemDepo Incorp. (Camarillo, CA). The 14 C-labeling position of carbendazim was 2-[14 C]-benzimidazole nuclei. Non-labelled carbendazim (chemical purity > 96%) was obtained from Sigma-Aldrich (Munich, Germany). Glycol ether, ethanolamine, methanol, hydrochloric acid, and sodium hydroxide were all analytical grade reagents. Scintillation grade reagents of 1,4-bis (5-phenyloxazoly-2-yl)benzene (POPOP) and 2, 5-diphenyloxazole (PPO) were obtained from Arcos Organics (Geel, Belgium). Scintillation cocktail I consisted of 0.5 g POPOP, 7.0 g PPO, 650 mL dimethyl benzene and 350 mL glycol ether. Scintillation cocktail II consisted of 0.5 g POPOP, 7.0 g PPO, 550 mL dimethyl benzene, 275 mL glycol ether, and 175 mL ethanolamine. Acetonitrile, water and glacial acetic acid were chromatography grade. The stock solution of 14 C-carbendazim was prepared by mixing non-labelled carbendazim and the labelled in methanol with a final specific activity of 4.625 × 104 Bq mg−1 . 14 C)

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2.2. Soil and SAPs Three samples of natural soils were collected from the first 0–15 cm-layer of soil from agricultural fields in Hangzhou (fluviomarine yellow loamy soil), Cixi (coastal saline soil), and Longyou (red clay soil), Zhejiang Province, China. These soils are abbreviated herein as S1 , S2 , and S3 . Some selected physico-chemical properties of soils were determined using standard methods [14,15] and summarized in Table 1. All soils were air-dried, passed through a 2-mm sieve and stored at room temperature before use. SAPs, starch-graft-polyacrylamide (St-g-PAM) superabsorbent crosslinked by N,N-methyl bisacrylamide were prepared using 10 MeV simultaneous electron beam irradiation at room temperature and subsequent alkaline hydrolysis [16]. The swelling ratio of SAPs (deionized water) was approximately 1000 g g−1 . SAPs were dried at room temperature in a vacuum drying apparatus. 2.3. Soil treatment and incubation experiment The incubation experiment was carried out under aerobic conditions as per the OECD guideline 307 [17]. Pre-incubation was conducted at 25 ± 1 ◦ C for 10 days and all soil water content was separately adjusted to 40% of the water-holding capacity. SAPs were then amended to 0.5‰ (w/w) in soils. Carbendazim was applied to the soils by dissolving in methanol and fully mixing with soil samples at 4 mg kg−1 (approximately 300 g soil, dry weight equivalent). Subsequently, soil moisture content was regulated to 60% of the water-holding capacity. Similarly, the SAPs-free treatment with carbendazim underwent the above procedures. The uniformity of 14 C-distribution was confirmed by the combustion of 1.0 g of the soil subsample (three replicates) in a biological oxidizer (RJ Harvey Instruments, Hillsdale, NJ). Blank controls without carbendazim and SAPs were used for microbial analysis and subjected to the same process. The evenly mixed soils were transferred to 500 mL brown jars fitted with a flow-through apparatus for trapping solutions, as described by Fu et al. [18]. The experimental settings were placed in an incubator at 25 ± 1 ◦ C and ventilated periodically. Soil subsamples (10 g, dry weight equivalent) were collected from each soil container at intervals of 0, 3, 6, 13, 20, 30, 45, 60, 80, and 100 days after treatment (DAT) and the experiments were conducted in triplicate for each treatment. An equivalent quantity of distilled water was added to maintain soil moisture at 60%, and all the trapping solutions were replaced regularly with fresh solutions at each sampling time. The trapping solutions were preserved to measure the radioactivity on a liquid scintillation counter (LSC, Quatalus-1220, Perkin-Elmer, Turku, Finland). An aliquot of 1-mL for each trap was obtained and added to 15 mL of cocktail I, then stored in the dark for 24 h before counting to avoid chemiluminescence. Only the 14 C-CO2 solution was detected the radioactivity in all the traps. Soil subsamples were removed to determine the radioactivity of extractable, and non-extractable residue. The amount of 14 C-carbendazim present in the form of parent and/or intermediates during sampling. 2.4. Soil extraction and combustion analysis Soil samples (10.0 g, dry weight) per treatment were processed in a polypropylene centrifuge and sequentially extracted following a modified procedure derived from Helweg [19] and Wang et al. [20]. Briefly, soil samples were extracted three times with 30 mL of methanol/0.1 M hydrochloric acid solution (4:1, v/v), blended thoroughly, and shaken for 2 h at 120 rpm on a rotary shaker, centrifuged at 6000g for 5 min. The deposits were then similarly re-extracted by shaking with methanol, and ethyl acetate, consecutively, until no more 14 C-radioactivity was detected in the extracts. The recovery extraction of 14 C activity was approximately

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Table 1 Basic physicochemical properties of the tested soils. Property

Soil type

Soil type

S1 Red sandy clay soil

S2 fluvio-marine yellow loamy soil

S3 coastal saline soil

pH(H2 O) OMa (g kg−1 ) Total N (%) CECb (cmol kg−1 ) Clay (%) Silt (%) Sand (%) P(mg kg−1 ) K(mg kg−1 )

4.20 8.40 0.34 6.62 39.0 41.1 19.9 3.21 4650

7.02 30.50 2.90 10.83 8.0 71.2 20.8 25.20 8122

8.84 9.50 1.80 10.17 24.3 71.1 4.6 10.80 9768

a b

Organic matter. Cation exchange capacity.

95.5–101.6% when freshly spiked soils were analyzed. A 1-mL aliquot of every treatment supernatant was removed with each addition of 10-mL cocktail I to measure the 14 C-activity on LSC. The 14 C-radioactivity of total extracted solvents was calculated as the extractable residue (ER). All remaining solutions were passed through a 0.22-␮m filter and reduced in bulk to near dryness by a Vacuum Rotary Evaporators (Eyela SB-1000, Eyela, Tokyo, Japan) at 45 ◦ C. The residue was re-dissolved in 10-mL methanol and condensed to 1-mL under a stream of nitrogen at ambient temperature for high performance liquid chromatography-tandem mass spectrometry (HPLC–MS/MS) analysis. All the post-extracted soils were air-dried. A homogenized soil sample of 1.0 g was combusted on the biological oxidizer and the released 14 C-CO2 was trapped in 15 mL of cocktail II for analysis on LSC. The combustion recovery was 95.7 ± 1.4% (n = 3). The amount of 14 C-radioactivity in the post-extracted soils was defined as bound residue (BR). 2.5. LC–MS/MS analysis A 40-␮L aliquot of each eluent fraction was injected into Waters 2695 HPLC system (Waters, Milford, MA) equipped with a Photodiode Array Detector and Agilent C18 column (5 ␮m, 4.6 × 250 mm, Elite Co., Dalian, China) at 254 nm and 280 nm. The column temperature was maintained at 25 ± 1 ◦ C. Mobile phase A was acetonitrile with 0.1% acetic acid (v/v) and mobile phase B was ultrapure water with 0.1% acetic acid (v/v). The following gradient program was used (0–20 min, 10–60% A; 20–30 min, 60–100% A; 30–32 min, 100–10% A; 32–35 min, 10% A) at 1.0 min mL−1 . The post-column eluent was collected into 20 mL glass scintillation vials at 1.0 min and measured by adding 10 mL of scintillation cocktail I using LSC. The extracts of soil samples were used to identify carbendazim and metabolites. A subsample was injected into the same HPLC system in tandem with a quadrupole time-of-flight (Q-TOF) high-definition mass analyzer (Agilent 6530, Santa Clara). The chromatography conditions were the same as given earlier. The electrospray ionization (ESI) was in positive mode, and Q-TOF-MS parameters were 250 ◦ C for ion source temperature, 350 ◦ C for the dry gas temperature, 8 L min−1 of flow rate, 35 psi for nebulizer and 4000 V for capillary voltage. The collision energy was between 5 and 50 eV and ion [M+H]+ for the m/z range from 50 to 1000. All acquisition and analysis of data were controlled by the Agilent Mass Hunter workstation software. 2.6. Microbial diversity and community structure analysis The total DNA was extracted from 0, 45, and 100 d soil samples for each treatment for soil bacteria analysis. The primers 338 F (5 -ACTCCTACGGGAGGCAGCA-3 ) and 806 R (5 GGACTACHVGGGTWTCTAAT-3 ) were used for PCR amplification

of 16S rRNA (Gene Amp 9700, ABI, U.S.A.). The PCR program was as follows: 2.5 mM of dNTP, 5 ␮M of each primer, 0.4 unit of Fast Pfu Polymerase; the cycling process was 95 ◦ C for 3 min, 27 cycles of 95 ◦ C for 30 s; 55 ◦ C for 30 s; 72 ◦ C for 45 s, the final extension step was at 72 ◦ C for 10 min. PCR products were sequenced using the Miseq-sequencing technique (Majorbio Co., Shanghai, China). All filtered sequences underwent bioinformatics and statistical analyses.

2.7. Data analysis The sample data are shown as the means and standard errors (means ± SEM) resulting from triplicate analyses. Using SPSS 20.0 (IBM SPSS Statistics, Armonk, NY, U.S.A.), we determined the significance based on one-way ANOVA at ␣ = 0.05. Figures were plotted by using Origin 8.0 (Microcal Software, Northampton, MA) and R programming language.

3. Results and discussion 3.1. The formation of ER in SAPs-amended soils Throughout the 100 d incubation, the whole 14 C-mass balance was calculated as the sum of ER, BR, and mineralization, and ranged from 92.5 to 105.0% after spiking 14 C-labelled carbendazim in the three test soils, indicating good mass recoveries for the analysis in this study. Fig. 1 shows the kinetic changes of ER of carbendazim for treatments with or without SAPs in soils as a function of incubation time. ER which consisted of the parent compounds and metabolites gradually decreased with time in all soils. For both treatments, the total ER in S1 was significantly higher than those in S2 and S3 (p < 0.05). After 13 days of incubation, the amount of ER was approximately 90% of the applied amount and followed a continuously decreasing trend in S1 . At the end of incubation, the proportion of ER in S1 decreased to 62.2% and 70.2% in soil with and without SAPs treatments, respectively, and a significant relative reduction of 11.4% was observed in the treatment with SAPs as compared to the SAPs-free treatment at 100 d (p < 0.05). This was markedly different from the results of Achtenhagen et al. [10], in which the ER of imazalil largely coincided in SAPs-amended soil, relative to the control. However, in loamy S2 and saline S3 , ER dropped sharply from the first 3 days, stabilized at 60 d, and remained constant at 6.9–11.4% of the 14 C-spiked amount. Further statistical analysis showed no significant difference in the ERs of carbendazim in S2 and S3 between samples with and without SAPs during the whole incubation (p > 0.05).

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Fig. 1. Kinetic changes of extractable residue of 14 C-spiked amount in the soils: a) soil 1 (S1 ); b) soil 2 (S2 ); c) soil 3 (S3 ). Values are means with standard deviations (n = 3).

3.2. Characterization of the parent compound and intermediates 3.2.1. Dissipation of carbendazim in SAPs-amended soils Fig. 2 shows the dissipation patterns of carbendazim in soils with and without SAPs as a function of incubation time. During the incubation, the percentage of the parent compound was significantly higher in S1 than that in S2 or S3 . At 100 d, about 51.0% of the 14 C-spiked amount was detected in SAPs treatment, compared to about 62.2% in SAPs-free treated S1 . However, the fraction of carbendazim decreased to 42.7% and 52.8% in soil with and without SAPs treatments at 20 d for S2 , 38.0% and 50.7% for S3 , respectively. The dissipation of the parent compound fitted well with the firstorder equation and regression parameters of R2 ranged from 0.986 to 0.996. The half-lives, first-order equations, and the degradation curves are shown in Table 2 and Supplementary Fig. A1 . Generally, the dissipation rates of carbendazim followed the order of S3 > S2 > S1 under both treatments with and without SAPs. When amended with SAPs, the half-lives were reduced from 154.0 d to 100.5 d for S1 , from 22.5 d to 19.4 d for S2 , and 21.9 d to 18.3 d for S3 . SAPs amendment enhanced the dissipation of carbendazim at different extents in the tested soils, especially for S1 . There was a significant difference between the treatments with and without SAPs in S1 (p < 0.05). The dissipation rate of carbendazim was enhanced by 34.7% in S1 as compared to the SAPs-free treatment. Similarly, Castillo et al. [21] showed that addition of O-vermicopost

in soil mitigated the half-life of diuron, and improved microbial activity and diversity. Karas et al. [22] found that thiabendazole and imazalil degraded rapidly in organic biomixture treatments as contrasted with the untreated. Helweg [19] suggested that carbendazim was a poor carbon source and its degradation was a co-metabolic process. Addition of easily degradable substrates promoted the biodegradation of chlorophenols and antibiotics [23,24]. SAPs, as hydrogels substrate, could be readily available nutrition for soil microbes, and has the potential to change microbial diversity and community structure to enhance the co-metabolic degradation of carbendazim in the test soils [25]. Based on the analysis of microbial diversity (Supplementary Fig. A 2a & b), our findings indicated that application of SAPs and carbendazim resulted in greater diversity and more richness for species compared with the controls during the incubation. Moreover, the results on the adsorption of carbendazim in all un-amended and amended soils were satisfactorily described by the Freundlich model with R2 > 0.985 and Kf values of 3.95-9.47 (Supplementary Table A1). No significant difference in adsorption capacity was found in S1 with and without SAPs, which indicated that the greater microbial diversity may have a greater influence on the dissipation of carbendazim in S1 . However, addition of SAPs in S2 and S3 significantly enhanced carbendazim sorption to soils, which was consistent with the results of experiments on organic compound adsorption enhancements with rice-straw-ash

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Fig. 2. Distribution of 14 C activity of carbendazim, metabolites in extracts in the soils: a) soil 1 (S1 ); b) soil 2 (S2 ); c) soil 3 (S3 ). Values are means with standard deviations (n = 3).

Table 2 Kinetics parameters for the dissipation of parent carbendazim in the soils with and without amendment of SAPs. Soil

Treatment

k(d−1 )

Correlation coefficient(R2 )

Half-life (d)

P

S1

without with without with without with

0.0045 ± 0.0002 0.0069 ± 0.0003 0.0308 ± 0.0012 0.0357 ± 0.0024 0.0317 ± 0.0022 0.0379 ± 0.0009

0.990 0.986 0.996 0.990 0.987 0.987

154.0a 100.5b 22.5a 19.4a 21.9a 18.3a

<0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001

S2 S3 a-b

k value at the different treatment differ significantly in the same soil (p < 0.05).

Y. Yang et al. / Journal of Hazardous Materials 328 (2017) 70–79

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Table 3 Mass spectrometry data for the identification of carbendazim and metabolites in soils. Compound

Retention time (min)

Theoretical m/z

Experimental m/z

Determination m/z

MBC

7.4

192.0782

192.0679

160.0468 132.0516 117.0406 105.0411 65.0360

2-AB

4.5

134.0674

134.0547

119.0142 107.0429 92.0344 80.0349 65.0253

H-AB

9.3

135.0514

135.0592

107.0610 92.0209 80.0503 65.0386 53.0391

amendments [26]. The increased sorption effectively reduced the bioavailability of the parent compound in SAPs-amended soils, and could inhibit the dissipation of the parent compound. The increased microbial diversity usually promoting the pesticide dissipation may be compensated for the enhanced sorption in SAPs-amended S2 and S3 , resulting in the negligible enhancement dissipation rate of carbendaizm. Similarly, Achtenhagen et al. [10] found that SAPs amendments did not have any substantial influence on the dissipation of 14 C-imazalil, although microbial community was stimulated and increased adsorption was observed. Panades et al. [27] demonstrated that carbendazim was stable in acidic and barren soils, which is consistent with our observation in red clayey soil. SAPs amendment enhanced the degradation of carbendazim substantially in acidic soil, and would be an effective measure to reduce the persistence and potential environmental risk of carbendazim in soils. 3.2.2. Characterization of intermediate products HPLC–MS/MS analysis showed that the three radioactive compounds were detected in extracts and identified as carbendazim, 2-aminobenzimidazole (2-AB) and 2-Hydroxybenzimidazole (HAB). The structural and fragmentation information for carbendazim and metabolites are shown in Table 3 and Supplementary Fig. A3 . The contents of 2-AB and H-AB are shown in Fig. 2. In S1 treated with SAPs, 2-AB reached a maximum value of 7.5% of the applied amount at 45 d and accounted for 0.8–7.5% of the total throughout the whole incubation. While for the SAPs-free treatment, 2-AB content was initially present at 6 d and achieved a maximum value of 4.4% at 80 d. In S2 treated with SAPs, the content of 2-AB was 1.1–8.8%, which was relatively higher than the range of 0.3–4.0% in SAPs-free treatment. In S3 , when SAPs were added, 2-AB varied from 1.3 to 8.6% with the maximum value appearing at 20 d, compared to 1.8–6.0% in SAPs-free treatment. H-AB was likely a transient intermediate and accounted for 0.2–2.6%. Obviously, to some extent, SAPs changed the varying pattern of the two main metabolites (2-AB and H-AB) in all soils. 3.3. The formation of BR in SAPs-amended soils The dynamic trends of BR content over time are shown in Fig. 3. During incubation, BR displayed an increasing trend in S1 . However, BR increased rapidly for 45 d and then plateaued in S2 and S3 until 100 d. At the end of incubation, the amount of BR was responsible for 40.5%, 77.7% and 82.3% of the 14 C-applied amount in S1 , S2 , and S3 treated with SAPs, respectively as compared to 34.0%, 69.8% and 74.1% in the SAPs-free treatment. A significant differ-

Chemical structure

ence in BR of carbendazim was observed between samples with and without SAPs treatment in all the soils (p < 0.05), and the relative enhancement of BR was 11.1–19.1% compared to SAPs-free treatment. The BR values for S2 and S3 notably exceeded the criteria of the Commission of the European Community, which indicated that no authorization would be provided if BR was formed at >70% of the initial amount with mineralization to CO2 at <5% in laboratory tests after 100 days of incubation. Unless there was a demonstration that no accumulation of residues occurred in soils under field conditions or tests on the environmental fate, long term effects and crop residue analysis was conducted to identify any risks posed by the BR [28,29]. The addition of SAPs produced higher percentages of BR which included carbendazim and metabolites. Physical entrapment of SAPs, carbendazim, and metabolites in soil organic and inorganic matrices stimulated by microorganisms could lead to the formation of organoclay complexes and soil aggregates, which could result in the enhancement of BR in soils. Gevao et al. [30] showed that pesticides and metabolites containing amino groups or hydroxyl would potentially prefer to adsorb to soil, leading to an increase in BR formation by chemical bonding. Chemically, with polar groups of −COOH, −NH2 , and −OH, SAPs can interact with the surface active sites of carbendazim, 2-AB, and H-AB. Carbendazim/metabolites or their possible complexes would bind to soil organic matter such as humic carbonyl, phenolic and hydroxyl groups through ionic binding, hydrogen bonding and covalent bonding forming highly un-hydrolyzable bonds. Higher BR indicates that more carbendazim/metabolites bind to the soil matrix, making them less available for leaching or runoff. Some studies suggested that the BR, as the “potential form” of the original compound, could be released via biochemical processes and have the long-term biological and ecological effects [31,32]. Whether or not higher BR would trigger lasting toxicity in microbial flora, soil fauna, and succeeding crops after applied with SAPs needs further study to determine.

3.4. Mineralization of 14 C-carbendazim in SAPs-amended soils The cumulative mineralization of carbendazim in soils along with incubation time is shown in Fig. 4. Mineralization in all soils appeared to have a lag phase lasting from the beginning to about 20 d, indicating that a period of time was needed for degradation of chemical compound and the indigenous microorganisms required an adaption phase for the compound. After 20 d, the 14 CCO2 enhanced rapidly in S2 and S3 , and increased moderately from 60 d to 100 d. While mineralized 14 C-CO2 was lower in S1 than those in both S2 and S3 . At the end of incubation, the mineraliza-

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Fig. 3. Bound residue of 14 C-spiked amount in the soils: a) soil 1 (S1 ); b) soil 2 (S2 ); c) soil 3 (S3 ). Values are means with standard deviations (n = 3).

tion of carbendazim was 0.18% and 0.19% of the 14 C applied amount in S1 treated with and without SAPs amendment, respectively, which was consistent with the extremely slow rate of carbendazim degradation in S1 . Panades et al. [27] also reported that carbendazim had longer persistence and lower bio-degradability in acid soil. In neutral S2 and basic S3 treated with SAPs, the fractions of 14 C-CO were 11.3% and 7.7%, respectively. On the other hand, the 2 14 C-CO amounts were approximately 18.1% (S ) and 13.1% (S ) in 2 2 3 SAPs-free treatments at the end of incubation. The mineralized 14 Ccarbendazim was significantly decreased and the relative reduction was approximately 37.6% and 41.2% in S2 and S3 , respectively, compared to SAPs-free treatment at 100 d (p < 0.05). Similarly, Li et al. [33] found that the addition of 10% bio-solids into soil resulted in a substantial decrease in 14 C-CO2 production of Carbamazepine. The mineralization of pesticides was usually closely associated with sorption and microbes [34,35]. Our sorption results demonstrated that addition of SAPs significantly increased the carbendazim sorption in loamy S2 and saline S3 (Supplementary Table A1). The increased sorption of pesticides could limit their availability to soil microorganisms and affect their mineralization potential in soil. Similarly, Loganathan et al. [36] found that the release of 14 C-CO was reduced in crop-residue-derived-char-amended soil 2 due to its increased adsorption capacity. Additionally, a preferential theory proposed if two substances with different availability are both present in one location, soil microbes would prefer to first

degrade the more readily available substrate. The benzimdazolic ring is difficult to break and remains stable in the environment [37]. SAPs might be more readily available nutrient to microorganisms than carbendazim/metabolites. The relatively higher contents of metabolites were also detected in SAPs-treated soils. Based on microbial analysis results (Supplementary Fig. A2c & d), the relative abundance of some dominant species such as Proteobacteria, Sphingomonas, and Methylobacterium increased, while Lactococcus and Marmoricola decreased in SAPs and carbendazim treatments as compared to the controls during the incubation. Previous studies reported that these strains were involved in the degradation of hydrocarbon pollution [38–41], and their combination could impact the complete degradation of carbendazim in different soils. Microorganisms always play a primary role in the degradation of chemical compound. Applications of SAPs and carbendazim produced greater microbial diversity especially in acidic soils (Supplementary Fig. A 2a & b). The results were consistent with the transformation processes of carbendazim in the acidic soil treated with SAPs, which the ER decreased dramatically from 98.3 to 62.2% with a significant relative reduction of 11.4% as compared to the control. The dissipation rate of carbendazim in acidic soil was enhanced by 34.7%. The variation in bacterial diversity was also accompanied by changes in the microbial community structure throughout the 100 cultivation days (Fig. 5 and Supplementary Fig. A2c & d). The relative abundance of some predominant

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Fig. 4. Mineralization of 14 C-spiked amount in the soils: a) soil 1 (S1 ); b) soil 2 (S2 ); c) soil 3 (S3 ). Values are means with standard deviations (n = 3).

species such as Proteobacteria, Bradyrhizobium, Sphingomonas, Ktedonobacter, and Methylobacterium all increased by more than 2 fold, while Lactococcus, Marmoricola, and Firmicutes decreased by about 30% more in soil treated with SAPs and carbendaizm than in the control. Similar results were reported the size and composition of microorganisms were significantly different from the control in amendment with organic carbons, propargyl bromide, and 1, 3-dichloropropene spiked soil [42]. Such exogenous additives into soil implied potential variations in soil conditions, which could affect the transformation of pesticides in different soils. For example, Marmoricola was reported to have multiple hydrocarbon catabolic genes and participated in the degradation of pollution compounds [40]. Sphingomonas was the main degradable strain of the aromatic hydrocarbon compounds in soil [39]. Microbial state is a key indicator of prevalent soil conditions and has an important role in maintaining the health of agricultural soil ecosystem [43]. The alteration of microbial states indicated that the soil microbial function encountered a variation which was closely related to the intrinsic bioremediation of the environment ecosystem and postcrop. It is imperative that the soil microbial state after the SAPs and pesticides incubation must be fully understood before any further agriculture production and environmental protection measures are taken [44,45].

4. Conclusion Applications of SAPs could alter the transformation processes of carbendazim in soil including mineralization, ER, BR, the parent compound dissipation, and metabolites during the incubation. When SAPs coexisted with carbendazim, carbendazim dissipation was significantly increased in acidic soil. The DT50 value of carbendazim was shortened by 50 d in comparison to SAPs-free treatment, reducing the persistence of carbendazim in soils. The varying patterns of carbendazim metabolites obviously altered during the incubation, although its metabolic pathway did not change after SAPs application. The eco-toxicological effect of these metabolites should also receive attention. Besides, SAPs exacerbated the formation of carbendazim-BR, which could result in the reduction of the mobility and bioavailability of the parent/metabolites in soils. Therefore, further studies on the potential adverse effects (phytotoxicity and ecotoxicity) need to be expounded clearly. When SAPs and pesticides coexist in soils, evaluation of the environmental safety and eco-toxicology of pesticides might deviate if only in terms of pesticide spikes in soils. These findings would bring attention to the environmental risk assessment of pesticides when SAPs and pesticides coexisted in soils. Therefore, we emphasize the necessity of conducting further field studies to assess the fate of pesticides and soil microbial state regularly exposed to SAPs over time.

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Fig. 5. Distribution heatmap of microbial genus arranged by hierarchical clustering in different soils at 0, 45, and 100 DAT: (BS 0 d, BS 45 d and BS 100 d) blank soil without MBC and SAPs spray at 0, 45, and 100 days after treatment (DAT); (S1 MBC and S1 MBC S) S1 with MBC, MBC and SAPs at 45 and 100 DAT; (S2 MBC and S2 MBC S) S2 with MBC, MBC and SAPs at 45 and 100 DAT; (S3 MBC and S3 MBC S) S3 with MBC, MBC and SAPs at 45 and 100 DAT.

Conflicts of interest The authors declare no competing financial interest.

Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.jhazmat.2016.12. 057.

Acknowledgments This work was financially funded in part by the National Key Research and Development Program of China (Grant No. 2016YFD0200201-Y), and the National Natural Science Foundation of China (Grant Nos. 11275170, 21507110).

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