Simultaneous remediation of sediments contaminated with sulfamethoxazole and cadmium using magnesium-modified biochar derived from Thalia dealbata

Science of the Total Environment 659 (2019) 1448–1456

Contents lists available at ScienceDirect

Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv

Simultaneous remediation of sediments contaminated with sulfamethoxazole and cadmium using magnesium-modified biochar derived from Thalia dealbata Qi Tao a,b, Bing Li a, Qiquan Li a, Xuan Han b, Yin Jiang b, Radek Jupa c, Changquan Wang a,⁎⁎, Tingqiang Li b,⁎ a b c

College of Resources, Sichuan Agricultural University, Chengdu 611130, China Ministry of Education Key Laboratory of Environmental Remediation and Ecological Health, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou 310029, China Department of Experimental Biology, Faculty of Science, Masaryk University, Kotlářská 2, 61137 Brno, Czech Republic

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

• MgCl2 modification significantly increased surface area of biochar derived from Thalia dealbata. • The addition of the MgCl2-modified biochar (BCM) significantly increased the sorption of sulfamethoxazole (SMX) and Cd on sediments. • SMX sorption in sediments was improved with the addition of Cd2+. • In situ remediation with BCM decreased the mobility and bioavailability of SMX and Cd in sediments. • BCM significantly reduced the phytotoxicity of sediments simultaneously contaminated with SMX and Cd.

a r t i c l e

i n f o

Article history: Received 31 May 2018 Received in revised form 23 December 2018 Accepted 24 December 2018 Available online 27 December 2018 Editor: Xinbin Feng Keywords: Cadmium Magnesium-modified biochar Phytotoxicity Remediation Sediment Sulfamethoxazole

a b s t r a c t In situ remediation and assessment of sediments contaminated with both antibiotics and heavy metals remains a technological challenge. In this study, MgCl2-modified biochar (BCM) was obtained at 500 °C through slow pyrolysis of Thalia dealbata and used for remediation of sediments contaminated by sulfamethoxazole (SMX) and Cd. The BCM showed greater surface area (110.6 m2 g−1) than pristine biochar (BC, 7.1 m2 g−1). The SMX sorption data were well described by Freundlich model while Langmuir model was better for the Cd2+ sorption data. The addition of 5.0% BCM significantly increased the sorption of SMX (by 50.8–58.6%) and Cd (by 24.2–25.6%) on sediments in both single and binary systems as compared with 5.0% BC. SMX sorption in sediments was significantly improved by addition of Cd2+, whereas SMX has no influence on Cd sorption on sediments. The addition of BCM distinctly decreased both SMX (by 51.4–87.2%) and Cd concentrations (by 56.2–91.3%) in overlying water, as well as in TCLP extracts (by 55.6–86.1% and 58.2–91.9% for SMX and Cd, respectively), as compared with sediments without biochar. Both germination rate and root length of pakchoi increased with increasing doses of BCM in contaminated sediments, 5.0% BCM showed greater promotion on pakchoi growth than 5.0% BC. Overall, BCM in the sediments does not only decrease the bioavailability of SMX and Cd, but it also diminishes the phytotoxicity, and thereby shows great application potential for in situ remediation of sediments polluted with antibiotics and heavy metals. © 2018 Elsevier B.V. All rights reserved.

⁎ Correspondence to: T. Li, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou 310058, China. ⁎⁎ Corresponding author. E-mail addresses: [email protected] (C. Wang), [email protected] (T. Li).

https://doi.org/10.1016/j.scitotenv.2018.12.361 0048-9697/© 2018 Elsevier B.V. All rights reserved.

Q. Tao et al. / Science of the Total Environment 659 (2019) 1448–1456

1. Introduction Antibiotics have been recognized as an emerging class of environmental contaminants that have attracted special research attentions due to their potential ecotoxicity and harm to human beings (Hirsch et al., 1999; Nakayama et al., 2017; Zhang et al., 2016). Sulfamethoxazole (SMX) is a sulfonamide bacteriostatic antibiotic, which is widely used for treatment and prevention of both human and animal diseases. Due to its wide spectrum of applications and poor ability to be metabolized, it is one of the most frequently detected antibiotics in sediments and other environmental samples (Wang et al., 2017; Xu et al., 2011). Similarly, cadmium (Cd) is a heavy metal toxic to organisms, which belongs to widespread contaminants present in sediments and soils (Cabral et al., 2015; Du Laing et al., 2009). Cadmium usually comes into the environment through mining, smelting, waste discarding and the application of agrochemicals (Cabral et al., 2016). Aquatic sediments act as the ultimate repositories of past and ongoing discharges of antibiotics and heavy metals. Therefore, these sediment–bound pollutants represent a potential risks to aquatic organism and eventually to humans through the food chain and drinking water (Ghosh et al., 2011). For this reason, efficient remediation of contaminated sediments, especially for antibiotic and heavy metal combined pollution, remains a technological challenge (Du et al., 2017; Du Laing et al., 2009). Current strategies and approaches for sediment remediation are divided into ex situ and in situ methods (Ghosh et al., 2011). The ex situ methods are based on removing of the polluted sediments from the location and their further treatment. However, approaches used in ex situ methods, such as dredging, fail to achieve risk reduction goals for human health and ecosystem protection and their usage typically results in the destruction of existing benthic ecosystems (Erftemeijer et al., 2012; Ghosh et al., 2011). In contrast, the in situ methods aim to improve the stabilization of pollutants in sediments by reducing their mobility, bioavailability, and toxicity with the aid of various amendments (Perelo, 2010; Song et al., 2017a). In situ methods have become quite common in many countries due to low cost, simple operation and low impact on aquatic ecosystems (Gomes et al., 2013; Song et al., 2017a). For this purpose, many sorbents, such as zeolites, apatite, activated carbon, carbon nanotubes, and zerovalent iron are explored and introduced for purposes of in situ remediation of contaminated sediments (Gu et al., 2017; Perelo, 2010; Wu et al., 2017). However, most of these sorbents have limitations of high cost, low efficiency, application constraints, or disposal restrictions. Furthermore, most of above researches were conducted on hydrophobic organic compounds (HOCs) or heavy metal single contamination, little information is available about the simultaneous remediation of antibiotics and heavy metals combined contaminated sediments (Perelo, 2010; Song et al., 2017a). Hence, cost-effective and efficient sorbents are needed for simultaneously enhancing stabilization of antibiotic and heavy metals in sediments. Biochar, a solid material obtained from the thermochemical conversion of plant biomass in an oxygen-limited environment, has received increasing interest for agricultural and environmental applications (Ennis et al., 2012). The porous structure, large surface area and enriched surface functional groups provide biochar a strong sorption affinity to various contaminants. Due to these properties, biochar are used to reduce mobility of various contaminants in soils, sediments and aqueous solutions (Ahmad et al., 2014; Peiris et al., 2017). Recently, several studies have investigated the remediation of contaminated sediments with biochar (Dong et al., 2017; Lou et al., 2011; Xiao et al., 2011). Lou et al. (2011) reported that the addition of 2.0% biochar derived from rice–straw lowered the pentachlorophenol (PCP) concentration in the extraction liquid of sediments and significantly increased wheat germination rates. Xiao et al. (2011) found that sorption of tributyltin (TBT) on sediments was significantly enhanced by the amendment of wood chips biochar. Dong et al. (2017) demonstrated

1449

that Fe3O4–based biochar exhibited a substantial improvement in PAH degradation efficiency, and thus it can be advantageously applied in the remediation of sediments contaminated with PAHs. These few examples provide evidence that biochar can effectively decrease ecological risk of contaminated sediments. However, the majority of these studies focused on remediation of HOCs while no information is available about applicability of biochar on combined contaminations by antibiotics and Cd. Moreover, stabilized contaminants in sediments may be released into overlying water again when the hydrological conditions change. Therefore, to guarantee a long–term stability of the immobilized contaminants, it is necessary to evaluate the efficiency of in situ remediation of contaminated sediments (Cho et al., 2009; Zeng et al., 2015). To our knowledge, numerous current evaluations of in situ remediation of contaminated sediments focus on the content of pollutants, it is difficult to illuminate the changes of concentrations, toxicity, and bioavailability of the target pollutant (Song et al., 2017a, 2017b). Hence, a specific assessment for in situ remediation of contaminated sediments is needed. In this study, SMX and Cd were selected as typical representatives of pollutants from antibiotics and heavy metals. It has been documented that SMX and Cd often coexist in the real sediment (Li et al., 2018; Liang et al., 2015; Yang et al., 2016). SMX is difficult to be hydrolyzed and biodegraded, thus, residues have been predominantly detected in the water phase and sediments (Yang et al., 2018). In addition, aquatic sediment has been identified as an important medium to retain SMX (Zhou and Broodbank, 2014). For example, the high SMX concentrations in sediments from Honghu Lake (570.32 μg kg−1) and East Dongting Lake, China (300.57 μg kg−1) were reported by Yang et al. (2016). On the other hand, the Cd concentrations in surface sediments of Honghu Lake and Dongting Lake were 0.53 mg kg−1 and 4.39 mg kg−1(Liang et al., 2015), respectively, which were higher than the background values. An MgCl2-modified biochar (BCM) was obtained at 500 °C through slow pyrolysis of Thalia dealbata, which is a typical emergent aquatic plant, and is widely used in constructed wetlands for purifying eutrophic water. The objectives of the study were: (1) to investigate the simultaneous adsorption isotherms of SMX and Cd; (2) to carry out remediation of sediments contaminated with SMX and Cd with BCM, and (3) to evaluate the efficiency of in situ remediation by phytotoxicity tests. 2. Materials and methods 2.1. Biochar preparation Samples of T. dealbata were collected from the Qingshanhu constructed wetland, Linan, Zhejiang Province, China. The raw material was three times washed with water, air–dried for a week and then dried at 80 °C for 24 h. The plant material was ground using a stainless grinding machine (MM400, Retsch GmbH, Haan, Germany) and passed through a 2 mm sieve. The plant powder was placed in a ceramic pot, covered with a fitting lid and pyrolysed in a Muffle Furnace (KBF11Q, Zhengguang, Shanghai, China) under N2 atmosphere for 4 h at 500 °C, this pristine biochar was identified as BC. The MgCl2 modified biochar was produced according to Cui et al. (2016a) with some modifications. Briefly, the raw material was ground using a stainless grinding machine and passed through a 2 mm sieve. Then, 10 g grounded biomass were soaked in 100 mL 1 M MgCl2 solution, after 0.5 h mixing under magnetic stirring, the pre-treated biomass was then separated from the solution and pyrolyzed at 500 °C as described above, the MgCl2-modified biochar was identified as BCM. Both BC and BCM were ground to pass through a 0.5 mm sieve prior they were used. The pH, ash content, total C, N, H, and O, and surface area (SA) were detected as in a previous study (Cui et al., 2016a). The surface functional groups were determined using a Fourier transform infrared spectrometer (FTIR; Nicolet 6700, Thermo Fisher Scientific Inc., MA, USA). The mineral crystallographic structure and surface chemical composition were measured by X-ray

1450

Q. Tao et al. / Science of the Total Environment 659 (2019) 1448–1456

diffraction (XRD, Bruker, Karlsruhe, Germany). The morphology analysis was conducted using a scanning electron microscope (SEM, TEM-1000, Hitachi, Tokyo, Japan), and surface element was further analyzed by the energy dispersive spectroscopy (EDS, INCA100, Oxfordshire, U.K.). 2.2. Sediment sampling and preparation of BCM-amended sediments The sediment used in this study is lake sediment, which was collected from Jianhu Lake in Shaoxin, Zhejiang Province, China. Samples of surface sediments (0–20 cm) were collected and air-dried at room temperature, crushed in a porcelain mortar, sieved through a 2 mm mesh, and stored in a refrigerator at 4 °C. The pH of the sediment was 8.17, the CEC was 13.14 cmol kg−1, and the composition of the sediment was 13.82% sand, 20.80% silt, and 65.38% clay. The total organic carbon (TOC) content of the sediment was 46.98 g kg−1. SMX and Cd concentrations in sediment were measured using high performance liquid chromatography (HPLC, Agilent 1200 series, Agilent Technologies, Karlsruhe, Germany) and inductively coupled plasma mass spectrometry (ICP-MS; Agilent 7500a, Agilent Technologies, CA, USA), and were 0.06 mg kg−1 and 0.37 mg kg−1, respectively. The chemical composition of the sediments interferes in the whole process of remediation, thus different sediments has different sorption ability of pollutants. Moreover, chemical composition will influence the bioavailability of pollutants in the sediment (Lee et al., 2011; Xue et al., 2018). Thus BCM–amended sediments with different chemical composition were prepared by mixing the sediment and BCM at different ratios. The percentages of BCM in the amended sediments were 0%, 1.0%, 2.5%, and 5.0% (w/w). The BCM–amended sediments were thoroughly mixed before they were used in the sorption, release and germination tests. In order to compare the effect before and after modification, 5% pristine biochar (BC) amended sediment were prepared as described above.

Cd was artificially added into SMX–spiked sediments by adding Cd solutions. Spiked sediments were homogenized using a glass stirring rod. The moisture content of spiked–sediment was adjusted at 50% water holding capacity (WHC) with deionized water. The treated sediments were equilibrated in a greenhouse for one month to achieve equilibrium of diffusion processes within the sediments. At the end of incubation, triplicate samples were collected for analyses. The results showed that the actual concentration of SMX and Cd in incubated sediments were 20.6 mg kg−1 and 20.1 mg kg−1, respectively. These sediments were used within following contaminants release experiments and phytotoxicity tests. 2.5. Contaminants release experiments First, 50 g of sediments spiked with SMX and Cd were mixed with 500 mL of ultrapure water and 200 mg L−1 of NaN3. Bottles containing this mixture were shaken at 30 rpm for 24 h. Subsequently, the mixture was kept in a static position for 10 days allowing progressive sedimentation. After that, triplicate water samples were taken out and immediately filtered through 0.22 μm filters. SMX and Cd concentrations in water samples were determined using HPLC and ICP-MS, respectively, as described above. Another release experiment was conducted under different static time periods using 2.5% BCM–amended sediments. The toxicity characteristic leaching procedure (TCLP) was applied to the sediments after release experiments (USEPA, 1992). Sediments treated with different BCM were removed from the bottles and air– dried. The TCLP extractant was made from a buffer solution of acetic acid of pH adjusted to 4.93 by NaOH. Solid samples were then mixed with the extraction fluid at a weight ratio of 1:20 (Song et al., 2017b). After shaking at room temperature for 18 h, the mixtures were centrifuged at 8000 g for 20 min, the supernatant was filtered, and the filtrates were analyzed for SMX and Cd as described before. 2.6. Phytotoxicity tests

2.3. Sorption experiments The sorption isotherms of SMX and Cd were measured by the batch equilibration experiments in single and binary systems. SMX and Cd stock solutions (500 mg L−1) were prepared using a background solution consisting of 0.01 mol L−1 NaNO3 and 200 mg L−1 NaN3 (bio–inhibitor) (Zheng et al., 2013). The pH of the solution was adjusted to around 7.0 using HCl or NaOH. In single systems, SMX and Cd stock solutions were diluted in background solution to eight different concentrations (1–100 mg L−1). In binary systems, 20 mg L−1 of competitor (SMX or Cd) was added into Cd or SMX single systems as described above (Wang et al., 2013; Zhang et al., 2011). Batch experiments were initiated by adding 20 mL of single (SMX/Cd) or binary (SMX+Cd) solutions to 0.5 g samples of BCM–amended sediments placed in 25 mL glass vials and they were sealed with teflon–lined screw caps. The vials were kept in the dark and rotated vertically on a rotator set to 150 r/min at room temperature (25 ± 2 °C) for 24 h. Preliminary tests indicated that 24 h was sufficient to reach the apparent equilibrium. After equilibration, the sorbent and aqueous phases were separated by centrifugation, and the concentrations of SMX and Cd in the aqueous phase were analyzed by HPLC and ICP-MS, respectively. All treatments were performed in triplicate.

The phytotoxicity tests were performed with pakchoi in accordance with the OECD guidelines for the testing of chemicals (OECD, 2006). Before sowing, the seeds were surface–sterilized by soaking in 70% (v/v) ethanol for 1 min and 3% (v/v) sodium hypochlorite for 5 min, and then rinsed thoroughly with deionized water. After that, thirty seeds were sown on sediments spiked with SMX and Cd that were enriched by 0%, 1.0%, 2.5% and 5.0% of BCM. The moisture content of spiked– sediment was maintained at 60% of WHC and adjusted daily. The Petri dishes were placed in a growth chamber at 25 °C with a 14/10 h day/ night cycle. The experiments were terminated after 5 d cultivation. Seed germination rate and root length were recorded. All treatments were replicated four times. The phytotoxicity of SMX and Cd in sediment with six different concentrations(0–100 mg kg−1)was also investigated as described above. 2.7. Data analysis All data were analyzed using the SPSS package (version 11.0; SPSS Inc., Chicago, IL, USA). Analysis of variance (ANOVA) was performed on the datasets. Means of significant differences were separated by t-test or Duncan's multiple range test at the P b 0.05 level.

2.4. Sediment-spiking procedures

3. Results and discussion

Spiking of the biochar–amended sediments with SMX and Cd was conducted according to previously reported methods with appropriate modification (Brinch et al., 2002). SMX was firstly dissolved in methanol and then added to dry biochar–amended sediments (25% of the total weight). The mixture was stirred every 15 min to completely evaporate the methanol. Then, the treated sediments were progressively mixed with the rest of 75% of sediments not spiked with SMX. Subsequently,

3.1. Physico-chemical properties of BCM Selected physico–chemical properties of BCM are listed in Table 1. The pH values of both pristine (BC) and modified biochars (BCM) were around 10. BCM showed greater pH values due to the accumulation of alkalic salts and the loss of acidic functional groups (Ahmad et al., 2014). Owing to the formation of Mg–compounds during the

Q. Tao et al. / Science of the Total Environment 659 (2019) 1448–1456

1451

Table 1 Physico–chemical properties of the original biochar (BC) and MgCl2 modified biochar (BCM). Sample

BC BCM

pH

10.09 10.60

Ash (%)

22.0 29.5

Elemental content (%)

Atomic ratio

Surface area

N

C

H

O

H/C

O/C

1.81 1.46

64.36 54.50

2.95 2.64

13.84 20.58

0.550 0.582

0.161 0.0.283

pyrolysis (Fig. 1E), the relative content of ash in BCM was higher as compared to the BC. While no significant differences in N and H contents were observed between BC and BCM, the MgCl2 modification of biochar reduced the C content and increased O content. This indicated that more oxygen–containing functional groups are present on the BCM. Moreover, molar ratios of elements could be used to estimate the aromaticity and polarity of both biochars. After biochar modification with MgCl2, the atomic ratios of H/C, O/C, and (O + N)/C have significantly increased, suggesting that MgCl2 modification resulted in formation of more aromatic structures and less hydrophilic surface (Ennis et al., 2012). This result was also confirmed by the FTIR spectra (Fig. 1F). After biochar modification, band at 1610 cm−1 assigned to aromatic \\C_C and \\C_O, band at 1100–1046 cm−1 assigned to C\\O\\C group, and band at 874–759 cm−1 assigned to aromatic C\\H became more pronounced. The BET specific surface area of BCM was 110.6 m2 g−1, which was approximately 15 times greater than that of BC (Table 1). Increased specific surface area after modification with MgCl2 is consistent with results of a recent study on a biochar modified with magnesium ferrite (Jung et al., 2017), which further demonstrated that magnesium modification promotes the development of fine pore structures on the surface of BC. This was also confirmed by SEM observations of surfaces of both biochars (Fig. 1A, D). While BC had relatively smooth surface with only few pores (Fig. 1A), many mesopores, as well as pores of widths of a few microns, were newly distributed on the surface of BCM (Fig. 1D). The MgCl2 modification does not only change the element content and surface morphological structures of biochars, but it also modifies the mineralization characteristics. The EDS spectrum demonstrated that the carbon and oxygen were dominant components on the surface of both biochars, and magnesium took quite a large proportion in BMC

(O + N)/C 0.185 0.306

(m2 g−1) 7.1 110.6

(Fig. 1B, E). As shown in Fig. 1C, the XRD patterns of both biochars had different peaks, indicating the presence of mineral crystals. In BCM, two strong peaks at 42.5° and 62.0° were identified as magnesium oxide, suggesting that the microns–sized crystals on the surface of BCM were MgO (Fig. 1C). This result was confirmed by FTIR spectra (Fig. 1F), where a peak assigned to Mg\\O bonds was observed in the wavenumbers of around 470 cm−1. In summary, our result demonstrate that MgCl2 modification significantly promotes the development of mineral components (including magnesium oxides), which play an important role in the sorption of ionizable contaminants due to ion exchange and surface complexation (Jung et al., 2017). 3.2. Sorption of SMX and Cd on BCM–amended sediments Sorption data of SMX and Cd to sediments amended with different contents of BCM (Fig. 2) were fitted with both Langmuir and Freundlich models (Table 2). The results showed that both Langmuir and Freundlich models provided good fits to the isotherms of Cd in both single and binary systems (R2 N 0.944; Table 2). However, Langmuir model was not suitable to describe the SMX isotherms (R2 b 0.698). Therefore, Freundlich fitting parameters were much better for comparison of potential sorption capacities of SMX to BCM-amended sediments. The Freundlich sorption coefficient values (KF) of SMX increased with increasing ratio of BCM in sediments (from 0% to 5%) in both single (from 114.8 to 266.1) and binary (from 159.6 to 281.8) systems. This indicated that the addition of BCM improved the sorption of SMX on sediments. Although the addition of 5% BC also increased SMX sorption on sediments, the increase was significantly lower than BCM at the same dose (Table 2). The increased KF was consistent with previous results reported in different literatures (Lian et al., 2014; Lou et al., 2011).

Fig. 1. Images of biochar surface captured by a scanning–electron microscope (A, D) and corresponding EDS spectra (B, E) of the original biochar (BC) and a biochar modified with MgCl2 (BCM). Moreover, X–ray diffraction patterns (C) and FTIR spectra (F) are provided for both biochars.

1452

Q. Tao et al. / Science of the Total Environment 659 (2019) 1448–1456

Fig. 2. The sorption isotherms of sulfamethoxazole (SMX; A) and Cd (B) on sediments amended with various BCM contents in single and binary systems. Data represent means ±SE (n = 4).

For single systems, the SMX isotherms became more nonlinear with increasing BCM content, as apparent from decreasing n values (from 0.537 to 0.517; Table 2). The nonlinear sorption could be explained by two reasons. First, the organic fractions, such as humic acids in

sediments, provide numerous functional groups (e.g., aliphatic and aromatic structures), which may interact with SMX through various mechanisms, including hydrogen and covalent bonds. This may result in a strong nonlinear sorption (Chefetz and Xing, 2009; Hou et al., 2010; Zheng et al., 2013). Second, the bio–polymeric phase in T. dealbata may be decomposed and converted into condensed aromatic domain during pyrolysis process. Consequently, the increased BCM in sediment would provide more heterogeneous sorption sites for SMX (Cui et al., 2016a; Wang et al., 2017; Zheng et al., 2013). In contrast to single systems, the n values for SMX in binary systems increased from 0.509 to 0.581 with increasing BCM. Simultaneously, greater KF value was observed (Fig. 2, Table 2), implying that SMX sorption in sediments was improved significantly with the addition of Cd2+. Previous studies reported that various mechanisms, such as complexation between metal ions and organic chemicals, formation of hydration shell of metal ions, electrostatic interaction as well as cation–bridge, affected adsorptions of organic chemicals when metal ions were added (Lertpaitoonpan et al., 2009; Morel et al., 2014; Zhang et al., 2011; Zheng et al., 2013). The major species of SMX were cationic (SMX+), neutral (SMX0), and anionic (SMX−) at pH b 1.7 b pH b 5.7, and pH N 5.7, respectively (Lucida et al., 2000; Zhang et al., 2011). In our study, complexation of SMX with Cd2+ could increase SMX hydrophobicity and decrease the electrostatic repulsion between SMX− and negatively charged sediments at pH around 7.0 (Jia et al., 2016). In addition, the Cd2+ adsorbed on the surface of BCM and sediments could also act as a Cd bridge, similarly to those of Ca2+ and Mg2+ (Wan et al., 2010). Finally, both mechanisms can possibly contribute to an increase in SMX sorption on sediments. Our results indicated that the addition of suitable concentration of Cd2+ has the potential to improve the remediation of SMX in sediments using BCM, which is in agreement with previous studies (Wu et al., 2012; Zhang et al., 2011). In both single and binary systems, the Cd2+ sorption data were better described by Langmuir isotherm (R2 = 0.989–0.998) than the Freundlich model (R2 = 0.944–0.969) (Table 2), suggesting that chemisorption of Cd2+ mainly occurs on the homogeneous surfaces of BCM– amended sediments (Cui et al., 2016b; Li et al., 2017). In both systems, the calculated maximum adsorption capacity (Q) increased with increasing enrichment of BCM in sediments (from 0% to 5%). Specifically, from 3067.4 mg kg−1 to 4329.3 mg kg−1 for single system and from 3030.0 mg kg−1 to 4366.8 mg kg−1for binary system (Table 2). Interestingly, 5% BC showed the same enhancement on Cd sorption as 1.0% BCM, which implied that the addition of BCM could significantly increase Cd sorption on sediments, as compared BC. The greater surface

Table 2 Fitting characteristics of sulfamethoxazole (SMX) and Cd sorptions on BCM–amended sediments in single and binary systems by Langmuir and Freundlich models. Adsorbate

Biochar (%)

Langmuir Q(mg kg−1)

SMX

SMX (+Cd)

Cd

Cd (+SMX)

0.0BCM 1.0BCM 2.5BCM 5.0BCM 5.0BC 0.0BCM 1.0BCM 2.5BCM 5.0BCM 5.0BC 0.0BCM 1.0BCM 2.5BCM 5.0BCM 5.0BC 0.0BCM 1.0BCM 2.5BCM 5.0BCM 5.0BC

1140.5 1408.5 1677.8 2132.2 1452.8 1369.8 1538.5 2096.4 2409.6 1558.9 3067.4 3521.1 4032.5 4329.3 3490.8 3030.0 3584.2 4032.2 4366.8 3480.1

Freundlich b

R2

0.095 0.118 0.158 0.198 0.124 0.159 0.170 0.171 0.154 0.165 0.051 0.054 0.071 0.072 0.059 0.055 0.050 0.067 0.076 0.062

0.589 0.636 0.600 0.650 0.698 0.638 0.674 0.675 0.594 0.664 0.991 0.995 0.998 0.992 0.986 0.995 0.996 0.997 0.989 0.968

KF(mg1−nLn kg−1) 114.8 147.9 209.8 266.1 167.7 159.6 185.8 243.2 281.8 186.8 193.1 231.2 335.7 367.3 251.8 204.8 220.9 316.2 363.0 256.8

n

R2

0.537 0.529 0.519 0.517 0.521 0.509 0.513 0.536 0.581 0.532 0.859 0.915 0.951 1.007 0.919 0.824 0.926 0.981 1.014 0.957

0.818 0.843 0.852 0.880 0.908 0.832 0.860 0.883 0.904 0.889 0.944 0.955 0.969 0.962 0.958 0.952 0.958 0.967 0.968 0.981

Q. Tao et al. / Science of the Total Environment 659 (2019) 1448–1456

1453

Table 3 The average distribution coefficients (Kd) of SMX and Cd in BCM–amended sediments in single and binary systems. ⁎ indicates significant difference between appropriate single and binary systems. Biochar (%)

0.0 BCM 1.0 BCM 2.5 BCM 5.0 BCM 5.0BC

Kd medium SMX

SMX (+Cd)

89.7 116.8 184.3 257.4 120.6

135.6⁎ 161.7⁎ 230.4⁎ 273.3⁎ 169.8⁎

Cd 166.1 219.0 331.9 380.0 222.7

Cd (+SMX) 170.3 209.2 329.2 381.2 2241.4

area, more negative surface charge, and higher contents of functional groups of BCM may contribute to the greater adsorption of Cd observed with increasing BCM/sediments ratios (Ahmad et al., 2014; Cui et al., 2016a). Our previous study showed that the interaction with minerals (precipitation of minerals and metal ion exchange) primarily drove the Cd2+ sorption on BCM (Cui et al., 2016b). Moreover, the bonding energy coefficient (b) is a useful parameter to characterize the sediments affinity for metal ions. The b values for BCM–amended sediments were in the range of 0.050–0.076, implying that sorption of Cd2+ on these BCM–amended sediments was favorable under the experimental conditions, as the surfaces of BCM–amended sediments were negatively charged and had a high affinity for Cd2+ (Li et al., 2017; Sun et al., 2015). Interestingly, no difference in b was observed between single and binary system, indicating that SMX has no influence on Cd sorption on sediments. The distribution coefficient (Kd) allows comparison of the sorption capacities of different sorbents for a given adsorbate under the same experimental conditions. A high Kd value indicates a high retention by the solid phase through sorption and chemical reactions, leading to a low potential bioavailability of the adsorbate. The distribution coefficients for Cd were approx. 2 times greater than that for SMX (Table 3). This result is in agreement with the observations of Wang et al. (2017) and Sun et al. (2015) and suggested that sediment used in this study showed greater sorption capacity for Cd than for SMX. The Kd value for SMX in competitive sorption system was significantly greater (P b 0.05) than in the single sorption system, implying that SMX may pose less threat to aquatic organism under the competitive sorption conditions. Kd values for both SMX and Cd increased significantly (P b 0.05) in both single and binary systems with BCM increasing from 0% to 5.0% in sediment. Therefore, addition of BCM increases the retention capacity for both SMX and Cd, which may substantially contribute to reduction in bioavailability of both pollutants as demonstrated in other studies (Lou et al., 2011; Song et al., 2017a). 3.3. SMX and Cd release from BCM–amended sediments In aquatic ecosystems, pollutants in sediment are able to diffuse from sediment into overlying water. Therefore, it is necessary to determine the pollutant concentration in the overlying water for the assessment and management of contaminated sediments (Song et al., 2017a). In this study, the in situ remediation with BCM significantly decreased the concentrations of SMX and Cd in overlying water (Fig. 3). Comparing with control (i.e., without biochar), the concentrations of SMX and Cd in water were decreased by 51.4–87.2% and 56.2–91.3%, respectively (Fig. 3A), depending on BCM dose. However, 1.0% BCM showed greater suppression of SMX and Cd release than 1.0% BC. On the other hand, that the reduction of Cd concentrations was more pronounced than that of SMX and this reduction could be explained by the greater sorption capacity of BCM for Cd (Table 2, Fig. 2). Similar results were reported in studies of Zhang et al. (2017) and Liu et al. (2017) who found that biochar can efficiently suppress the release of Cu2+, 4–chlorophenol and total Hg from the sediments. This result further supports the

Fig. 3. Aqueous concentrations of sulfamethoxazole (SMX) and Cd released from sediments treated with different BCM doses (A) or contact time (B). Sediments used for measurements of concentrations of SMX and Cd in different static times were enriched with 2.5% BCM. Data represent means ±SE (n = 4). Different letters indicate significant differences among individual treatments at P b 0.05.

feasibility of BCM for in situ remediation of SMX and Cd co– contaminated sediments. Interestingly, both SMX and Cd concentrations in the overlying water were reduced with increasing exposure time until 15th and 30th day after the exposure beginning, respectively (Fig. 3B). Therefore, due to high retention of SMX and Cd, BCM is able to efficiently remediate those pollutants from water for relatively long period of time. Our observation was consistent with previous results (Beesley and Marmiroli, 2011; Song et al., 2017a), and further confirmed that the aqueous concentration of contaminants released from sediments is an accurate and convincing indicator, which can be utilized to assess the potential risks and the remediation efficiency. It should be point out, after amendment of biochar into sediments, the interaction between biochar and sediment particles will transfer contaminants from the sediment to the strongly binding biochar particles, reducing bioavailability to benthic organisms. Sediment turnover by benthic organisms and other natural mixing processes can further incorporate the added biochar into deeper or newly depositing sediment layers (Ghosh et al., 2011; Sun and Ghosh, 2007). These processes will have profound influence on the physical and chemical properties, as well as the surface functional group of biochar, thus further research on physicochemical property of biochar in sediment is needed. Previous study showed that activated carbon is physically stable in the environment, and remains effective at binding contaminants in sediments several years after application (Cho et al., 2009). In present study, BCM is able to efficiently suppress the release of SMX and Cd from the sediment for relatively long period of time (45d). However, even longer (e.g. one year or longer) ecological and residual impacts remain unclear and need to be investigated further.

1454

Q. Tao et al. / Science of the Total Environment 659 (2019) 1448–1456

Fig. 4. Concentrations of sulfamethoxazole (SMX) and Cd in TCLP extracts from sediments treated with different BCM doses. Data represent means ±SE (n = 4). Different letters indicate significant differences among treatments at P b 0.05.

The TCLP has been used to assess the mobility and the bioavailability of contaminants in solid waste as well as the success of remediation techniques applied to contaminated soils and sediments (Vithanage et al., 2014). After release experiments, both SMX and Cd concentrations in TCLP extracts were significantly reduced in the BCM–treated sediments, and the reduction increased with increasing BCM dose (Fig. 4). Addition of 5.0% BCM reduced SMX and Cd concentrations in the TCLP extract by 86.1% and 91.9%, as compared with sediment without biochar, however, the corresponding value for 5.0% BC was 47.9% and 49.8%, respectively. These results were in agreement with the findings in the adsorption isotherm experiment, and indicated that BCM was effective in immobilizing both SMX and Cd in the sediment and decreased the releasing of the contaminants in the surrounding water. The simultaneous immobilization of both contaminants was likely attributed to different mechanisms. SMX stabilization may result from its adsorption onto organic fractions in sediment and BCM, whereas precipitation of minerals and adsorption on functional groups of BCM was probably responsible for Cd immobilization (Ahmad et al., 2014; Cui et al., 2016b; Radke et al., 2009). 3.4. Phytotoxicity of BCM–amended sediments 3.4.1. Phytotoxicity of SMX and Cd Pakchoi germination test was conducted to evaluate the phytotoxicity of SMX and Cd in sediment. Both SMX and Cd exhibited phytotoxicity to pakchoi (Fig. 5), because the relative germination rate and root length decreased significantly with the increasing concentrations of SMX and Cd in the sediments. Tight, negative, linear correlations between relative germination rates and SMX concentration (R2 = 0.969) or Cd concentration (R2 = 0.910), between root length and SMX concentration (R2 = 0.991) or Cd concentration (R2 = 0.900) illustrated that the pakchoi germination and growth was inhibited in the SMX or Cd contaminated sediments in a concentration–dependent manner. It was observed that both germination rate and root length were reduced more rapidly when they were exposed to Cd compared with SMX of the same concentrations (Fig. 5A, B). The half maximal effective concentrations (EC50) of germination rate inhibition were 107.6 mg kg−1 for SMX and 44.3 mg kg−1 for Cd, respectively. For root length, the EC50 was 81.9 mg kg−1 for SMX and 39.8 mg kg−1 for Cd, respectively. All these results indicated that pakchoi seeds were more sensitive to Cd than SMX. Nevertheless, it is important to realize that the phytotoxicity of different pollutants may depend not only on the pollutant type but also on the plant species used. Previous study (Liu et al., 2009) found that rice was more sensitive to sulfamethoxazole (EC10 value of 0.1 mg L−1) than sweet oat and cucumber. Hillis et al. (2011) found that root elongation of carrot was more sensitive to SMX than

Fig. 5. Changes in seed germination rate (A) and root length (B) of pakchoi under exposure to different concentrations of sulfamethoxazole (SMX) and Cd in sediments. Data represent means ±SE (n = 4). Different letters indicate significant differences among treatments at P b 0.05.

germination. Song et al. (2017b) observed a significant inhibition of root length and biomass production in Phaseolus radiatus and Raphanus sativus and both species were more sensitive to Cd than phenanthrene. Consistent with previous studies, we found that root elongation of pakchoi was more sensitive to SMX concentration than seed germination, and both root elongation and seed germination were more sensitive to Cd than SMX. Of course, other factors, such as seed properties, seed culture time, root physiology, etc., may also influence the plant's response to the pollution (Hillis et al., 2011; Lou et al., 2011).

3.4.2. Effect of BCM on the toxicity of SMX and Cd in the sediment Germination test was conducted to evaluate effects of BCM on the toxicity of SMX and Cd in the sediment. In this study, the sediment was simultaneously polluted with SMX and Cd (20.6 mg kg−1 and 20.1 mg kg−1, respectively). The phytotoxicity of the contaminated sediments was depended on the BCM dose (Fig. 6). Both germination rate and root length significantly increased with increasing concentration of BCM from 0% to 5.0%. Compared to control, addition of 5.0% of BCM in the contaminated sediments increased the germination rate and root length by 75% and 136%, respectively, while for 5.0% of BC, the corresponding value was 42.5% and 32.6% The increased germination rate and root length were consistent with the decreased SMX and Cd concentration in TCLP extract (Fig. 4) and further indicated that BCM efficiently immobilized both SMX and Cd and decreased the bioavailability of the pollutants in the sediment. Thereforeet et al., we can draw a conclusion that the phytotoxicity of SMX and Cd in the sediment is mainly depend on their bioavailability concentration, and the

Q. Tao et al. / Science of the Total Environment 659 (2019) 1448–1456

A

1455

Our results suggested that the application of BCM in the sediments does not only decrease the bioavailability of the pollutants in the sediment, but it also significantly reduces their phytotoxicity. 4. Conclusions

1 cm 0.0% BCM 1.0% BCM 2.5% BCM 5.0% BCM 5.0% BC

B

a

Seed germination (%)

100 b

80 60

a b

c

40 20

e

0

Acknowledgements 0.0%

1.0%

2.5%

5.0%BC

This study was financially supported by the National Natural Science Foundation of China (21477104, 41671315, 41807126); National Key Research and Development Projects of China (2016YFD0800802, 2017YFD0200102); the Applied Basic Research Programs of Sichuan Science and Technology Department (2018JY0002); Zhejiang Provincial Natural Science Foundation of China (No. LZ18D010001).

a

40 Root length (mm)

5.0%

BCM content in sediments

C

b 30 c 20

In this work, simultaneous remediation of sediments contaminated by SMX and Cd using a magnesium modified biochar (BCM) derived from T. dealbata was assessed. Compared with pristine biochar (BC), the addition of BCM significantly increased the sorption of SMX and Cd on sediments in both single and binary systems. SMX sorption in sediments was significantly improved with the addition of Cd2+, whereas SMX has no influence on Cd sorption on sediments. BCM showed greater ability to immobilize both SMX and Cd in the sediment than BC, and thus decreased the concentrations of SMX and Cd in overlying water as well as in TCLP extracts. Enhanced germination rates and root lengths of pakchoi plants with the increasing doses of BCM in sediments provided a clear evidence that remediation with BCM significantly reduces the phytotoxicity of sediments simultaneously contaminated with SMX and Cd. Therefore, BCM shows great application potential for in situ remediation of sediments polluted with antibiotics and heavy metals.

c

References

d

10

0 0.0%

1.0% 2.5% 5.0% BCM content in sediments

5.0%BC

Fig. 6. The effects of BCM on the phytoxicity of SMX and Cd in the sediment. (A) Pakchoi plants after 5 days of cultivation in contaminated sediment that was enriched by appropriate dose of BCM. Changes in seed germination rates (B) and root length (C) of pakchoi plants exposed to sediments with different BCM doses. Data represent means ± SE (n = 4). Different letters indicate significant differences among treatments at P b 0.05.

addition of BCM could significantly decrease bio-available concentration of pollutants, as compared with BC. The addition of 1.0% BCM significantly increased the germination rate (compared to the control, p b 0.05). However, when the amount of BCM was ≥2.5%, the germination rates were close to those of uncontaminated sediments (Fig. 5), indicating that higher concentrations of BCM had almost no effect on the germination rate. Compared to seed germination, the root length showed a persistent increase even at the dose of 5.0%. This result indicated that root elongation of pakchoi was more sensitive to BCM than germination. One explanation may be that BCM in the sediment could decrease the SMX and Cd concentrations in water below level of limiting toxicity to pakchoi germination (SMX and Cd concentrations were 0.22 mg L−1and 0.15 mg L−1, when BCM was 2.5%) (Ahmad et al., 2014; Liu et al., 2009). Additionally, root length is easily affected by the pollution level due to direct exposure to sediments, whereas the seed germination is more stable under unfavourable conditions since it is mostly influenced by the nutrient supply from the isolated embryo (Huang et al., 2017; Lou et al., 2011).

Ahmad, M., Rajapaksha, A.U., Lim, J.E., Zhang, M., Bolan, N., Mohan, D., Vithanage, M., Lee, S.S., Ok, Y.S., 2014. Biochar as a sorbent for contaminant management in soil and water: a review. Chemosphere 99, 19–33. Beesley, L., Marmiroli, M., 2011. The immobilisation and retention of soluble arsenic, cadmium and zinc by biochar. Environ. Pollut. 159, 474–480. Brinch, U.C., Ekelund, F., Jacobsen, C.S., 2002. Method for spiking soil samples with organic compounds. Appl. Environ. Microbiol. 68, 1808–1816. Cabral, M., Toure, A., Garcon, G., Diop, C., Bouhsina, S., Dewaele, D., Cazier, F., Courcot, D., Tall-Dia, A., Shirali, P., Diouf, A., Fall, M., Verdin, A., 2015. Effects of environmental cadmium and lead exposure on adults neighboring a discharge: evidences of adverse health effects. Environ. Pollut. 206, 247–255. Cabral, L., Lacerda, G.V., de Sousa, S.T.P., Dias, A.C.F., Cadete, L.L., Andreote, F.D., Hess, M., de Oliveira, V.M., 2016. Anthropogenic impact on mangrove sediments triggers differential responses in the heavy metals and antibiotic resistomes of microbial communities. Environ. Pollut. 216, 460–469. Chefetz, B., Xing, B.S., 2009. Relative role of aliphatic and aromatic moieties as sorption domains for organic compounds: a review. Environ. Sci. Technol. 43, 1680–1688. Cho, Y.M., Ghosh, U., Kennedy, A.J., Grossman, A., Ray, G., Tomaszewski, J.E., Smithenry, D.W., Bridges, T.S., Luthy, R.G., 2009. Field application of activated carbon amendment for in-situ stabilization of polychlorinated biphenyls in marine sediment. Environ. Sci. Technol. 43, 3815–3823. Cui, X.Q., Dai, X., Khan, K.Y., Li, T.Q., Yang, X.E., He, Z.L., 2016a. Removal of phosphate from aqueous solution using magnesium-alginate/chitosan modified biochar microspheres derived from Thalia dealbata. Bioresour. Technol. 218, 1123–1132. Cui, X.Q., Fang, S.Y., Yao, Y.Q., Li, T.Q., Ni, Q.J., Yang, X.E., He, Z.L., 2016b. Potential mechanisms of cadmium removal from aqueous solution by Canna indica derived biochar. Sci. Total Environ. 562, 517–525. Dong, C.D., Chen, C.W., Hung, C.M., 2017. Synthesis of magnetic biochar from bamboo biomass to activate persulfate for the removal of polycyclic aromatic hydrocarbons in marine sediments. Bioresour. Technol. 245, 188–195. Du Laing, G., Rinklebe, J., Vandecasteele, B., Meers, E., Tack, F.M.G., 2009. Trace metal behaviour in estuarine and riverine floodplain soils and sediments: a review. Sci. Total Environ. 407, 3972–3985. Du, J., Zhao, H., Liu, S., Xie, H., Wang, Y., Chen, J., 2017. Antibiotics in the coastal water of the South Yellow Sea in China: occurrence, distribution and ecological risks. Sci. Total Environ. 595, 521–527. Ennis, C.J., Evans, A.G., Islam, M., Ralebitso-Senior, T.K., Senior, E., 2012. Biochar: carbon sequestration, land remediation, and impacts on soil microbiology. Crit. Rev. Environ. Sci. Technol. 42, 2311–2364. Erftemeijer, P.L.A., Riegl, B., Hoeksema, B.W., Todd, P.A., 2012. Environmental impacts of dredging and other sediment disturbances on corals: a review. Mar. Pollut. Bull. 64, 1737–1765.

1456

Q. Tao et al. / Science of the Total Environment 659 (2019) 1448–1456

Ghosh, U., Luthy, R.G., Cornelissen, G., Werner, D., Menzie, C.A., 2011. In-situ sorbent amendments: a new direction in contaminated sediment management. Environ. Sci. Technol. 45, 1163–1168. Gomes, H.I., Dias-Ferreira, C., Ribeiro, A.B., 2013. Overview of in situ and ex situ remediation technologies for PCB-contaminated soils and sediments and obstacles for fullscale application. Sci. Total Environ. 445, 237–260. Gu, B.W., Lee, C.G., Lee, T.G., Park, S.J., 2017. Evaluation of sediment capping with activated carbon and nonwoven fabric mat to interrupt nutrient release from lake sediments. Sci. Total Environ. 599, 413–421. Hillis, D.G., Fletcher, J., Solomon, K.R., Sibley, P.K., 2011. Effects of ten antibiotics on seed germination and root elongation in three plant species. Arch. Environ. Contam. Toxicol. 60, 220–232. Hirsch, R., Ternes, T., Haberer, K., Kratz, K.L., 1999. Occurrence of antibiotics in the aquatic environment. Sci. Total Environ. 225, 109–118. Hou, J.A., Pan, B., Niu, X.K., Chen, J.Z., Xing, B.S., 2010. Sulfamethoxazole sorption by sediment fractions in comparison to pyrene and bisphenol A. Environ. Pollut. 158, 2826–2832. Huang, D.L., Liu, L.S., Zeng, G.M., Xu, P., Huang, C., Deng, L.J., Wang, R.Z., Wan, J., 2017. The effects of rice straw biochar on indigenous microbial community and enzymes activity in heavy metal-contaminated sediment. Chemosphere 174, 545–553. Jia, M.Y., Wang, F., Jin, X., Song, Y., Bian, Y.R., Boughner, L.A., Yang, X.L., Gu, C.G., Jiang, X., Zhao, Q.G., 2016. Metal ion-oxytetracycline interactions on maize straw biochar pyrolyzed at different temperatures. Chem. Eng. J. 304, 934–940. Jung, K.W., Lee, S., Lee, Y.J., 2017. Synthesis of novel magnesium ferrite (MgFe2O4)/biochar magnetic composites and its adsorption behavior for phosphate in aqueous solutions. Bioresour. Technol. 245, 751–759. Lee, S., An, J., Kim, Y.J., Nam, K., 2011. Binding strength-associated toxicity reduction by birnessite and hydroxyapatite in Pb and Cd contaminated sediments. J. Hazard. Mater. 186, 2117–2122. Lertpaitoonpan, W., Ong, S.K., Moorman, T.B., 2009. Effect of organic carbon and pH on soil sorption of sulfamethazine. Chemosphere 76, 558–564. Li, B., Yang, L., Wang, C.Q., Zhang, Q.P., Liu, Q.C., Li, Y.D., Xiao, R., 2017. Adsorption of Cd(II) from aqueous solutions by rape straw biochar derived from different modification processes. Chemosphere 175, 332–340. Li, F., Xiao, M.S., Zhang, J.D., Liu, C.Y., Qiu, Z.Z., Cai, Y., 2018. Spatial distribution, chemical fraction and fuzzy comprehensive risk assessment of heavy metals in surface sediments from the Honghu Lake, China. Int. J. Environ. Res. Public Health 15, 207. Lian, F., Sun, B., Song, Z., Zhu, L., Qi, X., Xing, B., 2014. Physicochemical properties of herbresidue biochar and its sorption to ionizable antibiotic sulfamethoxazole. Chem. Eng. J. 248, 128–134. Liang, J., Liu, J.Y., Yuan, X.Z., Zeng, G.M., Lai, X., Li, X.D., Wu, H.P., Yuan, Y.J., Li, F., 2015. Spatial and temporal variation of heavy metal risk and source in sediments of Dongting Lake wetland, mid-south China. J. Environ. Sci. Health A Tox. Hazard. Subst. Environ. Eng. 50, 100–108. Liu, F., Ying, G.G., Tao, R., Jian-Liang, Z., Yang, J.F., Zhao, L.F., 2009. Effects of six selected antibiotics on plant growth and soil microbial and enzymatic activities. Environ. Pollut. 157, 1636–1642. Liu, P., Ptacek, C.J., Blowes, D.W., Finfrock, Y.Z., Gordon, R.A., 2017. Stabilization of mercury in sediment by using biochars under reducing conditions. J. Hazard. Mater. 325, 120–128. Lou, L.P., Wu, B.B., Wang, L.N., Luo, L., Xu, X.H., Hou, J.A., Xun, B., Hu, B.L., Chen, Y.X., 2011. Sorption and ecotoxicity of pentachlorophenol polluted sediment amended with rice-straw derived biochar. Bioresour. Technol. 102, 4036–4041. Lucida, H., Parkin, J.E., Sunderland, V.B., 2000. Kinetic study of the reaction of sulfamethoxazole and glucose under acidic conditions - I. Effect of pH and temperature. Int. J. Pharm. 202, 47–61. Morel, M.C., Spadini, L., Brimo, K., Martins, J.M.F., 2014. Speciation study in the sulfamethoxazole-copper-pH-soil system: implications for retention prediction. Sci. Total Environ. 481, 266–273. Nakayama, T., Tran Thi Tuyet, H., Harada, K., Warisaya, M., Asayama, M., Hinenoya, A., Lee, J.W., Tran Minh, P., Ueda, S., Sumimura, Y., Hirata, K., Nguyen Thanh, P., Yamamoto, Y., 2017. Water metagenomic analysis reveals low bacterial diversity and the presence of antimicrobial residues and resistance genes in a river containing wastewater from backyard aquacultures in the Mekong Delta, Vietnam. Environ. Pollut. 222, 294–306. OECD, 2006. Test no. 208: terrestrial plant test: seedling emergence and seedling growth Test. OECD Guidelines for the Testing of Chemicals, Section 2. OECD Publishing, Paris. Peiris, C., Gunatilake, S.R., Mlsna, T.E., Mohan, D., Vithanage, M., 2017. Biochar based removal of antibiotic sulfonamides and tetracyclines in aquatic environments: a critical review. Bioresour. Technol. 246, 150–159.

Perelo, L.W., 2010. Review: in situ and bioremediation of organic pollutants in aquatic sediments. J. Hazard. Mater. 177, 81–89. Radke, M., Lauwigi, C., Heinkele, G., Muerdter, T.E., Letzel, M., 2009. Fate of the antibiotic sulfamethoxazole and its two major human metabolites in a water sediment test. Environ. Sci. Technol. 43, 3135–3141. Song, B., Zeng, G.M., Gong, J.L., Liang, J., Xu, P., Liu, Z.F., Zhang, Y., Zhang, C., Cheng, M., Liu, Y., Ye, S.J., Yi, H., Ren, X.Y., 2017a. Evaluation methods for assessing effectiveness of in situ remediation of soil and sediment contaminated with organic pollutants and heavy metals. Environ. Int. 105, 43–55. Song, B., Zeng, G.M., Gong, J.L., Zhang, P., Deng, J.Q., Deng, C.H., Yan, J., Xu, P., Lai, C., Zhang, C., Cheng, M., 2017b. Effect of multi-walled carbon nanotubes on phytotoxicity of sediments contaminated by phenanthrene and cadmium. Chemosphere 172, 449–458. Sun, X.L., Ghosh, U., 2007. PCB bioavailability control in Lumbriculus variegatus through different modes of activated carbon addition to sediments. Environ. Sci. Technol. 41, 4774–4780. Sun, W.L., Jiang, B.F., Wang, F., Xu, N., 2015. Effect of carbon nanotubes on Cd(II) adsorption by sediments. Chem. Eng. J. 264, 645–653. USEPA, 1992. Test Methods for Evaluating Solid Waste, Physical/Chemical Methods, SW846. 3rd ed. U.S. Environmental Protection Agency, Washington, DC. Vithanage, M., Rajapaksha, A.U., Tang, X.Y., Thiele-Bruhn, S., Kim, K.H., Lee, S.E., Ok, Y.S., 2014. Sorption and transport of sulfamethazine in agricultural soils amended with invasive-plant-derived biochar. J. Environ. Manag. 141, 95–103. Wan, Y., Bao, Y.Y., Zhou, Q.X., 2010. Simultaneous adsorption and desorption of cadmium and tetracycline on cinnamon soil. Chemosphere 80, 807–812. Wang, C., Li, H., Liao, S., Zheng, H., Wang, Z., Pan, B., Xing, B., 2013. Coadsorption, desorption hysteresis and sorption thermodynamics of sulfamethoxazole and carbamazepine on graphene oxide and graphite. Carbon 65, 243–251. Wang, P., Zhang, D., Zhang, H., Li, H., Ghosh, S., Pan, B., 2017. Impact of concentration and species of sulfamethoxazole and ofloxacin on their adsorption kinetics on sediments. Chemosphere 175, 123–129. Wu, D., Pan, B., Wu, M., Peng, H.B., Zhang, D., Xing, B.S., 2012. Coadsorption of Cu and sulfamethoxazole on hydroxylized and graphitized carbon nanotubes. Sci. Total Environ. 427, 247–252. Wu, Y.X., Wang, Y., Huang, X.F., Chen, S.Y., Zhong, X., Ni, Z.B., Cai, X.D., Liu, X.W., Simonnot, M.O., Qiu, R.L., 2017. Zerovalent iron in conjunction with surfactants to remediate sediments contaminated by polychlorinated biphenyls and nickel. Chemosphere 189, 479–488. Xiao, X.Y., Sheng, G.D., Qiu, Y.P., 2011. Improved understanding of tributyltin sorption on natural and biochar-amended sediments. Environ. Toxicol. Chem. 30, 2682–2687. Xu, B., Mao, D., Luo, Y., Xu, L., 2011. Sulfamethoxazole biodegradation and biotransformation in the water-sediment system of a natural river. Bioresour. Technol. 102, 7069–7076. Xue, W.J., Huang, D.L., Zeng, G.M., Wan, J., Zhang, C., Xu, R., Cheng, M., Deng, R., 2018. Nanoscale zero-valent iron coated with rhamnolipid as an effective stabilizer for immobilization of Cd and Pb in river sediments. J. Hazard. Mater. 341, 381–389. Yang, Y.Y., Cao, X.H., Lin, H., Wang, J., 2016. Antibiotics and antibiotic resistance genes in sediment of Honghu Lake and east Dongting Lake, China. Microb. Ecol. 72, 791–801. Yang, Y.Y., Song, W.J., Lin, H., Wang, W.B., Du, L.N., Xing, W., 2018. Antibiotics and antibiotic resistance genes in global lakes: a review and meta-analysis. Environ. Int. 116, 60–73. Zeng, G.M., Wu, H.P., Liang, J., Guo, S.L., Huang, L., Xu, P., Liu, Y.Y., Yuan, Y.J., He, X.X., He, Y., 2015. Efficiency of biochar and compost (or composting) combined amendments for reducing Cd, Cu, Zn and Pb bioavailability, mobility and ecological risk in wetland soil. RSC Adv. 5, 34541–34548. Zhang, D., Pan, B., Wu, M., Wang, B., Zhang, H., Peng, H.B., Wu, D., Ning, P., 2011. Adsorption of sulfamethoxazole on functionalized carbon nanotubes as affected by cations and anions. Environ. Pollut. 159, 2616–2621. Zhang, W., Li, Y., Wang, C., Wang, P., Hou, J., Yu, Z., Niu, L., Wang, L., Wang, J., 2016. Modeling the biodegradation of bacterial community assembly linked antibiotics in river sediment using a deterministic stochastic combined model. Environ. Sci. Technol. 50, 8788–8798. Zhang, S., Tian, K., Jiang, S.F., Jiang, H., 2017. Preventing the release of Cu2+ and 4-CP from contaminated sediments by employing a biochar capping treatment. Ind. Eng. Chem. Res. 56, 7730–7738. Zheng, H., Wang, Z.Y., Zhao, J., Herbert, S., Xing, B.S., 2013. Sorption of antibiotic sulfamethoxazole varies with biochars produced at different temperatures. Environ. Pollut. 181, 60–67. Zhou, J., Broodbank, N., 2014. Sediment-water interactions of pharmaceutical residues in the river environment. Water Res. 48, 61–70.