Graphene Oxide Promoted Cadmium Uptake by Rice in Soil | ACS

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Graphene oxide promoted cadmium uptake by rice in soil Yijia He, Lichao Qian, Ke Zhou, Ruirui Hu, Meirong Huang, Min Wang, Guoke Zhao, Yule Liu, Zhiping Xu, and Hongwei Zhu ACS Sustainable Chem. Eng., Just Accepted Manuscript • DOI: 10.1021/ acssuschemeng.8b06823 • Publication Date (Web): 13 May 2019 Downloaded from http://pubs.acs.org on May 18, 2019

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ACS Sustainable Chemistry & Engineering

Graphene oxide promoted cadmium uptake by rice in soil Yijia He1, Lichao Qian2, Ke Zhou3, Ruirui Hu1, Meirong Huang1, Min Wang1, Guoke Zhao1, Yule Liu2, Zhiping Xu3, Hongwei Zhu1* 1State

Key Lab of New Ceramics and Fine Processing, School of Materials Science and Engineering, Tsinghua University, Beijing 100084, China

2Center

for Plant Biology and MOE Key Laboratory of Bioinformatics, School of Life Sciences, Tsinghua University, Beijing 100084, China

3Applied

Mechanics Laboratory, Department of Engineering Mechanics, Tsinghua University, Beijing 100084, China *Corresponding

author. Email: [email protected].

Abstract Graphene oxide (GO) has shown enormous potential applications in improving crop yield and soil cultivation quality. However, in heavy metal contaminated soil, the effect of GO on heavy metals and the indirect toxicity of GO to plants remain unclear. In this work, we reveal the GOpromoted cadmium (Cd) uptake by rice in a Cd-contaminated soil system. The oxygen-rich functional groups and the large specific surface area of mono-layer GO result in strong Cd(II) adsorption (with a maximum adsorption capacity of 265.8 mg/g), which significantly change the existing forms of Cd(II) in the soil. In particular, GO converts the inorganic-bound form Cd(II) that is not readily absorbed by plants into the exchangeable form that is more available for plant absorption. As a result, Cd(II) content in rice seedlings is increased by 12.5% with the application of GO. Therefore, it can be concluded that GO exhibited indirect toxicity to plants in heavy metal-enriched soil. Keywords: graphene oxide, adsorption, cadmium, rice, soil

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Introduction Graphene oxide (GO) is an important graphene derivative with excellent physicochemical properties due to its unique carbon-based graphene structure that bears abundant oxygencontaining functional groups. Indeed, GO has been widely used in various fields, such as biomedicine, electrochemical, environmental protection, and energy storage applications [15]. The effect of GO on plant production and quality is an emerging research topic in recent years. It was found that the state of culture medium had a significant effect on GO toxicity. For example, under the hydroponic conditions, GO solution shows severe toxicity to plants. Begum et al. reported that under Hoagland medium, a large amount of GO accumulated on the roots of tomato, red spinach, and cabbage, which increased the accumulation of reactive oxygen species (ROS) and eventually inhibited the growth of these kinds of plants [6]. Similarly, GO solution has significantly induced stress damage of tobacco cells and shortened the length of tobacco roots [7]. In contrast, in the case of soil cultivation, GO played a promoting role in plant growth. Since the soil environment limits the movement of GO, the effect of GO agglomeration on roots is eliminated. In our previous work, because of the hydrophilic and water transport properties, GO increased the germination rate and promoted the growth of spinach [8]. Moreover, GO is also used as a new fertilizer carrier to provide more nutrients for plants [9]. Therefore, GO has shown enormous potential application for improving crop yield and soil system quality. However, in many regions, the heavy metal content in soil exceeds the safety standard because of mine exploitation, exhaust emission, and sewage irrigation [10]. As a result, a significant amount of heavy metals accumulate in crops, which eventually enter human bodies through food chains and lead to an enormous threat to human health. Furthermore, it has been reported that GO possessed a considerable adsorption capability for metals in solution [4, 11-15]. Thus, it is necessary and of great significance to investigate the adsorption mechanism of heavy metals by GO, the effect of GO on the existing form of heavy metals in soil, as well as the effect of GO on the absorption of heavy metals by plants. Among various heavy metals, cadmium (Cd) is one of the most hazardous elements, which is easy to be absorbed and deposited in organisms, but difficult to be excreted and degraded with a long half-life of 10 to 30 years. Itai-Itai disease in Japan and cancer village in Guangdong province, China, are both caused by excessive exposure to Cd [16, 17]. The adsorption 2 ACS Paragon Plus Environment

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capacities of GO for heavy metal Cd(II) have been reported and revealed in many research papers [4, 18-23]. For example, Zhao et al. reported that the adsorption capacity of few-layered GO for Cd(II) was 106.3 mg/g [4]. The study by Bian et al. concluded that the phenolic hydroxyl group and the carboxyl group of GO dominated the adsorption of Cd(II), but the maximal adsorption capacity was only 23.9 mg/g [19]. Huang et al. put forward that the complex of inner-sphere surface played a leading role on Cd(II) adsorption with a calculated capacity of 111.11 mg/g [20]. Furthermore, GO has been functionalized to enhance its adsorption capacity for Cd(II). A sponge-like polysiloxane-GO gel adsorbent exhibited a maximum adsorption capacity of 137 mg/g according to the Langmuir model [21]. However, starch-functionalized GO composite possessed a reduced Cd(II) adsorption capacity of 43.20 mg/g [18]. The maximum uptake capacity of sulfanilic acid-grafted magnetic GO for Cd(II) was approximately 54.83 mg/g at 303 k [22]. On the other hand, the adsorption capacity of 3D sulfonate reduced GO aerogel on Cd(II) was determined to be 234.8 mg/g according to the Langmuir model [23]. Effects of GO and Cd(II) on seed germination, seedling growth, and uptake to Cd(II) in solution culture were also investigated [24]. With high adsorption capacity, GO reduced the residual Cd(II) concentration in solution. The presence of GO alleviated the inhibitive effects of Cd(II) on plant growth, while the concentration of Cd in the root was generally increased by GO. Although the adsorption of Cd(II) by GO and effects of GO and Cd(II) on plants in aqueous phase have been intensively investigated, the study of the effect of GO on the adsorption of Cd(II) in soil has been seldom reported. In this study, we synthesized monolayer GO with high oxygen content by employing a modified Hummers method. Moreover, the impacts of contact time, pH values of the solution, and the initial concentration of Cd(II) on the uptake capacity of GO for Cd(II) were systematically investigated. The maximum adsorption capacities of this type of GO for Cd(II) ion were 265.8 and 269.5 mg/g from experiment result and from Langmuir model calculation, respectively, which are higher than the values in the literature mentioned above results and even higher than those of functionalized GO. Subsequently, the prepared GO was applied in Cd(II) contaminated soil. The sequential extraction method was employed to detect the content of Cd(II) with various fractions in soil. Rice was selected as the plant for study because rice is not only an important staple food for Asian but also is particularly susceptible to Cd 3 ACS Paragon Plus Environment


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contamination. The effect of GO on the adsorption of Cd(II) is illustrated in Figure 1. Cd(II) could be loaded on the surface of GO via electrostatic interaction and coordination, as reported in our previous work and many other studies [9, 11, 12, 18, 25]. A large specific surface area of monolayer GO, and a high content of oxygen-containing functional groups provide more adsorption sites and significantly increase the adsorption capacity. In soil, the adsorption of GO converts Cd(II) from inorganic-bound fraction to exchangeable fraction. Since Cd(II) in the exchangeable fraction is more easily absorbed by plants, the presence of GO in soil promotes the content of Cd(II) in rice.

P

(a)

(b) Cd(II)

ICPOES Electrostatic adsorption

Figure 1. Schematic diagrams of (a) GO in solution and paddy soil, and (b) the interaction between GO and Cd(II). Experimental Synthesis and characterizations of GO The synthesis method of GO was as we reported previously [26]. 0.6g of expanded graphite was dispersed in concentrated H2SO4 (75 mL) and then oxidants (KMnO4 and NaNO3) were added. This mixture was stirred in concentrated H2SO4 for 24 h to make sure the intercalation effect of oxidants and this whole oxidation reaction was performed under an ice bath. Subsequently, DI water was used to dilute the mixture, and then heated it until 95 °C. H2O2 (10 wt.%) was slowly added to the suspension until gas evolution ceased. The mixture was washed by HCl (20 wt.%) solution and water. Then, dialysis treatment was carried out for one week to purify products. Finally, the prepared GO solution was directly sonicated for 4 h for later use. GO solution was diluted and transferred to copper grids and silicon wafers respectively for Raman spectroscopy (HORIBA, LabRAM HR Evolution) and atomic force microscopy (AFM) 4 ACS Paragon Plus Environment

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(MFP-3D Infinity) measurements. GO membrane synthesized by vacuum filtration was for Fourier transform infrared spectrometer (FTIR) (NETZSCH X70) and X-ray photoelectron spectrometer (XPS) (ESCALAB 250Xi) measurements. The microstructures of GO before and after adsorption were evaluated by optical microscopy (ZEISS, Axio Scope A1; ProgRes CapturePro 2.7) and transmission electron microscopy (TEM) (JEM-2100F). Adsorption test in solution The experiments of Cd(II) adsorption on GO were conducted at the temperature of 293 K. The stock solutions of CdCl2·2.5H2O and GO were prepared for the batch experiments. 0.1 M HCl and 0.1 M NaOH were employed for adjusting the pH to a suitable value. To study the effect of contact time, the stock solutions were added and diluted in the tubes to get the desired concentration of GO (100 mg/L) and Cd(II) (10 mg/L). Throughout this experiment, pH value is fixed at 6.0 which is the same as the pH value of soil cultivation for rice. At certain time intervals, determinate volume solution was extracted and filtered by pressure-assisted method to collect the filtrate. Then inductively coupled plasma optical emission spectroscopy (ICP OES) (ThermoFisher, IRIS Intrepid II XSP) was employed to test the Cd(II) concentration of the filtrate, as the equilibrium concentration of Cd(II). In pH effect part, pH values in the solutions were adjusted in the range of ~3 to 10. The concentration of GO and Cd(II) in the solution were 100 mg/L and 10 mg/L, respectively. 2 days of shake treatment of solutions ensured that GO and Cd(II) reached adsorption equilibrium before filtration. In the investigation of initial concentration effect, the concentration of GO was 100 mg/L and pH value was 6.0. The initial concentration of Cd(II) changed in the range of 5 to 50 mg/L. Through the following known data, initial concentration of Cd(II) (C0 (mg/L)), equilibrium concentration of Cd(II) (Ce (mg/L)), volume of solution (V (L)) and mass of GO (m (g)), the equilibrium adsorption amount of GO on Cd(II) (qe (mg/g)) could be calculated by the following equation: 𝑞𝑒 = (𝐶0 ― 𝐶𝑒) × 𝑉/𝑚

(1)

Each experiment was done in triplicate to get the average value of data. Density functional theory (DFT) calculations DFT calculations were performed by using the Vienna Ab initio simulation package (VASP). We use the generalized gradient approximation (GGA) parameterized by Perdew, Burke and 5 ACS Paragon Plus Environment


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Ernzerhof (PBE) for the exchange-correlation functional [27-29]. The electron-ion interactions are modelled by the projector augmented wave (PAW) potentials with a valence electron configuration of 4d105s2 for Cd [30, 31]. The energy criteria for self-consistent calculations is set to 10-6 eV. The atomic structure set up for study is shown in Figure 6a, where one edge of a 1.28-nm-wide zigzag graphene nanoribbon is decorated by a single carboxylate group for the three unit cells in the y direction. Periodic boundary conditions (PBCs) are applied in all directions, and the thickness of vacuum layers is 2 and 3 nm in x and z direction respectively. A net positive charge of 1.0e is added to the system to model the ionic state. The cut-off energy for plane-wave energy of 500 eV for the valence electron wave functions, and a 1 × 7 × 1 kmesh is used for the Brillouin zone sampling, the convergence of which are validated. After structural relaxation of the hybrid with a force criterion of 0.01 eV/Å, the differential charge density is calculated as ∆𝜌 = 𝜌(GO + Cd2 + ) ―𝜌(GO) ―𝜌(Cd2 + )

(2)

where 𝜌(GO + Cd2 + ), 𝜌(GO) and 𝜌(Cd2 + ) are the charge densities for Cd2+-decorated GO, GO, and an isolated Cd2+ ion, respectively. The Bader atom-in-molecule theory is adopted for atomic charge analysis [32]. Molecular dynamics (MD) simulations We performed MD simulations to model the ion adsorption/desorption process using the largescale atomic/molecular massively parallel simulator (LAMMPS) [33]. A three-dimensional model is constructed with PBCs applied. A 2-nm-wide graphene sheet (in the x direction) is dissolved in a water box with the size of 6.7×2.9×3.0 nm (Figure S1). The graphene edge along the y direction (periodic) is decorated by charged carboxylate groups (-COO-) with a density of 1 group per 2 unit cells (or 0.2/Å) following the experimental evidence [34]. The all-atom optimized potentials for liquid simulations (OPLS) are used to model the graphene sheet and carboxylate groups [35]. The SPC/E model is used for water, which predicts reasonable static and dynamic properties of water [36]. The van der Waals interaction between the oxygen atoms in water molecules and carbon atoms in graphene is modeled in the Lennard-Jones 12-6 form, that is, V = 4ε[(σ/r)12 - (σ/r)6]. The potential parameters for pairs between carbon atoms in graphene and oxygen atoms in water are 𝜀C ― O = 4.063 meV and 𝜎C ― O = 0.319 nm. This set of parameters predicts a water contact angle of graphene as 98.4o, which aligns well with 6 ACS Paragon Plus Environment

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experimental measurements [37]. Force-field parameters for ions are taken from work by Kenneth and co-workers [38]. All the force-field parameters are summarized in Table S1. In order to understand the absorption/desorption process of ions at the functionalized graphene edges, we analyze the free energy landscape by calculating the PMFs. The reaction coordinate d is chosen as the distance between the Cd ion and the carbon atom in carboxylate groups in x-z plane (Figure S1). The PMF is calculated by using the umbrella sampling (US) method [39]. We use a harmonic spring to restrain the ionic position through d. The force constant is 30 and 5 kcal/mol/Å2 for d = 0.15-0.35 nm and d = 0.4-1.5 nm, where the width of US window is 0.05 nm and 0.1 nm, respectively. The simulation of each window runs for 6 ns that is beyond the typical correlation time for ionic motion and validated to be long enough to extract well-converged PMFs. The data is collected every 250 ps. The overlap between distribution of d in adjacent windows is large enough to minimize the statistical errors in the estimation of PMF [39], which is generated by recombining individually-biased distributions using the weighted histogram analysis method (WHAM) implemented by Grossfield [39, 40]. Soil preparation Yellow brown soil collected from Jiangsu Province, China was used in this study. According to the FAO classification, yellow brown soil was classified as Cambisol [41]. The organic matter content was ~1.3% determined by potassium dichromate volumetric method. The cation exchange capacity (CEC) of the soil was ~10 cmol(+)/kg determined by extracting cations with 1 M NH4OAc. The pH value of soil was ~6 by soil pH meter measurement. The result of singleextraction with 0.1 mol/L HCl showed that the soil was Cd-free. CdCl2·2.5H2O in the form of aqueous solution was added to Cd-free soil to make the concentration of Cd(II) in the soil was 10 mg/kg. Soil was stirred to make the distribution of Cd(II) uniformity. Soil is incubated under a humid state for one month. After that, different mass of GO were added to Cd-contaminated soil to obtain three levels of GO in soil (0, 1 and 3 g/kg, denoted as Cd10GO0, Cd10GO1 and Cd10GO3 respectively). All conditions of soils were incubated under paddy conditions for one month for the next step of Cd(II) sequential extraction and rice planting. Cd(II) fractionation Cd-free soil (denoted as Cd0GO0) and Cd-contaminated soils with different amount of GO were respectively spread on a plastic wrap in an air-circulating room. The dried soils were 7 ACS Paragon Plus Environment


ground and passed through 0.15 mm nylon sieve for Cd(II) fractionation. The sequential extraction method was conducted to fractionate Cd(II) according to the reported papers [4245]. 2 grams of soil from each condition was added to Ca(NO3)2 solution respectively. Samples were shaken for one day and then centrifuged to get the supernatant as the exchangeable fraction. 20 mL of 2.5% CH3COOH was added to the residue and shake it for one day. The supernatant obtained by centrifugation was inorganic-bound fraction. Subsequently, H2O2 was used to digest the residue in a boiling water bath until H2O2 decomposed completely. CH3COOH was employed to extract Cd(II) as organic-bound fraction. Finally the residue was infiltrated in the mixture of ascorbic acid, (NH4)2C2O4, and H2C2O4 at 373 K. After one hour, the mixture was centrifuged to get the oxides-occluded fraction. Planting and measurement of rice Seeds of rice (Oryza sativa L. ssp. japonica) were placed on wet filter paper for germination. After two weeks, germinating seedlings with similar heights were transferred to paddy soils with different treatment (Cd0GO0, Cd10GO0, Cd10GO1 and Cd10GO3), respectively. After 40 days of soil cultivation, rice seedlings were harvested. The fresh weight and height were measured for each seedling in different groups. Seedlings in the same group were collected together and roots were cut off. Samples were dried in oven at 353 K until the weight was unchanged. Rice seedlings were ground into powder and digested. Cd(II) content of rice seedlings was analyzed by ICP OES. Statistical analysis Significance of differences was analyzed by one-way analysis of variance (ANOVA). Tukey's test was performed to identify significant differences among various treatments (p < 0.05).

Results and discussion Characterizations of GO As shown in Figure 2a, the AFM image of GO sheets indicated that GO sheets were monolayer with a lateral size ranging from hundreds of nanometers to several micrometers. Figure 2b shows the wrinkled structure of GO in the TEM image. The amorphous ring of the electron diffraction pattern in the selected area revealed the existence of C–O groups (sp3) that accounts for the adsorption property of GO (Figure 2c). According to the XPS spectrum of GO shown 8 ACS Paragon Plus Environment

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in Figure 2d, it was evident that GO sheets contained various oxygen-containing functional groups. By calculation, the atomic percentage of the C–C bonds of the GO was 47.69%, whereas the percentages of C-O bonds and C=O bonds were 42.58% and 9.93%, respectively. According to the C to O atomic ratio of 2.18, it can be concluded that GO was highly oxidized. Figure 2e shows FTIR spectroscopic result with more detailed information about the oxygen functional groups. The D band (~1,350 cm−1) in Raman spectrum represented the disordered structure of graphene mainly caused by oxidation (Figure 2f). (a)

(b)

(c)

~1.3 nm

~1.4 nm

2 μm 47.49% 42.58% 9.93%

C:O (at.)

2.18

282

284

286

GO C-C C-O C=O

288

290

292

(e)

(f) Intensity (a.u.)

C-C C-O C=O

2 1/nm

200 nm

Transmittance (a.u.)

(d) Intensity (a.u.)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


800

Binding energy (eV)

1600

2400

3200

4000

Wavenumber (cm-1)

1000

1500

2000

2500

3000

Raman shift (cm-1)

Figure 2. (a) AFM image of GO sheets. The inset shows the height profiles of GO sheets. (b) TEM image and (c) selected area electron diffraction (SAED) pattern of GO sheet. (d) XPS C1s spectra, (e) FTIR spectrum and (f) Raman spectrum of GO. Adsorption capacity of GO for Cd(II) To investigate the adsorption performance and mechanism of GO prepared in this work for Cd(II), we measured the amount of adsorbed Cd(II) at different reaction times, pH values, and initial concentration of Cd(II). As shown in Figure 3a, the adsorption amount of Cd(II) on GO increased rapidly and reached adsorption equilibrium in the initial 35 min. The maximum adsorption capability of GO was 99.09 mg/g, and almost all Cd(II) was removed from the water, which is attributed to the structure of GO. The mono-layer GO with abundant oxygencontaining functional groups provides sufficient adsorption sites. Furthermore, pseudo-first9 ACS Paragon Plus Environment


order and pseudo-second-order models were applied to elucidate the adsorption mechanism (Figure 3b, c). The pseudo-first-order and pseudo-second-order models are represented by the following equations [46]: 𝑙𝑛(𝑞𝑒 ― 𝑞𝑡) = 𝑙𝑛𝑞𝑒 ― k1𝑡

(3)

𝑡 𝑞 = 1 𝑘 𝑞2 + 𝑡 𝑞 2 𝑒 𝑡 𝑒

(4)

where 𝑞𝑡 (mg/g) represents the adsorption amount of GO on Cd(II) at time 𝑡 (min). And k1 (min-1) and k2 (g·(mg·min)-1) are reaction rate constants of pseudo-first-order and pseudosecond-order models, respectively. The results of the relative kinetic parameters (k1, k2, qe, and R2) are illustrated in Table 1. The correlation coefficient R2 in pseudo-second-order model was about 0.9999, which is much higher than that in pseudo-first-order model (0.3142). The qe calculated by pseudo-second-order was ~99.3 mg/g, which is consistent with the experimental qe of 99.09 mg/g. Therefore, the adsorption process can be better simulated by pseudo-secondorder kinetic model, indicating the Cd(II) uptake by GO tends to be a chemical interaction [46, 47]. (b)

pseudo-first order model

3 2

ln(qe-qt)

q (mg/g)

(a) 100

90

80

1 0

0

50

100

150

200

250

0

50

100

t (min)

(c)

2.5

150

200

250

t (min)

(d)

pseudo-second order model

2.0

100

q (mg/g)

90

1.5

t/qt

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

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1.0 0.5

80 70 60

0.0 0

50

100

150

200

2

250

3

4

5

6

7

8

9

10

pH

t (min)

Figure 3. (a) Adsorption of Cd(II) on GO as a function of contact time. Adsorption kinetics of Cd(II) on GO: (b) pseudo-first order model; (c) pseudo-second order model. (d) Adsorption of Cd(II) on GO as a function of pH.


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Table 1. Parameters in kinetic models of Cd(II) adsorption on GO. pseudo-first-order kinetic model qe (mg·g-1)

k1 (min-1)

R2

5.64

0.0100

0.3142

pseudo-second-order kinetic model qe (mg·g-1) 99.30

k2 (g·(mg·min)-1)

R2

0.0090

0.9999

The pH value has a significant influence on the adsorption of Cd(II) on GO. In this experiment, the pH value was set from ~3 to 10 to avoid the self-agglomeration of GO at the pH value below 3 [12]. The uptake of Cd(II) increased from 60.85 to 99.60 mg/g with the initial pH increasing from 2.93 to 7.29 (Figure 3d), and then the adsorption amount remained almost constant. Since the zeta potential of GO is negative in the pH range of 1.7 to 12.2, the GO surface carries the negative charges in the investigated pH range [11]. A large number of functional groups (-COOH and –OH) charge GO negatively and enable GO the capability to adsorb Cd(II). Nevertheless, when the pH value was lower, the GO surface could be partially protonated by H+. As a result, the positively charged H+ and Cd(II) ions compete to be adsorbed on GO. With increasing pH, the oxygen-containing groups, –COOH and –OH, turn into –COOand –O-, and these negative adsorption sites attract Cd(II) via electrostatic interaction. According to the experimental results, the uptake value reached 99.09 mg/g at pH 7.29. The effect of the initial concentration of Cd(II) on adsorption property was assessed as shown in Figure 4a. The adsorption efficiency of GO remained more than 95% when the initial concentration of Cd(II) was in the range of 5 to 20 mg/L, which indicated that GO had sufficient adsorption sites at the early stage of adsorption. The maximum uptake amount of GO was 265.8 mg/g, which corresponds to the Cd(II) initial concentration of 45 mg/L. Commonly used Langmuir and Freundlich isotherms were employed to fit the correlation between uptake capacity of GO and equilibrium concentration of Cd(II), as shown in Figure 4b,c. The Langmuir and Freundlich isotherms were evaluated by the following equations [18, 48]: 𝐶𝑒/𝑞𝑒 = 1/b𝑞𝑚𝑎𝑥 + 𝐶𝑒/𝑞𝑚𝑎𝑥 1

𝑙𝑛𝑞𝑒 = 𝑙𝑛𝑘𝑓 + 𝑛𝑙𝑛𝐶𝑒

(5) (6)

where Ce (mg/L) is Cd(II) concentration in solution when the reaction reaches equilibrium. In Langmuir isotherm equation, the relative parameters, qmax (mg/g) is a calculated value, 11 ACS Paragon Plus Environment


representing the maximum adsorption amount. In the Eq. (5), kf and n are constants in relative to adsorption capability and intensity, respectively. These relative parameters and correlation coefficient R2 are listed in Table 2. The comparison of the value of R2 demonstrated that the Langmuir model was more fitted to describe the correlation between uptake capacity of GO and equilibrium concentration of Cd(II) than the Freundlich model, indicating there was monolayer coverage on the adsorbent. The maximum adsorption amount was calculated to be 269.54 mg/g by Langmuir model in this experiment, which is more than 2-fold higher than that in Zhao’s study (106.3 mg/g) [4]. Evidently, the advantages of GO in our study include monolayer structure and high oxygen content (47.69% of the C–C bonds) compared with the few-layered GO with lower oxygen content (71.4% of the C–C bonds).

(a) 300

(b) 0.10

(c)

Langmuir mode

Ce/qe (g/L)

265.8

200 150 100 50

0.08

5.5

0.06

5.0

lnqe

250

q (mg/g)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

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0.04

4.5

0.02 4.0

0.00 0

10

20

30

40

50

Freundlich mode

0

5

C0 (mg/L)

10

15

Ce (mg/L)

20

25

-2

-1

0

1

2

3

4

lnCe

Figure 4. (a) Adsorption of Cd(II) on GO as a function of initial concentration of Cd(II) in the solution. Adsorption isotherms of Cd(II) on GO: (b) Langmuir model; (c) Freundlich model. Table 2. Parameters in adsorption isotherms of Cd(II) adsorption on GO. Langmuir

Freundlich

qmax

b

R2

kf

n

R2

269.54

1.484

0.9977

135.90

3.888

0.6925

The structure change of GO after adsorption was also investigated in this study. Figure S2a in supporting information shows a visual observation of GO flocculation after 2 days under different initial concentrations of Cd(II). Bulky precipitation and darker color could be observed at the concentration of 35 mg/L. The supernatant became gradually clear with increasing Cd(II) concentration. To further investigate the microstructure transformation of GO, 12 ACS Paragon Plus Environment

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we conducted TEM experiments (Figure S2b). Compared with the flat structure of GO with a slight wrinkle, GO underwent a three-dimensional agglomeration during the adsorption process. Figure S2c shows the optical image of GO, in which the inconspicuous light blue sheets on the substrate corresponded to few-layered GO [49]. After adsorption, bright bulks could be observed which corresponded to multilayer aggregates with large size (Figure S2d). According to the study on the morphology transformation of GO in heavy metal solutions [12], the complexes of heavy metals and GO could be tube-like, multiple folded, or bulk aggregations at first. Finally, these aggregations interacted with each other, producing large aggregates. The result of our study is consistent with these previously reported studies.

Adsorption mechanisms To identify the adsorption mechanism and species of Cd(II) on GO, XPS analysis was conducted. XPS spectra obtained before and after Cd adsorption are shown in Figure 5a-c and Figure 5d-e, respectively. The C1s spectrum showed the binding energies corresponded to CO and O-C=O at 287.1 and 288.3 eV (Figure 5a), respectively, and the O1s spectrum showed the binding energy corresponding to C-O at 532.8 eV and C=O at 531.4 eV (Figure 5b) [19, 50, 51]. The adsorption of Cd(II) induced noticeable changes in C1s and O1s spectra (Figure 5d,e). The binding energy of O-C=O in C1s spectrum increased to 288.6 eV while that associated with C=O in the O1s spectrum shifted to 531.6 eV. These changes demonstrated that carboxyl-Cd complex was the main product during the adsorption process. The increase of binding energy indicated that GO acted as an electron donor in the interaction with Cd(II) [52].



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Figure 5. XPS spectra before adsorption: (a) C1s, (b) O1s and (c) survey, and after adsorption: (d) C1s, (e) O1s, (f) survey. The experimental results here indicate that the carboxylate groups at GO edges offer active sites for Cd2+ absorption. Our previous theoretical work suggests that oxygen-containing groups in GO can perturb the hydration shells (HSs) of ions by replacing water molecules in HSs, as driven by the specific ion interaction with functional groups [53]. To further understand charge transfer upon the absorption/desorption process, DFT calculations were performed for Cd(II) ions absorbed by carboxylate groups at GO edges. The isosurfaces of the differential charge density in the GO-Cd(II) hybrid show both charge depletion and accumulation around the Cd(II) ion (Figure 6a), and the net value is positive, that is, electron is transferred from GO to Cd(II). Bader charge analysis shows that the transferred charge is 1.18e, aligning well with the experimental data (Figure 5). To analyze the free energy landscape of ion adsorption/desorption in the aqueous condition, we perform molecular dynamics (MD) simulations. We calculated PMFs for these processes as a function of the Cd-O distance d (Figure S3a, see details in the Experimental section), the amplitude of which decreases as the ion approaches the carboxylate group, with several peaks and valleys. The calculation results show that ion absorption at the functionalized GO edges are energetically favorable compared to those in the solution, but is a multi-step process experiencing free energy barriers of a few kBT before reaching the site of absorption. 14 ACS Paragon Plus Environment

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Specifically, there is a deep valley in the PMF curve at d = 0.30 nm, indicating direct absorption of the ion on one of the oxygen atoms in carboxylate groups by substituting a water molecule in the 1st HS (Figure S3b). Additionally, two local minima are identified. The first is located at d = 0.23 nm, where the ion is trapped by two oxygen atoms in carboxylate groups, substituting two water molecules in the 1st HS (Figure S3c). The other minimum at d = 0.40 nm indicates ion absorption mediated by hydrogen bonds (H-bonds) between water molecules on the 1st HS and the oxygen-containing groups (Figure S3d). The free energy barriers between the local minima and the most energetically favorable site at d = 0.30 nm are 1.0 and 4.0 kBT as identified in the PMF. The free energy barriers for absorption (ΔGabs) and desorption (ΔGdes) defined through the highest barrier in the multi-step process are ~ 4 kBT and 6 kBT, respectively. These results suggest that the Cd(II) ion can be absorbed as trapped by one or two oxygen atom on carboxylate groups or mediated by H-bonds between water molecules in the 1st HS and the oxygen-containing groups by thermal fluctuation (Figure 6b).

Figure 6. (a) Differential charge density isosurfaces at 0.047 |e|/Å3, which are plotted in both top and side views (yellow for accumulation, cyan for depletion). C, O and Cd atoms are shown as gray, red and green balls. (b) Absorption of hydrated Cd(II) at the carboxylate groups. The absorption can occur while the ion is trapped by one or two atoms in the carboxylate group, or mediated by the H-bonds (green dash lines) between the water molecules on the 1HS of ions and the oxygen-containing groups. The water molecules are shown as red (O) and white (H) circles surrounding the ions. The gray rectangle indicates the graphene sheet. Effect of GO on growth and Cd(II) uptake by plant Cd-free soil (Cd0GO0) and other three groups of Cd-contaminated soils (Cd10GO0, Cd10GO1, and Cd10GO3) were planted with germinating rice seedlings after incubation. During planting, 15 ACS Paragon Plus Environment


water in the pots was kept over ~3 cm of the soil surface to ensure the condition of paddy soil. Seedlings were harvested after 40 days of planting. As shown in Figure 7a, no significant differences in the physical characteristics of rice were observed in different groups. Rice treated in four groups of soils (Cd0GO0, Cd10GO0, Cd10GO1, and Cd10GO3) exhibited similar heights (Figure 7b). Nonetheless, rice seedlings treated in Cd10GO3 group soil showed the largest fresh weight value (Figure 7c). GO itself is a soil conditioner that moisturizes soil and provides water for plant growth, as mentioned in our previous research [8]. It was evident that the addition of GO caused the color of soil darker (Figure S4). GO could effectively prevent soil compaction, and at the same time, as an organic substance, it could increase the carbon content in the soil and enhance the soil fertility [9]. Figure 7d shows the content of Cd(II) in rice seedlings treated with different soil groups measured by ICP-OES. Rice treated in the control group (Cd0GO0) contained only a small amount of Cd(II) (0.75 mg/kg) which might originate from watered tap water. The present of GO promoted Cd(II) uptake by rice from the soil. The accumulation of Cd(II) in rice treated with Cd10GO3 group soil was 12.5% higher than that of treated with Cd10GO0 group soil. 14

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Figure 7. (a) Photographs of rice seedlings in Cd0GO0, Cd10GO0, Cd10GO1 and Cd10GO3 soils. (b) Height of rice seedlings. (c) Fresh weight of seedlings. (d) Cd(II) concentration in rice seedlings. Different lowercase letters indicate a significant difference among three GO concentrations at p < 0.05. Results are shown as means ± SD of 6 replicates in (b, c) and 3 replicates in (d). Effect of GO on the forms of Cd(II) in Soil To further elucidate the mechanism that GO promoted Cd(II) adsorption by rice, we analyzed the distribution of Cd(II) in various forms in soil with GO application by employing sequential extraction method. The fractionation results of the forms of Cd(II) in the soil before and after rice planting are shown in Figure 8a,b. Cd(II) adsorbed on clay and organic particles by negatively charged adsorption sites is described as exchangeable Cd(II). This part of Cd(II) is the first portion to be extracted and is the most readily absorbed by the plant. According to the order of extraction, the later Cd(II) is extracted, the more difficult Cd(II) is to be absorbed by plants. The secondly extracted Cd(II) belongs to inorganic-bound which generates coprecipitation with carbonate. The complexation of Cd(II) with organic ingredients forms organic-matter-bound form Cd(II) while the reaction of Cd(II) with oxides forms oxideoccluded form Cd(II). The remaining Cd(II) is tightly bound to minerals and needs to be extracted with a mixed strong acid, which is ineffective for plant absorption.



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Figure 8. Effect of GO on the forms of Cd(II) in soil (a) before and (b) after rice planting. Different lowercase letters indicate a significant difference among three GO concentrations at p < 0.05. Results are shown as means ± SD of 3 replicates. Figure 8a shows the distribution of Cd(II) in various forms in Cd(II) contaminated soil treated with a different amount of GO. The contents of exchangeable Cd(II) in group Cd10GO1 and Cd10GO3 were 1.04 and 1.19 mg/kg, respectively, which are higher than those in group Cd10GO0 (0.78 mg/kg). In previous studies, it was reported that Si and Fe nanoparticles played the key role in reducing Cd accumulation in rice plant [54-56]. Si as a fertilizer could be absorbed by plant, and Si deposition in apoplasts and co-precipitation with Cd in the cell walls of rice plants could reduce the transportation of Cd in apoplasts or into the cells. Furthermore, the gene expression of Cd uptake and transport (OsLCT1 and OsNramp5) was inhibited by Si. The contents of Fe in the amorphous iron oxides were significantly and negatively correlated with the contents of Cd in the exchangeable fraction and the carbonate-bound fraction. Fe turned Cd into a low bioavailability. As for GO, our previous work showed that GO sheets were captured by soil and not able to enter the plant. Therefore, the effect of GO was simply 18 ACS Paragon Plus Environment

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from its influence on the form of Cd in the soil. The result showed that GO significantly promoted the conversion of inorganic-bound Cd(II) into exchangeable Cd(II) which is more available for plant absorption. The pH value of soil remained constant after the addition of GO, and the pH value was ~6 in all groups by soil pH meter measurement. In the preceding result of the experiment, when the pH was raised to 6, adsorption efficiency of Cd(II) on GO reached 97.2%. Furthermore, the adsorption of Cd(II) on GO only took 35 min to achieve an adsorption equilibrium. In paddy soil experiment, as an organic nanoparticle, GO adsorbs Cd(II) via electrostatic adsorption by the oxygen-containing functional groups on the surface of GO. According to the definition of exchangeable Cd(II), namely Cd(II) adsorbed to clay and organic particles by negatively charged adsorption sites, the fraction of Cd(II) adsorbed by GO is exchangeable form and extremely easy to be absorbed by plants. As a result, the strong adsorption capability of Cd(II) by GO destroys the reaction equilibrium of Cd(II) by forming carbonate and shifts the reaction to the opposite direction. At the same time, the carboxyl group endows GO an organic acid property, which reacts with carbonate to release the Cd(II). When the rice was grown in soil with GO application, GO constantly changed the existing form of Cd(II) and provided absorbable exchangeable Cd(II) for rice to promote the Cd(II) uptake. The distribution of Cd(II) in the soil after the harvest of rice is shown in Figure 8b. It can be seen that the content of Cd(II) did not exhibit a significant change in organic-matter-bound form and oxides-occluded form. The role of GO is mainly to convert inorganic-bound Cd(II) into exchangeable Cd(II). With the treatment of GO, the total amount of Cd(II) remaining in the soil is reduced. Compared with the total amount of Cd(II) in the group Cd10GO0 soil (8.69 mg/kg), the total amount of Cd(II) is significantly reduced to 7.43 mg/kg in group Cd10GO3.

Conclusions In conclusion, the results of this work revealed that GO could significantly increase the content of exchangeable Cd(II) that is bioavailable for the plant in Cd-enriched soil and promote the accumulation of Cd(II) in rice. Firstly, we investigated the adsorption mechanism of GO for Cd(II) and the critical parameters affecting the adsorption reaction. It was found that GO exhibited strong adsorption capacity under the neutral condition. GO mainly adsorb Cd(II) through oxygen-containing functional groups on the surface of GO via electrostatic interaction. 19 ACS Paragon Plus Environment


The paddy soil conditions for planting rice provides GO an optimal environment for the adsorption of Cd. Furthermore, the adsorption of Cd(II) on GO increased the fraction of exchangeable Cd(II) in the soil which is more ready for the plant to absorb. Although it showed indirect toxicity to plant, GO has the potential value for heavy metal removal when integrated with other technologies. Moreover, GO can be used as a promoter in bioremediation technology, facilitating sacrificial plants to adsorb and remove more heavy metals. According to the effect of GO that could efficiently convert Cd(II) to exchangeable form, GO might be utilized as an eluent for the soil remediation. Further work will focus on these positive potential applications utilizing GO. Given the existing form of Fe in soil and the iron plaque on roots of rice have a significant influence on the adsorption of heavy metals by rice [57, 58], we will further study the effects of GO on other metals such as Fe in the soil, microbial community, and iron plaque on roots to elucidate the mechanism of GO promoted Cd absorption by plants in more detail. Acknowledgements This work was supported by Beijing Natural Science Foundation (2172027). Supporting Information MD simulation model, parameters, and characterizations of GO and GO treated soils.

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TABLE OF CONTENTS GRAPHIC Graphene oxide can efficiently convert the inorganic-bound form Cd(II) into the exchangeable form, thus can be utilized as an eluent for the soil remediation.

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