Dissolved Oxygen and Visible Light Irradiation Drive the Structural

Jun 4, 2019 - The dissolved ions did not induce apparent phytotoxicity. ... of chlorophyll a, ROS generation in algal cell, and metabolite analysis (P...
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Article Cite This: Environ. Sci. Technol. 2019, 53, 7759−7769

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Dissolved Oxygen and Visible Light Irradiation Drive the Structural Alterations and Phytotoxicity Mitigation of Single-Layer Molybdenum Disulfide Wei Zou,† Qixing Zhou,‡ Xingli Zhang,† and Xiangang Hu*,‡

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†

School of Environment, Key Laboratory for Yellow River and Huai River Water Environment and Pollution Control, Ministry of Education, Henan Key Laboratory for Environmental Pollution Control, Henan Normal University, Xinxiang 453007, P. R. China ‡ Key Laboratory of Pollution Processes and Environmental Criteria (Ministry of Education)/Tianjin Key Laboratory of Environmental Remediation and Pollution Control, College of Environmental Science and Engineering, Nankai University, Tianjin 300350, P. R. China S Supporting Information *

ABSTRACT: Understanding environmental fate is a prerequisite for the safe application of nanoparticles. However, the fundamental persistence and environmental transformation of single-layer molybdenum disulfide (SLMoS2, a 2D nanosheet attracting substantial attention in various fields) remain largely unknown. The present work found that the dissolution of SLMoS2 was pH and dissolved oxygen dependent and that alterations in phase composition significantly occur under visible light irradiation. The 1T phase was preferentially oxidized to yield soluble species (MoO42− and SO42−), and the 2H phase remained as a residual. The transformed SLMoS2 exhibited a ribbon-like and multilayered structure and low colloidal stability due to the loss of surface charge. Dissolved oxygen competitively captured the electrons of SLMoS2 to generate superoxide radicals and accelerated the dissolution of nanosheets. Compared to pristine 1T−phase SLMoS2, the transformed 2H−phase SLMoS2 could not easily enter algal cells and induced a low developmental inhibition, oxidative stress, plasmolysis, photosynthetic toxicity and metabolic perturbation. The downregulation of amino acids and upregulation of unsaturated fatty acids contributed to the higher toxicity of 1T−phase SLMoS2. The dissolved ions did not induce apparent phytotoxicity. The connections between environmental transformation (phase change and ion release) and phytotoxicity provide insights into the safe design and evaluation of 2D nanomaterials.

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INTRODUCTION Single-layer molybdenum disulfide (SLMoS2), a typical twodimensional (2D) transition metal dichalcogenide (TMD), has been widely applied in electronics and optoelectronics,1 catalysis,2,3 energy storage,4 biology,5 biomedicine,6,7 and environmental protection.8,9 Given the potential of environmental and organism exposure to SLMoS2 during the nanomaterial lifecycle (e.g., fabrication, use, and disposal), environmental fate and safety should be considered in detail.10,11 Compared to pristine nanoparticles, environmentally transformed nanoparticles may exhibit different morphologies, structures, and stabilities, leading to the alteration of ecological and health effects.12 For example, light irradiation has driven changes in graphene morphology and reduced the toxicity of graphene to aquatic algae.13 Ion release from metal and metallic oxide nanoparticles in water has contributed to the enhancement or mitigation of nanotoxicity.14,15 However, the role of dissolved oxygen (DO) and visible light irradiation, which are both common environmental factors, in the nanoparticle properties (e.g., © 2019 American Chemical Society

phase change), environmental stability (e.g., ion release), and ecotoxicity of SLMoS2 remains largely unknown. The SLMoS2 surface can be quickly oxidized to produce molybdenum oxide (MoO3) at defect sites after exposure to oxygen at temperatures above 340 °C.16 In the presence of oxygen or other strong oxidizing agents (hydroxyl radicals and H2O2), SLMoS2 can be fast-etched and release soluble species.17 These results demonstrate that SLMoS2 can be oxidized under extensive conditions. At room temperature, sunlight-induced reactions (oxidation and reduction) also affect the oxidation state, the generation of reactive oxygen species (ROS), and the persistence of nanomaterials, although the process is slow.18 Photoactive nanomaterials, including metal- and carbon-based nanoparticles, can absorb visible light and react with oxygen to produce ROS.19 As a typical Received: Revised: Accepted: Published: 7759

January 5, 2019 April 29, 2019 June 4, 2019 June 4, 2019 DOI: 10.1021/acs.est.9b00088 Environ. Sci. Technol. 2019, 53, 7759−7769

Article

Environmental Science & Technology

Characterization of Pristine and Transformed SLMoS2. The transformed SLMoS2 samples in the groups (pH = 3, 7, and 11) with saturated DO (9.52 mg/L) after 56 days of incubation (named T3-SLMoS2, T7-SLMoS2, and T11SLMoS2, respectively) were collected. Then, the morphology, structure, colloidal stability, and chemical and optical properties of pristine and transformed SLMoS2 were characterized by transmission electron microscopy (TEM, HT7700, Hitachi, Japan), atomic force microscopy (AFM, Agilent 5420, U.S.A.), Raman spectroscopy (Thermo Scientific, DXR, U.S.A.), dynamic light scattering (DLS, Brookhaven, U.S.A.), electrochemical workstation analysis (CHI660E, Shanghai Chenhua, China), UV−vis analysis (T90, Purkinje General, China), Fourier transform infrared spectroscopy (FTIR, Bruker Tensor 27, U.S.A.), X-ray photoelectron spectroscopy (XPS, Kratos, Japan), and X-ray powder diffraction (XRD, Rigaku Ultima IV, Japan). The details are provided in the Supporting Information (SI). Free Radical Measurements. Peroxy radical (•O2−) was determined using the spin trap 5,5-dimethyl-1-pyrroline-Noxide (DMPO, 10 mM) in methanol solution using an electron spin resonance (ESR) spectroscope (MiniScope 400, Germany). •OH was detected by monitoring the fluorescence intensity of 2-hydroxyterephthalic acid (TAOH) at 435 nm in aqueous solution using a UV−vis spectrometer (T90, Purkinje General, China). The details are provided in the SI. C. vulgaris Cultivation. C. vulgaris and its culture medium (BG-11) were obtained from the Freshwater Algae Culture Collection at the Institute of Hydrobiology, China. The environmental exposure of nanoparticles at high concentrations can occur in relevant wastewater from manufacturing facilities, although the environmentally relevant concentrations are currently unclear. Significant toxicity was observed when the SLMoS2 concentration was over 10 mg/L in a previous cytotoxicity study.24 Given the rapid development of 2D nanomaterials, nanomaterials at 1, 10, and 25 mg/L were prepared in algal BG-11 culture medium to compare the toxicology of pristine and transformed SLMoS2. The initial density of algal cells was 1.5 × 105 CFU/mL. SLMoS2 was exposed to algal cells in 250 mL glass flasks, and algal cells without SLMoS2 were used as controls. To study the effects of released molybdate salts, the algae were also exposed to 100 μM Na2MoO4 (the corresponding mass concentration of MoO42− was 15.9 mg/L), which was higher than the concentrations of ions released by SLMoS2 at 25 mg/L. The glass flasks were shaken at 150 rpm for 10 min once every 8 h and placed in an illumination incubator (LRH-250 Gb, China) at 24.0 ± 0.5 °C and 80% humidity. Each treatment was performed in triplicate. The effects of SLMoS2 on algal division were measured by counting the number of algal cells by flow cytometry (FCM, BD FACSCalibur, U.S.A.) at 24, 48, 72, and 96 h. Cellular Ultrastructure Observation, Nanomaterial Uptake, and ROS. The cell suspension (5 mL) was centrifuged at 9000g for 5 min, and the supernatant was discarded. The pellets were washed with phosphate buffered saline (PBS), and then the algal cells were fixed in 2.5% glutaraldehyde at 4 °C overnight, post fixed in 1% osmium tetroxide for 2 h, dehydrated in an ethanol gradient (30%, 50%, 70%, 80%, 90%, 95%, and 100%), and then embedded in an epoxy resin. Ultrathin sections (approximately 90 nm) of algal cells were cut using a diamond knife on an ultramicrotome (EM FC7, Leica, Germany) and stained with uranyl acetate

semiconductor material, SLMoS2 exhibits a lower bandgap (1.8 eV) than that of TiO2 nanoparticles (3.0−3.2 eV),20 which is beneficial for visible light adsorption. Herein, it was hypothesized that the environmental transformation of SLMoS2 can occur slowly in an oxygen-containing aqueous phase with visible light irradiation at room temperature. Nanotoxicity is highly relevant to the physicochemical properties (e.g., morphology, colloidal stability, layer structure, and crystal structure) of nanomaterials.13,21,22 For example, anatase TiO2 with octahedral coordination was more chemically active than rutile TiO2 with square prismatic coordination in the production of ROS, which are positively related to the toxicity of TiO2 in vitro.23 Environmental factors may change the morphology and phase of SLMoS2, leading to the enhancement or mitigation of nanotoxicity. The objective of the present study is to understand the physicochemical transformation of SLMoS2 nanosheets in oxygen-containing water with visible light irradiation and the effects on the aquatic toxicity of the nanosheets. pH, as another environmental factor, is also taken into consideration. Specifically, the following issues are addressed: (i) the chemical dissolution kinetics of SLMoS2; (ii) the morphology, colloidal stability, layer structure, and phase alterations of SLMoS2; and (iii) the ecotoxicity (e.g., photosynthesis, ROS, and metabolic profile) of pristine and transformed SLMoS2 to a model species (Chlorella vulgaris). The results provide insights into the safe design and evaluation of 2D nanomaterials. By analyzing the connections between environmental transformation (phase change and ion release of nanoparticles) and ecotoxicity, the present work will provide insights into the safety evaluation and design of SLMoS2.

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MATERIALS AND METHODS Environmental Transformation of SLMoS2 Nanosheets. Pristine SLMoS2 nanosheets (chemically exfoliated, single layer >99%) were obtained from Nanjing XFNANO Materials Tech Co., Ltd., China. Deionized water (18.2 Ω/cm) was heated to boiling to remove DO and then cooled to room temperature in a nitrogen-filled glovebox. SLMoS2 nanosheets (5 mg) were suspended in 200 mL of prepared water. The SLMoS2 suspension (25 mg/L) was placed in a shaking incubator (24 °C, 150 rpm, humidity 80%) and incubated for 8 weeks with and without irradiation (light/dark = 14:10) by a xenon arc lamp (CEL-HXF300, Ceaulight, Beijing, China) with a UV cutoff (λ < 420 nm) of 35 W/m2. To analyze the effects of pH, the pH values of the SLMoS2 suspensions were adjusted to 3−11 by 0.1 mM HCl and 0.1 mM NaOH. To study the effect of DO, the suspension was aerated with pure oxygen (0.01, 0.05, 0.1, and 0.5 L/min), and the tested concentrations of DO were 3.21, 6.76, 9.23, and 9.52 mg/L (saturated), respectively. The groups placed in a nitrogen-filled glovebox were set up as the control (0 mg/L DO). After 8 weeks of reaction, the SLMoS2 nanosheets were separated using a 0.1 μm polyether sulfone (PES) filter and then lyophilized. To analyze the release kinetics of ions from the SLMoS2 nanosheets, the filtrates on the 7th, 14th, 21st, 28th, and 56th days were collected by ultrafiltration centrifugation (Amicon Ultra-15 3kD, Millipore, U.S.A.). Then, the contents of the dissolved Mo and S species were determined by inductively coupled plasma mass spectrometry (ICP−MS, Agilent 7700, U.S.A.). Each treatment was performed in triplicate. 7760

DOI: 10.1021/acs.est.9b00088 Environ. Sci. Technol. 2019, 53, 7759−7769

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Environmental Science & Technology

Figure 1. Kinetics of pH-dependent chemical dissolution. (a,b) The contents of dissolved Mo and S species from SLMoS2 nanosheets without dissolved oxygen (DO) and light irradiation. (c,d) The contents of Mo and S species released by SLMoS2 nanosheets treated with DO but without light irradiation. (e,f) The contents of dissolved Mo and S species from SLMoS2 nanosheets treated with saturated DO and light irradiation. The saturated concentration of DO was 9.52 mg/L. The values in parentheses represent the final concentrations of released ions (mg/L) on the 56th day.

supernatant was mixed with the previously collected supernatant. Then, water (1.5 mL) was added to the above supernatant and centrifuged at 9000g for 5 min. The lower phase was separated and filtered through a 10 cm silica gel column, followed by nitrogen blowing. The upper phases, which consisted of methanol and water, were dried by nitrogen blowing and lyophilization, respectively, and then mixed with the residual lower-layer phase. N-Methyl-N-(trimethylsilyl)trifluoroacetamide (80 μL) and methoxamine hydrochloride (20 mg/mL, 50 μL) were added as derivatives. After derivatization, the samples (1 μL) were injected into a gas chromatography column (HP-5MS, Agilent, U.S.A.) in split mode (1:25), and the metabolites were identified. Metabolic analysis was conducted using gas chromatography with mass spectrometry (GC−MS; 6890N/5973, Agilent, U.S.A.). The MS was operated in full scan mode with a detection slope of m/z 80−800. The metabolites were identified using the National Institute of Standards and Technology (NIST 14.0) mass spectra library in ChemStation software. Statistical Analysis. All experiments were performed in triplicate. The results are presented as the mean ± standard deviation. The statistical significance was analyzed with one− way analysis of variance (ANOVA) followed by Tukey’s test. A p value less than 0.05 was considered statistically significant. All statistical analyses were performed using IBM SPSS 22.0.

and lead citrate for 15 min. The distribution of SLMoS2 was observed by TEM (HT7700, Hitachi, Japan), and the uptake of SLMoS2 was quantified by ICP-MS (Agilent 7700, U.S.A.). In brief, a known amount of 105 algal cells was collected and digested using HNO3/H2O2 (v:v, 3:1) until no color was observed. After filtration through a 0.45 μm water membrane, the concentration of Mo ions was determined by ICP−MS (Agilent 7700, U.S.A.). The endocytosis pathway and mechanisms of SLMoS2 by algal cells were investigated using physical and pharmacological inhibitors. The algal cells were preincubated at 4 °C for 1 h to inhibit energy-dependent uptake, and then, the SLMoS2 nanosheets were exposed for 1 h at room temperature. To determine the specific mechanisms of cellular uptake, the algal cells were pretreated with methyl− betacyclodextrin (MβCD, 20 mM), chlorpromazine hydrochloride (CPZ, 100 μM), and 5-(N-ethyl-N-isopropyl) amiloride (EIPA, 50 μM) for 1 h. Subsequently, SLMoS2 was exposed to the algae for 1 h. The cellular contents of Mo ions in algal cells were detected as described above. On the basis of the S/Mo molar ratio (approximately 2) of pristine and transformed SLMoS2 (eq S1, details below), the concentration of Mo ions was then converted to the SLMoS2 nanosheet content per 105 cells. The measurement of ROS is presented in the SI. Algal Metabolism. The algal suspension (30 mL) was centrifuged at 9000g for 5 min to collect cells. To completely break the cell walls, the collected algal cells underwent three cycles of freezing in liquid nitrogen and thawing at room temperature. Subsequently, 4.5 mL of a methanol/chloroform/ water (volume ratio = 2.5:1:1) solution was added to the cell suspension, and the cells were completely broken using an ultrasonic probe (150 W, 10 min) in an ice−water bath. The metabolites were extracted using sonication (200 W, 30 min), followed by centrifugation at 9000 g for 5 min at 4 °C. After sonication and centrifugation, the supernatant was collected, and the pellet was extracted again as described above. The

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RESULTS AND DISCUSSION Visible Light Irradiation, DO, and Alkalinity Accelerate Ion Release from SLMoS2 Nanosheets. The timeand pH-dependent dissolution of Mo and S species from SLMoS2 nanosheets is presented in Figure 1. The concentrations of released Mo and S species at pH = 11 after 56 days of reaction were 3.122 and 2.088 mg/L, respectively, which were higher than those at pH = 3 (0.631 and 0.424 mg/L for released Mo and S species, respectively). MoS2 nanosheets produced soluble ions in aqueous media accompanied by 7761

DOI: 10.1021/acs.est.9b00088 Environ. Sci. Technol. 2019, 53, 7759−7769

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Figure 2. Effect of pH on the ion release and phase composition of SLMoS2. (a) UV−vis spectra of pristine SLMoS2, T3-SLMoS2, T7-SLMoS2, and T11-SLMoS2. (b) XPS spectra of pristine SLMoS2, T3-SLMoS2, T7-SLMoS2, and T11-SLMoS2. The changed intensity in phase−associated bonds (a) and the deconvolution analysis (b) confirmed the alterations comprising the disappearance of the 1T phase and the enrichment of the 2H phase proportion under visible light irradiation.

protons,10 and the hydroxyl ions in alkaline conditions contributed to the dissolution of SLMoS2 (eq S1 in the SI). Importantly, SLMoS2 dissolved slowly without oxygen (Figure 1a,b). The concentrations of released Mo and S species at pH = 11 reached 6.218 and 4.405 mg/L, respectively, when DO was supplemented (Figure 1c,d). The details of dissolved Mo released from SLMoS2 under DO conditions at different pH values are provided in Table S1. Visible light irradiation also significantly increased the release of Mo and S (Figure 1e,f), with approximately 4-fold higher dissolved concentrations than those in the dark (Table S1). The highest contents of Mo and S species after 56 days of irradiation in the alkaline groups (pH = 11) were 12.035 and 7.836 mg/L, respectively. Noticeably, the soluble ionic contents significantly increased with the DO concentration in the visible-light-irradiated groups (Figure S1). The contents of dissolved Mo species at the 56th day in the pH = 11 groups reached 9.017, 10.518, and 11.568 mg/L when the DO concentrations were at 3.21, 6.76, and 9.23 mg/L, respectively. The majority (80.23%) of SLMoS2 nanosheets dissolved with the supplementation of saturated DO (9.52 mg/ L) and visible light irradiation in the pH = 11 groups. In contrast, 20.81% and 41.45% of the nanosheets were dissolved under dark and single-DO treatment, respectively (Table S1). The above data suggested that DO and visible light irradiation significantly accelerated the chemical dissolution of SLMoS2. SLMoS2 was chemically oxidized, while molybdate ions (MoO42−) and sulfate (SO42−) were the detected main products, as shown in eq S1. XPS spectra revealed the existence of a Mo6+3d band in SLMoS2, ascribed to molybdenum trioxide (MoO3). The Mo6+3d band in the

XPS spectrum disappeared after visible light treatment (as presented below), implying the dissolution of MoO3. MoO3 can also be dissolved to molybdate in alkaline conditions (eq S2), further producing excess MoO42−. Therefore, the molar ratios of soluble S/Mo were less than 2 in the visible-lighttreated groups (Figure S2), as a result of the release of extra MoO42− due to the photoreduction of MoO3 in the SLMoS2 nanosheets. Visible Light Irradiation, DO, and Alkalinity Promote Phase Alteration. According to the UV−vis spectra (Figure 2a), pristine SLMoS2 exhibited a considerable adsorption band at ∼217 nm, which was attributed to the predominance of the metallic 1T phase.25,26 With the release of soluble species, the absorption intensities at 200−300 nm significantly decreased, indicating the dissolution of the 1T phase. Compared to pristine SLMoS2, the adsorption band of transformed SLMoS2 was blueshifted (∼10 nm). The characteristic peaks of the 2H phase at ∼610 and ∼670 nm became strong, and the absorbance at 500−800 nm increased (Figure 2b), suggesting a reduction in the 1T phase and the enrichment of the 2H phase. The Mo 3d spectra in Figure 2c revealed that the 1T and 2H phases accounted for 72.9% and 27.1%, respectively, of pristine SLMoS2. However, the proportion of the 1T phase significantly decreased with exposure to DO and visible light irradiation. The proportion of the 1T component decreased from 72.9% in pristine SLMoS2 to 57.4%, 43.5%, and 11.4% in T3-SLMoS2, T7-SLMoS2, and T11-SLMoS2, respectively, which was consistent with the UV−vis spectra in Figure 2b. A significant decrease in the 1T phase of SLMoS2 in the visiblelight-irradiation group with the increase in exposed DO is also 7762

DOI: 10.1021/acs.est.9b00088 Environ. Sci. Technol. 2019, 53, 7759−7769

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Figure 3. Alterations in morphology, surface chemistry, layer structure, and colloidal stability of SLMoS2 driven by dissolved oxygen and visible light irradiation. (a−d) AFM images of pristine SLMoS2, T3-SLMoS2, T7-SLMoS2, and T11-SLMoS2. (e) FTIR spectra. (f) Raman spectra. The shifts of the E2g and A1g modes are denoted by arrows. Correlations between the A1g−E2g shifts and the layer number of MoS2 nanosheets are presented in the SI. (g) Time profile of the average hydrodynamic diameter of SLMoS2 at pH 7.0. d1, d2, d3, and d4 represent the initial aggregation rates of pristine SLMoS2, T3-SLMoS2, T7-SLMoS2, and T11-SLMoS2, respectively. (h) Zeta potential.

dissolution, the (002) reflection, which was associated with the interplanar crystal spacing of SLMoS2,28 was significantly blueshifted, and the width of the peak became narrow. The (002) reflection peak of T11-SLMoS2 was centered at a 2θ of 14.46°, which was similar to that (a 2θ of 14.4°) of pure 2H MoS2.28 The intensities of the (100), (103), (105), and (112) reflections became stronger, while the (105) and (112) peaks were contracted in transformed SLMoS2 compared to that of pristine SLMoS2, indicating that the nanostructure of SLMoS2 was affected and transformed to the 2H phase with the chemical dissolution of the 1T polymorph. Morphological and Structural Alterations. As shown in Figure 3a, the lateral size of pristine SLMoS 2 was approximately 100−200 nm, and the thickness was 1.243 ± 0.051 nm, which were consistent with the reported properties of SLMoS2 nanosheets.29 In addition, abnormal pores and dentate edges existed on and around the nanosheets, which was ascribed to inherent defects of SLMoS2.30 After treatment with visible light irradiation, the Mo and S atoms on the nanosheets were chemically dissolved, and the lateral size became substantially smaller (Figure 3b−d). The large nanosheets also transformed to ribbon morphology, and

observed in Figure S3, implying the crucial role of DO in the phase alteration of SLMoS2. Additionally, the Mo 3d core-level spectrum of pristine SLMoS2 consisted of three peaks located at ∼235.5, ∼232, and ∼229 eV, which were related to 3d Mo6+ and 3d3/2 and 3d5/2 of Mo4+, respectively. Visible light irradiation induced the dissolution of Mo oxides (Figure 1), resulting in the disappearance of the 3d Mo6+ band in T11SLMoS2. The 3d Mo4+ peaks shifted to higher binding energies in Figure 2c, confirming the enrichment of the 2H phase in transformed SLMoS2. The alteration in the phase composition of SLMoS2 was further verified by the S 2p core-level spectrum in Figure 2d. The peaks of the S 2p1/2 and S 2p3/2 bands also shifted to higher binding energies, suggesting the enrichment of the 2H phase in the transformed SLMoS2, especially in T11SLMoS2. Another convincing result was the distinguishable broad band in transformed SLMoS2, which consisted of two peaks ascribed to 2H doublets. The crystal structure alteration of SLMoS2 was also investigated by XRD. The characteristic XRD peaks centered at 2θ values of 14.92° (002), 39.28° (103), and 44.26° (006) were observed in all samples (Figure S4), suggesting that the major component was SLMoS2 nanosheets.27 With the 7763

DOI: 10.1021/acs.est.9b00088 Environ. Sci. Technol. 2019, 53, 7759−7769

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Environmental Science & Technology

T3-SLMoS2, T7-SLMoS2, and T11-SLMoS2 ranged from −30.3 to −36.3 mV, − 28.4 to −33.2 mV, and −27.5 to −31.1 mV, respectively. Thus, dissolution and the alteration of phase, morphology, and structure reduced the dispersity of SLMoS2 in water. Photoinduced Electronic Competition and Chemical Dissolution Assisted by DO. The UV−vis−near-infrared (UV−vis−NIR) diffuse reflection spectrum suggested that the direct band gap of pristine SLMoS2 was 1.8 eV (Figure S7a), which was similar to the data in the literature.39 The available wavelength for the band gap was 690.2 nm, based on the threshold of the available wavelength (nm = 1242.375/band gap). Moreover, Mott−Schottky plots showed that the flat− band potential of pristine SLMoS2 was −0.45 eV (Figure S7b), which was similar to that of the conduction band (CB).40 The CB potential was −0.45 eV, which is sufficient to oxidize O2 to produce peroxy radical (•O2−)[Eθ(O2/•O2−) = −0.16 eV versus reversible hydrogen electrode]. However, •O 2 − generation was inhibited due to the rapid electron−hole recombination of SLMoS2. Without DO, the signal of DMPO•O2− in the SLMoS2 suspension was very weak (Figure 4a,b). One study revealed that there is competition between electronhole recombination in materials and acquisition by other reactions (such as oxygen reduction and oxidation).41 The

more defects were formed on the nanosheets, especially for T11-SLMoS2. The thicknesses of the T3-SLMoS2, T7-SLMoS2, and T11-SLMoS2 nanosheets increased from approximately 1.243 to 2.598 nm (2.533 ± 0.065 nm, n = 3), 2.742 nm (2.701 ± 0.041 nm, n = 3), and 4.267 nm (4.214 ± 0.053 nm, n = 3), respectively; these results were consistent with the TEM images in Figure S5. As presented in the FTIR results in Figure 3e, a significant peak ascribed to Mo−S stretching vibrations located at ∼600 cm−1 was observed for pristine SLMoS2.26 In contrast, the intensity of the Mo−S stretching bond in the transformed SLMoS2 became very weak. The peak located at ∼800 cm−1 in pristine SLMoS2 and associated with the Mo−O stretching bond also disappeared, particularly in T11-SLMoS2. These results indicated that the chemical dissolution of SLMoS2 and Mo oxides significantly altered the functional bonds on the surface of SLMoS2. The Raman phonon modes associated with the in-plane (E2g) and out-ofplane (A1g) lattice vibrations of pristine SLMoS2 are located at ∼385 and 403 cm−1, respectively.31 A previous study reported that the intensity of Raman phonon modes (E2g and A1g) was positively correlated with defects in two-dimensional nanosheets.32 In Figure 3f, the peak intensity of E2g and A1g bonds significantly increased in the transformed SLMoS2, attributed to ion release (Figure 1) and the abundance of defects on the nanosheets, denoted by red arrows in Figure 3d. Moreover, the E2g and A1g vibrations in the Raman spectra of transformed SLMoS2 nanosheets exhibited considerable red and blueshifts, respectively. The blueshift in A1g vibrations indicated that the nanosheets transitioned from single-layer to bulk-layer thickness. The redshift in E2g vibrations represented the stacking of nanosheets.33 Generally, the layer number of MoS2 nanosheets can be evaluated by the Raman shift of A1g−E2g.34 In the present study, the Raman shift of A1g−E2g for pristine SLMoS2, T3-SLMoS2, T7-SLMoS2, and T11-SLMoS2 was 18.0, 20.7, 22.2, and 24.1 cm−1, respectively. Correspondingly, the layer numbers of T3-SLMoS2, T7-SLMoS2, and T11-SLMoS2 were calculated to be 2, 3, and 4, respectively (Figure S6). It has been reported that the loss of colloidal stability (as presented below, Figure 3g) can cause the restacking of MoS 2 nanosheets.35,36 Chemical dissolution on the surfaces and edges of SLMoS2 induced the destruction of ring structure and the enrichment of defects (Figure 2d), which probably led to the scrolling and bending of SLMoS 2 . 37 The SLMoS 2 nanosheets were restacked, and the plane structure was scrolled; thus, the layer number of transformed SLMoS2 increased, as supported by AFM (Figure 3) and TEM (Figure S5) images. Alterations in Colloidal Stability. The aggregation kinetics were assessed using the initial aggregation rate (d) when the hydrodynamic diameter reached 1.5-fold higher than the initial size.38 As shown in Figure 3g, the average size of pristine SLMoS2 increased with an initial aggregation rate of 0.487 nm/s. In contrast, transformed SLMoS2 exhibited higher instability, and the initial aggregation rates were 0.963, 1.271, and 1.763 nm/s for T3-SLMoS2, T7-SLMoS2, and T11-SLMoS2, respectively. At 96 h, the hydrodynamic diameters of pristine SLMoS2, T3-SLMoS2, T7-SLMoS2, and T11-SLMoS2 were 1228, 1833, 1956, and 2145 nm, respectively. Furthermore, the zeta potential results revealed that pristine SLMoS2 was dispersive (−32.5∼−39.9 mV) when the pH was over 7 (Figure 3h) due to the electrostatic repulsion among negatively charged nanosheets.35 In contrast, the zeta potential decreased after chemical dissolution (Figure 3h). The zeta potentials of

Figure 4. Generation of free redials and photochemical reaction mechanisms. (a−c) the production of peroxy radicals (•O2−) by pristine SLMoS2 with or without dissolved oxygen (DO), (d) the generation of hydroxyl radicals (•OH) by pristine and transformed SLMoS2, and (e) the photochemical reaction mechanisms of SLMoS2. 7764

DOI: 10.1021/acs.est.9b00088 Environ. Sci. Technol. 2019, 53, 7759−7769

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Environmental Science & Technology ROS intensity was significantly strengthened after oxygen was aerated (Figure 4c). The continuous supplementation of DO competitively captured the separated electrons to produce •O2− under light irradiation (eq S3), accelerating the chemical dissolution of SLMoS2 (Figure 4a−c). According to the CB potential and band gap energy, the valence band (VB) potential was calculated to be 1.35 eV, which cannot directly oxidize OH− to produce •OH (Eθ(OH−/•OH) = 2.40 eV versus reversible hydrogen electrode). •OH radicals were notably generated under alkaline conditions (Figure 4d), probably due to the acquisition of electrons from OH− by soluble Mo6+ species under visible light irradiation (eq S4). In sum, the electrons from SLMoS2 were competitively utilized by O2 to produce •O2− under DO treatment and visible light irradiation, and •OH radical was also generated, thus leading to the chemical dissolution of SLMoS2 (Figure 4e). Mitigation of Algal Division, Cellular Uptake, Ultrastructure, and ROS. The effects of the above photoinduced physicochemical transformations of SLMoS2 on algal ecotoxicity were investigated. For algal division, the initial number (1.5 × 105 CFU/mL) of algae increased with incubation time, as shown in Figure S8. During this period, the division of algal cells was significantly inhibited by exposure to SLMoS2 in a dose-dependent manner. In contrast, transformed SLMoS2 induced significantly lower inhibition than pristine SLMoS2, except for T3-SLMoS2 (Figure S8b−d). The effects of T11SLMoS2 on cell division were the lowest, and the inhibition percentages were only 10.9−15.2%. The algal cells in the control groups presented intact ultrastructural morphology, including cell walls, chloroplasts, cell nuclei, and other cytoplasmic compartments (Figure 5a). Mo ions (Na2MoO4)

damaged and blurred chloroplasts, and the biosynthesis of chlorophyll a was remarkably inhibited (up to 58%) compared to the control (Figure S9b). However, the damage to the cellular ultrastructure by transformed SLMoS2 was weak (Figure 5d−f). The cellular uptake of transformed SLMoS2 was also reduced to 2.316, 1.806, and 1.103 μg/105 cells for T3-SLMoS2, T7-SLMoS2, and T11-SLMoS2, respectively, at 25 mg/L (Figure S9a). Physical and pharmacological inhibitions were used to analyze the uptake mechanisms of pristine and transformed SLMoS2 by algal cells. The energy-dependent endocytosis of algal cells could be inhibited at low temperatures. The uptakes of pristine SLMoS2, T3-SLMoS2, T7SLMoS2, and T11-SLMoS2 (25 mg/L) by algae at 4 °C were reduced by 45.63%, 48.59%, 50.26%, and 47.87%, respectively (Figure S10a), compared to that of the control, suggesting the energy dependence of SLMoS2 internalization. Furthermore, the algal cells were treated with MβCD, CPZ, and EIPA to prevent caveolae-mediated endocytosis, clathrin-mediated endocytosis, and uptake by micropinocytosis, respectively. Algal uptake of pristine SLMoS2(25 mg/L) with the pretreatments of MβCD, CPZ, and EIPA was reduced by 21.68%, 5.77%, and 39.67%, respectively. By contrast, the uptake inhibition effects of transformed SLMoS 2 by pharmacological pretreatment were considerably more significant, especially for T11-SLMoS2. MβCD, CPZ, and EIPA decreased the cellular contents of T11-SLMoS2(25 mg/L) by 36.78%, 19.56%, and 48.76%, respectively (Figure S10b−10d). The above data demonstrated that the uptake mechanisms of pristine and transformed SLMoS2 were slightly different and that micropinocytosis was the dominant pathway for the uptake of SLMoS2 nanosheets. Therefore, the bioavailability and cellular contents of transformed SLMoS2 were evidently lower than those of pristine SLMoS2, owing to the higher aggregation of transformed SLMoS2 (Figure 3g,h) and inhibited micropinocytosis. The intracellular ROS levels in pristine SLMoS2 compared to those in the control were significantly increased by 186.9−313.2% (Figure S9c). The ROS levels in transformed SLMoS2, especially in the T11SLMoS2 group, were lower than those in pristine SLMoS2, which was consistent with the results of nanomaterial uptake and photosynthesis. Metabolic Mechanisms of Phytotoxicity Mitigation. Metabolomic analysis provides a global view on the perturbation of a metabolism.42 Fifty-three metabolites were identified by analyzing approximately 250 peaks for each sample using GC−MS (Tables S2 and S3). The identified metabolites included fatty acids, amino acids, carbohydrates, alkanes, and other biomolecules. Hierarchical clustering (HCL) analysis indicated that the samples could be divided into two clusters: (1) pristine SLMoS2 (1, 10, and 25 mg/L) and T3-SLMoS2 (10 and 25 mg/L) and (2) others (the control and most of the transformed SLMoS2). The results suggested that pristine SLMoS2 significantly perturbed the cellular metabolism of algae and the perturbation of metabolism was mitigated by environmental transformation (Figure S11a). Furthermore, ANOVA with Tukey’s test found that SLMoS2 at 10 and 25 mg/L significantly downregulated the levels of amino acids and fatty acids (p < 0.05) (Figure S11b). After transformation, significant differences in amino acids and fatty acids between T3-SLMoS2 (10 and 25 mg/L) and control groups were also observed. In contrast, the influence of T7SLMoS2 and T11-SLMoS2 exposure on amino acid and fatty acid production was not significant, which was further

Figure 5. Ultrastructure of algal cells and internalization of SLMoS2 as shown by TEM images. (a) The control without nanomaterial exposure, (b) 100 μM Na2MoO4 exposure, (c) 25 mg/L pristine SLMoS2, (d) 25 mg/L T3-SLMoS2, (e) 25 mg/L T7-SLMoS2, and (f) 25 mg/L T11-SLMoS2. The yellow and red arrows indicate SLMoS2 and plasmolysis, respectively. Cw, cell wall; S, starch grain; Chl, chloroplast; and Cn, cell nucleus.

did not induce obvious alterations in cell ultrastructure (Figure 5b). In contrast, pristine SLMoS2 was visible in cellular cytoplasm and chloroplasts (Figure 5c, yellow arrows). The nanosheet content in the pristine SLMoS2 groups (25 mg/L) reached 2.428 μg/105 cells (Figure S9a), and plasmolysis (red arrows) was also significantly induced by pristine SLMoS2 (Figure 5c). The plasma membrane shrank and separated from the cell walls. In addition, exposure to pristine SLMoS2 7765

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Figure 6. Pathways of the metabolic responses and amino acid and fatty acid disturbances in algal cells treated with pristine and transformed SLMoS2. The metabolic pathways were established based on the Kyoto Encyclopedia of Genes and Genomes (KEGG) database. Red and green words represent down- and up-regulated metabolites induced by pristine SLMoS2, respectively, compared to those of the control. The metabolites labeled with up and down purple arrows are the metabolites that are upregulated and downregulated, respectively, by transformed SLMoS2 compared to pristine SLMoS2.

the toxicological mechanisms by which environmental transformation mitigates nanotoxicity. Outlook on the Environmental Transformation of SLMoS2. SLMoS2 has been applied in various fields and presents great potential for release into the environment during its life cycle (e.g., fabrication, use, and disposal). The phase, morphology, and dissolution (accompanied by defects) of SLMoS2 play a dominant role in surface chemistry, colloidal stability, and activity,50 determining the uptake and ecotoxicity of this material to organisms. DO and visible light irradiation are two fundamental factors in the water environment. However, the effects of DO and visible light irradiation on the physicochemical transformation and nanostructure of SLMoS2, especially ion release and phase transformation, remain largely unknown. The 1T phase of pristine SLMoS2 was preferentially dissolved in alkaline conditions, and then a ribbon structure and abundant defects on the surfaces of nanosheets were formed. Transformed SLMoS2 nanosheets were thickened into multilayer structures, and the colloidal stability was reduced. The phase and single-layer structure of SLMoS2 play critical roles in photocatalysis and pollutant removal.51,52 The environmental transformations presented in this work unequivocally affect photocatalysis and pollutant removal when using SLMoS2. Regarding biological responses, pristine SLMoS2 (1T-rich) with a negative surface charge (pH > 7.0) was stable (Figure 3g−f) and was more effectively absorbed by algal cells than transformed SLMoS2 (2H-rich), as illustrated in Figure 5. Transformed SLMoS2(2H-rich phase) induced lower intracellular ROS levels than pristine 1T-rich SLMoS2 (Figure S9c), indicating the mitigation of nanotoxicity.53 Transformed SLMoS2 also triggered a weaker perturbation of metabolism (Figure S11). In other words, the environmental risks of SLMoS2 would be high in lowoxygen and dark conditions. Soluble ionic species that coexist with nanomaterials are more bioavailable and have been confirmed to be the drivers of the toxicological response.54,55 In the present study, 100 μM Na2MoO4 showed no statistically significant inhibitory effect on algal cell growth (Figure 5). The synthesis of chlorophyll a and intracellular ROS was also not remarkably influenced by Na2MoO4 (Figure S9b,c). The above

supported by the results of principal component analysis (PCA) (Figure S11c). A schematic pathway for the metabolic disturbance was established to intuitively understand the effects of nanosheets on the biological responses of algal cells, as provided in Figure 6. The SLMoS2 nanosheets at a high-concentration exposure promoted the generation of ROS and induced chloroplast dysfunction and plasmolysis, which was relative to the amino acid and fatty acid metabolic pathways. For the amino acid metabolism, it was proposed that the downregulation of amino acids was associated with oxidative stress,43 and most amino acids served as precursors for the synthesis of defense−related metabolites.44 A strong negative correlation (VIP > 1) between ROS and ornithine/threonine/tyrosine/serine is observed in Figure S12, implying the inhibition of amino acid syntheses and the destruction of the defense system induced by ROS. Serine takes part in the biosynthesis of purines, pyrimidines and chlorophyll.45 Pristine SLMoS2 reduced the serine level, which supported the decrease in chlorophyll a content. Furthermore, unsaturated fatty acid metabolism has been correlated with cell membrane fluidity.46 The levels of unsaturated fatty acids in the transformed SLMoS2 groups were significantly lower than those in the pristine SLMoS2 groups (Figure S11a), which was consistent with the results of plasmolysis in Figure 5. Fatty acids are vigorously responsive to extra stimulation during the growth process.47,48 Herein, unsaturated and saturated fatty acids presented positive and negative relationships, respectively, with the ROS level (Figure S12). Arachidonic acid is a polyunsaturated fatty acid released from membrane phospholipids in response to ROS.48 The arachidonic acid levels in transformed SLMoS2 treatments were significantly lower than those in pristine SLMoS2 groups, supporting the negligible plasmolysis of algal cells exposed to transformed SLMoS2. Salicylic acid is a signaling molecule that plays an important role in the plant defense response.49 Pristine SLMoS2 inhibited the levels of salicylic acid, but the inhibition was remarkably diminished in transformed SLMoS2 (Figure S11a), indicating the recovery of the defense system of algal cells. By metabolomic analysis, the above results explore 7766

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(3) Gupta, U.; Rao, C. N. R. Hydrogen Generation by Water Splitting using MoS2 and Other Transition Metal Dichalcogenides. Nano Energy 2017, 41, 49−65. (4) Lei, Z.; Zhan, J.; Tang, L.; Zhang, Y.; Wang, Y. Recent Development of Metallic (1T) Phase of Molybdenum Disulfide for Energy Conversion and Storage. Adv. Energy Mater. 2018, 8, 1703482. (5) Majd, S. M.; Salimi, A.; Ghasemi, F. An Ultrasensitive Detection of miRNA-155 in Breast Cancer via Direct Hybridization Assay using Two-Dimensional Molybdenum Disulfide Field-Effect Transistor Biosensor. Biosens. Bioelectron. 2018, 105, 6−13. (6) Chen, S. C.; Lin, C. Y.; Cheng, T. L.; Tseng, W. L. 6Mercaptopurine-Induced Fluorescence Quenching of Monolayer MoS2 Nanodots: Applications to Glutathione Sensing, Cellular Imaging, and Glutathione-Stimulated Drug Delivery. Adv. Funct. Mater. 2017, 27, 1702452. (7) Xie, W.; Gao, Q.; Wang, D.; Guo, Z.; Gao, F.; Wang, X.; Cai, Q.; Feng, S. S.; Fan, H.; Sun, X.; Zhao, L. Doxorubicin-loaded Fe3O4@ MoS2-PEG-2DG Nanocubes as a Theranostic Platform for Magnetic Resonance Imaging-Guided Chemo-Photothermal Therapy of Breast Cancer. Nano Res. 2018, 11, 2470−2487. (8) Alam, I.; Guiney, L. M.; Hersam, M. C.; Chowdhury, I. Antifouling Properties of Two-Dimensional Molybdenum Disulfide and Graphene Oxide. Environ. Sci.: Nano 2018, 5, 1628−1639. (9) Hirunpinyopas, W.; Prestat, E.; Worrall, S. D.; Haigh, S. J.; Dryfe, R. A. W.; Bissett, M. A. Desalination and Nanofiltration through Functionalized Laminar MoS2 Membranes. ACS Nano 2017, 11, 11082−11090. (10) Wang, Z.; von demBussche, A.; Qiu, Y.; Valentin, T. M.; Gion, K.; Kane, A. B.; Hurt, R. H. Chemical Dissolution Pathways of MoS2Nanosheets in Biological and Environmental Media. Environ. Sci. Technol. 2016, 50, 7208−7217. (11) Zou, W.; Zhou, Q.; Zhang, X.; Hu, X. Environmental Transformations and Algal Toxicity of Single-Layer Molybdenum Disulfide Regulated by Humic Acid. Environ. Sci. Technol. 2018, 52, 2638−2648. (12) Ding, X.; Wang, J.; Rui, Q.; Wang, D. Long-Term Exposure to Thiolated Graphene Oxide in the Range of μg/L Induces Toxicity in Nematode Caenorhabditis Elegans. Sci. Total Environ. 2018, 616, 29− 37. (13) Hu, X.; Zhou, M.; Zhou, Q. Ambient Water and Visible-Light Irradiation Drive Changes in Graphene Morphology, Structure, Surface Chemistry, Aggregation, and Toxicity. Environ. Sci. Technol. 2015, 49, 3410−3418. (14) Mansano, A. S.; Souza, J. P.; Cancino-Bernardi, J.; Venturini, F. P.; Marangoni, V. S.; Zucolotto, V. Toxicity of Copper Oxide Nanoparticles to Neotropical Species Ceriodaphniasilvestrii and Hyphessobrycon Eques. Environ. Pollut. 2018, 243, 723−733. (15) Marchioni, M.; Gallon, T.; Worms, I.; Jouneau, P.-H.; Lebrun, C.; Veronesi, G.; Truffier-Boutry, D.; Mintz, E.; Delangle, P.; Deniaud, A.; Michaud-Soret, I. Insights into Polythiol-Assisted AgNP Dissolution Induced by Bio-Relevant Molecules. Environ. Sci.: Nano 2018, 5, 1911−1920. (16) Yamamoto, M.; Einstein, T. L.; Fuhrer, M. S.; Cullen, W. G. Anisotropic Etching of Atomically Thin MoS2. J. Phys. Chem. C 2013, 117, 25643−25649. (17) Wang, Z.; Zhu, W.; Qiu, Y.; Yi, X.; von demBussche, A.; Kane, A.; Gao, H.; Koski, K.; Hurt, R. Biological and Environmental Interactions of Emerging Two-Dimensional Nanomaterials. Chem. Soc. Rev. 2016, 45, 1750−1780. (18) Qu, X.; Alvarez, P. J. J.; Li, Q. Photochemical Transformation of Carboxylated Multiwalled Carbon Nanotubes: Role of Reactive Oxygen Species. Environ. Sci. Technol. 2013, 47, 14080−14088. (19) Wang, D.; Liu, L.; Zhang, F.; Tao, K.; Pippel, E.; Domen, K. Spontaneous Phase and Morphology Transformations of Anodized Titania Nanotubes Induced by Water at Room Temperature. Nano Lett. 2011, 11, 3649−3655. (20) Kang, K.; Xie, S.; Huang, L.; Han, Y.; Huang, P. Y.; Mak, K. F.; Kim, C.-J.; Muller, D.; Park, J. High-Mobility Three-Atom-Thick

results indicated different environmental risks than those derived from released Ag ions from Ag nanoparticles.55 One study found that the formation of abundant surface defects was beneficial for the antibacterial activity of nanomaterials (e.g., carbon materials and metal nanoparticles) on a Gram-negative bacterium (E. coli),56 and could also strengthen the toxicity of nanomaterials to organisms (RT−W1 cells and embryos).57 The interdependence between the defect/phase composition and ionic dissolution of SLMoS2 deserves substantial attention in future applications and risk evaluations.

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.est.9b00088. Methods regarding characterization techniques; the detection of peroxy radicals, hydroxyl radicals and ROS; and a theoretical analysis of the photoinduced redox reaction; tables regarding the dissolution rate of SLMoS2 and metabolites of algal cells; figures regarding the chemical dissolution of SLMoS2 nanosheets, the molar ratio of S/Mo species, XPS spectra, X-ray powder diffraction spectra, TEM images, the dependence of E2g−A1g Raman shifts on the number of MoS2 layers, the inhibition of algal cell growth, quantifications of cellular SLMoS2, the inhibition of chlorophyll a, ROS generation in algal cell, and metabolite analysis (PDF)

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AUTHOR INFORMATION

Corresponding Author

*Phone: 0086−022−23507800; fax: 0086−022−23507800; email: [email protected]. ORCID

Qixing Zhou: 0000-0003-2804-2360 Xiangang Hu: 0000-0002-9403-816X Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was financially supported by the National Natural Science Foundation of China (grant nos. 21722703, 31770550, 21577070, and 21677080), the China Postdoctoral Science Foundation (No. 2018M642757), the Opening Foundation of Ministry of Education Key Laboratory of Pollution Processes and Environmental Criteria (No. 201801), the Doctoral Scientific Research Foundation of Henan Normal University (No. 5101219170133), the Ministry of Education (People’s Republic of China) as an innovative team rolling project (grant no. IRT_17R58), the Tianjin Natural Science Foundation (grant no.18JCYBJC23600), a 111 program (grant no. T2017002), and the Special Funds for Basic Scientific Research Services of Central Colleges and Universities.

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