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Ecotoxicology and Human Environmental Health

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 Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.9b00088 • Publication Date (Web): 04 Jun 2019 Downloaded from http://pubs.acs.org on June 4, 2019

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Environmental Science & Technology

TOC

ACS Paragon Plus Environment


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Dissolved Oxygen and Visible Light Irradiation Drive the Structural Alterations

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and Phytotoxicity Mitigation of Single−layer Molybdenum Disulfide

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Wei Zou1, Qixing Zhou2, Xingli Zhang1, Xiangang Hu2,*

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1 School

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Environment and Pollution Control, Ministry of Education, Henan Key Laboratory for

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Environmental Pollution Control, Henan Normal University, Xinxiang

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453007, China.

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2

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Education)/Tianjin Key Laboratory of Environmental Remediation and Pollution

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Control, College of Environmental Science and Engineering, Nankai University,

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Tianjin 300350, China.

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Corresponding authors: Xiangang Hu, [email protected].

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Fax, 0086−022−23507800; Tel, 0086−022−23507800.

of Environment, Key Laboratory for Yellow River and Huai River Water

Key Laboratory of Pollution Processes and Environmental Criteria (Ministry of

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ABSTRACT

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Understanding environmental fate is a prerequisite for the safe application of

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nanoparticles.

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transformation of single−layer molybdenum disulfide (SLMoS2, a 2D nanosheet

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attracting substantial attention in various fields) remain largely unknown. The present

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work found that the dissolution of SLMoS2 was pH and dissolved oxygen dependent

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and that alterations in phase composition significantly occur under visible light

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irradiation. The 1T phase was preferentially oxidized to yield soluble species (MoO42−

However,

the

fundamental

persistence

1


and

environmental

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and SO42−), and the 2H phase remained as a residual. The transformed SLMoS2

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exhibited a ribbon−like and multilayered structure and low colloidal stability due to

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the loss of surface charge. Dissolved oxygen competitively captured the electrons of

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SLMoS2 to generate superoxide radicals and accelerated the dissolution of

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nanosheets. Compared to pristine 1T−phase SLMoS2, the transformed 2H−phase

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SLMoS2 could not easily enter algal cells and induced a low developmental inhibition,

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oxidative stress, plasmolysis, photosynthetic toxicity and metabolic perturbation. The

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downregulation of amino acids and upregulation of unsaturated fatty acids contributed

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to the higher toxicity of 1T−phase SLMoS2. The dissolved ions did not induce

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apparent phytotoxicity. The connections between environmental transformation

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(phase change and ion release) and phytotoxicity provide insights into the safe design

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and evaluation of 2D nanomaterials.

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KEYWORDS: nanoparticle, phytotoxicity, environmental transformation, phase

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alteration, nanotoxicity

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INTRODUCTION

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Single−layer molybdenum disulfide (SLMoS2), a typical two−dimensional (2D)

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transition metal dichalcogenide (TMD), has been widely applied in electronics and

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optoelectronics,1 catalysis,2,

3

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environmental protection.8,

Given the potential of environmental and organism

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exposure to SLMoS2 during the nanomaterial lifecycle (e.g., fabrication, use and

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energy storage,4 biology,5 biomedicine,6,

2


7

and


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disposal), environmental fate and safety should be considered in detail.10, 11 Compared

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to pristine nanoparticles, environmentally transformed nanoparticles may exhibit

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different morphologies, structures and stabilities, leading to the alteration of

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ecological and health effects.12 For example, light irradiation has driven changes in

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graphene morphology and reduced the toxicity of graphene to aquatic algae.13 Ion

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release from metal and metallic oxide nanoparticles in water has contributed to the

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enhancement or mitigation of nanotoxicity.14,

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oxygen (DO) and visible light irradiation, which are both common environmental

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factors, in the nanoparticle properties (e.g., phase change), environmental stability

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(e.g., ion release) and ecotoxicity of SLMoS2 remains largely unknown.

55

15

However, the role of dissolved

The SLMoS2 surface can be quickly oxidized to produce molybdenum oxide

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(MoO3) at defect sites after exposure to oxygen at temperatures above 340°C.16 In the

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presence of oxygen or other strong oxidizing agents (hydroxyl radicals and H2O2),

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SLMoS2 can be fast−etched and release soluble species.17 These results demonstrate

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that SLMoS2 can be oxidized under extensive conditions. At room temperature,

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sunlight−induced reactions (oxidation and reduction) also affect the oxidation state,

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the generation of reactive oxygen species (ROS), and the persistence of

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nanomaterials, although the process is slow.18 Photoactive nanomaterials, including

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metal− and carbon−based nanoparticles, can absorb visible light and react with

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oxygen to produce ROS.19 As a typical semiconductor material, SLMoS2 exhibits a

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lower bandgap (1.8 eV) than that of TiO2 nanoparticles (3.0~3.2 eV),20 which is

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beneficial for visible light adsorption. Herein, it was hypothesized that the 3


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environmental transformation of SLMoS2 can occur slowly in an oxygen−containing

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aqueous phase with visible light irradiation at room temperature.

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Nanotoxicity is highly relevant to the physicochemical properties (e.g., morphology,

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colloidal stability, layer structure and crystal structure) of nanomaterials.13, 21,22 For

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example, anatase TiO2 with octahedral coordination was more chemically active than

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rutile TiO2 with square prismatic coordination in the production of ROS, which are

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positively related to the toxicity of TiO2 in vitro.23 Environmental factors may change

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the morphology and phase of SLMoS2, leading to the enhancement or mitigation of

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nanotoxicity. The objective of the present study is to understand the physicochemical

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transformation of SLMoS2 nanosheets in oxygen−containing water with visible light

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irradiation and the effects on the aquatic toxicity of the nanosheets. pH, as another

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environmental factor, is also taken into consideration. Specifically, the following

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issues are addressed: (i) the chemical dissolution kinetics of SLMoS2; (ii) the

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morphology, colloidal stability, layer structure and phase alterations of SLMoS2; and

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(iii) the ecotoxicity (e.g., photosynthesis, ROS and metabolic profile) of pristine and

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transformed SLMoS2 to a model species (Chlorella vulgaris). The results provide

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insights into the safe design and evaluation of 2D nanomaterials. By analyzing the

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connections between environmental transformation (phase change and ion release of

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nanoparticles) and ecotoxicity, the present work will provide insights into the safety

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evaluation and design of SLMoS2.

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MATERIALS AND METHODS 4



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Environmental Transformation of SLMoS2 Nanosheets

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Pristine SLMoS2 nanosheets (chemically exfoliated, single layer>99%) were obtained

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from Nanjing XFNANO Materials Tech Co., Ltd., China. Deionized water (18.2

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Ω/cm) was heated to boiling to remove DO and then cooled to room temperature in a

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nitrogen−filled glovebox. SLMoS2 nanosheets (5 mg) were suspended in 200 mL of

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prepared water. The SLMoS2 suspension (25 mg/L) was placed in a shaking incubator

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(24°C, 150 rpm, humidity 80%) and incubated for eight weeks with and without

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irradiation (light/dark = 14:10) by a xenon arc lamp (CEL−HXF300, Ceaulight,

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Beijing, China) with a UV cutoff (λ < 420 nm) of 35 W/m2. To analyze the effects of

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pH, the pH values of the SLMoS2 suspensions were adjusted to 3~11 by 0.1 mM HCl

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and 0.1 mM NaOH. To study the effect of DO, the suspension was aerated with pure

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oxygen (0.01, 0.05, 0.1, and 0.5 L/min), and the tested concentrations of DO were

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3.21, 6.76, 9.23 and 9.52 mg/L (saturated), respectively. The groups placed in a

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nitrogen−filled glovebox were set up as the control (0 mg/L DO). After eight weeks

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of reaction, the SLMoS2 nanosheets were separated using a 0.1 μm polyether sulfone

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(PES) filter and then lyophilized. To analyze the release kinetics of ions from the

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SLMoS2 nanosheets, the filtrates on the 7th, 14th, 21st, 28th, and 56th days were

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collected by ultrafiltration centrifugation (Amicon Ultra−15 3kD, Millipore, USA).

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Then, the contents of the dissolved Mo and S species were determined by inductively

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coupled plasma mass spectrometry (ICP−MS, Agilent 7700, USA). Each treatment

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was performed in triplicate.

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Characterization of Pristine and Transformed SLMoS2 5


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The transformed SLMoS2 samples in the groups (pH=3, 7, and 11) with saturated DO

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(9.52 mg/L) after 56 days of incubation (named T3−SLMoS2, T7−SLMoS2, and

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T11−SLMoS2, respectively) were collected. Then, the morphology, structure, colloidal

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stability, and chemical and optical properties of pristine and transformed SLMoS2

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were characterized by transmission electron microscopy (TEM, HT7700, Hitachi,

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Japan), atomic force microscopy (AFM, Agilent 5420, USA), Raman spectroscopy

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(Thermo Scientific, DXR, USA), dynamic light scattering (DLS, Brookhaven, USA),

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electrochemical workstation analysis (CHI660E, Shanghai Chenhua, China), UV−vis

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analysis (T90, Purkinje General, China), Fourier transform infrared spectroscopy

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(FTIR, Bruker Tensor 27, USA), X−ray photoelectron spectroscopy (XPS, Kratos,

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Japan), and X−ray powder diffraction (XRD, Rigaku Ultima IV, Japan). The details

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are provided in the supporting information (SI).

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Free Radical Measurements

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Peroxy radical (•O2−) was determined using the spin trap

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5,5−dimethyl−1−pyrroline−N−oxide (DMPO, 10 mM) in methanol solution using an

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electron spin resonance (ESR) spectroscope (MiniScope 400, Germany). •OH was

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detected by monitoring the fluorescence intensity of 2−hydroxyterephthalic acid

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(TAOH) at 435 nm in aqueous solution using a UV−vis spectrometer (T90, Purkinje

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General, China). The details are provided in the SI.

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C. vulgaris Cultivation

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C. vulgaris and its culture medium (BG−11) were obtained from the Freshwater

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Algae Culture Collection at the Institute of Hydrobiology, China. The environmental 6



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exposure of nanoparticles at high concentrations can occur in relevant wastewater

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from manufacturing facilities, although the environmentally relevant concentrations

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are currently unclear. Significant toxicity was observed when the SLMoS2

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concentration was over 10 mg/L in a previous cytotoxicity study.24 Given the rapid

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development of 2D nanomaterials, nanomaterials at 1, 10, and 25 mg/L were prepared

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in algal BG−11 culture medium to compare the toxicology of pristine and transformed

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SLMoS2. The initial density of algal cells was 1.5×105 CFU/mL. SLMoS2 was

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exposed to algal cells in 250 mL glass flasks, and algal cells without SLMoS2 were

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used as controls. To study the effects of released molybdate salts, the algae were also

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exposed to 100 μM Na2MoO4 (the corresponding mass concentration of MoO42− was

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15.9 mg/L), which was higher than the concentrations of ions released by SLMoS2 at

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25 mg/L. The glass flasks were shaken at 150 rpm for 10 min once every 8 h and

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placed in an illumination incubator (LRH−250 Gb, China) at 24.0 ±0.5°C and 80%

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humidity. Each treatment was performed in triplicate. The effects of SLMoS2 on algal

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division were measured by counting the number of algal cells by flow cytometry

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(FCM, BD FACSCalibur, USA) at 24, 48, 72 and 96 h.

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Cellular Ultrastructure Observation, Nanomaterial Uptake and ROS

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The cell suspension (5 mL) was centrifuged at 9000 g for 5 min, and the supernatant

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was discarded. The pellets were washed with phosphate buffered saline (PBS), and

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then the algal cells were fixed in 2.5% glutaraldehyde at 4°C overnight, post fixed in

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1% osmium tetroxide for 2 h, dehydrated in an ethanol gradient (30%, 50%, 70%,

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80%, 90%, 95%, and 100%), and then embedded in an epoxy resin. Ultrathin sections 7


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(approximately 90 nm) of algal cells were cut using a diamond knife on an

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ultramicrotome (EM FC7, Leica, Germany) and stained with uranyl acetate and lead

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citrate for 15 min. The distribution of SLMoS2 was observed by TEM (HT7700,

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Hitachi, Japan), and the uptake of SLMoS2 was quantified by ICP−MS (Agilent 7700,

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USA). In brief, a known amount of 105 algal cells was collected and digested using

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HNO3/H2O2 (v:v, 3:1) until no color was observed. After filtration through a 0.45 μm

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water membrane, the concentration of Mo ions was determined by ICP−MS (Agilent

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7700, USA). The endocytosis pathway and mechanisms of SLMoS2 by algal cells

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were investigated using physical and pharmacological inhibitors. The algal cells were

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preincubated at 4°C for 1 h to inhibit energy−dependent uptake, and then, the SLMoS2

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nanosheets were exposed for 1 h at room temperature. To determine the specific

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mechanisms of cellular uptake, the algal cells were pretreated with

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methyl−betacyclodextrin (MβCD, 20 mM), chlorpromazine hydrochloride (CPZ, 100

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μM), and 5−(N−ethyl−N−isopropyl) amiloride (EIPA, 50 μM) for 1 h. Subsequently,

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SLMoS2 was exposed to the algae for 1 h. The cellular contents of Mo ions in algal

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cells were detected as described above. Based on the S/Mo molar ratio (approximately

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2) of pristine and transformed SLMoS2 (equation S1, details below), the concentration

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of Mo ions was then converted to the SLMoS2 nanosheet content per 105 cells. The

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measurement of ROS is presented in the SI.

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Algal Metabolism

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The algal suspension (30 mL) was centrifuged at 9000 g for 5 min to collect cells. To

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completely break the cell walls, the collected algal cells underwent three cycles of 8



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freezing in liquid nitrogen and thawing at room temperature. Subsequently, 4.5 mL of

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a methanol/chloroform/water (volume ratio=2.5:1:1) solution was added to the cell

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suspension, and the cells were completely broken using an ultrasonic probe (150 W,

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10 min) in an ice−water bath. The metabolites were extracted usingsonication (200 W,

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30 min), followed by centrifugation at 9000 g for 5 min at 4°C. After sonication and

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centrifugation, the supernatant was collected, and the pellet was extracted again as

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described above. The supernatant was mixed with the previously collected

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supernatant. Then, water (1.5 mL) was added to the above supernatant and

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centrifuged at 9000 g for 5 min. The lower phase was separated and filtered through a

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10 cm silica gel column, followed by nitrogen blowing. The upper phases, which

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consisted of methanol and water, were dried by nitrogen blowing and lyophilization,

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respectively, and then mixed with the residual lower−layer phase.

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N−methyl−N−(trimethylsilyl)trifluoroacetamide (80 μL) and methoxamine

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hydrochloride (20 mg/mL, 50 μL) were added as derivatives. After derivatization, the

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samples (1 μL) were injected into a gas chromatography column (HP−5MS, Agilent,

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USA) in split mode (1:25), and the metabolites were identified. Metabolic analysis

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was conducted using gas chromatography with mass spectrometry (GC−MS;

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6890N/5973, Agilent, USA). The MS was operated in full scan mode with a detection

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slope of m/z 80−800. The metabolites were identified using the National Institute of

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Standards and Technology (NIST 14.0) mass spectra library in ChemStation software.

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Statistical Analysis

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All experiments were performed in triplicate. The results are presented as the mean ± 9


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standard deviation. The statistical significance was analyzed with one−way analysis

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of variance (ANOVA) followed by Tukey’s test. A p value less than 0.05 was

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considered statistically significant. All statistical analyses were performed using IBM

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SPSS 22.0.

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RESULTS AND DISCUSSION

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Visible Light Irradiation, DO and Alkalinity Accelerate Ion Release from

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SLMoS2 Nanosheets

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The time− and pH−dependent dissolution of Mo and S species from SLMoS2

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nanosheets is presented in Figure 1. The concentrations of released Mo and S species

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at pH=11 after 56 days of reaction were 3.122 and 2.088 mg/L, respectively, which

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were higher than those at pH=3 (0.631 and 0.424 mg/L for released Mo and S species,

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respectively). MoS2 nanosheets produced soluble ions in aqueous media accompanied

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by protons,10 and the hydroxyl ions in alkaline conditions contributed to the

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dissolution of SLMoS2 (equation S1 in the SI). Importantly, SLMoS2 dissolved slowly

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without oxygen (Figure 1a−1b). The concentrations of released Mo and S species at

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pH=11 reached 6.218 and 4.405 mg/L, respectively, when DO was supplemented

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(Figure 1c−1d). The details of dissolved Mo released from SLMoS2 under DO

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conditions at different pH values are provided in Table S1. Visible light irradiation

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also significantly increased the release of Mo and S (Figure 1e−f), with approximately

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fourfold higher dissolved concentrations than those in the dark (Table S1). The

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highest contents of Mo and S species after 56 days of irradiation in the alkaline 10



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groups (pH=11) were 12.035 and 7.836 mg/L, respectively. Noticeably, the soluble

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ionic contents significantly increased with the DO concentration in the

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visible−light−irradiated groups (Figure S1). The contents of dissolved Mo species at

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the 56th day in the pH=11 groups reached 9.017, 10.518, and 11.568 mg/L when the

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DO concentrations were at 3.21, 6.76, and 9.23 mg/L, respectively. The majority

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(80.23%) of SLMoS2 nanosheets dissolved with the supplementation of saturated DO

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(9.52 mg/L) and visible light irradiation in the pH=11 groups. In contrast, 20.81% and

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41.45% of the nanosheets were dissolved under dark and single−DO treatment,

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respectively (Table S1). The above data suggested that DO and visible light

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irradiation significantly accelerated the chemical dissolution of SLMoS2. SLMoS2

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was chemically oxidized, while molybdate ions (MoO42−) and sulfate (SO42−) were the

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detected main products, as shown in equation S1. XPS spectra revealed the existence

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of a Mo6+ 3d band in SLMoS2, ascribed to molybdenum trioxide (MoO3). The Mo6+

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3d band in the XPS spectrum disappeared after visible light treatment (as presented

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below), implying the dissolution of MoO3. MoO3 can also be dissolved to molybdate

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in alkaline conditions (equation S2), further producing excess MoO42−. Therefore, the

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molar ratios of soluble S/Mo were less than 2 in the visible−light−treated groups

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(Figure S2), as a result of the release of extra MoO42−due to the photoreduction of

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MoO3 in the SLMoS2 nanosheets.

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Visible Light Irradiation, DO and Alkalinity Promote Phase Alteration

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According to the UV−vis spectra (Figure 2a), pristine SLMoS2 exhibited a

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considerable adsorption band at ~217 nm, which was attributed to the predominance 11


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of the metallic 1T phase.25, 26 With the release of soluble species, the absorption

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intensities at 200−300 nm significantly decreased, indicating the dissolution of the 1T

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phase. Compared to pristine SLMoS2, the adsorption band of transformed SLMoS2

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was blueshifted (~10 nm). The characteristic peaks of the 2H phase at ~610 and ~670

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nm became strong, and the absorbance at 500−800 nm increased (Figure 2b),

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suggesting a reduction in the 1T phase and the enrichment of the 2H phase. The Mo

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3d spectra in Figure 2c revealed that the 1T and 2H phases accounted for 72.9% and

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27.1%, respectively, of pristine SLMoS2. However, the proportion of the 1T phase

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significantly decreased with exposure to DO and visible light irradiation. The

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proportion of the 1T component decreased from 72.9% in pristine SLMoS2 to 57.4%,

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43.5%, and 11.4% in T3−SLMoS2, T7−SLMoS2, and T11−SLMoS2, respectively,

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which was consistent with the UV−vis spectra in Figure 2b. A significant decrease in

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the 1T phase of SLMoS2 in the visible−light−irradiation group with the increase in

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exposed DO is also observed in Figure S3, implying the crucial role of DO in the

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phase alteration of SLMoS2. Additionally, the Mo 3d core−level spectrum of pristine

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SLMoS2 consisted of three peaks located at ~235.5, ~232, and ~229 eV, which were

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related to Mo6+ and 3d3/2 and 3d5/2 of Mo4+, respectively. Visible light irradiation

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induced the dissolution of Mo oxides (Figure 1), resulting in the disappearance of the

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3d Mo6+ band in T11−SLMoS2. The 3d Mo4+ peaks shifted to higher binding energies

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in Figure 2c, confirming the enrichment of the 2H phase in transformed SLMoS2. The

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alteration in the phase composition of SLMoS2 was further verified by the S 2p

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core−level spectrum in Figure 2d. The peaks of the S 2p1/2 and S 2p3/2 bands also 12



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shifted to higher binding energies, suggesting the enrichment of the 2H phase in the

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transformed SLMoS2, especially in T11−SLMoS2. Another convincing result was the

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distinguishable broad band in transformed SLMoS2, which consisted of two peaks

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ascribed to 2H doublets.

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The crystal structure alteration of SLMoS2 was also investigated by XRD. The

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characteristic XRD peaks centered at 2θ values of 14.92° (002), 39.28° (103) and

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44.26° (006) were observed in all samples (Figure S4), suggesting that the major

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component was SLMoS2 nanosheets.27 With the dissolution, the (002) reflection,

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which was associated with the interplanar crystal spacing of SLMoS2,28 was

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significantly blueshifted, and the width of the peak became narrow. The (002)

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reflection peak of T11-SLMoS2 was centered at a 2θ of 14.46°, which was similar to

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that (a 2θ of 14.4°) of pure 2H MoS2.28 The intensities of the (100), (103) (105) and

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(112) reflections became stronger, while the (105) and (112) peaks were contracted in

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transformed SLMoS2 compared to that of pristine SLMoS2, indicating that the

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nanostructure of SLMoS2 was affected and transformed to the 2H phase with the

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chemical dissolution of the 1T polymorph.

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Morphological and Structural Alterations

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As shown in Figure 3a, the lateral size of pristine SLMoS2 was approximately

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100~200 nm, and the thickness was 1.243±0.051 nm, which were consistent with the

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reported properties of SLMoS2 nanosheets.29 In addition, abnormal pores and dentate

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edges existed on and around the nanosheets, which was ascribed to inherent defects of

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SLMoS2.30 After treatment with visible light irradiation, the Mo and S atoms on the 13


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nanosheets were chemically dissolved, and the lateral size became substantially

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smaller (Figure 3b−d). The large nanosheets also transformed to ribbon morphology,

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and more defects were formed on the nanosheets, especially for T11−SLMoS2. The

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thicknesses of the T3−SLMoS2, T7−SLMoS2, and T11−SLMoS2 nanosheets increased

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from approximately 1.243 nm to 2.598 nm (2.533±0.065 nm, n=3), 2.742 nm

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(2.701±0.041 nm, n=3), and 4.267 nm (4.214±0.053 nm, n=3), respectively; these

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results were consistent with the TEM images in Figure S5. As presented in the FTIR

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results in Figure 3e, a significant peak ascribed to Mo−S stretching vibrations located

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at ~600 cm−1 was observed for pristine SLMoS2.26 In contrast, the intensity of the

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Mo−S stretching bond in the transformed SLMoS2 became very weak. The peak

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located at ~800 cm−1 in pristine SLMoS2 and associated with the Mo−O stretching

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bond also disappeared, particularly in T11−SLMoS2. These results indicated that the

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chemical dissolution of SLMoS2 and Mo oxides significantly altered the functional

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bonds on the surface of SLMoS2. The Raman phonon modes associated with the

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in−plane (E2g) and out−of−plane (A1g) lattice vibrations of pristine SLMoS2 are

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located at ~385 cm−1 and 403 cm−1, respectively.31 A previous study reported that the

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intensity of Raman phonon modes (E2g and A1g) was positively correlated with defects

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in two−dimensional nanosheets.32 In Figure 3f, the peak intensity of E2g and A1g bonds

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significantly increased in the transformed SLMoS2, attributed to ion release (Figure 1)

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and the abundance of defects on the nanosheets, denoted by red arrows in Figure 3d.

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Moreover, the E2g and A1g vibrations in the Raman spectra of transformed SLMoS2

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nanosheets exhibited considerable red and blueshifts, respectively. The blueshift in 14



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A1g vibrations indicated that the nanosheets transitioned from single−layer to

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bulk−layer thickness. The redshift in E2g vibrations represented the stacking of

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nanosheets.33 Generally, the layer number of MoS2 nanosheets can be evaluated by the

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Raman shift of A1g−E2g.34 In the present study, the Raman shift of A1g−E2g for pristine

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SLMoS2, T3−SLMoS2, T7−SLMoS2, and T11−SLMoS2 was 18.0, 20.7, 22.2, and 24.1

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cm−1, respectively. Correspondingly, the layer numbers of T3−SLMoS2, T7−SLMoS2,

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and T11−SLMoS2 were calculated to be 2, 3 and 4, respectively (Figure S6). It has

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been reported that the loss of colloidal stability (as presented below, Figure 3g) can

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cause the restacking of MoS2 nanosheets.35, 36 Chemical dissolution on the surfaces

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and edges of SLMoS2 induced the destruction of ring structure and the enrichment of

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defects (Figure 2d), which probably led to the scrolling and bending of SLMoS2.37

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The SLMoS2 nanosheets were restacked, and the plane structure was scrolled; thus,

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the layer number of transformed SLMoS2 increased, as supported by AFM (Figure 3)

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and TEM (Figure S5) images.

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Alterations in Colloidal Stability

324

The aggregation kinetics were assessed using the initial aggregation rate (d) when the

325

hydrodynamic diameter reached 1.5−fold higher than the initial size.38 As shown in

326

Figure 3g, the average size of pristine SLMoS2 increased with an initial aggregation

327

rate of 0.487 nm/s. In contrast, transformed SLMoS2 exhibited higher instability, and

328

the initial aggregation rates were 0.963, 1.271, and 1.763 nm/s for T3−SLMoS2,

329

T7−SLMoS2, and T11−SLMoS2, respectively. At 96 h, the hydrodynamic diameters of

330

pristine SLMoS2, T3−SLMoS2, T7−SLMoS2, and T11−SLMoS2 were 1228, 1833, 1956, 15


Page 16 of 41

Page 17 of 41


331

and 2145 nm, respectively. Furthermore, the zeta potential results revealed that

332

pristine SLMoS2 was dispersive (−32.5 mV~−39.9 mV) when the pH was over 7

333

(Figure 3h) due to the electrostatic repulsion among negatively charged nanosheets.35

334

In contrast, the zeta potential decreased after chemical dissolution (Figure 3h). The

335

zeta potentials of T3−SLMoS2, T7−SLMoS2, and T11−SLMoS2 ranged from −30.3 to

336

−36.3 mV, −28.4 to −33.2 mV, and −27.5 to −31.1 mV, respectively. Thus,

337

dissolution and the alteration of phase, morphology and structure reduced the

338

dispersity of SLMoS2 in water.

339

Photoinduced Electronic Competition and Chemical Dissolution Assisted by DO

340

The UV−vis−near−infrared (UV−vis−NIR) diffuse reflection spectrum suggested that

341

the direct band gap of pristine SLMoS2 was 1.8 eV (Figure S7a), which was similar to

342

the data in the literature.39 The available wavelength for the band gap was 690.2 nm,

343

based on the threshold of the available wavelength (nm = 1242.375/band gap).

344

Moreover, Mott−Schottky plots showed that the flat−band potential of pristine

345

SLMoS2 was −0.45 eV (Figure S7b), which was similar to that of the conduction band

346

(CB).40 The CB potential was −0.45 eV, which is sufficient to oxidize O2 to produce

347

peroxy radical (•O2−)[Eθ(O2/•O2−) = −0.16 eV versus reversible hydrogen electrode].

348

However, •O2− generation was inhibited due to the rapid electron−hole recombination

349

of SLMoS2. Without DO, the signal of DMPO−•O2− in the SLMoS2 suspension was

350

very weak (Figure 4a and 4b). One study revealed that there is competition between

351

electron−hole recombination in materials and acquisition by other reactions (such as

352

oxygen reduction and oxidation).41 The ROS intensity was significantly strengthened 16



353

after oxygen was aerated (Figure 4c). The continuous supplementation of DO

354

competitively captured the separated electrons to produce •O2− under light irradiation

355

(equation S3), accelerating the chemical dissolution of SLMoS2 (Figure 4a−4c).

356

According to the CB potential and band gap energy, the valence band (VB) potential

357

was calculated to be 1.35 eV, which cannot directly oxidize OH− to produce •OH

358

(Eθ(OH−/•OH) = 2.40 eV versus reversible hydrogen electrode). •OH radicals were

359

notably generated under alkaline conditions (Figure 4d), probably due to the

360

acquisition of electrons from OH− by soluble Mo6+ species under visible light

361

irradiation (equation S4). In sum, the electrons from SLMoS2 were competitively

362

utilized by O2 to produce •O2−under DO treatment and visible light irradiation, and

363

•OH radical was also generated, thus leading to the chemical dissolution of SLMoS2

364

(Figure 4e).

365

Mitigation of Algal Division, Cellular Uptake, Ultrastructure and ROS

366

The effects of the above photoinduced physicochemical transformations of SLMoS2

367

on algal ecotoxicity were investigated. For algal division, the initial number (1.5×105

368

CFU/mL) of algae increased with incubation time, as shown in Figure S8. During this

369

period, the division of algal cells was significantly inhibited by exposure to SLMoS2

370

in a dose−dependent manner. In contrast, transformed SLMoS2 induced significantly

371

lower inhibition than pristine SLMoS2, except for T3−SLMoS2 (Figure S8b−d). The

372

effects of T11−SLMoS2 on cell division were the lowest, and the inhibition

373

percentages were only 10.9−15.2%. The algal cells in the control groups presented

374

intact ultrastructural morphology, including cell walls, chloroplasts, cell nuclei, and 17


Page 18 of 41

Page 19 of 41


375

other cytoplasmic compartments (Figure 5a). Mo ions (Na2MoO4) did not induce

376

obvious alterations in cell ultrastructure (Figure 5b). In contrast, pristine SLMoS2 was

377

visible in cellular cytoplasm and chloroplasts (Figure 5c, yellow arrows). The

378

nanosheet content in the pristine SLMoS2 groups (25 mg/L) reached 2.428 μg/105

379

cells (Figure S9a), and plasmolysis (red arrows) was also significantly induced by

380

pristine SLMoS2 (Figure 5c). The plasma membrane shrank and separated from the

381

cell walls. In addition, exposure to pristine SLMoS2 damaged and blurred

382

chloroplasts, and the biosynthesis of chlorophyll a was remarkably inhibited (up to

383

58%) compared to the control (Figure S9b). However, the damage to the cellular

384

ultrastructure by transformed SLMoS2 was weak (Figure 5d–5f). The cellular uptake

385

of transformed SLMoS2 was also reduced to 2.316, 1.806, and 1.103 μg/105 cells for

386

T3−SLMoS2, T7−SLMoS2, and T11−SLMoS2, respectively, at 25 mg/L (Figure S9a).

387

Physical and pharmacological inhibitions were used to analyze the uptake

388

mechanisms

389

energy−dependent endocytosis of algal cells could be inhibited at low temperatures.

390

The uptakes of pristine SLMoS2, T3−SLMoS2, T7−SLMoS2, and T11−SLMoS2 (25

391

mg/L) by algae at 4°C were reduced by 45.63%, 48.59%, 50.26, and 47.87%,

392

respectively (Figure S10a), compared to that of the control, suggesting the energy

393

dependence of SLMoS2 internalization. Furthermore, the algal cells were treated with

394

MβCD, CPZ, and EIPA to prevent caveolae−mediated endocytosis, clathrin−mediated

395

endocytosis, and uptake by micropinocytosis, respectively. Algal uptake of pristine

396

SLMoS2 (25 mg/L) with the pretreatments of MβCD, CPZ, and EIPA was reduced by

of

pristine

and

transformed

SLMoS2

18


by

algal

cells.

The


397

21.68%, 5.77%, and 39.67%, respectively. By contrast, the uptake inhibition effects

398

of transformed SLMoS2 by pharmacological pretreatment were considerably more

399

significant, especially for T11−SLMoS2. MβCD, CPZ, and EIPA decreased the cellular

400

contents of T11−SLMoS2 (25 mg/L) by 36.78%, 19.56%, and 48.76%, respectively

401

(Figure S10b−10d). The above data demonstrated that the uptake mechanisms of

402

pristine and transformed SLMoS2 were slightly different and that micropinocytosis

403

was the dominant pathway for the uptake of SLMoS2 nanosheets. Therefore, the

404

bioavailability and cellular contents of transformed SLMoS2 were evidently lower

405

than those of pristine SLMoS2, owing to the higher aggregation of transformed

406

SLMoS2 (Figure 3g−h) and inhibited micropinocytosis. The intracellular ROS levels

407

in pristine SLMoS2 compared to those in the control were significantly increased by

408

186.9−313.2% (Figure S9c). The ROS levels in transformed SLMoS2, especially in

409

the T11−SLMoS2 group, were lower than those in pristine SLMoS2, which was

410

consistent with the results of nanomaterial uptake and photosynthesis.

411

Metabolic Mechanisms of Phytotoxicity Mitigation

412

Metabolomic analysis provides a global view on the perturbation of a metabolism.42

413

Fifty−three metabolites were identified by analyzing approximately 250 peaks for

414

each sample using GC−MS (Tables S2 and S3). The identified metabolites included

415

fatty acids, amino acids, carbohydrates, alkanes and other biomolecules. Hierarchical

416

clustering (HCL) analysis indicated that the samples could be divided into two

417

clusters:1) pristine SLMoS2 (1, 10, and 25 mg/L) and T3−SLMoS2 (10 and 25 mg/L)

418

and 2) others (the control and most of the transformed SLMoS2). The results 19


Page 20 of 41

Page 21 of 41


419

suggested that pristine SLMoS2 significantly perturbed the cellular metabolism of

420

algae and the perturbation of metabolism was mitigated by environmental

421

transformation (Figure S11a). Furthermore, ANOVA with Tukey's test found that

422

SLMoS2 at 10 and 25 mg/L significantly downregulated the levels of amino acids and

423

fatty acids (p1)

436

between ROS and ornithine/threonine/tyrosine/serine is observed in Figure S12,

437

implying the inhibition of amino acid syntheses and the destruction of the defense

438

system induced by ROS. Serine takes part in the biosynthesis of purines, pyrimidines

439

and chlorophyll.45 Pristine SLMoS2 reduced the serine level, which supported the

440

decrease in chlorophyll a content. Furthermore, unsaturated fatty acid metabolism has 20



441

been correlated with cell membrane fluidity.46 The levels of unsaturated fatty acids in

442

the transformed SLMoS2 groups were significantly lower than those in the pristine

443

SLMoS2 groups (Figure S11a), which was consistent with the results of plasmolysis in

444

Figure 5. Fatty acids are vigorously responsive to extra stimulation during the growth

445

process.47, 48 Herein, unsaturated and saturated fatty acids presented positive and

446

negative relationships, respectively, with the ROS level (Figure S12). Arachidonic

447

acid is a polyunsaturated fatty acid released from membrane phospholipids in

448

response to ROS.48 The arachidonic acid levels in transformed SLMoS2 treatments

449

were significantly lower than those in pristine SLMoS2 groups, supporting the

450

negligible plasmolysis of algal cells exposed to transformed SLMoS2. Salicylic acid is

451

a signaling molecule that plays an important role in the plant defense response.49

452

Pristine SLMoS2 inhibited the levels of salicylic acid, but the inhibition was

453

remarkably diminished in transformed SLMoS2 (Figure S11a), indicating the recovery

454

of the defense system of algal cells. By metabolomic analysis, the above results

455

explore the toxicological mechanisms by which environmental transformation

456

mitigates nanotoxicity.

457

Outlook on the Environmental Transformation of SLMoS2

458

SLMoS2 has been applied in various fields and presents great potential for release into

459

the environment during its life cycle (e.g., fabrication, use and disposal). The phase,

460

morphology and dissolution (accompanied by defects) of SLMoS2 play a dominant

461

role in surface chemistry, colloidal stability and activity,50 determining the uptake and

462

ecotoxicity of this material to organisms. DO and visible light irradiation are two 21


Page 22 of 41

Page 23 of 41


463

fundamental factors in the water environment. However, the effects of DO and visible

464

light irradiation on the physicochemical transformation and nanostructure of SLMoS2,

465

especially ion release and phase transformation, remain largely unknown. The 1T

466

phase of pristine SLMoS2 was preferentially dissolved in alkaline conditions, and then

467

a ribbon structure and abundant defects on the surfaces of nanosheets were formed.

468

Transformed SLMoS2 nanosheets were thickened into multilayer structures, and the

469

colloidal stability was reduced. The phase and single−layer structure of SLMoS2 play

470

critical roles in photocatalysis and pollutant removal.51, 52 The environmental

471

transformations presented in this work unequivocally affect photocatalysis and

472

pollutant removal when using SLMoS2. Regarding biological responses, pristine

473

SLMoS2 (1T−rich) with a negative surface charge (pH>7.0) was stable (Figure 3g−f)

474

and was more effectively absorbed by algal cells than was transformed SLMoS2

475

(2H−rich), as illustrated in Figure 5. Transformed SLMoS2 (2H−rich phase) induced

476

lower intracellular ROS levels than pristine 1T−rich SLMoS2 (Figure S9c), indicating

477

the mitigation of nanotoxicity.53 Transformed SLMoS2 also triggered a weaker

478

perturbation of metabolism (Figure S11). In other words, the environmental risks of

479

SLMoS2 would be high in low−oxygen and dark conditions. Soluble ionic species that

480

coexist with nanomaterials are more bioavailable and have been confirmed to be the

481

drivers of the toxicological response.54, 55 In the present study, 100 μM Na2MoO4

482

showed no statistically significant inhibitory effect on algal cell growth (Figure 5).

483

The synthesis of chlorophyll a and intracellular ROS was also not remarkably

484

influenced by Na2MoO4 (Figure S9b and S9c). The above results indicated different 22



485

environmental risks than those derived from released Ag ions from Ag

486

nanoparticles.55 One study found that the formation of abundant surface defects was

487

beneficial for the antibacterial activity of nanomaterials (e.g., carbon materials and

488

metal nanoparticles) on a Gram−negative bacterium (E. coli),56 and could also

489

strengthen the toxicity of nanomaterials to organisms (RT−W1 cells and embryos).57

490

The interdependence between the defect/phase composition and ionic dissolution of

491

SLMoS2 deserves substantial attention in future applications and risk evaluations.

492 493

ASSOCIATED CONTENT

494

Supporting Information

495

Methods regarding characterization techniques; the detection of peroxy radicals,

496

hydroxyl radicals and ROS; and a theoretical analysis of the photoinduced redox

497

reaction. Tables regarding the dissolution rate of SLMoS2 and metabolites of algal

498

cells. Figures regarding the chemical dissolution of SLMoS2 nanosheets, the molar

499

ratio of S/Mo species, XPS spectra, X-ray powder diffraction spectra, TEM images,

500

the dependence of E2g−A1g Raman shifts on the number of MoS2 layers, the inhibition

501

of algal cell growth, quantifications of cellular SLMoS2, the inhibition of chlorophyll

502

a, ROS generation in algal cell, and metabolite analysis.

503 504

AUTHOR INFORMATION

505

Corresponding Author

506

*E–mail: [email protected] (X.H.). Phone: +86–022–23507800. Fax: +86– 23


Page 24 of 41

Page 25 of 41

507


022–66229562.

508 509

NOTES

510

The authors declare that there are no competing financial interests.

511 512

ACKNOWLEDGEMENTS

513

This work was financially supported by the National Natural Science Foundation of

514

China (grant nos. 21577070 and 21307061), the China Postdoctoral Science

515

Foundation (No. 2018M642757), and the Opening Foundation of Ministry of

516

Education Key Laboratory of Pollution Processes and Environmental Criteria (No.

517

201801). This work was also supported by the Doctoral Scientific Research

518

Foundation of Henan Normal University (No. 5101219170133).

519 520

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705 706 707

Figure Legends

708

Figure 1. Kinetics of pH−dependent chemical dissolution. (a−b) The contents of

709

dissolved Mo and S species from SLMoS2 nanosheets without dissolved oxygen (DO)

710

and light irradiation. (c−d) The contents of Mo and S species released by SLMoS2

711

nanosheets treated with DO but without light irradiation. (e−f) The contents of

712

dissolved Mo and S species from SLMoS2 nanosheets treated with saturated DO and

713

light irradiation. The saturated concentration of DO was 9.52 mg/L. The values in

714

parentheses represent the final concentrations of released ions (mg/L) on the 56th day.

715 716

Figure 2. Effect of pH on the ion release and phase composition of SLMoS2. (a)

717

UV−vis spectra of pristine SLMoS2, T3−SLMoS2, T7−SLMoS2, and T11−SLMoS2. (b)

718

XPS spectra of pristine SLMoS2, T3−SLMoS2, T7−SLMoS2, and T11−SLMoS2. The

719

changed intensity in phase−associated bonds (a) and the deconvolution analysis (b)

720

confirmed the alterations comprising the disappearance of the 1T phase and the

721

enrichment of the 2H phase proportion under visible light irradiation.

722 723

Figure 3. The alterations in morphology, surface chemistry, layer structure, and

724

colloidal stability of SLMoS2 driven by dissolved oxygen and visible light irradiation.

725

(a~d) AFM images of pristine SLMoS2, T3−SLMoS2, T7−SLMoS2, and T11−SLMoS2.

726

(e) FTIR spectra. (f) Raman spectra. The shifts of the E2g and A1g modes are denoted 33


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727

by arrows. Correlations between the A1g−E2g shifts and the layer number of MoS2

728

nanosheets are presented in the SI. (g) Time profile of the average hydrodynamic

729

diameter of SLMoS2 at pH 7.0. d1, d2, d3, and d4 represent the initial aggregation rates

730

of pristine SLMoS2, T3−SLMoS2, T7−SLMoS2, and T11−SLMoS2, respectively. (h)

731

Zeta potential.

732 733

Figure 4. Generation of free redials and photochemical reaction mechanisms. (a–c)

734

the production of peroxy radicals (•O2−) by pristine SLMoS2 with or without

735

dissolved oxygen (DO), (d) the generation of hydroxyl radicals (•OH) by pristine and

736

transformed SLMoS2, and (e) the photochemical reaction mechanisms of SLMoS2.

737 738

Figure 5. Ultrastructure of algal cells and internalization of SLMoS2 as shown by

739

TEM images. (a) The control without nanomaterial exposure, (b) 100 μM Na2MoO4

740

exposure, (c) 25 mg/L pristine SLMoS2, (d) 25 mg/L T3−SLMoS2, (e) 25 mg/L

741

T7−SLMoS2, and (f) 25 mg/L T11−SLMoS2. The yellow and red arrows indicate

742

SLMoS2 and plasmolysis, respectively. Cw, cell wall; S, starch grain; Chl,

743

chloroplast; Cn, cell nucleus.

744 745

Figure 6. Pathways of the metabolic responses and amino acid and fatty acid

746

disturbances in algal cells treated with pristine and transformed SLMoS2. The

747

metabolic pathways were established based on the Kyoto Encyclopedia of Genes and

748

Genomes (KEGG) database. Red and green words represent down− and upregulated 34



749

metabolites induced by pristine SLMoS2, respectively, compared to those of the

750

control. The metabolites labeled with up and down purple arrows are the metabolites

751

that are upregulated and downregulated, respectively, by transformed SLMoS2

752

compared to pristine SLMoS2.

753 754

755 756

Figure 1.

757

35


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758 759

Figure 2.

36



760 761

Figure 3.

37


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762 763

Figure 4.

764 765 38



766 767

Figure 5.

768 769 770 771 772 773 774

39


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Glycine

Glucose

Serine

Glyceric acid-3-phosphate

Phenylalanine Tyrosine

ROS

Pyruvate

Valine

Plasmolysis

Isoleucine Metabolic disturbance

Chl

Phosphoenolpyruvic acid

Acetyl-CoA

Arginine

Threonine Isoleucine

Oxaloacetate

Critrate

Malic acid

Isocitric acid

Fumarate

Aconitic acid

Succinate

775 776

Fatty acid metabolism 9,12-Octadecadienoic acid 9-Hexadecenoic acid Eicosatrienoic acid Octadecenoic acid Arachidonic acid Stearic acid

Asparate Methionine

Nucleus

Lactic acid

leucine Asparagine

Alanine

Salicylic acid

2-Oxoglutarate Butanoic acid

Figure 6.

40


Dodecanoic acid Palmitic Acid Ornithine

Urea

Glutamate

Glutamine

Glutathione

5-Oxoproline

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