Portable Colorimetric Detection of Mercury(II) Based on a Non-Noble

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Portable Colorimetric Detection of Mercury(II) Based on a NonNoble Metal Nanozyme with Tunable Activity Lunjie Huang,† Qingrui Zhu,† Jie Zhu,† Linpin Luo,† Shuhan Pu,† Wentao Zhang,† Wenxin Zhu,† Jing Sun,‡ and Jianlong Wang*,†,‡ †

College of Food Science and Engineering, Northwest A&F University, Yangling 712100, Shaanxi, China Qinghai Key Laboratory of Qinghai-Tibet Plateau Biological Resources, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining 810008, Qinghai, China



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S Supporting Information *

ABSTRACT: The nanozyme-based strategy is currently one of the frontiers in the detection of toxic heavy metal ions. However, the utilization of noble metal free nanozymes to construct an economically and environmentally sustainable methodology remains largely unknown. Here, chitosan-functionalized molybdenum(IV) selenide nanosheets (CS-MoSe2 NS), greenly synthesized by an ionic liquid-assisted grinding method, were exploited for the colorimetric sensing of mercury ions (Hg2+). The sensing principle was based on the activating effect of Hg2+ on CS-MoSe2 NS nanozyme activities, triggered by the in situ reduction of chitosan-captured Hg2+ ions on a MoSe2 NS surface. Using 3,3′,5,5′-tetramethylbenzidine (TMB) as a colorimetric indicator, the concentrations of activator-like Hg2+ ions could be quantitatively and selectively monitored, reaching a limit of detection of 3.5 nM with the ultraviolet−visible spectrophotometer. In addition, the integration system of CS-MoSe2 NS with a smartphone achieved a portable detection limit as low as 8.4 nM Hg2+ within 15 min and showed high specificity and anti-interfering ability over other ions and great practicability in real water and serum samples. The eco-friendly properties of such sensing system were also confirmed. This work emphasizes the rational portable assembly of biocompatible nanozymes like CS-MoSe2 NS for the field detection of Hg2+ in food, biological, and environmental samples.

1. INTRODUCTION Mercury(II) ions, the primary form of mercury pollution in water, can be easily transformed into hypertoxic organic mercury (mainly methylmercury) by aquatic microorganisms.1 The accumulation of trace organic mercury in the human body through the food chain can be strongly neurotoxic to the central nervous system and cause severe damage to human organs.2 To cope with the serious threat of mercury contamination to the ecosystem and human health, many instrumental methods, electrochemical methods, and optical methods have been developed to detect aqueous Hg2+ and to assess its risks.3−7 Among them, nanomaterial-based colorimetric strategies,8−11 which can allow field-portable, costeffective, and rapid analysis of mercury ions, have attracted a remarkable amount of attention. Nanozymes, as a collection of nanomaterials with enzymelike activities, have been on the cutting edge in the field of biosensors and used for signal generation and amplification in an enzyme-mimicking catalytic manner.12−16 Because of the sensitive colorimetric reactions that can be read by the naked eye, peroxidase (POD) and oxidase (OD) mimics such as noble metal nanomaterials have exhibited great potential in the detection of inorganic ions, mycotoxins, and bacterial contamination in aquatic environments.17−20 Via the cooperation of Hg2+-mediated surface chemistry with catalytic © XXXX American Chemical Society

activities of noble metal nanostructures, many high-performance colorimetric mercury sensors based on the Hg2+enhanced or -inhibited catalysis of noble metal (Au, Ag, Pt, Pd, etc.) nanozymes have been developed.21−27 Compared with traditional morphological approaches,8,9,11 such nanozyme detection techniques involve accurately controlling catalytic colored reactions by Hg2+ ions and exhibit excellent detection sensitivity, specificity, and anti-interference ability for Hg2+ detection in complicated systems. However, besides expensive and rare noble metal nanomaterials, the rational design of earth-abundant, economic non-noble metal nanozymes for Hg2+ responsive catalysis has scarcely been exploited in the detection of Hg2+ ions. As representative non-noble metal nanozymes, two-dimensional transition metal dichalcogenides (TMDCs) such as tungsten diselenide (WSe2), molybdenum disulfide (MoS2), and molybdenum diselenide (MoSe2) have emerged as promising candidates in various fields, including catalysis, sensing, and medical therapy applications.28−30 Compared to nondegradable noble metal NPs, TMDCs are cost-effective and readily available and usually exhibit relatively lower biotoxicities and accumulation effects in organisms.31−35 Received: November 14, 2018

A

DOI: 10.1021/acs.inorgchem.8b03193 Inorg. Chem. XXXX, XXX, XXX−XXX

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Inorganic Chemistry

Figure 1. Synthesis and characterization of CS-MoSe2 NS. (A) Schematic illustration of the simultaneous exfoliation and functionalization of MoSe2 by IL-assisted grinding in the presence of chitosan, forming CS-MoSe2 NS nanozymes. (B) X-ray diffraction pattern of bulk MoSe2 and CSMoSe2 NS. (C) Transmission electron microscopy (TEM) image of MoSe2 NS. The scale bar is 500 nm. (D) High-resolution TEM image of MoSe2 NS. (E) Atomic force microscopy image of CS-MoSe2 NS and height profile across the CS-MoSe2 NS in panel D. The scale bar is 100 nm. (F) Fourier transform infrared spectra of chitosan, CS-MoSe2 NS, and bulk MoSe2. (G) Dispersion solutions of (a) CS-MoSe2 NS, (b) MoSe2 NS, and (c) G-MoSe2 NS before and after standing for 10 days.

Among the attractive TMDCs, MoSe2 nanosheets that retain an unsaturated d orbital of Mo atoms were recently found to exhibit peroxidase-like activity and good biocompatibility in vitro.28,33,34 The large surface area of MoSe2 nanosheets also makes it compatible with various surface engineering strategies. Moreover, the affinity between mercury and selenium (Se) is one of the best known examples of biological antagonism,36,37 implying a possible interaction between MoSe2 and Hg species. To the best of our knowledge, the detection of Hg2+ by MoSe2 nanosheets ions has not been investigated. Herein, a field-portable, versatile, and economical colorimetric Hg2+ sensor was first proposed using the biocompatible chitosan-functionalized MoSe2 nanosheet (CS-MoSe2 NS) enzyme mimics. The CS-MoSe2 NS, facilely obtained by simultaneous exfoliation and functionalization via a one-step ionic liquid-assisted grinding method (Figure 1A), exhibited good dispersion stability but poor POD- and OD-like activities in the catalytic oxidation of 3,3′,5,5′-tetramethylbenzidine (TMB). Upon introduction of Hg2+, the POD- and OD-like activities of CS-MoSe2 NS were significantly promoted, due to the capture of Hg2+ by chitosan molecules and in situ reduction of partial Hg2+ to Hg0 on the CS-MoSe2 NS surface. On the basis of this sensing mechanism, the results of CSMoSe2 NS-based colorimetry can be monitored by the naked eye with an ultraviolet−visible (UV−vis) spectrophotometer due to the characteristic color and absorption peak of oxidized TMB (oxTMB). The possible influences of other ions were

also excluded by the results of selectivity and interference experiments. Moreover, a portable probe CS-MoSe2 NS integrated with a smartphone enabled us to detect Hg2+ in real water and serum samples in a facile, sensitive, fast, and onsite way. Finally, the environmental impact and ecocompatibility of such a sensing system were also examined.

2. EXPERIMENTAL SECTION Reagents and Materials. Molybdenum(IV) diselenide (MoSe2) powder (25-fold as estimated via the absorbance at 652 nm. Additionally, the color of the reaction solution changed from nearly colorless to bright blue as a result

3. RESULTS AND DISCUSSION Synthesis and Characterization. CS-MoSe2 NS were prepared through a one-step IL-assisted grinding of bulk MoSe2 in the presence of chitosan (Figure 1A), achieving simultaneous exfoliation and functionalization of MoSe2 NS. Figure 1B depicts the crystal structure of the as-exfoliated CSMoSe2 NS measured by XRD. The diffraction peaks of bulk MoSe2 and the as-exfoliated MoSe2 nanosheets were well matched to JCPDS Card 17-0887. After exfoliation, the peaks C

DOI: 10.1021/acs.inorgchem.8b03193 Inorg. Chem. XXXX, XXX, XXX−XXX

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like and OD-like activities of CS-MoSe2 NS for a highefficiency colorimetric reaction. We also examined the effects of other common cations (Ag+, + K , Li+, Na+, NH4+, Ba2+, Ca2+, Cd2+, Co2+, Cu2+, Fe2+, Mg2+, Mn2+, Ni2+, Pb2+, Zn2+, Al3+, Cr3+, and Fe3+) at 10 μM in POD (Figure S2 and Figure 2C) and OD (Figure S3) catalytic systems. The Hg2+ group is shown to have an obvious difference compared to the others in view of the high absorbance at 652 nm as well as the deep blue color. Meanwhile, the interference experiment (Figure 2D) further verified the insignificant influences from these cations on Hg activation. Moreover, the selectivity and interference investigations of common anions (10 μM Br−, Cl−, NO3−, CO32−, SO42−, PO43−, and CH3COO−) (Figure S4) provide coherent evidence that Hg activation is selective and stable. Hence, the selective role of Hg2+ implies the feasibility of Hg2+ detection based on CS-MoSe2 NS. Actually, several factors, including pH, temperature, and concentrations of TMB, were found to affect the mercurystimulated activities of CS-MoSe2 NS, which were optimized to 4.0 (Figure S5), 25 °C (Figure S6), and 0.5 mM (Figure S7), respectively. Then, we investigated the behavior of Hg2+treated CS-MoSe2 NS with aging time (1 week) by XRD pattern and catalytic measurements. As shown in Figure S8A, the XRD pattern exhibited no obvious difference from that of pristine CS-MoSe2 NS. The catalytic activities of CS-MoSe2 NS exhibited no further significant increase or loss during a one-week treatment with Hg2+ (Figure S8B). These results demonstrate the long-term stability of mercury-treated CSMoSe2 NS. Mechanism of CS-MoSe2 NS-Based Colorimetry for Hg2+ Detection. To explore the mechanism, the Hg2+

Figure 2. Activating effect of Hg2+ on CS-MoSe2 NS nanozymes. (A) UV absorption spectra of (a) H2O2 and TMB, (b) H2O2, TMB, and Hg2+, (c) H2O2, TMB, and CS-MoSe2 NS, and (d) H2O2, TMB, Hg2+, and CS-MoSe2 NS. (B) UV absorption spectra of (a) TMB, (b) TMB and Hg2+, (c) TMB and CS-MoSe2 NS, and (d) TMB, Hg2+, and CS-MoSe2 NS. Images in panels A and B are of the solutions after reaction for 15 min, separately. (C) Selectivity of Hg2+ (2 μM) over other ions (10 μM) in the POD catalytic system of CS-MoSe2 NS. The image shows the color changes. (D) Interference of other ions vs Hg2+ in POD and OD systems.

of the oxidation of TMB. The oxidase mimicking system also demonstrated a similar case (Figure 2B), in which the poor OD-like activity could be promoted nearly 13-fold by Hg2+. These results imply that Hg2+ can greatly stimulate the POD-

Figure 3. Mechanism of Hg2+-induced activation of the CS-MoSe2 NS nanozyme. (A) Increased rate of POD-like and OD-like activity of different materials after the addition of 2 μM Hg2+. All materials used here were at a concentration of 25 μg/mL (POD system) or 50 μg/mL (OD system). A0 and A are the absorbance values of oxTMB at 652 nm before and after the addition of mercury, respectively. (B and C) XPS spectra of CSMoSe2 NS in the Hg 4f region and N 1s region, respectively, before and after incubation with Hg2+. (D) Kinetic plot of ν against TMB concentration before and after the addition of Hg2+ (10 μM) in the POD system. D

DOI: 10.1021/acs.inorgchem.8b03193 Inorg. Chem. XXXX, XXX, XXX−XXX

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Inorganic Chemistry activator was first examined on several similar materials, including G-MoSe2, MoSe2, CS-MoS2, MoS2, a CS/MoSe2 mixture, and CS. As depicted in Figure 3A, G-MoSe2 NS exhibited 8.4-fold enhanced POD and 3.8-fold enhanced OD mimic activities in the presence of Hg2+, which are much lower than those of CS-MoSe2 (25- and 13-fold, respectively). In addition, the activities of unmodified MoSe2 NS showed weak enhancement induced by Hg2+. It is noted that chitosan molecules have an excellent ability to adsorb mercury ions mainly through nitrogen-containing groups, such as NH2− Hg−NH2 binding.43,44 Thus, we believe that chitosan molecules act as an affinity agent to “capture” mercury ions, allowing them an intense interaction with CS-MoSe2 NS rather than G-MoSe2 NS or MoSe2 NS. Moreover, the catalysis of MoS2 NS and CS-MoS2 NS, as TMDC analogues of MoSe2, was found to produce no obvious enhancement after the addition of Hg2+. This proves that MoSe2 is the irreplaceable for interaction with Hg2+ ions, which may be associated with the indefinite Hg−Se antagonism.36 The simple chitosan/ MoSe2 NS mixture was also investigated, which yielded slight Hg-increased activities. Moreover, chitosan molecules with Hg2+ cannot turn on the catalytic oxidation of TMB. The studies described above indicate that the highly efficient compositing structure of chitosan and MoSe2 allows the mercury-boosted colorimetric reaction of CS-MoSe2 NS. In addition, the Hg-affected CS-MoSe2 NS surface were determined by the XPS technique, and the spectra were processed by a standard Gaussian fitting method. In the Hg 4f region (Figure 3B), two peaks (green areas) at ∼100.12 eV (Hg 4f7/2) and ∼103.99 eV (Hg 4f5/2) were observed after incubation with Hg2+, which were attributed to the formation of Hg0.45 Figure 3C shows only one peak corresponding to C− N functional groups (∼399.27 eV) in the N 1s region of CSMoSe2 NS, while a new peak at ∼401.37 eV occurred after the addition of mercury, which could be assigned to the formation of mercury−NH2 complexes.46 The high-resolution C 1s spectra showed three single peaks at 284.8, 286.2, and 288.0 eV (Figure S9A), corresponding to the C−C/CC, C−N/ CN, and CO/O−C−O functional groups, respectively.47 An obvious decrease in the intensity of the peak assigned to C−N or CN was observed after incubation with mercury. Similarly, in the O 1s region (Figure S9B), the peak assigned to CO (531.7 eV) also showed a decrease after the addition of mercury, while the peak assigned to C−O (533.0 eV) remained unchanged. On the contrary, as shown in the spectra of Mo 3d (Figure S9C) and Se 3d (Figure S9D), the addition of mercury did not affect the valence condition of Mo and Se elements. In other words, surface-immobilized chitosan simultaneously captures and partially reduces Hg2+ into metallic Hg0 at the CS-MoSe2 NS surface, while the CSMoSe2 NS remains chemically stable. Subsequently, in situ Hg0 formation changed the surface properties of CS-MoSe2 NS to produce higher catalytic activities. To confirm the contribution of in situ Hg reduction to the nanozyme activities, NaBH4 was used as a strong reducer to promote the reduction of mercury. As shown in Figure S10, the addition of NaBH4 had no effect on pure CS-MoSe2 NS but improved the activities of Hgtreated CS-MoSe2 NS. The pathway of Hg-enhanced activity was then explored by steady-state kinetic studies. Typical Michealis−Menten curves were obtained for both H2O2 (Figure S11) and TMB (Figure 3D), and their corresponding double-reciprocal plots are shown in Figures S11 and S12, respectively. As listed in Table

1, the apparent Km value of the Hg-CS-MoSe2 NS (10.7 mM) with H2O2 as the substrate was similar to that of CS-MoSe2 NS Table 1. Effect of Hg on POD-like Kinetics of CS-MoSe2 NS H2O2

TMB

nanozyme

Km (mM)

Vmax (×10−8 M s−1)

Km (mM)

Vmax (×10−8 M s−1)

CS-MoSe2 Hg-treated

12.89 10.7

23.26 22.02

1.317 0.2

46.85 44.74

(12.89 mM), revealing that they have similar affinities for H2O2. Instead, the apparent Km value of the Hg-CS-MoSe2 NS (0.2 mM) with TMB was ∼6 times smaller than that of the CS-MoSe2 NS (1.317 mM). Therefore, interaction with Hg greatly promoted the binding affinity of CS-MoSe2 NS for TMB, donating the significantly enhanced POD activity. This is consistent with the fact that the OD activity (without H2O2 as a co-substrate) can also be greatly enhanced by Hg2+. Scheme 1 presents a systematical illustration of the interacting mechanism and the sensing principle for Hg2+ detection based on CS-MoSe2 NS. On one hand, chitosan molecules acting as an auxiliary affinity agent “capture” mercury ions, achieving sufficient adsorption of mercury ions on MoSe2 sheets. On the other hand, the Hg−Se antagonism strengthens the affinity process, further inducing the in situ reduction of Hg2+ on the active surfaces of CS-MoSe2 NS, which greatly promotes the catalytic activity of CS-MoSe2 NS. As a result, the mercury concentration, which determines the nanozyme activity of CS-MoSe2 NS in the catalytic oxidation of TMB, can be read by the naked eye (color), by the UV−vis spectrophotometer (spectra), and by the smartphone sensor (RGB function). Performance of CS-MoSe2 NS-Based Colorimetry. On the basis of the excellent specificity mentioned above, different concentrations of Hg2+ were incubated with CS-MoSe2 NS to accelerate TMB oxidation under the optimized conditions. Panels A and B of Figure 4 show the UV−vis absorption spectra of POD-like and OD-like sensing systems, respectively. The absorbance at 652 nm of these two systems increased gradually with an increasing amount of Hg2+ added from 0 to 10 μM (Figure S13). Moreover, even a small amount of Hg2+ ions (50 nM in the POD channel or 100 nM in the OD channel) was adequate to make a visually appreciable colorimetric difference between the solutions (Figure 4C). In addition, by plotting the correlation curve of absorbance and Hg2+ concentration, we found a linear correlation (R2 = 0.997) in the POD system in the Hg2+ concentration range of 25 nM to 2.5 μM (Figure 4D). The limit of detection (LOD) of Hg2+ was estimated to be 3.5 nM (3δ/S principle), which is lower than the permissible levels in drinking water set by the U.S. Environmental Protection Agency (US-EPA) (10 nM, 2 μg/L) and the World Health Organization (WHO) (30 nM, 6 μg/L). Similarly, a linear relationship (R2 = 0.998) existed in the range of 100 nM to 4.0 μM in the OD system (Figure 4E) with a LOD as low as 15 nM. Construction of a Portable CS-MoSe2 NS/Smartphone Sensor. To balance the sensitivity and portability of the current method, we developed a CS-MoSe2 NS/smartphone colorimetric platform. As illustrated in Figure 5A, the colorimetric reaction mixture processed on an absorbent pad would generate a colorimetric signal upon addition of Hg2+ (step 1), the variations of which can be monitored by the E

DOI: 10.1021/acs.inorgchem.8b03193 Inorg. Chem. XXXX, XXX, XXX−XXX

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Inorganic Chemistry Scheme 1. Illustration of the CS-MoSe2 NS-Based Versatile Colorimetric Detection of Mercury Ion

Figure 5. CS-MoSe2 NS/smartphone-based detection assay. (A) Principle of the detection assay with a smartphone. (B) CS-MoSe2 NS-based test strip for Hg2+ visualization. (C) Plot of the (G + B)/2R value vs Hg2+ concentration in the POD channel. The images show the color of the test strip varied with the concentration of Hg2+.

letters after 15 min, which verified the disguisable signal from the on-strip sensing system. Images in Figure 5C and Figure S14 show the mercury-dependent color changes of the test strips, which were used to model RGB formulas that correlate the RGB value with the amount of Hg2+. Among the empirical functions modeled for POD (Figure S15) and OD (Figure S16) systems, an optimal linear relationship can be achieved by using the (G + B)/2R function in both POD and OD systems. In the POD channel, the linear calibration curve (R2 = 0.985) of the (G + B)/2R value versus Hg2+ concentration is in the range of 25 nM to 2.5 μM with a LOD estimated to be 8.4 nM (Figure 5C), which can cover the maximum limit in drinking water set by the US-EPA. Similarly, a linear correlation (0.1−4.0 μM) is observed in the OD channel with a LOD of 27 nM (Figure S14). Additionally, the (G + B)/ 2R values were distinguishable in the presence of mercury ions (>1.0) or other ions (≤1.0) listed above (Figure S17).

Figure 4. CS-MoSe2 NS-based colorimetric mercury(II) assay. (A and B) UV absorption spectra of the reaction system that consisted of Hg2+, 25 μg/mL CS-MoSe2 NS, 20 mM H2O2, and 0.5 mM TMB and the reaction system that consisted of Hg2+, 50 μg/mL CS-MoSe2 NS, and 0.5 mM TMB, respectively. (C) Hg2+ concentration-related color changes of the reaction systems. (D and E) Linear relationships between the concentration of Hg2+ and the absorbance of the reaction system obtained from panels A and B, respectively.

smartphone application (Color Assist, downloaded from the Apple App Store) in RGB value mode (step 2). As a result, Hg2+ can be quantified by the fitting relationship between the RGB ratio and mercury concentration (step 3). To explore the feasibility, the mercury ion solution (10 μM) was used as the ink to write “NWSUAF” on the strip. As shown in Figure 5B, light blue letters could be observed after 1 min and dark blue F

DOI: 10.1021/acs.inorgchem.8b03193 Inorg. Chem. XXXX, XXX, XXX−XXX

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boosted by the Hg2+ ions. The rational functionalization of chitosan and in situ reduction of Hg2+ on the CS-MoSe2 NS surface account for the Hg2+-induced activating effect. In the CS-MoSe2 NS-based sensing system, the Hg2+ concentration was determined by Hg2+-triggered changes in the absorbance and color of oxTMB under optimized conditions, exhibiting high selectivity and good anti-interference against other cations. In addition, the successfully integrated CS-MoSe2 NS/smartphone sensor provided sensitive, and rapid, reliable detection of Hg2+ on site with a LOD of 8.4 nM, which performed well in water and serum samples. Moreover, the low cytotoxicity of CS-MoSe2 NS, as well as the green properties of TMB and H2O2, implies the sustainable practicality of our sensing platform for Hg2+ detection in food, biomedical, and environmental fields.

Therefore, by integrating the smartphone with the CS-MoSe2 NS-mediated colorimetric reaction, we can successfully detect nanomolar level Hg2+ in an on-site, rapid, sensitive, and portable manner. Compared with other recent methods summarized in Table S1, this method, adopting totally nonnoble metal nanozymes for the first time, is competitive in terms of sensitivity and selectivity and is more facile, versatile, cost-efficient, and field-portable. Practical Use in Water and Serum Samples. The practicality of our method was examined in real water and serum samples. Before the use of a CS-MoSe2 CS/smartphone sensor (POD system), Hg2+ levels in water and serum samples were confirmed to be too low to be detected by both our method and the ICP-MS method. Then, a certain concentration of Hg2+ was added to the real samples through a standard addition method. As shown in Table S2, the recoveries of the measurements are within 97.3−105.4%. The insignificant differences among the measured values, the ICP-MS data, and the added values demonstrated the reliable and potential applications of our method in the food, environmental, and medical fields. Eco-Compatibility of CS-MoSe2 NS-Based Calorimetry. As a sensing platform for detecting toxic Hg2+, it is advantageous to adopt nontoxic and eco-friendly building components, avoiding secondary toxicity to the aquatic ecosystems. In this sensing system, TMB is a cheap and safe chromogenic reagent without carcinogenic teratogenicity to living beings, and H2O2 is easy to naturally decompose into water and oxygen, which cause no damage to the ecosystem. The inherent toxicity of CS-MoSe2 NS was also explored through cytotoxicity studies using the MTT assay with HepG2 cells. As shown in Figure 6, the cellular viability could still be



ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.inorgchem.8b03193. UV−vis absorption spectra, selectivity and interference study, optimization of conditions, absorbance curves, XPS analysis, effect of NaBH4, enzymatic kinetics, stability tests, OD sensing curve, RGB modeling curves, cytotoxicity study, comparison of methods, and a table of real sample analysis (PDF)



AUTHOR INFORMATION

Corresponding Author

*Telephone and fax: +86 29-8709-2275. E-mail: wanglong79@ yahoo.com. ORCID

Jianlong Wang: 0000-0002-2879-9489 Notes

The authors declare no competing financial interest.



ACKNOWLEDGMENTS This research was financed by grants from National Natural Science Foundation of China (21675127), the Fundamental Research Funds for the Central Universities (2014YB093 and 2452015257), and the Capacity Building Project of Engineering Research Center of Qinghai Province (2017-GX-G03).



Figure 6. Viability of HepG2 cells treated with different concentrations of CS-MoSe2 NS for 24 h.

REFERENCES

(1) Pirrone, N.; Cinnirella, S.; Feng, X.; Finkelman, R. B.; Friedli, H. R.; Leaner, J.; Mason, R.; Mukherjee, A. B.; Stracher, G. B.; Streets, D. G.; Telmer, K. Global Mercury Emissions to the Atmosphere from Anthropogenic and Natural Sources. Atmos. Chem. Phys. 2010, 10, 5951−5964. (2) Clarkson, T. W.; Magos, L.; Myers, G. J. The Toxicology of Mercury - Current Exposures and Clinical Manifestations. N. Engl. J. Med. 2003, 349, 1731−1737. (3) Zhang, Y.; Liu, W.; Zhang, W.; Yu, S.; Yue, X.; Zhu, W.; Zhang, D.; Wang, Y.; Wang, J. DNA-Mediated Gold Nanoparticle Signal Transducers for Combinatorial Logic Operations and Heavy Metal Ions Sensing. Biosens. Bioelectron. 2015, 72, 218−224. (4) Kim, H. N.; Ren, W. X.; Kim, J. S.; Yoon, J. Fluorescent and Colorimetric Sensors for Detection of Lead, Cadmium, and Mercury ions. Chem. Soc. Rev. 2012, 41, 3210−3244. (5) Suherman, A. L.; Tanner, E. E. L.; Compton, R. G. Recent Developments in Inorganic Hg2+ Detection by Voltammetry. TrAC, Trends Anal. Chem. 2017, 94, 161−172.

>90% after incubation with CS-MoSe2 NS even at a high concentration of 200 μg/mL for 24 h. The observed high biocompatibility of CS-MoSe2 NS proves their eco-friendly features for practical applications. Therefore, this work demonstrates a simply practical, economically effective, and environmentally sustainable sensing platform for the detection of trace Hg2+ in the field.

4. CONCLUSION In summary, a new nanozyme strategy for mercury sensing was proposed, for the first time, using biocompatible CS-MoSe2 NS as POD and OD enzyme mimics. The ultrathin CS-MoSe2 nanosheets were fabricated by a simple and green IL-assisted grinding method in one step. The nanozyme activities of the CS-MoSe2 NS were found to be significantly and selectively G

DOI: 10.1021/acs.inorgchem.8b03193 Inorg. Chem. XXXX, XXX, XXX−XXX

Article

Inorganic Chemistry

Enzyme-Like Activity of Platinum/Gold Nanoparticles. Nanoscale 2012, 4, 6823−6830. (25) Chai, D.-F.; Ma, Z.; Qiu, Y.; Lv, Y.-G.; Liu, H.; Song, C.-Y.; Gao, G.-G. Oxidase-Like Mimic of Ag@Ag3PO4 Microcubes as a Smart Probe for Ultrasensitive and Selective Hg2+ Detection. Dalton Trans. 2016, 45, 3048−3054. (26) Li, H.; Liu, H.; Zhang, J.; Cheng, Y.; Zhang, C.; Fei, X.; Xian, Y. Platinum Nanoparticle Encapsulated Metal-Organic Frameworks for Colorimetric Measurement and Facile Removal of Mercury(II). ACS Appl. Mater. Interfaces 2017, 9, 40716−40725. (27) Zhang, S.; Zhang, D.; Zhang, X.; Shang, D.; Xue, Z.; Shan, D.; Lu, X. Ultratrace Naked-Eye Colorimetric Detection of Hg2+ in Wastewater and Serum Utilizing Mercury-Stimulated Peroxidase Mimetic Activity of Reduced Graphene Oxide-PEI-Pd Nanohybrids. Anal. Chem. 2017, 89, 3538−3544. (28) Wu, X.; Chen, T.; Wang, J.; Yang, G. Few-Layered MoSe2 Nanosheets as An Efficient Peroxidase Nanozyme for Highly Sensitive Colorimetric Detection of H2O2 and Xanthine. J. Mater. Chem. B 2018, 6, 105−111. (29) Li, B. L.; Wang, J.; Zou, H. L.; Garaj, S.; Lim, C. T.; Xie, J.; Li, N. B.; Leong, D. T. Low-Dimensional Transition Metal Dichalcogenide Nanostructures Based Sensors. Adv. Funct. Mater. 2016, 26, 7034−7056. (30) Chen, T. M.; Wu, X. J.; Wang, J. X.; Yang, G. W. WSe2 Few Layers with Enzyme Mimic Activity for High-Sensitive and HighSelective Visual Detection of Glucose. Nanoscale 2017, 9, 11806− 11813. (31) Chen, H.; Liu, T.; Su, Z.; Shang, L.; Wei, G. 2D Transition Metal Dichalcogenide Nanosheets for Photo/Thermo-Based Tumor Imaging and Therapy. Nanoscale Horiz. 2018, 3, 74−89. (32) Kreyling, W. G.; Möller, W.; Holzwarth, U.; Hirn, S.; Wenk, A.; Schleh, C.; Schaffler, M.; Haberl, N.; Gibson, N.; Schittny, J. C. AgeDependent Rat Lung Deposition Patterns of Inhaled 20 Nanometer Gold Nanoparticles and their Quantitative Biokinetics in Adult Rats. ACS Nano 2018, 12, 7771. (33) Pan, J.; Zhu, X.; Chen, X.; Zhao, Y.; Liu, J. Gd3+- Doped MoSe2 Nanosheets Used as a Theranostic Agent for Bimodal Imaging and Highly Efficient Photothermal Cancer Therapy. Biomater. Sci. 2018, 6, 372−387. (34) Lei, Z.; Zhu, W.; Xu, S.; Ding, J.; Wan, J.; Wu, P. Hydrophilic MoSe2 Nanosheets as Effective Photothermal Therapy Agents and Their Application in Smart Devices. ACS Appl. Mater. Interfaces 2016, 8, 20900−20908. (35) Lei, Z.; Zhou, Y.; Wu, P. Simultaneous Exfoliation and Functionalization of MoSe2 Nanosheets to Prepare ″Smart″ Nanocomposite Hydrogels with Tunable Dual Stimuli-Responsive Behavior. Small 2016, 12, 3112−3118. (36) Khan, M. A. K.; Wang, F. Mercury-Selenium Compunds and Their Toxicological Significance: Toward a Molecular Understanding of the Mercury-Selenium Antagonism. Environ. Toxicol. Chem. 2009, 28, 1567−1577. (37) Koeman, J. H.; Peeters, W. H.; Koudstaal-Hol, C. H.; Tjioe, P. S.; de Goeij, J. J. Mercury-Selenium Correlations in Marine Mammals. Nature 1973, 245, 385−386. (38) Zhang, W.; Wang, Y.; Zhang, D.; Yu, S.; Zhu, W.; Wang, J.; Zheng, F.; Wang, S.; Wang, J. A One-Step Approach to the LargeScale Synthesis of Functionalized MoS2 Nanosheets by Ionic Liquid Assisted Grinding. Nanoscale 2015, 7, 10210−10217. (39) Wang, J.; Zhang, W.; Wang, Y.; Zhu, W.; Zhang, D.; Li, Z.; Wang, J. Enhanced Exfoliation Effect of Solid Auxiliary Agent On the Synthesis of Biofunctionalized MoS2 Using Grindstone Chemistry. Part. Part. Syst. Charact. 2016, 33, 825−832. (40) Cunningham, G.; Lotya, M.; Cucinotta, C. S.; Sanvito, S.; Bergin, S. D.; Menzel, R.; Shaffer, M. S. P.; Coleman, J. N. Solvent Exfoliation of Transition Metal Dichalcogenides: Dispersibility of Exfoliated Nanosheets Varies Only Weakly between Compounds. ACS Nano 2012, 6, 3468−3480. (41) Jeon, J.-H.; Cheedarala, R. K.; Kee, C.-D.; Oh, I.-K. Dry-Type Artificial Muscles Based on Pendent Sulfonated Chitosan and

(6) Jiang, S.; Cheng, R.; Ng, R.; Huang, Y.; Duan, X. Highly Sensitive Detection of Mercury(II) Ions with Few-Layer Molybdenum Disulfide. Nano Res. 2015, 8, 257−262. (7) Guo, C.; Irudayaraj, J. Fluorescent Ag Clusters via a ProteinDirected Approach as a Hg(II) Ion Sensor. Anal. Chem. 2011, 83, 2883−2889. (8) Lee, J.-S.; Han, M. S.; Mirkin, C. A. Colorimetric Detection of Mercuric Ion (Hg2+) in Aqueous Media Using DNA-Functionalized Gold Nanoparticles. Angew. Chem., Int. Ed. 2007, 46, 4093−4096. (9) Wei, Q.; Nagi, R.; Sadeghi, K.; Feng, S.; Yan, E.; Ki, S. J.; Caire, R.; Tseng, D.; Ozcan, A. Detection and Spatial Mapping of Mercury Contamination in Water Samples Using a Smart-Phone. ACS Nano 2014, 8, 1121−1129. (10) Chen, N.; Zhang, Y.; Liu, H.; Wu, X.; Li, Y.; Miao, L.; Shen, Z.; Wu, A. High-Performance Colorimetric Detection of Hg2+ Based on Triangular Silver Nanoprisms. ACS Sens. 2016, 1, 521−527. (11) Dong, C.; Wang, Z.; Zhang, Y.; Ma, X.; Iqbal, M. Z.; Miao, L.; Zhou, Z.; Shen, Z.; Wu, A. High-Performance Colorimetric Detection of Thiosulfate by Using Silver Nanoparticles for Smartphone-Based Analysis. ACS Sens. 2017, 2, 1152−1159. (12) Huang, L.; Zhang, W.; Chen, K.; Zhu, W.; Liu, X.; Wang, R.; Zhang, X.; Hu, N.; Suo, Y.; Wang, J. Facet-Selective Response of Trigger Molecule to CeO2 {110} for Up-regulating Oxidase-Like Activity. Chem. Eng. J. 2017, 330, 746−752. (13) Gao, L.; Zhuang, J.; Nie, L.; Zhang, J.; Zhang, Y.; Gu, N.; Wang, T.; Feng, J.; Yang, D.; Perrett, S.; Yan, X. Intrinsic PeroxidaseLike Activity of Ferromagnetic Nanoparticles. Nat. Nanotechnol. 2007, 2, 577−583. (14) Wei, H.; Wang, E. Nanomaterials with Enzyme-Like Characteristics (Nanozymes): Next-Generation Artificial Enzymes. Chem. Soc. Rev. 2013, 42, 6060−6093. (15) Wang, X.; Hu, Y.; Wei, H. Nanozymes in Bionanotechnology: From Sensing to Therapeutics and Beyond. Inorg. Chem. Front. 2016, 3, 41−60. (16) Wu, J.; Wang, X.; Wang, Q.; Lou, Z.; Li, S.; Zhu, Y.; Qin, L.; Wei, H. Nanomaterials with Enzyme-Like Characteristics (Nanozymes): Next-Generation Artificial Enzymes (II). Chem. Soc. Rev. 2019, DOI: 10.1039/C8CS00457A. (17) Huang, L.; Zhu, W.; Zhang, W.; Chen, K.; Wang, J.; Wang, R.; Yang, Q.; Hu, N.; Suo, Y.; Wang, J. Layered Vanadium(IV) Disulfide Nanosheets as a Peroxidase-Like Nanozyme for Colorimetric Detection of Glucose. Microchim. Acta 2018, 185, 7. (18) Wang, Q.; Wei, H.; Zhang, Z.; Wang, E.; Dong, S. Nanozyme: An Emerging Alternative to Natural Enzyme for Biosensing and Immunoassay. TrAC, Trends Anal. Chem. 2018, 105, 218−224. (19) Huang, L.; Chen, K.; Zhang, W.; Zhu, W.; Liu, X.; Wang, J.; Wang, R.; Hu, N.; Suo, Y.; Wang, J. SsDNA-Tailorable OxidaseMimicking Activity of Spinel MnCo2O4 for Sensitive Biomolecular Detection in Food Sample. Sens. Actuators, B 2018, 269, 79. (20) Wu, L.-L.; Qian, Z.-J.; Xie, Z.-J.; Zhang, Y.-Y.; Peng, C.-F. Colorimetric Detection of Copper Ions Based on Surface Modification of Silver/Platinum Cluster Nanozyme. Chin. J. Anal. Chem. 2017, 45, 471−475. (21) Zhang, S.; Li, H.; Wang, Z.; Liu, J.; Zhang, H.; Wang, B.; Yang, Z. A strongly Coupled Au/Fe3O4/GO Hybrid Material with Enhanced Nanozyme Activity for Highly Sensitive Colorimetric Detection, and Rapid and Efficient Removal of Hg2+ in Aqueous Solutions. Nanoscale 2015, 7, 8495−8502. (22) Li, W.; Chen, B.; Zhang, H.; Sun, Y.; Wang, J.; Zhang, J.; Fu, Y. BSA-Stabilized Pt Nanozyme for Peroxidase Mimetics and Its Application on Colorimetric Detection of Mercury(II) Ions. Biosens. Bioelectron. 2015, 66, 251−258. (23) Peng, C.-F.; Zhang, Y.-Y.; Wang, L.-Y.; Jin, Z.-Y.; Shao, G. Colorimetric Assay for the Simultaneous Detection of Hg2+ and Ag+ Based on Inhibiting the Peroxidase-Like Activity of Core-Shell Au@Pt Nanoparticles. Anal. Methods 2017, 9, 4363−4370. (24) Tseng, C.-W.; Chang, H.-Y.; Chang, J.-Y.; Huang, C.-C. Detection of Mercury Ions Based on Mercury-Induced Switching of H

DOI: 10.1021/acs.inorgchem.8b03193 Inorg. Chem. XXXX, XXX, XXX−XXX

Article

Inorganic Chemistry Functionalized Graphene Oxide for Greatly Enhanced Ionic Interactions and Mechanical Stiffness. Adv. Funct. Mater. 2013, 23, 6007−6018. (42) Bao, H.; Pan, Y.; Ping, Y.; Sahoo, N. G.; Wu, T.; Li, L.; Li, J.; Gan, L. H. Chitosan-Functionalized Graphene Oxide as a Nanocarrier for Drug and Gene Delivery. Small 2011, 7, 1569−1578. (43) Miretzky, P.; Fernandez Cirelli, A. Hg(II) Removal from Water by Chitosan and Chitosan Derivatives: A Review. J. Hazard. Mater. 2009, 167, 10−23. (44) Jeon, C.; Holl, W. H. Chemical Modification of Chitosan and Equilibrium Study for Mercury Ion Removal. Water Res. 2003, 37, 4770−4780. (45) Wu, G.-W.; He, S.-B.; Peng, H.-P.; Deng, H.-H.; Liu, A.-L.; Lin, X.-H.; Xia, X.-H.; Chen, W. Citrate-Capped Platinum Nanoparticle as a Smart Probe for Ultrasensitive Mercury Sensing. Anal. Chem. 2014, 86, 10955−10960. (46) Li, N.; Bai, R. B.; Liu, C. K. Enhanced and Selective Adsorption of Mercury Ions on Chitosan Beads Grafted with Polyacrylamide via Surface-Initiated Atom Transfer Radical Polymerization. Langmuir 2005, 21, 11780−11787. (47) Vieira, R. S.; Oliveira, M. L. M.; Guibal, E.; RodriguezCastellon, E.; Beppu, M. M. Copper, Mercury and Chromium Adsorption on Natural and Crosslinked Chitosan Films: An XPS Investigation of Mechanism. Colloids Surf., A 2011, 374, 108−114.

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DOI: 10.1021/acs.inorgchem.8b03193 Inorg. Chem. XXXX, XXX, XXX−XXX