Copper-Based Metal–Organic Framework Nanoparticles with

Jul 10, 2017 - Lu Yang , Wenfang Deng , Chang Cheng , Yueming Tan , Qingji Xie ... Haibin Dong , Xiaojun Hu , Jialin Zhao , Hongjie Li , Kwangnak Koh ...
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Copper-Based Metal−Organic Framework Nanoparticles with Peroxidase-Like Activity for Sensitive Colorimetric Detection of Staphylococcus aureus Shuqin Wang, Wenfang Deng, Lu Yang, Yueming Tan,* Qingji Xie, and Shouzhuo Yao Key Laboratory of Chemical Biology and Traditional Chinese Medicine Research (Ministry of Education of China), College of Chemistry and Chemical Engineering, Hunan Normal University, Changsha 410081, China S Supporting Information *

ABSTRACT: Cu-MOF nanoparticles with an average diameter of 550 nm were synthesized from 2-aminoterephthalic acid and Cu(NO3)2 by a mixed solvothermal method. The Cu-MOF nanoparticles can show peroxidase-like activity that can catalyze 3,3′,5,5′-tetramethylbenzidine to produce a yellow chromogenic reaction in the presence of H2O2. The presence of abundant amine groups on the surfaces of Cu-MOF nanoparticles enables facile modification of Staphylococcus aureus (S. aureus) aptamer on CuMOF nanoparticles. By combining Cu-MOF-catalyzed chromogenic reaction with aptamer recognition and magnetic separation, a simple, sensitive, and selective colorimetric method for the detection of S. aureus was developed. KEYWORDS: metal−organic framework, peroxidase-like activity, chromogenic reaction, pathogenic bacteria, Staphylococcus aureus

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peroxidase-like activities.23,24 For instance, Fe(III)-based MOFs with peroxidase-like activities have been used for colorimetric detection of H2 O2 and ascorbic acid. 23 Although the peroxidase-like activities of Fe(III)-based MOFs are extensively studied, the investigation the peroxidase-like activities of other transition metal-based MOFs is still of great interest. Moreover, the application field of MOF-catalyzed chromogenic reactions is extremely narrow, which is limited to the colorimetric detection of some small molecules involved in MOF-catalyzed chromogenic reactions, such as H2O2, ascorbic acid, and glucose.23,24 Therefore, it is interesting to extend the application field of MOF-catalyzed chromogenic reactions. In this work, copper-based metal−organic framework (CuMOF) nanoparticles were used as labels for sensitive and selective colorimetric detection of Staphylococcus aureus (S. aureus). As far as we are aware, it is the first time that MOFs are used for the colorimetric detection of pathogenic bacteria. The Cu-MOF nanoparticles were synthesized from 2-aminoterephthalic acid and copper nitrate by a mixed solvothermal method. The Cu-MOF nanoparticles are shown to possess peroxidaselike activity that can catalyze 3,3′,5,5′-tetramethylbenzidine (TMB) to produce a yellow chromogenic reaction in the presence of H2O2. Besides the high peroxidase-like activity that ensuring the high sensitivity for S. aureus detection, some other unique characteristics of Cu-MOF nanoparticles compared with

athogenic bacteria have brought great threats to human health, so sensitive and selective detection of pathogenic bacteria is of great significance.1 Traditional culture-based methods for the detection of pathogenic bacteria are inexpensive but time-consuming.2 Polymerase chain reactionbased strategies for the detection of pathogenic bacteria have advantages of low detection limits and high specificity, but the requirement of expensive instruments and skilled staffs hinders their wide applications.3 To overcome the drawbacks of conventional methods, researchers have widely reported fluorescent, electrochemical, and colorimetric detection of pathogenic bacteria using molecular recognition agents (e.g., antibody and aptamer) to bind specifically with bacterial cells.4−7 Especially, colorimetric detection of pathogenic bacteria has aroused great attention because of the advantages of low cost, simplicity, rapidity, and no requirement of expensive instruments.8,9 However, colorimetric methods reported previously for the detection of pathogenic bacteria still show high detection limits (hundreds to thousands of CFU mL−1).10,11 Therefore, it is urgent to develop a novel colorimetric method for sensitive and selective detection of pathogenic bacteria. Metal organic frameworks (MOFs) formed by self-assembly of metal ions and organic linkers, have received special concerns, because of their attracting features including large surface area, high porosity, and good stabilities.12,13 MOFs have been extensively investigated for various applications including gas storage and separation,14,15 drug delivery,16,17 catalysis,18,19 and sensing.20−22 Recently, some MOFs are found to show © 2017 American Chemical Society

Received: May 23, 2017 Accepted: July 10, 2017 Published: July 10, 2017 24440

DOI: 10.1021/acsami.7b07307 ACS Appl. Mater. Interfaces 2017, 9, 24440−24445

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ACS Applied Materials & Interfaces

Figure 1. Schematic illustration of (a) the synthesis and structure, (b) SEM image, (inset of b) size distribution, (c) TEM image, and (d) elemental mapping analysis of Cu-MOF nanoparticles.

Figure 2. (a) Schematic illustration of Cu-MOF-catalyzed chromogenic reaction. (b) UV−vis absorption spectra of TMB-H2O2 solutions (10 mM H2O2 and 80 μM TMB in 0.1 M aqueous HCl) incubated with (red curve) and without (black curve) 0.12 mg mL−1 Cu-MOF nanoparticles at 45 °C for 10 min. (c) Typical photographs and (d) absorbance at 450 nm of TMB-H2O2 solutions incubated with Cu-MOF nanoparticles of different concentrations at 45 °C for 10 min.

resulting in good linearity in the S. aureus detection. By combining Cu-MOF-catalyzed chromogenic reaction with aptamer recognition and magnetic separation, a simple, sensitive, and selective colorimetric method for the detection of S. aureus was developed. The linear range for S. aureus detection is from 50 to 10 000 CFU mL−1 with a detection limit of 20 CFU mL−1.

those MOF materials reported previously enable the colorimetric detection of S. aureus. The presence of abundant amine groups on the surfaces of Cu-MOF nanoparticles enables facile modification of S. aureus aptamer on Cu-MOF nanoparticles, ensuring that Cu-MOF nanoparticles can selectively recognize Staphylococcus aureus. The regular morphology and uniform size of Cu-MOF nanoparticles can ensure that the same amount of Cu-MOF labels are linked to each bacterial cell, 24441

DOI: 10.1021/acsami.7b07307 ACS Appl. Mater. Interfaces 2017, 9, 24440−24445

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ACS Applied Materials & Interfaces

Figure 3. Schematic illustration of colorimetric detection of target bacteria.

ligands can change the electronic structure of metal ions, which should be responsible for the improved catalytic activity.28 Figure 2c shows photographs of TMB-H2O2 solutions incubated with Cu-MOF nanoparticles of different concentrations at 45 °C for 10 min. With the increase in Cu-MOF concentration, the yellow color of the TMB-H2O2 solutions gradually deepens. Especially, the generating chromogenic signals at the Cu-MOF concentrations from 0 to 0.12 mg mL−1 can be distinguished by naked eyes. As shown in Figure 2d, the absorbance at 450 nm almost linearly increased with the Cu-MOF concentrations from 0 to 0.20 mg mL−1. These results inspire us to develop a new colorimetric detection strategy based on the concentration change of Cu-MOF nanoparticles. To achieve an optimal colorimetric effect, we conducted the Cu-MOF-catalyzed chromogenic reaction in 0.1 M HCl aqueous solution containing 80 μM TMB and 10 mM H2O2 at 45 °C for 10 min (Figures S3 and S4). To exploit the new application of the Cu-MOF-catalyzed chromogenic reaction, we selected S. aureus as the target, and S. aureus aptamer was selected as the molecular recognition tool that can specifically bind to S. aureus cells.29 Both Fe3O4 nanoparticles (Figure S5) and Cu-MOF nanoparticles were modified with S. aureus aptamer. The successful modification of S. aureus aptamer on Fe3O4 nanoparticles and Cu-MOF nanoparticles was confirmed by X-ray photoelectron spectroscopy (XPS). Small P2p peaks are observed after modification of aptamer on Fe3O4 nanoparticles (Figure S6) and Cu-MOF nanoparticles (Figure S7), confirming that aptamer is successfully linked to Fe3O4 nanoparticles and Cu-MOF nanoparticles. Figure 3 illustrated the procedures for colorimetric detection of S. aureus. In the presence of target bacteria, aptamermodified Cu-MOF nanoparticles and aptamer-modified Fe3O4 nanoparticles will bind to bacterial cell surface because of the specific interaction of aptamer with bacterial cell membrane receptors.29 After magnetic separation, Cu-MOF nanoparticles bound to bacterial cells will be removed from the supernatant, the number of Cu-MOF nanoparticles in the supernatant decreases. In the presence of nontarget bacteria, Cu-MOF nanoparticles cannot be removed from the supernatant owing to the lack of specific recognition. Therefore, target bacteria can be specifically detected by measuring the residual Cu-MOF

For the synthesis of Cu-MOF nanoparticles, the precursors of Cu(NO3)2 and 2-aminoterephthalic acid were dissolved in a mixed solvent of ethanol and N,N-dimethylformamide, followed by solvothermal treatment (Figure 1a). The morphology of the as-prepared Cu-MOF nanoparticles was investigated by scanning electron microscopy (SEM, Figure 1b) and transmission electron microscopy (TEM, Figure 1c). Uniform spherical nanoparticles with an average diameter of 550 nm are observed. Energy-dispersive X-ray elemental mapping analysis reveals that Cu, N, O and C elements are uniformly distributed in Cu-MOF nanoparticles (Figure 1d). In the Fourier transform infrared (FTIR) spectrum of Cu-MOF (Figure S1), the stretching vibration peak of − OH at 2970 cm−1 disappears, confirming the occurrence of coordination interaction between Cu2+ and −COOH of 2-aminoterephthalic acid. Two peaks at 3452 and 3351 cm−1 assigned to asymmetric and symmetric stretching vibrations of − NH2 are observed in the Cu-MOF nanoparticles (Figure S1), confirming the presence of amino groups in the Cu-MOF nanoparticles.25 As reported previously, −COOH of 2-aminoterephthalic acid will coordinate with metal ions to form amino functionalized MOF materials.26,27 The presence of abundant amine groups will enable facile surface modification on Cu-MOF nanoparticles. The Cu-MOF nanoparticles were used to catalyze the oxidation of TMB in the presence of H2O2 (Figure 2a). Figure 2b shows ultraviolet−visible (UV−vis) absorption spectra of TMB-H2O2 solutions (10 mM H2O2 and 80 μM TMB in 0.1 M aqueous HCl) incubated with and without 0.12 mg mL−1 CuMOF nanoparticles at 45 °C for 10 min. In the presence of CuMOF nanoparticles, a sharp absorption peak at 450 nm is observed, because the Cu-MOF nanoparticles can catalyze the oxidation of colorless TMB in the presence of H2O2 to generate a yellow product. In contrast, no obvious absorption at 450 nm is observed in the absence of Cu-MOF nanoparticles, indicating that direct oxidation of TMB by H2O2 is sluggish. In addition, we found that free Cu2+ ions can also catalyze the oxidation of TMB in the presence of H2O2, indicating that Cu2+ ions in the MOF nanoparticles are the active centers (Figure S2). However, the catalytic activity of Cu-MOF nanoparticles is much higher than that of free Cu2+ ions, indicating that the formation metal−organic framework can improve the catalytic activity. Coordination interaction between metal ions and 24442

DOI: 10.1021/acsami.7b07307 ACS Appl. Mater. Interfaces 2017, 9, 24440−24445

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Figure 4. (a) Typical photographs, (b) UV−vis absorption spectra, (c) absorbance changes at 450 nm of the resulting solutions for the detection of different concentrations (0, 50, 500, 1000, 3000, 5000, 7000, 10000 CFU mL−1) of S. aureus.

selectivity of the proposed method. The concentration for each bacterial sample was 10 000 CFU mL−1. As shown in Figure S10, the signals for the other bacterial samples are much lower than that for S. aureus, resulting from the high affinity between the aptamer and S. aureus.29 The application potential of the proposed method was studied by detecting S. aureus in milks. Table S2 summarizes the results, the recoveries are between 95 and 111%, and the relative standard deviations (RSD) are between 4.8 and 5.7%. These results indicate that the proposed method can be used for the detection of S. aureus in real samples. In conclusion, Cu-MOF nanoparticles were synthesized from 2-aminoterephthalic acid and copper nitrate by a mixed solvothermal method. The Cu-MOF nanoparticles can catalyze TMB to produce a yellow chromogenic reaction in the presence of H2O2. The peroxidase-like activity of Cu-MOF is dependent on solution pH, temperature, and reaction time. By combining Cu-MOF-catalyzed chromogenic reaction with aptamer recognition and magnetic separation, a simple, sensitive, and selective colorimetric method for the detection of S. aureus was developed. This work not only describes a new enzyme mimic with peroxidase-like activity but also provides a new method for the detection of pathogenic bacteria.

nanoparticles in the supernatant with the Cu-MOF-catalyzed chromogenic reaction. Quantitative detection of S. aureus in phosphate buffer solution (PBS, pH 7.4) was carried out. Briefly, S. aureus cells were incubated with S. aureus aptamer-modified Cu-MOF nanoparticles and S. aureus aptamer-modified Fe3O4 nanoparticles in PBS at 37 °C. The optimal incubation time is 70 min (Figure S8). After magnetic separation, the supernatant containing residual Cu-MOF nanoparticles was used for colorimetric analysis. As shown in Figure 4a, in the presence of S. aureus of different concentrations, the Cu-MOF catalyzed TMB-H2O2 solutions show yellow color of different shades. With the increase of S. aureus concentration, the yellow color of TMBH2O2 solutions gradually fades, resulting from the decreased Cu-MOF nanoparticles in TMB-H2O2 solutions. The absorption peaks at 450 nm decrease with the increase of S. aureus concentration (Figure 4b). Figure 4c shows absorbance changes (A-A0) at 450 nm as functions of S. aureus concentration. The linear range for S. aureus detection is from 50 to 10,000 CFU mL−1 (R2 = 0.9972), with a detection limit of 20 CFU mL−1 (S/N = 3). As listed in Table S1, the detection limit is lower than those obtained with most colorimetric methods reported previously, being comparable with those obtained with highly sensitive fluorescence methods. Cu-MOF nanoparticles bound to bacterial cells after magnetic separation were also used for colorimetric analysis. As shown in Figure S9, a large background absorbance at 450 nm is observed, because Fe3O4 nanoparticles can also show peroxidase-like activity to some extent.30 Although obvious absorbance changes (A0 − A) at 450 nm as functions of S. aureus concentration can be observed, the generating chromogenic signals at S. aureus concentration concentrations from 50 to 10 000 CFU mL−1 cannot be distinguished easily by naked eyes, resulting from the peroxidase-like activity of Fe3O4 nanoparticles. Therefore, the residual Cu-MOF nanoparticles in the supernatant were proposed for colorimetric analysis. Some other bacterial samples including S. dysenteriae, S. typhimurium, and E. coli O157:H7 were used to study the



ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsami.7b07307. Experimental section, FT-IR spectra of Cu-MOF (Figure S1), UV−vis spectra of TMB-H2O2 solutions incubated with different catalysts (Figure S2), optimization of H2O2 concentration and TMB concentration (Figure S3), optimization of pH, reaction temperature, and reaction time (Figure S4), SEM images and FT-IR spectrum of Fe3O4 (Figure S5), XPS of aptamer modified Fe3O4 (Figure S6), XPS of aptamer modified Cu-MOF (Figure S7), optimization of incubation time (Figure S8), colorimetric detection of S. aureus using Cu-MOF nanoparticles bound to bacterial cells (Figure S9), 24443

DOI: 10.1021/acsami.7b07307 ACS Appl. Mater. Interfaces 2017, 9, 24440−24445

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selectivity of the proposed method (Figure S10), performance comparison (Table S1), and results of the determination of S. aureus in real samples (Table S2) (PDF)

AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected] or tanyueming0813@ hunnu.edu.cn. ORCID

Yueming Tan: 0000-0003-3356-9079 Notes

The authors declare no competing financial interest.



ACKNOWLEDGMENTS This work is supported by the National Natural Science Foundation of China (21305041), Program for Excellent Talents in Hunan Normal University (ET1503), and Key Project of Research and Development Plan of Hunan Province (2016SK2020).



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