Photogenerated Hole-induced Chemical Redox Cycling on Bi2S3

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Letter

Photogenerated Hole-induced Chemical Redox Cycling on Bi2S3/Bi2Sn2O7 Heterojunction: Toward General Amplified Split-Type Photoelectrochemical Immunoassay Juntao Cao, Bing Wang, Yu-Xiang Dong, Qian Wang, Shu-Wei Ren, Yan Ming Liu, and Wei-Wei Zhao ACS Sens., Just Accepted Manuscript • DOI: 10.1021/acssensors.8b00332 • Publication Date (Web): 31 May 2018 Downloaded from http://pubs.acs.org on May 31, 2018

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Photogenerated Hole-induced Chemical Redox Cycling on Bi2S3/Bi2Sn2O7 Heterojunction: Toward General Amplified Split-Type Photoelectrochemical Immunoassay Jun-Tao Cao,†∗ Bing Wang,†, ‡ Yu-Xiang Dong,† Qian Wang,‡ Shu-Wei Ren,§ Yan-Ming Liu,†,∗ and Wei-Wei Zhao‡,#,∗ †

College of Chemistry and Chemical Engineering, Institute for Conservation and Utilization of

Agro-bioresources in Dabie Mountains, Xinyang Normal University, Xinyang 464000, China ‡

State Key Laboratory of Analytical Chemistry for Life Science, School of Chemistry and

Chemical Engineering, Nanjing University, Nanjing 210023, China §

Xinyang Central Hospital, Xinyang 464000, China

#

Department of Materials Science and Engineering, Stanford University, Stanford, California

94305, United States

* To whom correspondence should be addressed. * E-mail: [email protected] * E-mail: [email protected] * E-mail: [email protected]; [email protected]

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ABSTRACT This work reports the elegant bridging of enzymatic generation of electron donor with photogenerated hole-induced chemical redox cycling amplification (RCA) for innovative photoelectrochemical (PEC) immunoassay, by the aid of a heterojunction photoelectrode with split-type strategy. Specifically, the system was exemplified by the alkaline phosphatase (ALP) catalytic generation of ascorbic acid (AA), the redox cycling of AA by tris (2-carboxyethyl) phosphine (TCEP) as reductant, and the use of a novel Bi2S3/Bi2Sn2O7 heterojunction and myoglobin (Myo) as the photoelectrode and the target, respectively. After the immunoreaction and ALP-induced production of AA, the subsequent oxidation of AA by the photogenerated holes of the Bi2S3/Bi2Sn2O7 heterojunction could be cycled via the regeneration of AA by TCEP from the oxidized product of dehydroascorbic acid, leading to easy signal amplification for the sensitive immunoassay of Myo in real samples. It is believed that this work provided a basis for further design and development of general RCA-based PEC immunoassays.

KEYWORDS: Photoelectrochemical immunoassay; Chemical redox cycling; Bi2S3/Bi2Sn2O7 heterojunction; Split-type strategy; Myoglobin

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Photoelectrochemical (PEC) immunoassay is now of soaring interest due to its potential utilization for future diagnosis.1-6 To achieve better performance, ideal photoelectrodes and novel signaling strategies have been actively pursued among the community.7-11 In the quest for ideal photoelectrodes, semiconductor heterojunctions consisting of different species are being considered as favorite schemes as compared to the pure ones. For example, TiO2-BiOI,12 TiO2-BiVO4,13 CdTe-Bi2S314 and CdS/g-C3N415 have recently been constructed for specific PEC analytical purposes. On the other hand, to amplify the signals, numerous ingenious strategies have been proposed, and most of which have resorted to the enzyme-assisted in situ generation of electron donor/acceptor,16-20 photoactive species,21-23 or light sources.24-27 Despite previous advances, some important hurdles still remain in current PEC immunoassays. Especially, these PEC immunoassays necessitate the immunoreactions on the photoelectrodes, the procedure of which are generally laborious and time-consuming, and the excited states of the semiconductors may cause biomolecules damage. Another example is that in the dominant protocol of in situ generation of electron donor, the consumption of these nonrenewable electron donor usually requires high enzyme loading and special care to avoid their denaturation and leakage during the entire procedure. To break these bottlenecks, developing advanced simple and sensitive strategies for facile PEC immunoassay is highly expected. Significantly, redox

cycling

amplification

(RCA),

a

popular

technique

referring

to

repeatedly-coupled reduction and oxidation reactions, has been validated as an effective method for regeneration of signaling species in electrochemical bioanalysis.28-30 Integrated with the split-type PEC bioanalysis, we believe the fusion of RCA and an appropriate photoelectrode holds great promise for circumventing the above-mentioned bottlenecks. This letter herein presents the elegant bridging of enzymatic generation of electron donor with photogenerated hole-induced chemical RCA for innovative PEC immunoassay, by the aid of a heterojunction photoelectrode with split-type strategy on 96-well plate. As shown in Scheme 1, the system was exemplified by the alkaline phosphatase (ALP) catalytic generation of ascorbic acid (AA), the redox cycling of 3


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AA by tris (2-carboxyethyl) phosphine (TCEP) as reductant, and the use of a novel Bi2S3/Bi2Sn2O7 heterojunction and myoglobin (Myo) as the photoelectrode and the target, respectively. Specifically, after the immunorecognition in the wells, the signal label of ALP linked anti-Myo polyclonal antibody (anti-Myo-SiO2-ALP) could catalyze the hydrolysis of ascorbic acid 2-phosphate (AAP) to produce AA. The subsequent oxidation of AA by the photogenerated holes of the Bi2S3/Bi2Sn2O7 heterojunction photoelectrode will then trigger the chemical redox cycling in the presence of TCEP as reductant, during which the AA underwent the oxidation at the electrode and then regenerated via reduction of the oxidized product (dehydroascorbic acid, DHA) by TCEP. Since the efficient regeneration of signaling species in a separated environment, the developed PEC format could not only eliminate the common drawbacks in previous reports but also enable easy signal amplification for the sensitive immunoassay of Myo in real sample. According to a recent review on PEC immunoassay,31 such a RCA-based PEC immunoassay has not been reported. Given the high efficiency and diversity of redox cycling routes, this work is expected to provide a general basis for further design and development of ultrasensitive PEC immunoassay protocols. Scheme 1. Schematic Illustration of (a) Sandwich Immunoreaction in One Well of 96-well Plate and ALP-catalyzed Generation of AA, (b) Redox Cycling for Signal Amplification on Bi2S3/Bi2Sn2O7 Heterojunction

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RESULTS AND DISCUSSION Scanning electron microscopy (SEM), transmission electron microscope (TEM), X-ray powder diffraction spectra (XRD) and X-ray photoelectron spectra (XPS) were utilized to reveal the structural and compositional information of the as-fabricated samples of Bi2Sn2O7, Bi2S3 and Bi2S3/Bi2Sn2O7 heterojunction. As shown in Figure 1a and 1b, the Bi2Sn2O7 appeared as quasi-spherical nanoparticles (NPs) with ca. 15 nm in diameter, whereas the Bi2S3 exhibited as nanorods (NRs) with 10-35 nm in width and 30-130 nm in length. Figure 1c then reflects the morphology of the Bi2S3/Bi2Sn2O7 heterojunction, the smooth surface of Bi2S3 NRs was clearly attached with many Bi2Sn2O7 NPs. Figure 1d of the TEM further verified the successful modification of Bi2Sn2O7 NPs onto these Bi2S3 NRs. The corresponding high-resolution TEM image of Figure S1 demonstrates the lattice fringes of 0.31 nm and 0.38 nm, which corresponded to the d-spacing of (222) plane of Bi2Sn2O7 and (101) plane of Bi2S3,32,33 respectively. The crystal structures of these samples were identified by XRD with the results shown in Figure 1e. As shown in the patterns, all the observed diffraction peaks could be indexed to cubic pyrochlore Bi2Sn2O7 (JCPDS No.87-0284) and orthorhombic Bi2S3 (JCPDS No.17-0320), respectively, indicating that no Bi-related impurities existed in the samples. Besides, the sharp peaks also reflected that the samples had relatively good crystallinity. The pattern of Bi2S3/Bi2Sn2O7 heterojunction manifested the coexistence of the Bi2Sn2O7 and Bi2S3, indicating the successful formation of the heterojunction. XPS was further conducted to measure the surface chemical compositions and oxidation states of the Bi2S3/Bi2Sn2O7 heterojunction. As shown in Figure 1f, the survey indicated that Bi, Sn, O, S and C elements were presented. The high-resolution XPS spectra of Bi 4f, S 2p and Sn 3d were also illustrated in Figure S2. As shown, the Bi 4f5/2 (158.9 and 164.3 eV) and Bi 4f7/2 (157.8 and 163.1 eV) peaks of Bi3+ were observed and the peak at 160.5 eV sandwiched between Bi 4f5/2 and Bi 4f7/2 was assigned to S 2p3/2, indicating the presence of Bi3+ and S2- in the heterojunction. The Sn 3d5/2 peak situated at 486.7 eV and Sn 3d3/2 peak situated at 495.1 eV confirmed the presence of Sn4+ in the heterojunction. 5


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Figure 1. SEM images of (a) Bi2Sn2O7, (b) Bi2S3 and (c) Bi2S3/Bi2Sn2O7 heterojunction; (d) TEM image of the Bi2S3/Bi2Sn2O7 heterojunction; (e) XRD spectra of the Bi2Sn2O7, Bi2S3 and Bi2S3/Bi2Sn2O7 heterojunction; (f) XPS survey spectrum of Bi2S3/Bi2Sn2O7 heterojunction. The peak positions were determined with a C 1s binding energy of 284.6 eV as the internal marked standard.

The Raman and fourier transform infrared (FT-IR) spectra of the samples were also investigated. Figure 2a shows the Raman spectra. In curve of Bi2Sn2O7, the peaks of 248 and 382 cm-1 were specified at the Eg and F1u mode of Bi-O stretching in Bi2Sn2O7, respectively, the peak at 400 cm-1 corresponded to F2g of Sn-O stretching mode in Bi2Sn2O7.34,35 The peaks of Bi2S3 located at 142 cm-1,183 cm-1, 236 cm-1 and 256 cm-1 were consistent with reported literature.36 The Raman peaks intensity of

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Bi2S3/Bi2Sn2O7 heterojunction visibly increased compared to that of pure Bi2Sn2O7 and Bi2S3. Meanwhile, in the case of the Bi2S3/Bi2Sn2O7 heterojunction, coincident peaks were also observed, which rooted in Bi2Sn2O7 and Bi2S3, indicating the formation of heterojunction. Figure 2b shows the corresponding FT-IR spectra. In curve of Bi2Sn2O7, the modes at about 526 cm-1 and 618 cm-1 corresponded to the Bi-O and the Sn-O stretching vibrations, respectively, which were consistent with the previous literature.37 The Bi2S3 displayed the peak at 842 cm-1, corresponding to the Bi-S stretching.38 The characteristic peaks of Bi2Sn2O7 and Bi2S3 emerged in the FT-IR spectrum of Bi2S3/Bi2Sn2O7 heterojunction. These optical results also indicated the Bi2S3/Bi2Sn2O7 heterojunction was successfully constructed. Incidentally, the UV-vis diffuses reflectance spectra were also recorded with the results shown in Figure S3.35

Figure 2. (a) Raman and (b) FT-IR spectra of Bi2Sn2O7, Bi2S3 and Bi2S3/Bi2Sn2O7 heterojunction.

The light harvesting properties of the samples were then probed by the photocurrent action spectra. Figure 3a shows the measured chronoamperometric I-t responses of the Bi2Sn2O7, Bi2S3 and Bi2S3/Bi2Sn2O7 on the transparent indium tin oxide (ITO)-coated glass substrate electrodes upon visible light irradiation. As shown, the Bi2Sn2O7/ITO exhibited very weak PEC response (curve a) due to the severe charge recombination on the surface of Bi2Sn2O7 (Figure S4),32,37 while the Bi2S3/ITO generated an obvious photocurrent intensity (curve b). After their combination, the Bi2S3/Bi2Sn2O7/ITO reached a more prominent response (curve c), which originated from the energy bands-match in the heterojunction. As illustrated in Scheme 1b, the light illumination 7


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causes the generation of electron-hole (e--h+) pairs, which occurred simultaneously in both Bi2S3 and Bi2Sn2O7. Subsequently, the electrons from the conduction band (CB) of Bi2S3 are rapidly migrated to the CB of Bi2Sn2O7, while the holes of Bi2Sn2O7 transferred to the Bi2S3, leaving the electrons collected as photocurrent and the holes trapped by the sacrificial donor. Such a synergy effect in Bi2S3/Bi2Sn2O7 heterojunction could extend the light utilization and restrain the recombination of photogenerated electron-hole pairs, thus greatly enhancing the photocurrent. To further evaluate the proposed TCEP-based chemical RCA strategy, the PEC responses of the Bi2S3/Bi2Sn2O7 electrode were studied against the ALP-induced AA in the absence and presence of TCEP. As shown in Figure 3b, in the absence of AA and TCEP, the fast electron-hole recombination in Bi2S3/Bi2Sn2O7 led to a low photocurrent (curve a). In the presence of AA, AA as electron donor could neutralize the photogenerated holes and thus inhibited the recombination of electron-hole, resulting in an enhanced signal (curve b). In the presence of both AA and TCEP, much higher signal was observed (curve c), which was due to the regeneration of AA by TCEP from the oxidized product DHA. Such a cycling provided a continuous supply of AA to contribute to the photocurrent generation. These results validated the feasibility of using this chemical RCA strategy to enhance the response of the Bi2S3/Bi2Sn2O7 electrode.

Figure 3. (a) Photocurrent of Bi2Sn2O7/ITO (curve a), Bi2S3/ITO (curve b) and Bi2S3/Bi2Sn2O7/ITO (curve c) in PBS (0.01 M, pH 7.4) solution including 0.1 M AA; (b) PEC responses obtained on Bi2S3/Bi2Sn2O7/ITO electrode in PBS solution (curve a), PBS solution

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including generated AA by enzymatic reaction of ALP (curve b) and PBS solution containing generated AA and 2.0 mM TCEP (curve c).

To study the performance of the proposed immunosensor, its PEC responses toward Myo of variable concentrations were recorded. As shown in Figure 4a, the signal gradually enhanced with the increase of Myo concentration, which was due to that the increased amount of Myo would cause more accumulation of AA and thus enhanced RCA for signal generation. Figure 4b shows the corresponding linear relationship ranged from 4.0 × 10-13 to 1.0 × 10-7 g/mL. The linear equation was I = 82.74 + 5.34 lg C with a correlation coefficient of 0.996, and the limit of detection (LOD) was experimentally found as 1.0 × 10-13 g/mL. This method exhibited a relatively wide linear range with a low detection limit than electrochemical biosensor,39,40 which were attributed to the effective signal amplification of photogenerated hole-induced chemical redox cycling and the excellent PEC behavior of the Bi2S3/Bi2Sn2O7 heterojunction. The selectivity of the immunosensor was then studied by using different kinds of interfering proteins including human serum albumin (HSA), human IgG (hIgG) and the mixture consisting of above proteins and target Myo, respectively. As shown in Figure 4c, a much stronger photocurrent appeared when Myo existed than those of HSA and hIgG alone, and the signal of the mixture was similar to that of target Myo, indicating the good selectivity of the immunosensor. Figure 4d shows the signal response from Bi2S3/Bi2Sn2O7/ITO electrode in experimental period of 300 s. No obvious change could be observed, indicating the good stability of the sensor. The feasibility of developed immunoassay for real sample was revealed by seven human serums samples. As shown in Table S1, the obtained results were in good agreement with the reference values from ROCHE ECL analyzer of Xinyang Central Hospital. The relative errors were within 5.3%, and the relative standard deviations (RSDs) were no larger than 5.2%. The recovery tests were conducted by spiking three concentrations of Myo in two serum samples. As shown in Table S2, the recovery ranged from 88.0% to 110.0%, and RSDs were no more than 5.5%. These results demonstrated the applicability of this system for serum sample assay.

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Figure 4. (a) Photocurrent of the immunosensor to variable concentrations of Myo; (b) The corresponding linear curve; (c) The selectivity test of the immunosensor for Myo assay, CHSA: 4.0 × 10-2 g/mL, ChIgG: 1.0 × 10-2 g/mL, CMyo: 1.0 × 10-9 g/mL; (d) The stability of Bi2S3/Bi2Sn2O7/ITO electrode in PBS solution including 0.1 M AA.

CONCLUSIONS In conclusion, on basis of the binary Bi2S3/Bi2Sn2O7 heterojunction photoelectrode, this work reported the ingenious combination of ALP-induced AA generation and chemical RCA strategy for novel split-type PEC immunoassay. Due to the efficient cycling of AA by TCEP from the oxidized product of DHA against the Bi2S3/Bi2Sn2O7 heterojunction electrode, enhanced signal could be achieved. Because of the efficient regeneration of signaling species in a separated environment, the developed PEC format could not only eliminate the common drawbacks in previous reports but also enable easy signal amplification for the sensitive immunoassay of Myo in real sample. This work features the first use of RCA strategy in PEC bioanalysis. We believe this work will provide a foothold for the future prosperity of various RCA-based PEC bioassays and broaden the perspective in the design and construction of ultrasensitive PEC bioanalytical protocols

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Supporting Information Experimental section, the synthesis and characterization of the Bi2S3/Bi2Sn2O7 heterojunction, the optimization of experimental conditions and the potential of this method for human serum sample detection. AUTHOR INFORMATION Corresponding Author * E-mail: [email protected] * E-mail: [email protected] * E-mail: [email protected]; [email protected] ORCID Jun-Tao Cao: 0000-0002-8983-4655 Yan-Ming Liu: 0000-0003-3381-2307 Wei-Wei Zhao: 0000-0002-8179-4775 Notes The authors declare no competing financial interest.

ACKNOWLEDGEMENT We gratefully appreciate the support from the National Natural Science Foundation of China (grant nos. 21675136 and 21675080), Plan for Scientific Innovation Talent of Henan Province (2017JR0016), the Natural Science Foundation of Jiangsu Province (grant BK20170073), Science & Technology Innovation Talents in Universities of Henan Province (grant 18HASTIT003), Funding Scheme for the Young Backbone Teachers of Higher Education Institutions in Henan Province (grant 2016GGJS-097) and the Nanhu Young Scholar Supporting Program of XYNU.

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Photogenerated Hole-induced Chemical Redox Cycling on Bi2S3

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