Bismuth Oxyiodide Couples with Glucose Oxidase: A Special

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Bismuth Oxyiodide Couples with Glucose Oxidase: A Special Synergized Dual-catalysis Mechanism for Photoelectrochemical Enzymatic Bioanalysis Ling Zhang, Yi-Fan Ruan, Yan Yu Liang, Wei-Wei Zhao, Xiao-Dong Yu, Jing-Juan Xu, and Hong-Yuan Chen ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.7b17647 • Publication Date (Web): 10 Jan 2018 Downloaded from http://pubs.acs.org on January 10, 2018

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ACS Applied Materials & Interfaces

Bismuth Oxyiodide Couples with Glucose Oxidase: A Special Synergized Dual-catalysis Mechanism for Photoelectrochemical Enzymatic Bioanalysis Ling Zhang,†,‡,a Yi-Fan Ruan,‡,a Yan-Yu Liang,*,† Wei-Wei Zhao,*,‡,§ Xiao-Dong Yu,*, ‡ Jing-Juan Xu‡ and Hong-Yuan Chen‡ †

School of Materials Science and Technology, Nanjing University of Aeronautics and

Astronautics, Nanjing 211106, China ‡

State Key Laboratory of Analytical Chemistry for Life Science and Collaborative Innovation

Center of Chemistry for Life Science, School of Chemistry and Chemical Engineering, Nanjing University, Nanjing 210023, China §

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

94305, United States a. These authors contributed equally. * To whom correspondence should be addressed.

* E-mail: [email protected]

* E-mail: [email protected]; [email protected]

* E-mail: [email protected]

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ABSTRACT: On the basis of a special synergized dual-catalysis mechanism, this work reports the preparation of BiOI-based heterojunction and its use for cathodic photoelectrochemical (PEC) oxidase biosensing, which, unexpectedly, revealed that H2O2 impacted greater than O2. Specifically, BiOI layer was in situ formed on the substrate through an impregnating hydroxylation method for the following coupling with the model enzyme of glucose oxidases (GOx). The constructed cathodic PEC enzyme sensor exhibited good analytical performance of rapid response, high stability, and good selectivity. Especially, the glucose-induced H2O2controlled enhancement of the photocurrent was recorded, rather than the commonly observed O2-dependent suppression of the signal. This interesting phenomenon was attributed to a special synergized dual-catalysis mechanism. Briefly, this study is expected to provide a new BiOIbased photocathode for general PEC bioanalysis development, and to inspire more interests in the design and construction of novel heterojunction for advanced photocathodic bioanalysis. More importantly, the mechanism revealed here would offer a totally different perspective for the use of biomimetic catalyst in the design of future PEC enzymatic sensing and the understanding of relevant signaling routes as well as the implementation of innovative PEC devices.

KEYWORDS: Photoelectrochemical bioanalysis, Cathodic, BiOI, Glucose Oxidases, H2O2


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O2/H2O2 redox couple is of essential importance in numerous biological processes such as signaling, protein folding, cell apoptosis, etc.1,2 The studies on its functions in physiological and pathological pathways and its specific utilizations in biocatalytic and bioanalytical systems have long been an important theme.3,4 In analytical chemistry, integrated with different detection modules, the ingenious use of various oxidases, which typically catalyze a redox reaction with O2 reduced to H2O2, has led to the high prosperity of biosensor field.5-8 Photoelectrochemical (PEC) bioanalysis has recently emerged and attracted increasing interest due to its different signaling mechanism and the associated advantages.9-30 In PEC bioanalysis, various oxidases/nanomaterials nanoarchitectures have been constructed addressing different targets of interest.31-33 Significantly, in these reports, O2 has generally been found more efficient than H2O2 in different configurations.33 Specifically, with the increased concentration of enzyme substrates, O2-dependent suppression of the photocurrent has consistently been observed, which was caused by the competition between the O2-sensitive photoelectrodes and the enzyme-induced biocatalytic O2 reduction for the dissolved O2.31,33 Based on the photocurrent decrease, this concept of oxidase-based PEC biosensor has been widely applied and adapted, and the same phenomenon/mechanism have been confirmed/applied extensively by numerous groups.34-39 This article reports a quite different and unexpected phenomenon that contrary to the traditional cognition, i.e., H2O2 was found impact greater than O2 in an oxidase-based PEC bioanalytical system. In detail, glucose-controlled increase of the cathodic photocurrent was observed in a PEC bioanalytical system consisted of hierarchical nanostructured BiOI nanosheets/NiO film and GOx as the photocathode and oxidase, respectively. As shown in Scheme 1, on the hydrothermal derived NiO/indium tin oxide (ITO) electrode,40 the BiOI layer


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was in situ formed through an impregnating hydroxylation method.41 After GOx anchorage, the developed sensor was applied for the PEC detection of glucose (the experimental details were included in the Supporting Information). Unexpectedly, O2-dependent suppression of the photocurrent was not appeared, but conversely, the glucose-induced H2O2-controlled signal enhancement was observed. This unique result was attributed to a special synergized dualcatalysis mechanism as discussed thereinafter, and the resulted biosensor also exhibited good analytical performance. According to recent reviews about PEC enzymatic biosensors,31,32 such a photocathodic BiOI-based oxidase bioanalysis and the unique signaling behavior has not been reported. More importantly, the mechanism illuminated here would offer a totally different perspective for future design of PEC enzymatic biosensor and the understanding of relevant signaling principle as well as the implementation of innovative PEC devices. Scheme 1. The GOx/BiOI/NiO-Based Cathodic PEC Bioanalysis System

RESULTS AND DISCUSSION For better photoelectrodes, heterojunctions composed of hybrid semiconductors are being looked upon as favorite schemes. It is believed that the heterostructures could integrate different properties of the individual semiconductors and thus generate enhanced, or peculiar, properties for advanced applications.42-49 As aforementioned, herein we coupled BiOI with NiO as


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heterojunction photocathode, due to the high accessibility and balanced economics of NiO (ptype with a large band gap of 3.6-4.0 eV)50-53 and the desired visible absorption efficiency of BiOI (p-type with a narrow band gap of ~1.8 eV).54-56 In order to achieve better photocurrent responses, three layers of BiOI nanofilm on the NiO/ITO had been optimized as shown in Figure S1. Materials Characterizations. Figure 1A revealed the morphology of as-fabricated NiO/ITO electrode by scanning electron microscope (SEM). Similar to previous work,50-53 the nanostructured NiO thin film exhibited a highly crossed three-dimensional (3D) porous architecture that composed of densely interconnected nanoflakes. The accurate height of the film was determined as ca. 1.1 µm by the cross-sectional view as shown in Figure 1A inset. The highmagnification SEM image in Figure S2 shows that these nanoflakes have lateral dimension in the micrometer size, height of several hundred nm and thin thickness. Figure 1B demonstrated the morphology of hybrid BiOI/NiO nanofilm. It can be seen that, after depositing BiOI, the NiO nanofilm was covered by many self-assembled nanoplates with a dimension of several hundred nm. Furthermore, the cross-sectional view of the hybrid nanofilm in Figure 1B inset exhibited that the thickness of the composite film on ITO was increased to ca. 1.2 µm. Obviously, such a 3D porous structure with high surface area would benefit for the subsequent loading of guest enzyme species, and also be advantageous to the efficient charge separation and transfer of the photogenerated electron-hole pairs.54 The composition of the hybrid nanofilm was then determined by the energy-dispersive X-ray spectroscopy (EDX) with the result shown in Figure 1C, and the strong peaks matched very well with the elements of Bi, I, Ni, O and no other impurity peaks were observed in the sample. Figure 1D of the elemental mapping further indicated the uniform distribution of these elements in the sample, which also confirmed that the


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BiOI was successfully coupled onto the NiO nanosheets. Besides, as shown in Figure S3, X-ray diffraction (XRD) was utilized to identified the crystal structures of the as-fabricated NiO nanofilm, the BiOI on glass, and the hybrid BiOI/NiO nanofilm, respectively. And the transmission electron microcopy (TEM) measurements were further performed to reveal the morphology of the materials as shown in Figure S4.

Figure 1. (A) SEM image of the NiO nanofilm. Inset: the cross-sectional view. (B) SEM image of the BiOI/NiO modified ITO electrode. Inset: the cross-sectional view. (C) The corresponding EDX spectrum of the electrode. (D) The elemental mapping of the hybrid BiOI/NiO nanofilm. The surface chemical compositions and oxidation states of the BiOI/NiO nanofilm were also studied by X-ray photoelectron spectroscopy (XPS). Figure 2A revealed the coexistence of BiOI and NiO. The high-resolution XPS spectra of Bi 4f, I 3d, O 1s, C1S, Ni 2p were illustrated in Figure 2(B-F). As shown in Figure 2B, The Bi 4f spectrum can be fitted into four peaks. The peaks in 158.7 and 164.0 eV are assigned to Bi 4f7/2 and Bi 4f5/2, respectively, which are characteristic of Bi3+ in BiOI.41,57 And the other two peaks show a shift of 0.4 eV toward lower binding energy, which indicates the existence of lower charge Bi ions in the prepared BiOI nanoplates.58 As for the high-resolution spectra of I 3d in Figure 2C, signal with peaks located at


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618.6 and 630.0 eV are attributed to I 3d5/2 and I 3d3/2, respectively, which can be ascribed to Iin pure BiOI.59 The O 1s spectrum can be fitted into three peaks at binding energies of 528.59, 529.05, and 530.42 eV. The peaks at 528.59 eV can be assigned to bridging O in NiO crystals, and the peaks at higher binding energies of 529.05 eV can be ascribed to the Bi-O bonds of BiOI layered structure. While the peak at 530.42 eV is attributed to the hydroxyl group.59,60 The peak for C 1S in Figure 2E should be assigned to the adventitious hydrocarbon from the instrument. As shown in Figure 2F, the Ni 2p exhibited several peaks in the range of 850 to 890 Ev, which are attributed to Ni 2p signal of NiO.60 Specifically, the peaks centered at 853.5 eV and 860.4 eV corresponded to Ni 2p3/2 and its satellite. While the peaks located at 872.4 eV and 878.7 eV were attributed to Ni 2p1/2 and its satellite, respectively. To shed light on their optical properties, the UV-visible diffuse reflectance spectra of these samples were also recorded with the results shown in Figure S5.

Figure 2. (A) The full-scan XPS spectrum of the as-fabricated hybrid nanofilm and (B-F) the corresponding high-resolution XPS spectra of Bi 4f, I 3d, O 1s, C 1s and Ni 2p.


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PEC Behavior. To obtain more enriched information on the light-harvesting properties of the samples, their PEC behaviors were then characterized. Figure 3A reveals the operational stability of the photocurrent response of NiO electrode and BiOI/NiO electrode upon visible light illumination. As shown, upon irradiation, NiO/ITO electrode showed a very small cathodic photocurrent, whereas the BiOI/NiO exhibited much enhanced cathodic photocurrent under no biased potential, suggesting the successful sensitization effect and also the good charge transport within the composite. Specifically, upon illumination, the photogenerated electrons transferred from the conduction band (CB) of BiOI to the electron acceptors (here in the dissolved O2) in the electrolyte, with the photogenerated valence band (VB) holes transfer to the VB of NiO and then easily captured by the ITO electrode, generating the cathodic photocurrent. As shown, over 15 repeated on/off illumination cycles, the electrode displayed reproducible responses without any noticeable decrease during this period, indicating its high mechanical and photophysical stability in the PEC measurements. Besides, upon the onset/offset of irradiation, the rapid rise and fall of the signals also suggested the fast charge excitation, separation, and transfer process with the heterojunction. Besides, the dependence of photocurrent intensity upon the potential bias was further recorded as shown in Figure S6.


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Figure 3. (A) The operational stability of the hybrid BiOI/NiO nanofilm by repeated on/off illumination cycles. Inset: the stability of NiO electrode. (B) Photocurrent responses of NiO nanofilm electrode (a) before, (b) after BiOI, (c) after GOx modification, and (d) further with the addition of 0.1 mM glucose. The PEC tests were performed with 0.0V applied voltage and 410 nm excitation light in 0.1 M Tris-HCl solution (pH=7.0). Figure 3B shows the unique phenomenon in the application of the as-fabricated photocathode for PEC bioanalysis. As expected, compared with curve a of the NiO/ITO electrode, BiOI/NiO/ITO electrode showed much enhanced cathodic photocurrent as reflected by curve b. After anchoring GOx, as recorded by curve c, the photocurrent exhibited an obvious decrease, which could be attributed to the insulating effect of the anchored protein layer onto the surface of the BiOI/NiO/ITO photoelectrode.61 Remarkably, when the GOx modified electrode was further incubated with the 0.1 mM glucose, the common O2-dependent suppression of the photocurrent was not observed, but on the contrary an enhanced current was achieved, as demonstrated by curve d. This unexpected signaling may indicate a different possibility among the applied photocathode and the oxidase for PEC bioanalysis application.


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Analytical Performances. We continued with the biosensor feasibility study. As expected and shown in Figure 4A, the cathodic photocurrent intensity enhanced with the increased glucose concentration. Figure 4A inset presents the corresponding derived calibration curve. The percentage of the photocurrent increase was proportional to the logarithm of the glucose concentrations in the linear range from 0.005 to 10 mM, and the detection limit was experimentally found to be 1.6 µM, which was comparable to previous reports.37 By assaying 0.1 mM glucose with five sensors prepared at the same experiment conditions, a relative standard deviation (RSD) of 6.8% was obtained. The feasibility of the proposed protocol for practical application was evaluated by detecting the real sample of the glucose injections. As shown in Table S1, two different samples had been detected by a recovery experiment. And the proposed result indicated that the method was promising for biological applications. Regarding the selectivity, as shown in Figure 4B, various interfering substances including several kinds of amino acids, ascorbic acid and inorganic salts had no obvious effect on the photocurrent signal. Such a good selectivity should be attributed not only to the inherent specificity of enzyme but also to the use of cathodic photoelectrode system.39 Different from the photoanodes that sensitive to the various electron donors (e.g., ascorbic acid, dopamine, cysteine etc.), for photocathodes, the photoinduced electrons would immigrate to the semiconductor surfaces with the holes to the electrode, resulting in their preferable interactions with electron acceptors (e.g. dissolved O2) in the electrolyte solution rather than electron donors. All these results had corroborated the feasibility of such an analyte-controlled cathodic PEC enzymatic bioanalysis with positive relation.


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Figure 4. (A) Photocurrent responses of glucose with different concentrations. Inset: Plot of photocurrent increase rate with the glucose concentration. (B) Effect of 0.1 mM different substances on the photocurrent responses of the enzyme modified electrodes. I0 and I were the photocurrents of enzyme modified electrode before and after reaction with different substances, respectively. Mechanism Discussion. We then conduct the experiments to validate the possible mechanism. During the GOx-induced enzymatic conversion of glucose to gluconic acid, H2O2 will be generated from the reduction of dissolved O2, the consumption of which normally associates with the decrease of the O2-dependent photocurrents in previous reports.34,38 However, as demonstrated in present case above, the enhancement of the cathodic photocurrent was observed. To elucidate this unique phenomenon, control experiments were performed. The photocurrent responses of the bare BiOI/NiO/ITO electrode to dissolved O2, glucose and H2O2 were recorded in Figure 5A. As shown in curve a, the cathodic photocurrent intensity in the air-saturated 0.1 M Tris-HCl solution (pH=7.0) was ~1.19 µA, which was due to the presence of dissolved O2 as the electron acceptor. When the air-saturated buffer was bubbled with highly pure nitrogen for 20


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min, the cathodic photocurrent was almost totally inhibited as shown in curve b. After the addition of 0.1 mM glucose in the air-saturated and deaerated electrolyte, there was no obvious influence on initial currents, as demonstrated by curve c and curve d, respectively. Especially, after the introduction of 1.0 mM H2O2 into the air-saturated buffer, as shown in curve e, a muchenhanced cathodic photocurrent of ~3.91 µA was exhibited. After the electrolyte was further deoxygenated by highly pure nitrogen, as shown in curve f, the photocurrent only decreased to ~2.73 µA. All these results clearly indicated that H2O2 was more efficient than O2 in such a system. The dependence of photocurrent intensity on the concentration of H2O2 was further revealed as shown in Figure 5B. As manifested, the photocurrent intensity was proportional to the concentration of H2O2.

Figure 5. (A) Photocurrent responses of hybrid BiOI/NiO nanofilm in 0.1 M Tris-HCl solution (pH=7.0) (a) before and (b) after O2 off state, containing 0.1mM glucose (c) before and (d) after O2 off state, when 1 mM H2O2 was added (e) before and (f) after O2 off state. (B) Photocurrent responses of BiOI/NiO/ITO electrodes in air-saturated Tris-HCl solution (pH 7.0) containing


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different concentrations of H2O2 (0, 0.001, 0.01, 0.1, 1, 10mM). The PEC tests were performed with 0.0V applied voltage and 410 nm excitation light. Scheme 2. The Proposed Mechanism for Peroxidase-like Activity of BiOI Toward the In Situ Generated H2O2 in the GOx-based PEC Glucose Bioanalysis

Essentially, the generation of this interesting phenomenon was due to the peculiar interaction between the ternary semiconductor BiOI and the GOx catalytic reaction in such a hybrid PEC system. Specifically, in addition to the general semiconducting property, BiOI further exhibits superior photocatalytic property in terms of the peroxides-like catalytic performance.62 As illustrated in Scheme 2, this strong H2O2-dependent photocurrent change should be attributed to the following reasons: (i) Intrinsic peroxidase-like activity of BiOI are produced from the crystal growth and morphology transition mechanism. In detail, in the exposed (001) facets of BiOI, the Bi-O square anti-prism would result in many oxygen defects from the unstable bonds between the Bi atoms and O atoms, while the oxygen vacancies around Bi cations would lead to the formation of Bi(+3-x) species on the surface of BiOI, which would initiate the reduction reaction of H2O2 to produce active radicals.63,64 In order to determine the kind of active species, the active species trapping experiments were conducted by adding IPA (a quencher of •OH radicals) and


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BQ (a quencher of O2•- radicals) into the BiOI-H2O2-TMB system respectively.65 As shown in Figure 6, the absorbance at 652 nm of the BiOI- H2O2-TMB solution has no evident increase with the addition of BQ and the color of the solution has no obvious variation (Figure 6 inset). While the absorbance was greatly improved when the IPA was introduced in the same system with the color changed to light blue. These results demonstrated that it was the O2•- radicals generated in the reduction of H2O2 played an important role in the peroxidase mimic catalytic reaction for BiOI, which could rapidly oxidize TMB to a blue color oxidation of TMB oxide. In addition, as the main reactive oxygen species, O2•- radicals generated in the proposed system had been further confirmed via 5,5’-dimethyl-1-pirroline-N-oxide (DMPO) spin-trapping electron spin resonance (ESR) technology with the result presented in Figure S7. (ii) When light applied, BiOI nanoplates would simultaneously absorb incident photons and produce charge carriers, i.e., photo-induced electrons and holes in the conduction bands (CB) and valence bands (VB), respectively. The electrons in the CB of BiOI would be scavenged by H2O2 efficiently to form O2•-. While the holes would transfer from the VB of BiOI to the VB of NiO nanofilm and then easily be filled through electron transfer from the ITO electrode to generate cathodic photocurrent. Overall, both the two processes can cooperatively promote the reduction of H2O2 by the BiOI nanoplates to produce more O2•-, hence significantly enhancing the peroxidase-like catalytic activity. (iii) When GOx was integrated for glucose sensing, H2O2 would be produced from the oxidization of glucose in the presence of O2 via enzymatic reaction, and the in situ generated H2O2 would then promptly participate the above described two processes. The fast consumption of H2O2 would not only further promote the GOx catalytic reaction but also produce many highly reactive O2•-radicals, which may have effect on the oxidation-reduction


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center of GOx and further enhance the catalytic activity of GOx.10,66 In such a process, the high GOx efficiency would obviously be advantageous for better biosensor performance.

Figure 6. UV-vis absorbance at 652 nm and related color changes (inset) of 0.2 mg/mL TMB in blank with addition of 0.5 mM H2O2, the presence of scavengers of 0.5 mM BQ, 0.5 mM IPA and the absence of quencher in 0.1 M Tris-HCl solution (pH=7.0) with addition of 0.5 mM H2O2 and BiOI electrodes at room temperature. CONCLUSIONS

Inspired by its intriguing properties and potentials in PEC bioanalytical application, we developed the innovative heterostructured BiOI-based photocathode and tested it for cathodic PEC GOx sensing. Unexpectedly, the commonly recognized phenomenon of O2-dependent suppression of the signal was not observed, but conversely, the glucose-induced H2O2-controlled enhancement of the photocurrent was recorded. Control experiments were performed and reached the conclusion that the enzymatic product of H2O2 impacted greater than O2 in this system. This unique result was attributed to a special synergized dual-catalysis mechanism, i.e., the effect of the biological catalyst (GOx as the natural oxidase) was succeeded by that of biomimetic catalyst (BiOI as the peroxidase mimetics). In brief, such a BiOI-based cathodic PEC


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enzymatic biosensor has not been reported, and the resulted sensor also exhibited good performance. Most importantly, the mechanism revealed in this proof-of-concept would offer a totally different perspective for the use of BiOI (and its analogues) in the design of future PEC enzymatic biosensing and the understanding of relevant signaling routes. Harnessing such cascade-type reactions would in principle permit the operation of PEC bioanalysis under new (bio)chemical principles as well as the implementation of innovative PEC devices. ASSOCIATED CONTENT Supporting Information The Supporting Information is available free of charge on the ACS Publications website at DOI: Figures S1-S7, Table S1, chemicals and apparatus, synthesis of materials, the biosensor development process, SEM, XRD, TEM, UV-vis DRS, I–V characteristic curves, ESR, real samples detection. (PDF) AUTHOR INFORMATION Corresponding Author * E-mail: [email protected] * E-mail: [email protected]; [email protected] * E-mail: [email protected] Notes The authors declare no competing financial interest. ACKNOWLEDGMENT


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We thank the National Natural Science Foundation of China (Grant Nos. 21327902, 21675080), Natural Science Foundation of Jiangsu Province (Grant Nos. BK20161484, BK20170073), the Fundamental Research Funds for the Central Universities (Grant NO. NE2015003), the “Six Talent Peaks Program” of Jiangsu Province (Grant No. 2013-XNY-010), and the Scientific Research Foundation of Graduate School of Nanjing University (Grant 2016CL06). This work was also supported by a Project Funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions. REFERENCES (1) Chen, H. C.; Tian, J. G.; He, W. J.; Guo, Z. J. H2O2-activatable and O2-evolving nanoparticles for highly efficient and selective photodynamic therapy against hypoxic tumor cells. J. Am. Chem. Soc. 2015, 137, 1539-1547. (2) Hayyan, M.; Hashim, M. A.; AlNashef, I. M. Superoxide ion: generation and chemical implications. Chem. Rev. 2016, 116, 3029-3085. (3) Shu, J.; Qiu, Z. L.; Zhou, Q.; Lin, Y. X.; Lu, M. H.; Tang, D. P. Enzymatic oxydatetriggered self-illuminated photoelectrochemical sensing platform for portable immunoassay using digital multimeter. Anal. Chem. 2016, 88, 2958-2966. (4) Reuillard, B.; Ly, K. H.; Hildebrandt, P.; Jeuken, L. J. C.; Butt, J. N.; Reisner, E. High performance reduction of H2O2 with an electron transport decaheme cytochrome on a porous ITO electrode. J. Am. Chem. Soc. 2017, 139, 3324-3327. (5) Tel-Vered, R.; Yildiz, H. B.; Yan, Y.M.; Willner, I. Plugging into enzymes with light: photonic ‘‘wiring’’ of enzymes with electrodes for photobiofuel cells. Small. 2010, 15, 15931597.


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Bismuth Oxyiodide Couples with Glucose Oxidase: A Special

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