BiOI Z-Scheme

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Liposomes Mediated In Situ Formation of AgI/Ag/BiOI Z-Scheme Heterojunction on Foamed Nickel Electrode: A Proof-of-Concept Study for Cathodic Liposomal Photoelectrochemical Bioanalysis Si-Yuan Yu, Li-Ping Mei, Yi-Tong Xu, Tie-Ying Xue, GaoChao Fan, DeMan Han, Guangxu Chen, and Wei-Wei Zhao Anal. Chem., Just Accepted Manuscript • DOI: 10.1021/acs.analchem.9b00352 • Publication Date (Web): 01 Mar 2019 Downloaded from http://pubs.acs.org on March 4, 2019

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Analytical Chemistry

Liposomes Mediated In Situ Formation of AgI/Ag/BiOI Z-Scheme Heterojunction on Foamed Nickel Electrode: A Proof-of-Concept Study for Cathodic Liposomal Photoelectrochemical Bioanalysis Si-Yuan Yu,1,2,5 Li-Ping Mei,2,5 Yi-Tong Xu,2 Tie-Ying Xue,2 Gao-Chao Fan,3 De-Man Han,1,* Guangxu Chen,4,* Wei-Wei Zhao2,* 1Department

2State

of Chemistry, Taizhou University, Jiaojiang 318000, China

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

Chemical Engineering, Nanjing University, Nanjing 210023, China 3Shandong

Key Laboratory of Biochemical Analysis, College of Chemistry and Molecular

Engineering, Qingdao University of Science and Technology, Qingdao 266042, China 4Department

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

94305, United States 5These

authors contributed equally to this work.

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

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ABSTRACT: This work reports the liposomes mediated in situ formation of AgI/Ag/BiOI Z-scheme heterojunction on foamed nickel electrode for signal-on cathodic photoelectrochemical (PEC) bioanalysis. Specifically, in a proof-of-concept study, Ag nanoparticles (NPs)-encapsulated liposomes were initially confined via the sandwich immunobinding and then processed to release numerous Ag+ ions, which were then directed to react with the BiOI/Ni electrode, resulting the in situ generation of AgI/Ag/BiOI Z-scheme heterojunction on the electrode. The enhanced cathodic signal could be correlated to the target concentration, which thus underlay a novel signal-on cathodic liposomal PEC bioanalysis strategy. Different from previous anodic liposomal PEC bioanalysis, this work features the first cathodic liposomal PEC bioanalysis on the basis of in situ formation of a Z-scheme heterojunction. More generally, integrated with various biorecognition events, this protocol could serve as a common basis for addressing numerous targets of interest. KEYWORDS: Photoelectrochemical, Bioanalysis, Liposome, Ag nanoparticles, BiOI, Z-scheme Heterojunction


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Liposomal photoelectrochemical (PEC) bioanalysis is the new synergy of functional liposomes and PEC bioanalysis with complementary advantages.1-4 This frontier has been of great potential due to the versatility of functional liposomes5-7 and their diverse possibilities to interact with various semiconductors. In such a protocol, high loading of functional species within the liposomes possess high capacities for signal amplification and improvement of sensitivity. Besides, separation of biorecognition event from the signal transduction could in principle contribute to the selectivity and minimize the undesirable effects to the maximum extent. Comparing with traditional PEC bioanalysis,8-12 serious consideration of liposomes for PEC bioanalysis is quite recent.1-4 Existing reports have resorted to the use of enediol-ligands,1 dopamine,2 alkaline phosphatase3 and Cu nanoclusters4 to enhance or impair the photocurrent signaling. However, all these reports were based on the anodic mode, i.e., on the anodic responses of corresponding semiconductors. In contrast to the anodic mode, cathodic PEC bioanalysis uses photocathodes to convert the biorecogniton events into cathodic signals. Since the photocathodes are prone to interact with electron acceptors (e.g., dissolved O2) than with electron donors (e.g., ascorbic acid) in an electrolyte, the cathodic PEC bioanalysis has great capability in anti-interference from reductive substances. In contrast to current state-of-the-art anodic liposomal PEC bioanalysis, this work presents the concept of cathodic liposomal PEC bioanalysis, on the basis of Ag nanoparticles (NPs)-loaded liposomes mediated in situ formation of AgI/Ag/BiOI Z-scheme heterojunction on foamed nickel electrode. Different from the conventional type-II heterojunctions that 3 ACS Paragon Plus Environment


separates the photogenerated electron-hole pairs through the band alignment between two semiconductors, Z-scheme heterojunctions have a unique charge-carrier migration pathway that resembles the letter “Z”, with high efficacy for spatially separating the charge-carriers and optimizing the redox ability of the heterojunction photoelectrodes. To our knowledge, on the basis of in situ formation of a Z-scheme heterojunction, such a cathodic liposomal PEC bioanalysis has not been reported. RESULTS AND DISCUSSION Scheme 1. Schematic Illustration for the Cathodic Liposomal PEC Bioanalysis

To proof the concept, Ag NPs-encapsulated liposomes were initially prepared (denoted as ANL) and then labeled with goat IgG antibodies to fabricate the probe bioconjugates (denoted as Ab2-ANL). As shown in Scheme 1, the sandwich protein binding would confine the Ab2-ANL in the 96-well plate, while the subsequent lysis treatments would release the Ag NPs and numerous Ag+ ions, which were then subjected to interact with the BiOI/Ni electrode (see Supporting Information for Experimental Section). The reaction of Ag+ ions with BiOI would lead to the in situ generation of AgI/Ag/BiOI Z-scheme heterojunction on the electrode to enhance the original cathodic photocurrent of p-type BiOI. In such a protocol, the increased 4 ACS Paragon Plus Environment

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immunorecognition resulted in the enhanced confinement of the ANL label and thus more amount of Ag NPs. The cathodic PEC response of the electrode was then proportional to the quantity of Ag+ ions, which in turn depended on the amount of target antigen. As compared to those anodic counterparts, this work features the first cathodic liposomal PEC bioanalysis and is thus endowed with the general advantages of cathodic PEC bioanalysis.13-17

Figure 1. (a) TEM image of Ag NPs. Inset: the UV-vis absorption spectrum of Ag NPs. (b) TEM image of Ag NPs-encapsulated liposomes. Inset: DLS of Ag NPs-encapsulated liposomes. SEM images of BiOI/Ni electrode (c) before and (d) after AgI deposition. (e) XPS spectra of BiOI/Ni electrode before (curve a) and after (curve b) AgI deposition. (f) High resolution XPS spectrum of Ag 3d.

Experimentally, Ag NPs, and Ag NPs-encapsulated liposomes were prepared through borohydride reduction method18 and the lipid film hydration method,1 respectively, while BiOI/Ni electrode was fabricated via successive ionic layer adsorption and reaction (SILAR) approach,19 as displayed in Scheme S1. The morphology information and optical properties of the as-prepared Ag NPs and BiOI/Ni electrode were characterized by scanning electron microscopy (SEM), 5 ACS Paragon Plus Environment


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transmission electron microscopy (TEM) and UV-vis absorption spectrum. As shown in Figure 1a, the morphology of Ag NPs was determined by TEM measurement as monodispersed and quasi-spherical particles with a mean diameter of ~10 nm. The inset of Figure 1a indicated the corresponding characteristic symmetrical plasmon peak of Ag NPs at ~400 nm. As shown in Figure 1b of the TEM image of ANL, the presence of Ag NPs in the cavity of liposomes could be observed clearly. The average diameter of ca. 50 nm was smaller than ca. 87 nm of corresponding dynamic light scattering (DLS) results as shown in the Figure 1b inset, the difference of which could be attributed the shrinkage caused by vacuum TEM condition. As shown in Figure S1, foamed Ni electrode had a highly crossed three dimensional (3D) porous structure, which can be accessible for the deposition of BiOI. Figure 1c shows the unique interconnected network structures of the as-deposited BiOI nanosheets (NSs),16, 20-22 with lateral dimension in the micrometer size, height of several hundred nm and average thickness of ~30 nm. The feasibility of the design for PEC bioanalysis was then testified. Corresponding to 100 ng mL−1 antigen, Figure 1d demonstrated morphology of BiOI after incubation with corresponding lysis solution (Ag+). As shown, the rougher surface of BiOI was distributed with some small NPs, which should be the formation of AgI from in situ ion exchange synthesis.23 Figure S2 of elemental mapping also indicated a uniform distribution of Ag, Bi, I, and O elements in the sample. Figure S3 of the corresponding UV−vis diffuse reflectance spectra further reveals the enhanced absorption of the BiOI/Ni electrode after the incubation procedure. The surface chemical compositions and oxidation states of BiOI/Ni 6 ACS Paragon Plus Environment

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electrode before (curve a) and after (curve b) incubation with the lysis solution were then studied by X-ray photoelectron spectroscopy (XPS). As shown in Figure 1e, a new characteristic peak of Ag 3d emerged at around 368.5 eV, suggesting the presence of silver element on the electrode. Figure 1f reveals the high-resolution XPS spectrum of Ag 3d, which could be fitted to four peaks, the feature peaks located at 368.34 eV and 374.36 eV were assigned to characteristic peaks of Ag+ in AgI NPs.24,25 The other two peaks, 368.68 eV and 374.78 eV, demonstrated the existence of metallic Ag0 species, which was due to the reduction of absorbed Ag+ to Ag.26,27 All these results indicated the ion exchange between BiO+ and Ag+ as well as the reduction of absorbed Ag+ to Ag occurred on the surface of BiOI layers, resulting in the in situ formation of AgI and Ag NPs on the BiOI/Ni electrode. Incidentally, X-ray diffraction

(XRD)

and

electrochemical

impedance

spectroscopy

(EIS)

characterizations were also performed with the results shown in Figure S4 and Figure S5, respectively.



Figure 2. (a) Photocurrent responses of the foamed nickel electrode (curve a), after BiOI modification (curve b), after incubation with the lysis solution corresponding to 10 ng mL−1 antigen before (curve c), and after bubbling with highly pure nitrogen for 20 min (curve d). (b) The proposed mechanism for the enhancement of photocurrent response. (c) Photocurrent intensities after incubation with lysis solution corresponding to increased IgG antigen concentration. (d) The derived calibration curve. (e) The operational stability test of AgI/Ag/BiOI by repeated on/off illumination cycles. (f) The corresponding selectivity of the proposed immunoassay to IgG with 1 ng mL−1 by comparing to the interfering proteins at 100 ng mL−1 level: cTnI, PSA, p53, CEA, and IgA. ΔI is the photocurrent increment corresponding to the various antigen concentrations. The PEC tests were performed in 0.1 M Tris-HCl solution (pH 7.0) with 0.0 V applied voltage and 410 nm excitation light.

To reveal the light-harvesting properties of the electrode before and after AgI formation, their PEC behaviors were then characterized by chronoamperometric i−t curves from the stepwise transient photocurrent responses upon intermittent light irradiation. As shown in Figure 2a, bare foamed nickel electrode had no photocurrent response (curve a), while the BiOI modification led to an obvious cathodic photocurrent signal (curve b). Significantly, after incubation with the lysis solution corresponding to 10 ng mL−1 antigen, the electrode exhibited much enhanced cathodic photocurrent (curve c), which was due to the formation of AgI and Ag NPs on the BiOI/Ni electrode. If highly pure nitrogen (N2) was purged to deoxygenate the solution, the common O2-dependent suppression of the photocurrent was observed (curve d), indicating the dependence of the photocathode to dissolved O2. On the basis of all above results and the band positions of BiOI and AgI, the mechanism for the formation of an AgI/Ag/BiOI Z-scheme heterojunction was proposed as shown in Figure 2b. Note that the formation of a conventional p-n heterojunction was not suitable for explaining the enhanced cathodic photocurrent here, according to the conduction band (CB) and valence band (VB) positions of BiOI and AgI.28 However, in a AgI/Ag/BiOI Z-scheme heterojunction,24, 29-32 the photo-excited electrons on the 8 ACS Paragon Plus Environment

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CB of BiOI could easily flow into metallic Ag and then transferred to the VB of AgI. Meanwhile, the photo-generated electrons in the CB of AgI could react with dissolved O2 to produce •O2- due to its negative CB potential (-0.42 eV vs. NHE). To validate the formation of Z-scheme heterojunction, radical species trapping test was then performed. As illustrated in Figure S6 and the associated discussion, the generation of •O2- radicals was confirmed by the use of benzoquinone (BQ).32 Incidentally, the signal optimization of BiOI modification was also performed as shown in Figure S7. Since the extent of signal increase depended upon the antigen concentration, a signal-on cathodic PEC bioanalysis can be developed. Figures 2c exhibited the increment of photocurrent after reaction with lysis solution corresponding to various antigen concentrations. Figures 2d shows that the photocurrent increment linearly increased with the antigen concentrations from 100 fg mL−1 to 100 ng mL−1 and the lowest detection limit of IgG was estimated at 100 fg mL−1 (S/N=3), which was comparable to some recent reports as listed in Table S1. Essentially, upon the increased immunobinding, more sandwich immunocomplexes could be introduced and more Ag NPs would be released for ion-exchanging. The signal enhancement over 100 ng mL−1 became placid which should be attributed to the near saturation of the displacement process on BiOI surface. Figure 2e shows the signal response of the AgI/Ag/BiOI/Ni electrode in experimental period of 300 s. No obvious change could be observed, indicating the good stability of the sensor. To verify the selectivity, as shown in Figure 2f, cardiac troponin I (cTnI), prostatic specific antigen (PSA), p53, carcinoembryonic antigen (CEA), immunoglobulin A (IgA) were investigated as 9 ACS Paragon Plus Environment


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interference. And the photocurrent responses of interfering agents with the addition of 100-fold excess in comparison with the target IgG were very close to the blank test. As a proof-of-concept, these results proved the feasibility of the proposed liposomes-based PEC bioanalysis. CONCLUSIONS In short, this work first realized the cathodic liposomal PEC bioanalysis, on the basis of Ag NPs-encapsulated liposomes, sandwich protein binding and BiOI/Ni electrode. Through the sequential immunobinding, lysis treatments, and directed interaction between Ag+ ions and BiOI, the in situ formation of AgI/Ag/BiOI Z-scheme heterojunction on the electrode was characterized and confirmed by SEM, XPS, optical spectra and radical species trapping test. Proposed mechanism with specific charge transfer routes was also illustrated and applied for signal-on cathodic liposomal PEC bioanalysis. Exemplified by human IgG as a model target, the representative PEC immunoassay could achieve good analytical performance in terms of good sensitivity, selectivity and stability. This work features the in situ formation of a Z-scheme heterojunction that mediated by functional liposomes for cathodic PEC bioanalysis. More generally, the mechanism underlay a common basis for PEC bioanalysis providing that other biorecognition events, bismuth oxyhalide compounds,32 and ion exchange reactions33 are appropriately integrated. Also, we believe it will provide a foothold for the future prosperity of cathodic liposomal PEC bioanalysis as well as the innovative implementation of various Z-scheme heterojunction for advanced PEC bioanalysis. 10 ACS Paragon Plus Environment

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ASSOCIATED CONTENT Supporting Information The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.analchem…. Experimental section, schematic illustration for the fabrication of the electrode, SEM image of foamed nickel electrode, elemental mapping, DRS, XRD, EIS, corresponding active species trapping tests, the signal optimization of BiOI modification, and performance comparison (PDF) AUTHOR INFORMATION Corresponding Author *E-mail: [email protected]; [email protected] *E-mail: [email protected] *E-mail: [email protected] ORCID Wei-Wei Zhao: 0000-0002-8179-4775 Author Contributions S.-Y.Y. and L.-P.M contributed equally to this work. Notes The authors declare no competing financial interest. ACKNOWLEDGMENT



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TOC Graphic


BiOI Z-Scheme

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