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Proton Transfer at Interaction Interface of Graphene Oxide Lie Wu, and Xiue Jiang Anal. Chem., Just Accepted Manuscript • DOI: 10.1021/acs.analchem.8b01596 • Publication Date (Web): 03 Aug 2018 Downloaded from http://pubs.acs.org on August 5, 2018

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Analytical Chemistry

Proton Transfer at Interaction Interface of Graphene Oxide Lie Wu,† Xiue Jiang∗,†,‡ †State Key Lab of Electroanalytical Chemistry, Changchun Institute of Applied Chemistry, Chinese Academy of Sciences, Changchun 130022, Jilin, China ‡University of Science and Technology of China, Hefei 230026, Anhui, China *Corresponding author: Changchun Institute of Applied Chemistry, Chinese Academy of Sciences, Changchun 130022, China; Phone: +86-431-85262069; e-mail: [email protected] ABSTRACT: Proton transfer plays a crucial role in a variety of biological phenomena. The transformation of nanomaterial in environment and biology makes probing the potential proton transfer between nanomaterials and biomolecules a crucial issue, but still remains a significant challenge. Here, we report proton transfer at interface of graphene oxide (GO) by studying the GO-induced vibrational changes of interfacial water and carboxyl-terminated self-assembled monolayer (SAM) with surface-enhanced infrared absorption (SEIRA) spectroscopy. In addition to simply act as a macromolecular buffer in solution, GO sheet behaves as a twodimensional hydrogen-bonded exchangeable proton pool to dissociate and transfer protons at interface with suitable Brønsted base pair, which may bear a significant potential toxic origin for biological systems with proton-coupled reactions.

Proton transfer is one of the most basic chemical reactions but plays central role in chemistry and biology.1 It is the key process in many biological phenomena, such as enzyme catalysis,2,3 signal transduction,4 and proton pumps of membrane proteins.5 Thus, unexpected proton transfer or disturbance of vital proton transfer pathway among biomolecules may be fatal to life. For example, the regulation of photocycle of membrane photoreceptor by transmembrane potential is based on the interplay between the change in local pH and the external electric field, and switch the protonation state of surface residues is believed to be a general mechanism to regulate the enzymatic reaction of membrane proteins.6 Likewise, the ultrahigh affinity of phosphatidylserine lipid in membrane towards copper ion is arose from the unquenchable surface potential upon ion binding, which is a result of the deprotonation of two phosphatidylserine molecules upon the bivalent binding of copper ion.7 Thus, protonation/deprotonation state of carboxylate and amino moieties of phosphatidylserine dramatically affect the interactions between copper ion and phosphatidylserine, which not only affect the physical properties of the membrane but also disrupt phosphatidylserine-dependent protein-membrane binding. It is also reported that local pH plays significant role in Na+ reabsorption in renal proximal tubule.8 Therefore, probing the potential proton transfer and/or local pH change result from external stimuli is of great significance. The booming of nanotechnology accelerates the transformation of nanomaterials in biology, which makes it significantly important to probe the potential proton transfer between biomolecules and nanomaterials. Graphene oxide (GO) possessing plenty of oxygen-containing functional groups, such as carboxyls on the edges and hydroxyls/epoxies on the basal plane,9 is an promising biomaterial with diversified applications.10 However, cytotoxicity of GO-based biomaterial poses a limitation of its possible application in biomedicine.11-13 So far, it is generally accepted that damaging biomembrane, cleaving and mutating DNA, and raising the level of intracellular reactive oxygen species (ROS) are the main cytotoxic origin of GO.11-17 However, GO is not only acidic in

nature due to the proton dissociation of its oxygenated functional groups,18,19 but also an excellent proton-conductive material with proton conductivity (σ) as high as 10-2 S cm-1.20 The proton conductivity of GO material is found to be anisotropic with respect to the conductive direction,20-22 and closely related to the multilayer assembly, interlayer distance, oxygen content and intercalation of hydrophilic materials.23-27 Thus, GO, which could be taken as a Brønsted acid, can potentially be involved in proton transfer process in biological milieu. High biocompatibility, ultra-sensitivity, high spatial-temporal resolution are essential qualities for small local pH sensing in biological systems. Fluorescence based optical technique is the most commonly used method for pH sensing in biological milieu by applying pH sensitive probes, including small molecular dyes, proteins, and nanoparticles.28,29 Nevertheless, it may suffer from quenching, photo-bleaching, and auto-fluorescence. Surfaceenhanced Raman spectroscopy (SERS)-based intracellular pH sensing is a noninvasive and high sensitive technique that overcomes these limitations.30,31 However, the spatial-temporal resolution is still limited. Microelectrode-based electrochemical sensors are capable to detect local pH transients in animal, but the drawback is their unclear underlying mechanism, substantial drift, and susceptibility to electronic noise.32 Magnetic resonance imaging (MRI) strategy is successfully applied to detecting localized pH changes in human brain.33 However, these method are established to detect pH changes and/or image pH distribution in cell or organ, and not well suited for proton transfer study. The structural information of proton donor and/or acceptor, especially the information of water structure, are missing in these strategies, which is of significant importance for proton transfer process (in SERS based sensor, the pH indicators selected are often not the proton donor and/or acceptor30,31). Infrared (IR) spectroscopy is a useful tool to determine the structures of acid and base in liquid solution from characteristic vibrational modes,34,35 and is capable of discerning the structural changes associated with proton transfer.36 With an enhancement factor of 10-1,000 by taking advantage of

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electromagnetic properties and near-field effects of nanostructured metal film,37-41 surface-enhanced infrared absorption (SEIRA) spectroscopy is an exquisite surface sensitive technique. Even 10-5 absorption change induced by external stimuli could be detected.6,42,43 Proton transfer in a monolayer of membrane protein was successfully probed by SEIRA spectroscopy.6,43 Carboxyl-terminated self-assembled monolayer (SAM) has been well investigated by SEIRA spectroscopy,44-49 changes of protonation state could be readily monitored by IR-active vibrational marker modes of protonated carboxyl group and deprotonated carboxylate group. Thus, carboxyl-terminated SAM is an ideal model for studying proton transfer. Here, GO and carboxyl-terminated SAM are chosen as potential Brønsted acid-base pair, and SEIRA spectroscopy is applied to probe the potential proton transfer.

EXPERIMENTAL SECTION Preparation and Characterization of GO Samples. Graphene oxide (GO) was prepared according to Marcano et al.50 Briefly, the mixture of (3.0 g) KMnO4 and (0.3 g) graphite flakes was added into the mixed acid of H2SO4/H3PO4 (36 mL/4 mL). The mixed solution was stirred for 20 h after heating to 50 °C, and then was cooled to room temperature. Oxidation reaction was terminated by adding excess H2O2. The as-obtained GO was centrifuged at 12000 rpm for 30 min to remove the solution, and washed in succession with 30% HCl, and ultrapure water. GO solution was obtained after dialysis against ultrapure water for 3 days. 3-(N-Morpholino) propanesulfonic acid (MOPS, ≥98%, Aladdin) and NaCl pre-treated GO samples were obtained similarly as previously reported.14 Briefly, MOPS solution and GO solution were mixed to reach a concentration of 0.5 mg/mL GO and 25 mM MOPS. The mixtures were stirred overnight and washed three times by repeated centrifugation, then dried in vacuum at 60 °C. NaCl pre-treated GO sample was obtained under the same procedure as MOPS pre-treated GO. The obtained GO samples were annotated as GO_ MOPS and GO_ NaCl, respectively. Ethylenediamine modified GO was prepared according to Hatakeyama et al23 with slight modification. Briefly, GO solution (5 mL, 0.8 mg/mL) and ethylenediamine (1 mL) were mixed and stirred for 5 h at room temperature. The mixture was thoroughly washed with ultrapure water by repeated centrifugation until the supernatant was neutral, and the sample obtained is referred as enGO. HCl-treated enGO was thoroughly washed with ultrapure water by repeated centrifugation until the supernatant was neutral, and the sample obtained is referred as H-enGO. Transmission electron microscopy (TEM) was performed on an H-600 electron microscope (Hitachi, Tokyo, Japan) operated at 75 keV. UV-Vis absorption spectrum was measured on LAMBDA 25 spectrometer (PerkinElmer, USA). The X-ray photoelectron spectroscopy (XPS) measurement was performed on an ESCALAB 250 X-ray photoelectron spectrometer with a monochromated X-ray source (AlKαhυ = 1486.6 eV). Atomic force microscopy (AFM) image was taken from multimode-V AFM (Veeco Instruments, USA) with tapping mode in air. Sample for AFM was prepared by depositing a dispersed GO solution on to a freshly cleaved mica surface and allow them to dry in air. Transmission infrared spectra were recorded on a VERTEX 70 Fourier transform infrared (FTIR) spectrometer (Bruker, Germany). Zeta potential was determined by dynamic light scattering using a Zetasizer (ZEN 3600, Malvern Instrument, UK). SEIRA Spectroscopy Setup. The experimental setup and procedures for preparing nanostructured Au film as enhanced substrate have been described elsewhere.14,42 Briefly, a thin gold film was deposited on the flat surface of a triangular silicon prism by chemical deposition. The surface of the Si substrate was polished with aluminum oxide powder of 1µm in size, followed by immer-

sion in a 40 wt% aqueous solution of NH4F for 1 min. Subsequently, the flat surface of the Si prism was exposed to a 1:1:1 volume mixture of (1) 0.03 M NaAuCl4, (2) 0.3 M Na2SO4 + 0.1 M Na2S2O3 + 0.1 M NH4Cl, and (3) 2.5 vol % HF solution for 60 s to get a shiny Au film. The electroless deposition reaction was stopped by thoroughly rinse with H2O. As-prepared Au film was electrochemically cleaned in 0.1 mol L-1 H2SO4 by electrochemical potential cycling between 0.1 V and 1.4 V (vs. Ag/AgCl). Then, the gold-coated prism was mounted into a house-made polytrifluorochloroethylene cell. SEIRA spectroscopy was performed with a Kretschmann-ATR configuration under an incidence angle of 60°. All spectra were recorded in a spectral window of 4000 cm-1 to 800 cm-1 with a resolution of 4 cm-1 using a FTIR spectrometer (IFS 66s/v, Bruker, Ettlingen, Germany) with a liquid nitrogen-cooled MCT detector. Typically, 512 scans were accumulated for one spectrum. Carboxyl-Terminated SAM Formation and Electrochemical Impedance Spectroscopy Characterization. After setup of SEIRA spectroscopy, the Au film was immersed in carboxylterminated thioalcohol solutions dissolved in ethanol for 35 min, 1 mM for 11-Mercaptoundecanoic acid (MUA, ≥98%, Sigma) and 10 mM for 3-Mercaptopropionic acid (MPA, ≥98%, Sigma). During this time, spectra were recorded at different time points with pure ethanol as a reference spectrum. After carboxyl-terminated SAM formation, the film was washed thoroughly with ethanol and dried under N2 stream. Electrochemical Impedance Spectroscopy (EIS) measurement was performed using a three-electrode configuration: the nanostructured Au film, a Pt-wire, and a Ag/AgCl (3 M KCl) electrode serving as working, counter, and reference electrodes, respectively (all potentials are referred to the Ag/AgCl electrode). EIS were recorded with PC controlled Potentiostat/Galvanostat (Metrohm Autolab AUT302N) with FRA32M module. Spectra were monitored in a frequency range of 0.1 to 10 kHz at open circle potential with an amplitude of 25 mV (rms value) in 10 mM KCl. SEIRA Difference Spectroscopy. To monitor the pH-Induced difference spectra of MUA SAM: after formation of a MUA SAM, the surface was immersed in H2O and equilibrated for certain time. Before sample spectra were acquired, a reference spectrum of MUA SAM immersed in H2O was recorded. Concomitant with the addition of HCl or NaOH solution (to reach a final concentration of 1 mM and 0.1 mM, respectively), a series of spectra has been recorded. To monitor the interaction between GO and carboxyl-terminated SAM: after formation of a carboxylterminated SAM, the surface was immersed in buffer and equilibrated with background solution for a certain time. Before sample spectra were acquired, a reference spectrum of background solution was recorded. Concomitant with the addition of GO solution (to reach a final concentration of 50 µg/mL), a series of spectra has been recorded. For control experiments, same amount solutions just without GO sheets were added. The pH of solutions used throughout all experiments was adjusted to 7.0 with HCl or NaOH. For HCOOH-induced difference spectra of MUA SAM, the MUA SAM was thoroughly rinsed with buffer and equilibrated for certain time before HCOOH solution was added to reach a final concentration of 50 µg/mL. Difference spectra were acquired by taking MUA SAM immersed in buffer as reference spectrum. For validate the effect of MOPS buffer on MUA SAM, the MUA SAM was thoroughly rinsed with H2O and equilibrated for certain time before MOPS buffer solution was added to reach a final concentration of 25 mM. MUA SAM incubated with H2O was recorded as references and the sample spectra were recorded after addition of MOPS buffer. For NaCl-induced difference spectra of MUA SAM, the MUA SAM was thoroughly rinsed with H2O or


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Analytical Chemistry MOPS buffer and equilibrated for a certain time before NaCl solution was added to reach a final concentration of 25 mM. MUA SAM incubated with H2O or MOPS buffer were recorded as references and the sample spectra were recorded after addition of NaCl. Quartz Crystal Microbalance with Dissipation (QCM-D) Monitoring. QCM-D experiments were performed with a QFM 401 flow module in Q-Sense Omega Auto instrument (Biolin Scientific, Sweden) under constant flow (50 µL/min) at 25 °C. Before the QCM-D experiments, the flow modules and sensors were first cleaned using a protocol in the QCM-D manual (manufacturer provided). To modify the sensor with MUA SAM, the Au-coated 4.95 MHz quartz crystal sensor (QSX301, Biolin Scientific) was immersed in 1 mM MUA in ethanol for 35 min, then thoroughly washed with ethanol and dried with N2 stream. All the sensor used are freshly ordered, and used only once. The measurements were performed at several harmonics (z= 3, 5, 7, 9, 11, and 13). All presented QCM-D data were recorded at the seventh harmonic, and frequency shifts were normalized by division with 7. The buffer solution used is 10 mM MOPS (pH 7.0). In QCM-D experiments, water was flowed across the sensor surface for initial stabilization while monitoring frequency and dissipation signals at the seventh overtone. The sensor surfaces were then rinsed with background solution until stabilized. To characterize the pHinduced hydration state changes of MUA SAM, 10 mM MOPS buffer with different pH (4, 7, 9) were introduced successively and the frequency and dispassion changes were recorded. For monitor the adsorption of GO sheet on MUA SAM, the MUA SAM modified sensor was rinsed with water and then 10 mM MOPS buffer (pH 7.0). Once a stable baseline was obtained, 50 µg/mL GO dispersed in 10 mM MOPS buffer (pH 7.0) was introduced into the flow chamber for 90 min, and the frequency and dispassion changes were recorded. After the adsorption of GO, 10 mM MOPS buffer (pH 7.0) was introduced to remove the free GO. AFM and Raman Characterizing the Adsorbed GO on MUA SAM. After the QCM-D experiment, the sensor was retrieved and dried in air. Then, the sensor was characterized by AFM and Raman spectroscopy to confirm the adsorption of GO sheet on MUA SAM. AFM image was taken from multimode-V AFM (Veeco Instruments, USA) with tapping mode in air. Raman spectrum of GO was obtain by RM-1000 laser confocal Raman micro-spectroscopy (Renishaw, U.K.) with 514 nm excitation. SEIRA Spectrum of GO Sheets in Solution. Taking bare Au film in air as reference spectrum, the SEIRA spectrum of pure H2O, 25 mM NaCl solution, GO in H2O solution, and GO in 25 mM NaCl solution were obtained by adding corresponding solution as sample spectra. SEIRA spectrum of GO sheets in solution was extracted by subtracting SEIRA spectrum of pure H2O or 25 mM NaCl solution from GO in H2O solution or GO in 25 mM NaCl solution, respectively.

RESULTS AND DISCUSSION GO sheets protonate MUA monolayer. Mercaptoundecanoic acid (MUA), a long chain (11 carbon atoms) thioalcohol with a terminal COOH group, which could readily form a dense monolayer on gold surface by self-assembly, is chosen as a model carboxylate interface. The formation of MUA SAM was confirmed by electrochemical impedance spectroscopy (EIS) (Figure S-1) and further characterized in situ by SEIRA spectroscopy (Figure 1a, lower panel and Figure S-2). The SEIRA spectrum of MUA SAM exhibits typical peaks in ν (CHn) region at 2920 cm-1 and 2850 cm-1 assigned to the νas (CH2) and νs (CH2) modes of the

Figure 1. GO sheets protonate MUA monolayer. (a-b), GOinduced SEIRA difference spectra of MUA SAM (a) and interfacial water (b) with MUA SAM immersed in 10 mM MOPS buffer as background spectrum; dark cyan line is the spectrum of MUA SAM with bare Au film immersed in ethanol as background spectrum (spectrum before 1650 cm-1 is scaled by 1/10 while after is scalded by 1/2); (c-d), HCl-induced SEIRA difference spectra of MUA SAM (c) and interfacial water (d) with MUA SAM immersed in H2O as background spectrum. Spectra shown from bottom to top were recorded at 1 min, 5 min, 10 min, 30 min, 60 min, and 90 min for (a, c), and 1 min, 2 min, 3 min for (b, d) right after the addition of GO (a, b) or HCl(c, d), respectively. (e), SEIRA spectrum of GO sheet in solution, obtained by subtracting SEIRA spectrum of GO solution and pure H2O; the corresponding SEIRA spectrum of GO solution and pure H2O are presented in Figure S-11. CH2 groups of MUA molecules, respectively. The fingerprint region shows characteristic peaks in ν (C=O) region (orange box) and ν (COO-) region (green box), which are attributed to ν (C=O) mode of the COOH groups, νas (COO-) and νs (COO-) modes of COO- groups at 1572 cm-1 and 1410 cm-1, respectively (detailed discussion is given in Figure S-2). After that, the spectrum of MUA modified Au surface immersed in buffer was taken as reference and then series SEIRA spectra were recorded after addition of fully characterized GO (Figure S-3 and S-4) at concentration of 50 µg/mL (Figure 1a, upper panel). In addition to an obvious positive peak at ν (C=O) region, two negative peaks are simultaneously observed in ν (COO-) region relative to control spectra without GO (Figure S-5), which are possibly originated from the consumed species and/or conformation (surface dipole selection rule) 51,52 and distance (optical near-field effect)37,53 changes of surface adsorbed species. However, the absence of spectral change in ν (CHn) region (blue box) eliminates the possibility of conformation and distance changes of MUA SAM. Thus, the negative peaks in GO-induced difference spectra of MUA SAM are ascribed to the consumed carboxylate groups. Considering the simultaneous appearance of positive peak in ν (C=O) region (orange box), it is easily to conclude that the consumed COO- groups were converted to COOH groups. To validate this possibility, pH-induced (de)-protonation of MUA SAM is monitored by SEIRA spectroscopy (Figure 1c-d



and Figure S-6). When H+ is added, the pH value of solution is lowered and de-protonated COO- group is converted to protonated COOH group (Figure 1c), resulting in enhanced intensity of COOH marker band (orange box) and decreased intensity of COO- marker bands (green box), which are basically consistent with the GO-induced difference spectra (Figure 1a). At the same time, protonation will decrease the negative surface charge, and thus lower the hydration degree of MUA SAM54 as revealed by highly sensitive quartz crystal microbalance with dissipation monitoring (QCM-D) (Figure S-7), resulting in a negative peak in interfacial water region (Figure 1d, purple box) (a discussion of pH-induced interfacial water change of MUA SAM is given in Supplementary Note 1). However, positive peak is observed in GO-induced difference spectra of MUA SAM (Figure 1b, purple box). Since MOPS buffer neither has specific effect on both GO and MUA SAM (Figure S-8 and S-9) nor has specific influence on GO-induced difference spectra of MUA SAM (Figure S-10), such inconsistency might be originated from the influence of surface-adsorbed GO. GO sheets adsorb on MUA monolayer. Figure 2a shows the frequency (f) and dissipation (D) shifts recorded during the exposure of MUA SAM to GO in 10 mM MOPS buffer by QCM-D. Concomitant with the introduction of GO, an obvious decrease in ∆ f and increase in ∆ D are observed immediately until to gradual saturation at 90 min. After the constant flow was changed to buffer solution without GO for thoroughly washing the sensor surface (for nearly 2 h) to diminish the effect of density, viscosity, elasticity of buffer solution originated from the dispersed GO sheets, the amplitudes in the changes of ∆ f and ∆ D are decreased, but cannot return back to the initial baseline (a discussion of the QCM-D data is given in Supplementary Note 2). This clearly indicates that GO sheets indeed adsorb on MUA SAM during interaction. The sensor that was incubated with GO solution followed thorough

Figure 2. GO sheets adsorb on MUA monolayer. (a), QCM-D monitoring the adsorption of GO on MUA SAM; blue line is the frequency shift and red line is the dissipation change recorded during the exposure of MUA SAM to GO in 10 mM MOPS buffer, the presented data were recorded at the seventh harmonic; (b), Raman spectra of MUA SAM modified Au-coated QCM-D sensor before (black line) and after (red line) exposure to GO; the blue line is Raman spectrum of MUA SAM adsorbed GO, which is obtained by subtracting red line with black line. Peaks centered at 1606 cm-1 and 1351 cm-1 are assigned to the G band and D band of GO, respectively; (c-d), AFM images of Au-coated QCMD sensor surface (c) and MUA SAM modified Au-coated QCM-D sensor surface after interaction with GO (d).

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washing shows typical Raman absorption of GO (Figure 2b) and AFM image of GO (Figure 2c, d), further proving the adsorption of GO. Thus, the surface-adsorbed GO sheets would induce additional IR absorption in GO-induced difference spectra of MUA SAM. SEIRA spectrum of GO sheet in solution, shown in Figure 1e, exhibits ν (OH) at 3200 cm-1 to 3700 cm-1, δ (OH) band overlapped with ν (sp2-C) band around 1650 cm-1, and ν (C=O) band at 1724 cm-1 (detailed peak assignment is given in Figure S-11). On one hand, the IR absorption at 3200 cm-1 to 3700 cm-1 region from surface-adsorbed GO sheets partially account for the positive peak observed in GO-induced difference spectra of MUA SAM (Figure 1b, purple box). On the other hand, the adsorbed GO could also disturb the hydration state at the interface of MUA SAM upon protonation, inducing a significant change in the absorbance of interfacial water. Therefore, given the similar characteristic changes in the fingerprint region between GO and protonation-induced SEIRA difference spectra of MUA SAM, it is reasonable to conclude that adding GO lowers the pH value of buffer solution due to the acidity of GO solution, triggering the protonation process although the δ (OH) band and characteristic ν (C=O) peak shown in the SEIRA spectrum of GO sheet in solution could lead to slight difference in the peak around 1650 cm-1 upon the adsorption of GO. Proton transfer at interaction interface of GO. Interestingly, it is found that GO is still capable of inducing robust protonation of MUA SAM when the concentration of MOPS solution was increased to 50 mM to enhance the buffering capability (Figure 3b, c). This is dramatically different from organic acid HCOOH, a simplified acidic group analog of GO under the same condition, although the acidity origin of GO is much more complicated. Protonation of MUA SAM induced by addition of 50 µg/mL HCOOH into 10 mM MOPS buffer (Figure S-12) disappeared in 50 mM MOPS buffer (Figure 3d, e) due to the negligible pH change (∆ pH = -0.02). On the contrary, GO is still capable of inducing robust protonation of MUA SAM in 50 mM MOPS (Figure 3b, c) though the pH of bulk solution is barely changed (∆ pH = -0.01). This indicates that the mechanism of GO-induced protonation of MUA SAM is different from that induced by HCOOH, which is simply from a change in solution pH, possibly due to the unique structure of GO. GO holds an atomically thin two-dimensional structure with a range of oxygen-containing functional groups, the dissociation of these oxygenated functional groups makes GO acid.9,18,19 The dissociable proton density of GO is estimated to be one proton per 17 carbon atoms semi-quantitatively,18,55 which may come from three different pathways based on different chemical structure models of GO: 1) dissociation of COOH group located at the edge of GO sheet;56 2) dissociation of phenolic/enolic groups randomly distributed on the surface of GO sheet;57 3) dissociation of vinylogous carboxylic acids that formed through reactions of GO sheet with water and protons generated during the reaction.18 These ionizable acidic groups are located on the adjacent or conjugated carbon atoms with different microenvironments, affecting each other’s ionization. For GO in solution, part of dissociated protons diffuses into bulk solution, making GO solution acid; while part of dissociated protons associates within the GO/water interface as revealed by Dimiev et al through co-precipitation of GO with protons.18 Furthermore, these oxygen-containing functional groups endow GO with excellent proton conductivity, among which carboxylate and epoxy groups are believe to be major contributor to efficient proton transport at the edge and interior of GO sheet, respectively.23,58,59 Due to the unique ultra-thin structure of GO sheet, the disassociated protons at GO/water interface form weak hydrogen bonding with surface adsorbed water molecules


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Figure 3. Proton transfer at interaction interface of GO. (a), Effect of NaCl on GO/water interface; (b-e), GO (b, c) and HCOOH (d, e)induced SEIRA difference spectra of MUA SAM (b, d) and interfacial water (c, e) with MUA SAM immersed in 50 mM MOPS buffer as background spectrum; (f-i), GO-induced difference spectra of MUA SAM in water (f, g) and in 10 mM MOPS buffer (h, i) without (f, h) and with (g, i) 25 mM NaCl with MUA SAM immersed in corresponding solution as background spectrum; (j, k), SEIRA difference spectra of MUA SAM induced by enGO (j) and H-enGO (k) in 10 mM MOPS buffer with MUA SAM immersed in corresponding solution as background spectrum. Spectra shown from bottom to top were recorded at 1 min, 5 min, 10 min, 30 min, 60 min, and 90 min for (b, d, f-k), and 1 min, 2 min, 3 min for (c, e) right after the addition of GO sample, respectively . and those closely located oxygenated functional groups, and propagate in the flat carbon network by gradually reforming these bonds. The acidic nature and high proton conductivity makes GO sheet in solution may behaves as a two-dimensional hydrogenbonded exchangeable proton pool. Such proton pool is capable of dissociating and transferring protons at interaction interface in the presence of suitable Brønsted base pair. Thus, it is proposed that, in addition to lower the pH value of bulk solution, GO may transfer the proton to deprotonated MUA molecule at GO/water/MUA SAM interface. To validate the proposed proton transfer at interaction interface of GO, the effect of interfacial proton and proton conductivity of GO on the protonation of MUA monolayer are investigated. Introducing of Na+ would replace the proton at GO/water interface (Figure 3a), decreasing proton density at GO/water interface and acidifying the bulk solution.18 As shown in Figure 3f and g, GOinduced protonation of MUA SAM is enhanced by NaCl in nonbuffered condition. However, in buffered condition, the acidification capability of the dissociated protons towards bulk solution is negligible while the proton density at GO/water interface decreases significantly. Thus, the extent of GO-induced protonation of MUA SAM in the presence of NaCl is weaker than that in the absence of NaCl in buffered condition (Figure 3h and i). Though introduction of Na+ facilitates de-protonation of COOH group60 and decreases apparent pKa of carboxylic acid in MUA SAM,61,62 the influence are the same in buffered and non-buffered conditions (shown in Figure S-13). Besides, the proton conductivity of GO is decreased from 6.7 × 10-4 S cm-1 to 6.2 × 10-5 S cm-1 in the presence of NaCl (Figure S-14), due possible to the nonspecific adsorption of Na+ on charged GO surface since the same phenomenon was also observed by Hatakeyama et al in GO with Na2SO4.63 Thus, the decreasing of proton conductivity may also

contribute to the observed weaker protonation of MUA SAM by GO in buffered condition with NaCl. To identify the contribution of proton conductivity on the protonation effect of GO, GO was modified with ethylenediamine (enGO) (Figure S-15). Treatment with ethylenediamine effectively blocks the epoxy sites which is the main contributor for proton conductivity and dramatically decreases the proton conductivity of GO.23 As shown in Figure 3j, enGO-induced protonation of MUA SAM is observably weaker than that of GO under the same condition. And two small peaks is observed in the ν (CHn) region in Figure 3j and k, which are assigned to the νas (CH2) and νs (CH2) of ethylenediamine, respectively. The presence of these two peaks is also an indicator of successful modification of GO with ethylenediamine and the absorption of enGO on MUA SAM. However, modification of GO with ethylenediamine would inevitably neutralize protons associated within the GO/water interface, since ethylenediamine is an organic base. Therefore, as-prepared enGO was further treated with HCl to replenish with proton. Interestingly, the protonation effect of H-enGO is recovered from enGO, and nearly the same as pristine GO under the same condition (Figure 3k). It is noted that modifying ethylenediamine also destroy carboxyl groups in a certain extent, since the intensity of ν (C=O) peak decrease in enGO sample and does not return back to its initial level after HCl treatment (Figure S-15c). This indicates that replenished protons are indeed associated within the GO/water interface, and the proton density at interface plays significant role in the proton transfer at interface of GO. This results also implies that GO could serve as a proton vector in solution, which is in consistent with proposed two-dimensional hydrogenbonded exchangeable proton pool of GO. Based on the recovered protonation effect of H-enGO sample, we believe that blocking



epoxy groups and decreasing proton conductivity has no influence on the protonation effect of GO. This conclusion is also supported by the same protonation effect of freshly prepared GO and aged GO samples (Figure S-16). Epoxy group of GO is metastable at room temperature and undergoes self-limiting decomposition processes with a relaxation half-lifetime of about one month,22,64 also the proton conductivity of GO material decreases with aging due to the decomposition of epoxy groups.65 However, no obvious difference is observed in SEIRA difference spectra of MUA SAM induced by fresh GO and aged GO (Figure S-16). Though decreasing of proton conductivity has no influence on the proton transfer of GO, we believe that the proton conductivity is the physical and chemical base for the proposed two-dimensional hydrogen-bonded exchangeable proton pool of GO and the observed proton transfer at interface. The acidic nature provides the protons to transfer while proton conductivity supports the protons to transport over GO/water interface and transfer toward other object. Thus, the proton conductivity should be closely related to the kinetics of proton transfer, while proton density at interface and hydrogen bonding network of interfacial water govern the observed proton transfer of GO at interaction interface. It should be pointed out that GO processes intrinsic hydrophobicity due to the sp2-bonded graphite region, when dispersed in solution, the hydrogen bonding of H2O molecules that adsorbed on surface of GO is relative weaker than those in bulk solution, indicated by the higher wavenumber of ν (OH) peaks of GO surface-adsorbed H2O than H2O in bulk (shown in Figure S-11, black line and blue line). Such relatively weak hydrogen bonding network of H2O molecule on GO surface may facilitate the proton transportation over the surface of GO and transfer at the interaction interface, as loose hydrogen bond network of confined water molecules is reported to be the possible origin of ultrafast water transport in carbon nanotubes (CNTs).66,67 This may help to understand the humidification and temperature dependent proton conductivity: H2O molecules bind to GO sheets through a strong hydrogen bonding at low humidity, while at high humidity the active sites on the GO sheets become saturated and excess water molecules bind through relative weak hydrogen bonding which are easier to rotate and diffuse. And the overall hydrogen bonding network weakens as temperature increases. Besides, exposure to GO might make the interfacial micro-environment of MUA SAM more hydrophobic indicated by the relative high wavenumber of ν (OH) peaks in GO-induced SEIRA difference spectra (Figure 1a). Though GO-induced interfacial water change is an integrated result of surface-adsorbed GO sheets and disturbed hydration state of MUA SAM, the weak hydrogen bonding network of interfacial water may facilitate the proton transfer between GO and MUA monolayer. Moreover, the hydrogen bonding network of both H2O molecule adsorbed on GO surface and GO-induced interfacial water change of MUA SAM are stronger in the presence of NaCl than in the absence (Figure S-17 and S-18). This might be partially account for the decreased proton conductivity of GO in the presence of NaCl. It also should be noted that the surface pKa of MUA SAM on “rough” surface is reported to be in the range of 5.7-6.3,61,62,68,69 which is higher than that of free MUA in bulk phase (pKa in solution 4.870). It has the possibility that the increased pKa value makes the proton transfer possible between GO and MUA SAM. However, proton transfer is also observed between GO and MPA SAM (contains only three carbon atoms) (Figure S-19), whose surface pKa is reported to be 5.2.71 Though it is of great difficulty to precisely determine the surface pKa of GO sheet in solution, the overall pKa value of GO in solution is reported to be in the range of 3.7-4.18,55 Such a value is lower than many pKa values of ioniz-

able groups of biomolecules, such as proteins.72 Thus, we speculate that such proton transfer at interaction interface of GO is a universal phenomenon, exiting in various nano-bio interface of GO.

CONCLUSION In summary, by application of SEIRA spectroscopy, we report the proton transfer at interface of GO for the first time through taking GO and carboxyl-terminated SAM as potential Brønsted acid-base pair. GO sheet in solution behaves as a two-dimensional hydrogen-bonded exchangeable proton pool, and is capable of dissociating and transferring protons at interface in the presence of suitable Brønsted base pair. Our works not only greatly deepen the understanding of the nano-bio interface, but also imply that proton transfer at nano-bio interface of GO might be a neglected origin of its biological toxicity.

ASSOCIATED CONTENT Supporting Information The Supporting Information is available free of charge on the ACS Publications website. Supplementing Experiments: Proton conductivity measurement of GO, GO_NaCl, GO_MPA, and GO_HCOOH films. Supplementing Figures: characterization of carboxyl-terminated SAMs and GO sampels; MOPS buffer-induced SEIRA difference spectra of MUA SAM; SEIRA spectroscopy and QCM-D monitor pH-induced (de)-protonation of MUA SAM; FTIR Spectra of MOPS, GO, GO_MOPS, GO_NaCl, enGO, and H-enGO; effect of MOPS buffer on MUA SAM; GO-induced SEIRA difference spectra of MUA SAM in different buffer solutions, SEIRA spectra of H2O, NaCl solution, GO in H2O and NaCl solution, GO sheets in H2O and NaCl solution; HCOOH and NaCl-induced SEIRA difference spectra of MUA SAM; proton conductivity of GO samples; protonation effect of freshly prepared GO and aged GO samples; GO-induced interfacial water change of MUA SAM in 10 mM MOPS with and without NaCl; GO-induced SEIRA difference spectra of MPA SAM. Supplementing Notes: about pH-induced interfacial water change of MUA SAM and QCM-D monitoring the adsorption of GO on MUA SAM.

AUTHOR INFORMATION Corresponding Author *E-mail: [email protected]

Notes The authors declare no competing financial interest.

ACKNOWLEDGMENT This work was financially supported by the National Natural Science Foundation of China (21675149, 21705146, 21761132028), the Key Research Program of Frontier Sciences, CAS (QYZDYSSW-SLH019), the Natural Science Foundation of Jilin Province (20170414037GH, 20170520133JH), and the K.C. Wong Education Foundation.

REFERENCES (1) Hynes, J. T. Nature 1999, 397, 565-567. (2) Sigala, P. A.; Fafarman, A. T.; Schwans, J. P.; Fried, S. D.; Fenn, T. D.; Caaveiro, J. M. M.; Pybus, B.; Ringe, D.; Petsko, G. A.; Boxer, S. G.; Herschlag, D. Proc. Natl. Acad. Sci. USA 2013, 110, E2552-E2561. (3) Stock, D.; Leslie, A. G. W.; Walker, J. E. Science 1999, 286, 1700-1705.


Page 6 of 9

Page 7 of 9 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Analytical Chemistry (4) Stoner-Ma, D.; Jaye, A. A.; Matousek, P.; Towrie, M.; Meech, S. R.; Tonge, P. J. J. Am. Chem. Soc. 2005, 127, 2864-2865. (5) Belevich, I.; Verkhovsky, M. I.; Wikström, M. Nature 2006, 440, 829-832. (6) Jiang, X.; Engelhard, M.; Ataka, K.; Heberle, J. J. Am. Chem. Soc. 2010, 132, 10808-10815. (7) Cong, X.; Poyton, M. F.; Baxter, A. J.; Pullanchery, S.; Cremer, P. S. J. Am. Chem. Soc. 2015, 137, 7785-7792. (8) Brasen, J. C.; Burford, J. L.; McDonough, A. A.; HolsteinRathlou, N.-H.; Peti-Peterdi, J. Am. J. Physiol. Renal. Physiol. 2014, 307, F1249-F1262. (9) Dreyer, D. R.; Park, S.; Bielawski, C. W.; Ruoff, R. S. Chem. Soc. Rev. 2010, 39, 228-240. (10) Chung, C.; Kim, Y.-K.; Shin, D.; Ryoo, S.-R.; Hong, B. H.; Min, D.-H. Acc. Chem. Res. 2013, 46, 2211-2224. (11) Sanchez, V. C.; Jachak, A.; Hurt, R. H.; Kane, A. B. Chem. Res. Toxicol. 2012, 25, 15-34. (12) Bianco, A. Angew. Chem., Int. Ed. 2013, 52, 4986-4997. (13) Seabra, A. B.; Paula, A. J.; de Lima, R.; Alves, O. L.; Durán, N. Chem. Res. Toxicol. 2014, 27, 159-168. (14) Wu, L.; Zeng, L.; Jiang, X. J. Am. Chem. Soc. 2015, 137, 10052-10055. (15) Ren, H.; Wang, C.; Zhang, J.; Zhou, X.; Xu, D.; Zheng, J.; Guo, S.; Zhang, J. ACS Nano 2010, 4, 7169-7174. (16) Liu, Y.; Luo, Y.; Wu, J.; Wang, Y.; Yang, X.; Yang, R.; Wang, B.; Yang, J.; Zhang, N. Sci. Rep. 2013, 3, 3469. (17) Tu, Y. S.; Lv, M.; Xiu, P.; Huynh, T.; Zhang, M.; Castelli, M.; Liu, Z. R.; Huang, Q.; Fan, C. H.; Fang, H. P.; Zhou, R. H. Nat. Nanotechnol. 2013, 8, 594-601. (18) Dimiev, A. M.; Alemany, L. B.; Tour, J. M. ACS Nano 2013, 7, 576-588. (19) Petit, C.; Seredych, M.; Bandosz, T. J. J. Mater. Chem. 2009, 19, 9176-9185. (20) Karim, M. R.; Hatakeyama, K.; Matsui, T.; Takehira, H.; Taniguchi, T.; Koinuma, M.; Matsumoto, Y.; Akutagawa, T.; Nakamura, T.; Noro, S.-i.; Yamada, T.; Kitagawa, H.; Hayami, S. J. Am. Chem. Soc. 2013, 135, 8097-8100. (21) Gao, W.; Singh, N.; Song, L.; Liu, Z.; Reddy, A. L. M.; Ci, L.; Vajtai, R.; Zhang, Q.; Wei, B.; Ajayan, P. M. Nat. Nanotechnol. 2011, 6, 496. (22) Gao, W.; Wu, G.; Janicke, M. T.; Cullen, D. A.; Mukundan, R.; Baldwin, J. K.; Brosha, E. L.; Galande, C.; Ajayan, P. M.; More, K. L.; Dattelbaum, A. M.; Zelenay, P. Angew. Chem., Int. Ed. 2014, 53, 3588-3593. (23) Hatakeyama, K.; Karim, M. R.; Ogata, C.; Tateishi, H.; Funatsu, A.; Taniguchi, T.; Koinuma, M.; Hayami, S.; Matsumoto, Y. Angew. Chem., Int. Ed. 2014, 53, 6997-7000. (24) Karim, M. R.; Islam, M. S.; Hatakeyama, K.; Nakamura, M.; Ohtani, R.; Koinuma, M.; Hayami, S. J. Phys. Chem. C 2016, 120, 21976-21982. (25) Hatakeyama, K.; Islam, M. S.; Michio, K.; Ogata, C.; Taniguchi, T.; Funatsu, A.; Kida, T.; Hayami, S.; Matsumoto, Y. J. Mater. Chem. A 2015, 3, 20892-20895. (26) Wakata, K.; Karim Mohammad, R.; Islam Md, S.; Ohtani, R.; Nakamura, M.; Koinuma, M.; Hayami, S. Chem. - Asian J. 2016, 12, 194-197. (27) Shudo, Y.; Karim Mohammad, R.; Ohtani, R.; Nakamura, M.; Hayami, S. ChemElectroChem 2017, 5, 238-241. (28) Miesenböck, G.; De Angelis, D. A.; Rothman, J. E. Nature 1998, 394, 192. (29) Wencel, D.; Abel, T.; McDonagh, C. Anal. Chem. 2014, 86, 15-29. (30) Zong, S.; Wang, Z.; Yang, J.; Cui, Y. Anal. Chem. 2011, 83, 4178-4183. (31) Zheng, X.-S.; Hu, P.; Cui, Y.; Zong, C.; Feng, J.-M.; Wang, X.; Ren, B. Anal. Chem. 2014, 86, 12250-12257. (32) Takmakov, P.; Zachek, M. K.; Keithley, R. B.; Bucher, E. S.; McCarty, G. S.; Wightman, R. M. Anal. Chem. 2010, 82, 9892-9900. (33) Magnotta, V. A.; Heo, H.-Y.; Dlouhy, B. J.; Dahdaleh, N. S.; Follmer, R. L.; Thedens, D. R.; Welsh, M. J.; Wemmie, J. A. Proc. Natl. Acad. Sci. USA 2012, 109, 8270-8273.

(34) Rini, M.; Magnes, B.-Z.; Pines, E.; Nibbering, E. T. J. Science 2003, 301, 349-352. (35) Mohammed, O. F.; Pines, D.; Dreyer, J.; Pines, E.; Nibbering, E. T. J. Science 2005, 310, 83-86. (36) Garczarek, F.; Gerwert, K. Nature 2006, 439, 109-112. (37) Osawa, M. In Near-Field Optics and Surface Plasmon Polaritons, Kawata, S., Ed.; Springer Berlin Heidelberg, 2001, pp 163-187. (38) Neubrech, F.; Huck, C.; Weber, K.; Pucci, A.; Giessen, H. Chem. Rev. 2017, 117, 5110-5145. (39) Brar, V. W.; Sherrott, M. C.; Jang, M. S.; Kim, S.; Kim, L.; Choi, M.; Sweatlock, L. A.; Atwater, H. A. Nat. Commun. 2015, 6, 7032. (40) Dong, L.; Yang, X.; Zhang, C.; Cerjan, B.; Zhou, L.; Tseng, M. L.; Zhang, Y.; Alabastri, A.; Nordlander, P.; Halas, N. J. Nano Lett. 2017, 17, 5768-5774. (41) Cerjan, B.; Yang, X.; Nordlander, P.; Halas, N. J. ACS Photonics 2016, 3, 354-360. (42) Wang, T.; Bai, J.; Jiang, X.; Nienhaus, G. U. ACS Nano 2012, 6, 1251-1259. (43) Jiang, X.; Zaitseva, E.; Schmidt, M.; Siebert, F.; Engelhard, M.; Schlesinger, R.; Ataka, K.; Vogel, R.; Heberle, J. Proc. Natl. Acad. Sci. USA 2008, 105, 12113-12117. (44) Jiang, X.; Ataka, K.; Heberle, J. J. Phys. Chem. C 2008, 112, 813-819. (45) Imae, T.; Torii, H. J. Phys. Chem. B 2000, 104, 9218-9224. (46) Méthivier, C.; Beccard, B.; Pradier, C. M. Langmuir 2003, 19, 8807-8812. (47) Sun, L.; Crooks, R. M.; Ricco, A. J. Langmuir 1993, 9, 17751780. (48) Sun, L.; Kepley, L. J.; Crooks, R. M. Langmuir 1992, 8, 21012103. (49) Yang, H. C.; Dermody, D. L.; Xu, C.; Ricco, A. J.; Crooks, R. M. Langmuir 1996, 12, 726-735. (50) Marcano, D. C.; Kosynkin, D. V.; Berlin, J. M.; Sinitskii, A.; Sun, Z. Z.; Slesarev, A.; Alemany, L. B.; Lu, W.; Tour, J. M. ACS Nano 2010, 4, 4806-4814. (51) Osawa, M.; Ataka, K.; Yoshii, K.; Nishikawa, Y. Appl. Spectrosc. 1993, 47, 1497-1502. (52) Johnson, E.; Aroca, R. J. Phys. Chem. 1995, 99, 9325-9330. (53) Ash, P. A.; Vincent, K. A. Chem. Commun. 2012, 48, 14001409. (54) Tyrode, E.; Johnson, C. M.; Kumpulainen, A.; Rutland, M. W.; Claesson, P. M. J. Am. Chem. Soc. 2005, 127, 16848-16859. (55) Gao, Y.; Yip, H.-L.; Chen, K.-S.; O’Malley, K. M.; Acton, O.; Sun, Y.; Ting, G.; Chen, H.; Jen, A. K. Y. Adv. Mater. 2011, 23, 1903-1908. (56) Lerf, A.; He, H.; Forster, M.; Klinowski, J. J. Phys. Chem. B 1998, 102, 4477-4482. (57) Szabó, T.; Berkesi, O.; Forgó, P.; Josepovits, K.; Sanakis, Y.; Petridis, D.; Dékány, I. Chem. Mater. 2006, 18, 2740-2749. (58) Koinuma, M.; Ogata, C.; Kamei, Y.; Hatakeyama, K.; Tateishi, H.; Watanabe, Y.; Taniguchi, T.; Gezuhara, K.; Hayami, S.; Funatsu, A.; Sakata, M.; Kuwahara, Y.; Kurihara, S.; Matsumoto, Y. J. Phys. Chem. C 2012, 116, 19822-19827. (59) Ikeda, Y.; Karim, M. R.; Takehira, H.; Matsui, T.; Taniguchi, T.; Koinuma, M.; Matsumoto, Y.; Hayami, S. Chem. Lett. 2013, 42, 1412-1414. (60) Tang, C. Y.; Allen, H. C. J. Phys. Chem. A 2009, 113, 73837393. (61) Smalley, J. F.; Chalfant, K.; Feldberg, S. W.; Nahir, T. M.; Bowden, E. F. J. Phys. Chem. B 1999, 103, 1676-1685. (62) Leopold, M. C.; Black, J. A.; Bowden, E. F. Langmuir 2002, 18, 978-980. (63) Hatakeyama, K.; Razaul Karim, M.; Ogata, C.; Tateishi, H.; Taniguchi, T.; Koinuma, M.; Hayami, S.; Matsumoto, Y. Chem. Commun. 2014, 50, 14527-14530. (64) Kim, S.; Zhou, S.; Hu, Y.; Acik, M.; Chabal, Y. J.; Berger, C.; de Heer, W.; Bongiorno, A.; Riedo, E. Nat. Mater. 2012, 11, 544.



(65) Karim, M. R.; Islam, M. S.; Rabin, N. N.; Ohtani, R.; Nakamura, M.; Koinuma, M.; Hayami, S. Aust. J. Chem. 2017, 70, 642-645. (66) Majumder, M.; Chopra, N.; Andrews, R.; Hinds, B. J. Nature 2005, 438, 44. (67) Dalla Bernardina, S.; Paineau, E.; Brubach, J.-B.; Judeinstein, P.; Rouzière, S.; Launois, P.; Roy, P. J. Am. Chem. Soc. 2016, 138, 10437-10443. (68) Kane, V.; Mulvaney, P. Langmuir 1998, 14, 3303-3311. (69) Shimazu, K.; Teranishi, T.; Sugihara, K.; Uosaki, K. Chem. Lett. 1998, 27, 669-670. (70) Wang, D.; Nap, R. J.; Lagzi, I.; Kowalczyk, B.; Han, S.; Grzybowski, B. A.; Szleifer, I. J. Am. Chem. Soc. 2011, 133, 21922197. (71) Zhao, J.; Luo, L.; Yang, X.; Wang, E.; Dong, S. Electroanalysis 1999, 11, 1108-1113. (72) Li, H.; Robertson, A. D.; Jensen, J. H. Proteins: Struct., Funct., Bioinf. 2005, 61, 704-721.


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