Letter pubs.acs.org/NanoLett
High-Performance Bioassisted Nanophotocatalyst for Hydrogen Production Shankar Balasubramanian,†,§ Peng Wang,†,§ Richard D. Schaller,†,‡ Tijana Rajh,† and Elena A. Rozhkova*,† †
Center for Nanoscale Materials, Argonne National Laboratory, Argonne, Illinois 60439, United States Department of Chemistry, Northwestern University, Evanston, Illinois 60208, United States
‡
S Supporting Information *
ABSTRACT: Nanophotocatalysis is one of the potentially efficient ways of capturing and storing solar energy. Biological energy systems that are intrinsically nanoscaled can be employed as building blocks for engineering nanobiophotocatalysts with tunable properties. Here, we report upon the application of light harvesting proton pump bacteriorhodopsin (bR) assembled on Pt/TiO2 nanocatalyst for visible light-driven hydrogen generation. The hybrid system produces 5275 μmole of H2 (μmole protein)−1 h−1 at pH 7 in the presence of methanol as a sacrificial electron donor under white light. Photoelectrochemical and transient absorption studies indicate efficient charge transfer between bR protein molecules and TiO2 nanoparticles.
KEYWORDS: Nanobiohybrid, energy, protons photoreduction, Pt/TiO2, bacteriorhodopsin
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photoelectrode.16 To date, a great progress has been made in visible light-driven H2 generation. However, systems employing dyes or biomolecules isolated from their natural system generally have limited stability to variations in environmental factors. Natural phototrophic systems utilize the light energy to produce and store it in a form of chemical compounds via two main evolutionary-distinct mechanisms. First multistep electron-shuttling mechanism known as photosynthesis that utilizes chlorophylls is found in plants, algae, and cyanobacteria. Another “simple” pathway is based on sunlight-driven proton transfer across the membrane by a proton pump bacteriorhodopsin (bR) that is found in Archaea, for example, Halobacteria.17 The resultant electrochemical gradient is further converted into chemical energy in the form of ATP that powers the cell. bR proton pumps are biologically occurring nanodevices capable of transporting ions against an electrochemical potential up to 250 millivolts, which translates into a 10 000fold difference in proton concentration on either side of the membrane.18 The bR pumps are relatively small 26 kDa prototype molecular membrane transporters. They are neatly arranged as a two dimentional (2D) nanocrystal lattice integrated into the bacterial cell membrane with a uniform orientation that is known as the purple membrane (PM). The transmembrane protein consists of seven α-helices burying a
irect conversion of solar energy to chemical fuels such as hydrogen promises technology for providing clean energy in the near future.1−3 Semiconductor photocatalysts such as TiO2 play a crucial role in the generation of hydrogen via water splitting using solar energy. Since the first demonstration of the water splitting to oxygen and hydrogen on TiO2 electrodes under UV light irradiation nowadays known as the HondaFujishima effect4 there is a great continuous interest in extending the visible light reactivity of TiO2 photocatalyst.5 Various synthetic and natural dyes have been utilized to sensitize TiO2 nanoparticles for visible light capture and to produce H2 either with Pt catalyst or hydrogenase enzyme.6−10 For example, Armstrong and co-workers8 showed that Ru (bpy)2 dye-sensitized TiO2 nanoparticles when coupled with Fe−Ni hydrogenase efficiently produce H2 under visible light irradiation with a turnover frequency of 50 (mole H2) s−1 (mole enzyme)−1 using triethanolamine (TEOA) as a sacrificial electron donor. Analogous construct was shown to photoreduce CO2 to CO when carbon monoxide dehydrogenase (CODH) enzyme was used instead of hydrogenase thereby demonstrating the versatility of visible light TiO2 photocatalysis.11 In addition to dye photosynthesizers, natural protein frameworks such as photosystem I (PSI) were exploited for solar H2 production when combined with Pt nanoparticles, cobaloxime (bis(dimethylglyoximato)cobalt(III)) complexes or hydrogenase enzymes as reduction cocatalysts.12−15 Other naturally occurring light-harvesting proteins phycocyanins, accessory pigments to chlorophyll, were recently exploited to enhance the photocurrent density on hematite thin-film © XXXX American Chemical Society
Received: May 7, 2013 Revised: June 18, 2013
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Figure 1. (Left) Principle of solar H2 generation based on bacteriorhodopsin (bR) and Pt nanoparticles supported on TiO2 photocatalyst. (Right) Structure of a natural transmembrane light-driven pump bacteriorhodipsin (top) and a cofactor retinal group (bottom) that covalently attached to the Lys 216 forms protonated Schiff base. All-trans/13-cis photoisomerization of the cofactor triggers proton transfer across a membrane.
Figure 2. (A) TEM image of the Pt/TiO2 (left) and HRTEM image of single Pt nanoparticles photodeposited on TiO2 (right). (B) Raman spectra of free (top spectrum) bR and bR adsorbed on the surface of Pt/TiO2 (lower spectrum) nanoparticle showing fingerprint regions of retinal chromophore and anatase TiO2.
retinal chromophore covalently linked to Lys 216 via a protonated Schiff base linkage, Figure 1. The retinal group is located approximately in the center of the PM, at a distance of nearly 2.5 nm from both PM surfaces.19 Upon visible light (568 nm) absorption, the retinal undergoes subpicosecond photoisomerization (all-trans to 13-cis). The Schiff base then releases
the proton followed by alterations in protonatable groups within bacteriorhodopsin molecule to the extracellular side to set up the vectorial proton gradient and hence driving the ATP synthesis.20−25 Being expressed by an extremophile host organism bR molecules are naturally evolved to be stable under demanding conditions such as high ionic strength (3 M B
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Figure 3. Photocatalytic H2 production in the presence of 25 mM methanol as electron donor at pH7 (A) under monochromatic green light, 560 ± 10 nm (13 mW/cm2) and (B) under white light illumination (350 nm ≤ λ ≤ 800 nm, 120 mW/cm2).
NaCl), temperature over 80 °C (in water) and 140 °C in dry condition as well in wide pH range (5−11) without loss of photochemical activity.20 Owing to these attractive features bR molecule as well as PM were proposed for photonics and energy conversion applications by a number of groups. For example, the natural light harvesting capability of natural bR nanodevice was significantly enhanced when the PM were tagged with semiconductor CdTe or CdSe/ZnS quantum dots. The quantum dots-tagged PM were able to harness blue light that would not be absorbed by bR alone.26 Similarly, Au, Ag, and Ag−Au alloy nanoparticles notably enhanced the proton pumping activity of bR under nanoparticles plasmonic field thereby decreasing the photocycle of bR from 15 ms to hundreds of nanoseconds.27−29 In addition, wild-type bR and 3Glu mutant bR molecules were successfully tested for efficient light harvesting in solar cells demonstrating their viability as photosensitizer.30 In this study, we aimed to employ the light-harvesting proton pump bR as a biological building block to harness the visible light reactivity of TiO2 photocatalyst for protons photoreduction using Pt nanocrystalline catalyst. Specifically, bR was assembled on the surface of Pt/TiO2 photocatalysts to serve as a photosensitizer. In addition, bR provided its biological function of the light-driven pumping or transferring of protons that consequently reduced to hydrogen over platinum nanocatalyst, Figure 1. The light-driven H2 evolution was assessed under monochromatic 560 nm as well as under white light illumination at neutral pH using electron donors. The time scale of electron transfer from bR to TiO2 was also directly evaluated using transient absorption spectroscopy. Results and Discussion. Principal scheme of the proposed solar-driven nanosystem employs the light-harvesting proton pump bR as an important building unit serving for harnessing the visible light reactivity of TiO2 photocatalyst and for driving protons toward platinum nanocatalyst for consequent reduction to hydrogen gas, as illustrated in Figure 1 (left). Figure 2a shows a representative TEM image of Pt nanoparticles with narrow size distribution (∼4 nm) photodeposited on the surface of TiO2 P25 nanoparticles. The inorganic nanophotocatalyst was modified with bR protein that absorbs the visible green light. In aqueous solution, bR self-assembles on the TiO2 nanoparticle to form a stable conjugate as observed in the UV−vis absorbance spectrum (Supporting Information Figure S3). bR molecule contains several positively and
negatively charged residues on the cytoplasmic side as well as on the extracellular side, Figure 1.17,18,20,22 Specifically, the carboxylic groups presented on the cytoplasmic side can allow the bR molecules to preferentially self-assemble on the exposed oxygen atoms of anatase surface of the TiO2 nanoparticles. The self-assembly of bR on TiO2 was further confirmed by Raman microscopy as shown in Figure 2B. Raman spectra of the nanobioassembly were dominated by a broad ethylenestretching mode of the retinal chromophore at 1530 cm−1 and fingerprint modes at 1171 and 1200 cm−1 for the lightadapted bR molecule that is in consistency with previous reports.31,32 In addition, the fingerprint modes of the anatase TiO2 were observed. Identical characteristic signals of bR were observed on the Pt/TiO2/bR hybrid material. Such spectra clearly illustrate that the bR self-assembled on the inorganic material retains its secondary structure as well as the retinal chromophore intact. The nanobio-photocatalyst was tested for the photocatalytic H2 generation in the presence of methanol as sacrificial electron donor (Figure 3). When exposed to green light (560 ± 10 nm), continuous H2 generation was observed with a turnover rate of 207 μmole of H2 (μmole protein)−1 h−1. Here, bR molecules are proposed to act as a visible light-harvesting molecule in addition to working as a protons pump. The photochemically produced holes were scavenged with methanol, which acts as a sacrificial electron donor, Figure 1. On average, under light illumination nearly constant H2 evolution by the nanobiocatalyst has been observed at least for 2.5 h. Control experiments with Pt/TiO2 without bR yielded in minute amount of H2 evolved for 1 h of illumination with green light. When monochromatic light was replaced with white light illumination with λ = 350−800 nm, H2 turnover rate was increased by 25 times to 5275 μmole of H2 (μmole protein)−1 h−1, Figure 3a and b, most possibly due to additional electrons coming from excitation of TiO2 nanoparticles. Thus, the Pt/ TiO2/bR hybrid photocatalyst outperforms many other reported nanobiosystems in hydrogen generation. In order to establish the role of bacteriorhodopsin in the above hybrid system, photoelectrochemical measurements were carried out. The photocurrent measurements of carotenoidssensitized TiO2 systems were well established to understand the energy transfer process from the dye molecules. TiO 2 nanoparticles were electrophoretically deposited on FTO electrodes to form a uniform film and then the electrode was C
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Figure 4. (A) I−V characteristics of TiO2 and TiO2/bR photoelectrode in dark and light illumination (100 mW/cm2), (B) Energy level diagram showing a possible charge carrier injection in bR/TiO2 in the presence of I−/I3− redox species, (C) Short-circuit photocurrent response of TiO2, TiO2/bR, and TiO2/bR bleached electrode in aqueous electrolyte containing 5 mM hydroquinone (HQ) in 10 mM MES, pH 6.2 buffer. (D) UV− vis spectra of bleached bR after treatment with hydroxylamine.
photocurrent increased rapidly and reached a steady-state current density of 0.27 μA/cm2. The photocurrent returned to the background level after illumination was turned off and the process could be repeated many times. On the other hand, unmodified TiO2 electrode did not show any change in current under similar condition. Similarly, TiO2 electrode modified with bleached bR protein (devoid of retinal chromophore, Figure 4d) showed no current response when illuminated with green light. This demonstrates that the origin of the photocurrent can be attributed to the excitation of bR retinal chromophore and associated energy transfer to the TiO2 nanoparticles. Transient absorption (TA) measurements further verified charge transfer from bR molecule to TiO2 nanoparticle. TA measurements were carried out using a pump wavelength of 560 nm such that it excited only the bR molecule leading to a charge injection to TiO2. The bleach of the excited bR molecule, monitored at 625 nm, was examined in the presence of different concentrations of TiO2 nanoparticles (0, 20, 100 μg ml−1). The decay traces at the probe wavelength were fitted with an exponential function
immersed in the bR solution overnight. Here, bR-modified TiO2/FTO electrodes were tested for the photocurrent generation with white light as well as under monochromatic illumination (560 nm). Figure 4a shows the linear sweep voltammograms measured on bR-modified TiO2/FTO electrodes under dark and under white light illumination. In dark, both the electrodes show negligible current response as the potential was scanned from −1.0 to 0.9 V (vs Ag/AgCl). Upon illumination, the bare TiO2 electrode has an onset photocurrent at −0.75 V and the current continues to increase before reaching a steady state value of 1.0 mA/cm2. When TiO2 photoelectrode was modified with bR, the steady-state photocurrent density value increased to 2.0 mA/cm2 that was ∼50% over pure TiO2 electrode. The analysis of energy levels between TiO2 and bR molecules in the presence of I−/I3− redox electrolyte shows that there is a favorable band alignment for successful electron injections from excited bR to TiO2 and subsequently transfer electrons from redox species under the experimental conditions (Figure 4b). This assumption is in agreement with a recent work by El-Sayed’s group33 on the bR/ TiO2 nanotube array hybrid electrode system that reported upon the increased photocurrent density of the biohybrid electrode over pure TiO2 under AM 1.5 illumination.33 Further, under monochromatic illumination (λ = 560 nm) the
⎛ −x ⎞ y = A exp⎜ ⎟ + y0 ⎝ τ ⎠ D
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where τ is the decay lifetime and A is the corresponding amplitude. While the decay of bR was itself fast, the average decay lifetime was consistently faster in the TiO2/bR system as compared to bR alone. Figure 5 shows the lifetime decay trend
candidate for fabrication of green energy devices consuming literally only infinite sources, salt water and sun light. Methods. TiO2 P25 nanoparticles (Evonik Industries), which contain anatase and rutile crystallites in 80:20 ratio with a surface area of ∼55 m2 g−1, was used as a main support. Bacteriorhodopsin (bR) from Halobacterium salinarum was obtained from Sigma-Aldrich and was used without further purification. Active bR protein concentrations were determined spectrophotometrically using the molar extinction coefficient of 62 700 M−1 cm−1 at λ max 568 nm. Sodium hexachloroplatinate, ethanol, methanol, hydroquinone (HQ), sodium chloride, magnesium chloride hexahydrate, magnesium sulfate heptahydrate, potassium chloride, calcium chloride dihydrate, hydroquinone (HQ), and triethanolamine (TEOA) were obtained from Sigma-Aldrich. Deionized (DI) ultrapure water (18 MΩ·cm) was used for solution preparation. Photocatalyst Preparation. Platinum nanoparticles were grown on TiO2 particles via photodeposition method reported before (see Supporting Information).1 A typical Pt photodeposition was carried out in a 100 mL round-bottom flask containing aqueous suspension of TiO2 (3 mg/mL) in the presence of 1 mL of ethanol and 0.375 × 10−4, 0.75 × 10−4, or 1.5 × 10−4 M sodium hexachloroplatinate. The slurry pH was adjusted to ∼3 using 1 M HCl. The suspension was stirred vigorously and purged with high-purity N2 to remove dissolved oxygen for 30 min. After purging, the slurry was irradiated in the ultraviolet (377 ± 50 nm) using a 200 W high-pressure Xe lamp (Perkin-Elmer Optoelectronics) for 30 min. The light was passed through a 10 cm water filter to cutoff IR radiation. Depending on the precursor concentration, the typical Pt loading was determined to be ca. ∼0.25−1 wt % by inductively coupled plasma−atomic emission spectroscopy analyses. After irradiation, the particles were centrifuged and washed with DI water. The process was repeated 3 times and the final Pt/TiO2 photocatalyst particles were stored in DI water before use. Assembly of Bacteriorhodopsin (bR) on Pt/TiO2 Photocatalyst for H2 Production. Bacteriorhodopsin (bR) protein molecules were suspended either in water or 25 mM methanol, pH 7.0. Pt/TiO2 (3 mg/mL) photocatalyst particles were suspended in 1 mL of the respective solvent and the bR solution (0.003 μmol) was added to the slurry. The mixture was stirred overnight to enable maximum bR adsorption to occur. Grafting of the protein molecules on the Pt/TiO2 nanoparticles surface was confirmed by Raman spectroscopy using a RENISHAW inVia Raman Microscope with laser operating at 633 nm wavelength and using UV−vis spectrophotomter Lambda 950, Perkin-Elmer. Hydrogen Evolution Measurements. Freshly prepared bR-modified Pt/TiO2 slurry particles were transferred to reaction vessel (total volume 2 mL) sealed tightly with a rubber septum. The mixture was degassed with high-purity N2 and gently stirred for 15 min. For H2 generation, the slurry was irradiated with 200 W Xe lamp with light intensity of 13 mW/ cm2 (green light only) or 120 mW/cm2 (white light). The light radiation was passed through a 10 cm IR water filter and a band-pass filter (560 ± 10 nm) or 420 nm cut off filter as required. Temperature rose up to ∼2−5 °C that was detected using ICI 7320 S-Series Infrared Thermal Imaging Camera. The amount of photogenerated H2 was detected and quantified with Agilent 7890A gas chromatograph (GC) equipped with HP PLOT Molesieve 5 Å column which was held isothermally at 40 °C and a thermal conductivity detector (TCD). Continuous stream of 99.999% + pure N2 was used as a
Figure 5. Ultrafast transient absorption measurements showing the lifetime decay of the excited bR species reveal charge transfer from bR molecules to TiO2 particles. The samples were pumped using 560 nm and probed at 625 nm laser pulses. Kinetic traces at 625 nm of bR and bR-TiO2 samples along with exponential fit.
for the bR molecule with and without TiO2 nanoparticles. For bR molecule, the excited state decays with a time constant of 1.03 ± 0.11 ps whereas for bR/TiO2 the decay lifetime was 0.42 ± 0.11 and 0.16 ± 0.02 ps for 20 and 100 μg ml−1 TiO2 nanoparticle concentration, respectively. These subpicosecond bleach recovery dynamics indicate a charge separation efficiency from excited bR to TiO2 of >85%. In summary, here we report upon successful application of a naturally occurring proton-pumping protein bacteriorhodopsin as a building block in the bioassisted nanocatalytic system for the light-driven hydrogen production. In this system, bR serves as a visible-light harvester on Pt/TiO2 photocatalyst and also assists in optimizing of the protons-Pt catalyst interface and therefore enhancing reduction of protons to hydrogen. Photoelectrochemical measurements in the presence of redox electrolyte shows a 50% increase in photocurrent density when TiO2 electrodes were modified with bR. We attribute this increases in photocurrent combined with transient absorption studies to charge injection from bR molecules to TiO2 nanoparticles. The turnover rate on a per μmole basis of the active properly folded protein (as determined spectrophotometrically) of the hybrid photocatalyst was found to be 207 μmole of H2 (μmole protein)−1 h−1 under monochromatic green light and 5275 mol of H2 (μmole protein)−1 h−1 under white light illumination. Such a remarkable ∼25 times rise in the photocatalytic efficiency of the system can be due to additional electrons that come from UV excitation of TiO2 nanoparticles. Hence, the bioassisted and a Pt/TiO2 photocatalyst containing a natural visible light-driven proton pump bR is promising system for solar hydrogen generation at ambient conditions. Such bioassisted hybrid might overcome the limited stability and structural complexity of other photocatalytic systems, for example, based on hydrogenases, and can offset carbon-based feedstock requirement for H2 generation. Furthermore, evolutionary evolved intrinsic robustness of bacteriorhodopsin and strong potential in development of low-cost biotechnological production of PM make it a good E
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carrier gas at a flow rate of 3.5 mL min−1). At the desired time, 20 μL of the sample from the reaction vessel’s headspace was collected and manually injected into the GC system for analysis. Before sample measurements, the instrument was calibrated with 1−3% H2 gas standards (AFC International, Inc. DeMotte, IN) under similar conditions. Photobleaching of bR. The retinal chromophore of bR was removed by photobleaching of the PM in 1 M hydroxylamine solution at pH 8.0. The bR solution was illuminated for 3 h with 200 W white light (λ > 420 nm and IR water filter) to completely remove the chromophore. The bleached sample was washed and centrifuged with DI water to remove excess of hydroxylamine. Preparation of TiO2 and TiO2/bR Photoanode. Aqueous solution of TiO2 nanoparticles (3 mg/mL) was adjusted to pH 3 using 1 M HCl and sonicated for 30 min. A nanocrystalline TiO2 film was prepared by carrying out electrophoretic deposition on to an FTO electrodes (area 0.35 cm2) using another FTO as a counter electrode. The film was then sintered in air at 400 °C for 1 h. A transparent TiO2 film was formed by this procedure with uniform coating. The FTO/TiO2 electrode was modified with bR (0.3 mg/mL) through overnight immersing in the dark and then rinsed with DI water before measurements. Photoelectrochemical Measurements. The photoelectrochemical characteristics were analyzed in a typical threeelectrode configuration with as-prepared TiO2 or TiO2/bR on FTO serving as the working electrode, Ag/AgCl (3 M NaCl) as the reference electrode and Pt wire as the counter electrode, Supporting Information Figure S1. An aqueous solution containing 2 mM iodine/iodide (Iodolyte Z-150) redox species in 1.0 M citrate buffer, pH 7.0 serves as redox electrolyte. Before the experiment, the solutions were purged with ultrapure Ar for 15 min to remove dissolved oxygen. The light intensity of 100 mW/cm2 from a 200 W Xe lamp that passed through a 10 cm IR water filter was used. Linear sweep voltammograms were carried out using a BAS-100W potentiostat at a scan rate of 10 mV/s to obtain the current density versus potential curve under dark and illuminated conditions. The short circuit (Jsc) photoresponses of different samples under intermittent illumination were carried out at potentiostatic conditions (0 V vs Ag/AgCl electrode) by connecting the reference to the counter electrode. For Jsc, an aqueous solution of 5 mM HQ in 10 mM MES buffer, pH 6.2 was added to the cell and purged with argon for 15 min; argon was continuously passed over the solution surface during the experiments. Transient Absorption Measurements. Transient absorption measurements were performed using a 2 kHz, 35 fs amplified titanium/sapphire laser. A portion of the 800 nm laser fundamental was mechanically delayed and focused into a sapphire plate to produce a broadband white light probe. Pump pulses at 560 nm were produced using an optical parametric amplifier. Samples with aqueous bR solutions (2 μM, OD adjusted to 0.2−0.3 at 560 nm) containing different concentrations of TiO2 nanoparticles (0, 20, and 100 μg/mL) were examined with a pump pulse at 560 nm and at a probe wavelength of 625 nm.
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AUTHOR INFORMATION
Author Contributions §
S.B. and P.W. equally contribute to this work.
Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS Use of the Center for Nanoscale Materials was supported by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences, under contract no. DE-AC0206CH11357. Authors thank Dr. Y. Liu (Argonne, CNM) for assistance with TEM imaging.
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ASSOCIATED CONTENT
S Supporting Information *
Additional figures and information. This material is available free of charge via the Internet at http://pubs.acs.org. F
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