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Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results and Discussion
  6. References

Current interest in natural photosynthesis as a blueprint for solar energy conversion has led to the development of a biohybrid photovoltaic cell in which bacterial photosynthetic membrane vesicles (chromatophores) have been adsorbed to a gold electrode surface in conjunction with biological electrolytes (quinone [Q] and cytochrome c; Magis et al. [2010] Biochim. Biophys. Acta1798, 637–645). Since light-driven current generation was dependent on an open circuit potential, we have tested whether this external potential could be replaced in an appropriately designed dye-sensitized solar cell (DSSC). Herein, we show that a DSSC system in which the organic light-harvesting dye is replaced by robust chromatophores from Rhodospirillum rubrum, together with Q and cytochrome c as electrolytes, provides band energies between consecutive interfaces that facilitate a unidirectional flow of electrons. Solar I–V testing revealed a relatively high Isc (short-circuit current) of 25 μA cm−2 and the cell was capable of generating a current utilizing abundant near-IR photons (maximum at ca 880 nm) with greater than eight-fold higher energy conversion efficiency than white light. These studies represent a powerful demonstration of the photoexcitation properties of a biological system in a closed solid-state device and its successful implementation in a functioning solar cell.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results and Discussion
  6. References

In response to the growing worldwide demand for clean, renewable and secure energy source as a substitute for fossil fuels, a considerable research effort is now being focused on the natural photosynthetic process as a blueprint for solar energy conversion devices (1,2). These biological systems have evolved over billions of years to assemble naturally optimized light harvesting (LH) and photochemical reaction center (RC) complexes that absorb available light and convert this radiant energy into chemical potential with strikingly high efficiencies. This has led to the development of biohybrid photoelectric cells based on natural algal photosynthetic systems (3,4) for the ultimate conversion of sunlight into hydrogen and the generation of electrical currents (5,6), as well as light-driven current formation from photosynthetic membrane vesicles (chromatophores; 7) of purple photosynthetic bacteria and their isolated RC (8–11) and RC-light harvesting 1 (LH1) protein core components (12).

In a recent study of biohybrid solar cells, light-dependent currents were generated with Rhodobacter sphaeroides chromatophores adsorbed to a gold electrode surface in the absence of specific functionalization of either the electrode or the membrane surfaces (7). The chromatophore membrane contains integral membrane LH proteins that in addition to absorbing blue light are capable of collecting near-IR photons (800–875 nm) and transferring the excitation energy to the RC bacteriochlorophyll a (BChl) special pair, which initiates a transmembrane charge separation (13). Thereafter, a cycle of electron transfer reactions commences between the primary iron-quinone acceptor (QA), the cytochrome bc1 complex and cytochrome c2, accompanied by the formation of an electrochemical proton gradient.

Light-driven current generation by the Rba. sphaeroides chromatophores adsorbed to a bare gold electrode was dependent on the presence of the biological electrolytes quinone (Q) and cytochrome c, together with an open circuit potential of −100 mV, which provided directionality to the electron flow. The need for the application of an open circuit potential prompted us to extend this system into an appropriately designed dye-sensitized solar cell (DSSC), capable of generating a significant solar-energy driven current. Although the Rba. sphaeroides LH1 complex, which functions at the interface of light harvesting and electron cycling, was found to be exceptionally stable, the LH2 peripheral antenna showed a light-intensity dependent decoupling from photoconversion (7). Because of this lack of long-term LH2 stability, our prototype DSSC was constructed with chromatophores from the related organism Rhodospirillum rubrum, which forms a robust LH1-RC core structure, while lacking LH2.

Dye-sensitized solar cells have come to represent an area of intense research since their inception in 1991 (14) as a promising photovoltaic technology owing to their low cost and simplicity of manufacture. A typical DSSC (Fig. 1) is composed of a mesoporous TiO2 film on a transparent conducting fluorine-doped tin oxide (FTO), in which the TiO2 layer is coated with a dye sensitizing monolayer (usually a ruthenium bipyridyl complex). The dye undergoes excitation upon illumination and injects electrons into the conduction band of the TiO2 particles. These electrons are channeled to an external circuit to do useful work and re-enter the cell through a Pt-coated counter electrode at the back-contact. A liquid electrolyte generally consisting of an I/I3 redox couple serves to reduce the photoexcited dye molecules. At the heart of DSSC functionality is the intimate agreement of band energies of the individual consecutive components to ensure electron directionality and flow.

image

Figure 1.  Current generation and energy level diagram of a nanocrystalline DSSC. Photoexcitation of the sensitizer dye (S) results in the injection of electrons into the conduction band of the mesoporous tin oxide semiconductor, which comprises the photoanode (14). The photoexcited dye is thereby oxidized, and in turn oxidizes the mediator, consisting of a redox species dissolved in the electrolyte. The oxidation state of the redox system at the counter electrode is regenerated by electrons that pass through the load. Potentials refer to the standard hydrogen electrode (SHE). The DSSC open-circuit voltage (maximum voltage) corresponds to the difference between the redox potential of the mediator and the Fermi level of the nanocrystallline TiO2 film, indicated by dashed line.

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Herein, we show that a DSSC system in which the organic light-harvesting dye is replaced by the robust chromatophores from Rsp. rubrum, in conjunction with a quinone (Q) and cytochrome c as electrolytes, represents a major step toward the development a self-contained biohybrid solar cell.

Materials and Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results and Discussion
  6. References

Cell growth and membrane isolation.  Wildtype Rsp. rubrum strain S1 was grown for ca 3 days at a light intensity of 100 W m−2 into mid-logarithmic phase on a modified synthetic medium (15,16) in 1 L Roux bottles at 30°C. Chromatophores were isolated from French pressure cell extracts by rate-zone sedimentation on sucrose density gradients as described previously (15), washed by ultracentrifugation and resuspended in 0.1 m Na2PO4 buffer (pH 7.2) at a protein concentration of 29 mg mL−1.

Fabrication of solar cell.  For fabrication of the chromatophore-sensitized solar cell (CSSC), the resuspended chromatophores were coupled to a mesoporous TiO2 layer, following a procedure (17) in which 12 g of P25 TiO2 particles (pore size = 25 nm; Evonik Degussa) were first ground in a porcelain mortar with 4 mL of deionized water and 0.4 mL of acetylacetone. The viscous paste was slowly diluted with an additional 16 mL of deionized water under continuous grinding and 0.2 mL of Triton X-100 was added to facilitate colloid spreading on the substrate. FTO-coated glass was used as the transparent conducting oxide substrate (15–30 Ω cm−2, Hartford Glass Co. Inc.). The coating of the photoanode from the TiO2 paste was performed by doctor blading with Scotch tape defining the coating area, location and thickness. The cell area defined by the TiO2 film was 2 cm × 1 cm (2 cm2), with film thickness varying from 10 to 12 μm. Film thickness and uniformity was measured by a profilometer (Alpha-step 200; Tencor). Films were dried in air for 1 h and sintered at 500°C for 1 h at a ramp rate of 5°C min−1, followed by cooling at the same ramp rate. Heat treatment converted the TiO2 to a100% anatase phase. The counter electrode consisted of a Pt layer, deposited by radio frequency sputtering for 2 min at 100 W, producing a 200 nm thick film on the FTO. For fabricating the cell, the two electrodes were held together with binder clips, and separated by a Teflon spacer with a thickness of 40 μm, used as the medium for soaking the electrolytes, which consisted of cytochrome c and Q0, a ubiquinone analog, lacking an isoprenoid side chain.

Characterization of solar cell.  Mercury porosimetry was performed with a Micromeritics Autopore 9400 porosimeter on the P25 TiO2 film as previously described (18) by intruding mercury into the pores through application of pressure to the surrounding phase to determine porosity, pore size, volume and pore size distribution. For sample preparation, a thick coating of titania dispersion was drop-cast and air dried for 2 h. This was followed by heating at 500°C for 30 min with a ramp rate of 2°C min−1. Flakes of the coating were carefully collected to prevent disturbance of the internal microstructure and prior to porosimetry measurements, samples were dried at 200°C for 24 h.

Field-emission scanning electron microscopy (FESEM) images of the microstructure of the titania films were obtained on a model Zeiss Sigma FESEM. Samples were coated with iridium using a Gatan Model 681 Ion Beam Coater to prevent charging effects.

Optoelectronic measurements.  Photovoltaic I–V characterization was performed under AM 1.5 (100 mW cm−2) white light illumination (200–1000 nm) by a 300 W Xenon solar simulator (18). The solar simulator and electrical characterization equipment were controlled by a labview program through which −1 to 1 V were fed to the solar cell with a step size of 10 mV. Solar behavior of cells under 890 nm illumination was examined at an input power of 5.88 mW cm−2 with an effective cell area of 0.25 cm2.

Results and Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results and Discussion
  6. References

The CSSC was assembled using sintered P25 titania as the photoanode (17), Rps. rubrum chromatophores in place of the sensitizing dye and cytochrome c and Q0 as electrolytes. The microstructure of the sintered P25 film was assessed by mercury porosimetry (Fig. 2) and FESEM (Fig. 3). Porosimetry demonstrated that cytochrome c and Q0 were capable of percolating freely through the P25 TiO2 matrix, allowing for enhanced charge transfer to take place across the interfaces, whereas chromatophores of ca 50 nm diameter were seen by FESEM to be partially inserted into the pores or to sit at the surface of the mesoporous TiO2 layer.

image

Figure 2.  Mercury porosimetry plot of incremental intrusion of mercury with respect to the pore diameter in the P25 TiO2 film. A single sharp pore peak is seen in the mesopore range at 29.4 nm. Total intrusion pore volume of the film was found to be 0.73 cm3 g−1, with a film porosity of 56%.

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image

Figure 3.  Field-emission scanning electron microscope (FESEM) images of the microstructure of the titania films. (A) Buffer (0.1 m Na2PO4, pH 7.2) alone. (B) Coupled chromatophores in buffer. In circled region, chromatophores are seen partially inserted into the pores or sitting at the surface.

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The results of an extensive solar characterization of the CSSC and the control samples are presented in Table 1 and Fig. 3. Rigorous J–V solar characterization under white light showed that as expected, the TiO2 only cell gave the best performance (Fig. 4A), as TiO2 has an absorption band edge below 400 nm, harvesting the highest energy photons. The device systems of TiO2 + cytochrome c, TiO2 + Q0, or TiO2 + Q0 + cytochrome c performed less efficiently, as they are incorporating liquid phase electrolytes (equivalents), which freely percolate through the TiO2 matrix. This opens up recombination centers at the pores, resulting in decreases in both VOC and JSC for these systems in comparison with the TiO2-only device. Most importantly, these measurements show that the adhered, underivatized chromatophore (TiO2 + chromatophores + Q0 + cytochrome c) system performs much better than the individual redox mediator only systems, second only to the TiO2 device system, thereby demonstrating that light harvesting is indeed occurring as a result of the presence of the chromatophores.

Table 1.   Solar J–V characteristics of solar cells under white light and 890 nm illumination.
Cell I SC (mA cm−2)* V OC (V)†FF (%)‡ η (%)§
  1. *Short-circuit current; †open-circuit voltage; ‡fill factor; §energy conversion efficiency; ¶normalized to input power of 5.882 mW cm−2.

TiO2 (white light)0.0600.360.286.05 × 10−3
TiO2 (890 nm filter)0.001220.160.000216.97 × 10−7
TiO2 + cytochrome c (white light)0.0400.320.263.33 × 10−3
TiO2 + cytochrome c (890 nm filter)0.001930.070.671.54 × 10−3
TiO2 + Q0 (white light)0.05100.340.233.98 × 10−3
TiO2 + Q0 (890 nm filter)0.001940.130.532.27 × 10−3
TiO2 + Q0 + cytochrome c (white light)0.02300.250.231.33 × 10−3
TiO2 + Q0 + cytochrome c (890 nm filter)0.006800.120.212.91 × 10−3
TiO2 + chromatophores + Q0 + cytochrome c (white light)0.05280.330.254.36 × 10−3
TiO2 + chromatophores + Q0 + cytochrome c (890 nm filter)0.02470.300.293.66 × 10−2
image

Figure 4.  Current-voltage curves of cells under white light and near-IR illumination. (A) Solar behavior of cells under white light, applied as described in Materials and Methods. ISC, short circuit; VOC, open-circuit voltage. (B) Solar behavior of cells under 890 nm illumination, applied as described in Materials and Methods. Note that the TiO2 only device does not exhibit a J–V curve and had an FF value ≈ 0 (Table 1), owing to absorption edge mismatch. See text for additional experimental details.

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As the LH1 complex, the major protein of Rsp. rubrum chromatophores, has an intense absorbance maximum at 880 nm (ε ≈ 120 mm−1 cm−1; Fig. 5), an 890 nm band pass filter was introduced, which effectively cut off the rest of the light spectrum. Under such conditions, the full CSSC TiO2 + chromatophores + Q0 + cytochrome c system performed substantially better than any of the controls (Fig. 4B). These results provide definitive proof of the retention of not only the light-harvesting capabilities of the in situ LH1 complex but also the overall functionality of the CSSC device.

image

Figure 5.  Absorption spectra of Rsp. rubrum chromatophores (solid line) and extracted spirilloxanthin in n-hexane (dotted line). The LH1 antenna complex, which surrounds the RC, consists of a ring-like array of 16 αβ-polypeptide subunits, each binding a pair of BChls and one molecule of the carotenoid spirriloxanthin (19). The BChl QX and QY bands are located near 590 and 880 nm, respectively, whereas the carotenoid absorption peaks are redshifted to 550, 520 and 485 nm, relative to their spectra in n-hexane. The peak at 805 nm arises from the monomeric BChl of the RC.

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Figure 6 shows the dark current behavior of the CSSC and control cells, which provides a more complete insight into the recombination kinetics occurring within the TiO2 matrices. Dark current trends of DSSC films serve as a qualitative measure of the recombination rate of electrons in the TiO2 conduction band in the presence of electrolyte. A reduction in the recombination rate was indicated by the positive shift in the breakdown voltage during the dark current onset. These data can be used in conjunction with the J–V data to further support dark current trends. The lowest recombination was encountered with the TiO2 only device system, as no additional components are present where recombination can occur. When compared to the redox mediators alone, the full CSSC (TiO2 + chromatophores + Q0 + cytochrome c) system showed the least recombination. We can explain this phenomenon by the chromatophores attached at the TiO2 surface serving as a barrier layer between electrons recombining with the Q0/cytochrome c. When chromatophores were bound to the surface of the working electrode in the presence of electrolytes, the significant reduction in back transfer rate suggests a very good coupling between the biological electrolytes and the electrode, whereas the unidirectionality of electron flow within the “biological” dye is in agreement with the band diagram (see elsewhere). This also suggests that the chromatophores bind to the TiO2 surface with the cytosolic face of the RC oriented toward TiO2. The probability of back transfer of excitation energy in Rsp. rubrum chromatophores from the RC to LH1 has been reported to be 25% (20), providing additional support that the flow of excitation is also unidirectional within the chromatophores.

image

Figure 6.  Dark current behavior of cells. Forward bias provided is from −1 to +1 V with step size of 10 mV. Dark current trends show the following performance ranking in terms of least recombination: TiO2 > TiO2 + chromatophores + Q0 + cytochrome c > TiO2 + cytochrome c > TiO2 + Q0 >> TiO2 + Q0 + cytochrome c. This is essentially in accordance with J–V performance under white light (Table 1). When both Q0 and cytochrome c were present, their effects were additive and recombination at the TiO2 electrode was the most affected. See text for additional experimental details.

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The energetics and band matching of the various components serve as critical factors in governing the operation of a DSSC device. Figure 7 illustrates the simple band energy diagram for a biohybrid solar cell in a CSSC format, based on the above results. The agreement between the energy levels is the key factor for the functionality of the CSSC, as it provides the necessary driving force for an electron to jump through consecutive levels. Therefore, we have provided a solid fundamental proof to show that this biohybrid equivalent of a DSSC is indeed viable, and that this device can be utilized for energy harvesting from a light source, particularly in using near-IR irradiation, which is relatively underutilized in conventional DSSCs.

image

Figure 7.  Band energy diagram of biological dye-sensitized solar cell. Oxidation–reduction potentials are presented in volts (V) vs standard hydrogen electrode (SHE). Upon irradiation by light, electrons in the RC are raised from their ground state (S0) to an excited state (S*), resulting in the initial charge separation. The energy level of the latter is above the conduction band edge of TiO2, allowing the injection of the photoelectron into the TiO2. The electron travels through an external circuit to perform useful work, and is reintroduced back into the cell through a Pt counter electrode. The potential of Q0 and cytochrome c (equivalent to redox electrolyte of a conventional DSSC) was slightly higher than the ground state of the chromatophores, and therefore the electron can be injected back into the RC to restore its original electronic configuration. It is important to note that the Q0 and cytochrome c potential was found using a back-calculation, where VOC is the difference between TiO2 conduction/Fermi level and the Q0/cytochrome c potential. With the VOC value obtained from the J–V measurements (ca 0.3 V), the actual potential of Q0/cytochrome c could be determined. This potential is capable of producing the necessary driving force for the electron to jump through consecutive levels.

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As noted elsewhere, the recent development of an electrode utilizing chromatophores to generate light-dependent current in the presence of an external potential (7), raised the question of the function such applied voltages might play. Similar potentials have been utilized in the past to maintain quinone in an oxidized form (21) and it is possible that they facilitate electron cycling. Alternatively, such a potential might be required to give directionality to electron flow and to minimize charge recombination. Matching of the conductive band gaps in our CSSC provided a platform to directly test the latter explanation. As electron flow is energetically favorable from TiO2 to FTO, even an unmodified working electrode should be able to confer unidirectional movement of current. Indeed, this is what is observed with our CSSC device. When no “chromatophore dye” was present, the device was capable of generating a current (Fig. 4A), but the current was significantly reduced when 890 nm light was used instead (Fig. 4B), as it lies beyond the absorbance by TiO2. Moreover, RCs of Rsp. rubrum chromatophores excite electrons in a light-dependent fashion to levels above the conduction band of TiO2, and when coupled to the TiO2/FTO electrode, current is then carried from RCs to TiO2 and ultimately to the FTO electrode. Quinone, which functions as primary electron acceptor in natural systems, has a midpoint potential of −200 mV during light-induced electron flow (21). As the midpoint potential of the conductive band of TiO2 is −500 mV, the maximal voltage represents the difference between this value and the primary electron acceptor, or 300 mV. Indeed, during illumination with 890 nm light, the voltage measured was 0.29 V (Table 1). Noteworthy are the efficiency measurements, which showed the highest value when chromatophores, together with the biological electrolytes were irradiated with 890 nm light, surpassing even the efficiency of controls using white light.

A variation of the approach described here, could extend the light-harvesting capabilities of a tandem PSII–PSI system by replacing PSI with a near-IR photon absorbing LH1-RC core structure, resulting in increased solar conversion efficiencies and a better match of the solar spectrum to the electrochemical study (2,22). Although the current generated in our system was not as high as that of the typical photovoltaic cells or DSSCs (14) when white light was used, it represents the highest light-dependent current yet generated by natural photosynthetic complexes coupled to an electrode. It is also significant that such current did not require the application of any external voltage. Moreover, this study represents a highly viable approach for near-IR light utilization in which a natural system is synthetically replicated as a self-sustaining device. Further optimization is aimed at increasing both the long-term stability and quantum efficiency (now at ca 0.04%) of this promising CSSC device.

With regard to the issue of chromatophore stability, recent studies (J. W. Harrold, K. Woronowicz and M. Vittadello, unpublished data) have shown that when Rsp. rubrum chromatophores are interfaced directly onto a gold surface in a biohybrid photoelctrochemical device, a sustained photocurrent was generated with a maximum of 1.5 μA cm−2 under 850 nm light at 181 mW cm−2, which after gradually leveling off was stable for 160 h at ca 0.40 μA cm−2. Under illumination with white light at 220 mW cm−2, a current of 1.8 μA cm−2 was achieved which leveled off to ca 0.50 μA cm−2 over an additional 110 h.

In summary, our novel approach in which a natural photosynthetic membrane vesicle system is introduced in place of an organic light-harvesting dye has lead to the development of a functional CSSC, which in the presence of redox mediators of biological origin, is capable of tunneling electrons to the TiO2 electrode and generate a light-induced current through conversion of both visible and near-IR irradiation. Indeed, our system, utilizing native robust chromatophores from Rsp. rubrum, without surface functionalization together with Q and cytochrome c as electrolytes, represents a major step toward the development of a self-contained biosolar cell. Excellent band energy agreement and unidirectional electron flow occurred between consecutive interfaces: Pt [RIGHTWARDS ARROW] quinone/cytochrome [RIGHTWARDS ARROW] Rsp. rubrum chromatophore [RIGHTWARDS ARROW] TiO2. Rigorous solar I–V testing demonstrated that this device represents a working solar cell, with a 25 μA cm−2ISC (short-circuit current), which is not only the highest for any biological material used to date but is also observed in the absence of an external potential. The utilization of abundant near-IR photons centered at ca 880 nm showed greater than eight-fold higher energy conversion efficiency than white light. Overall, these studies represent a powerful demonstration of the photoexcitation properties of a biological system in a solid-state device and its successful implementation in a functioning solar cell.

Acknowledgements— This work was supported by the U.S. Department of Energy (grant no. DE-FG02-08ER15957) from the Chemical Sciences, Geosciences and Biosciences Division, Office of Basic Energy Sciences, Office of Science (RAN). TA gratefully acknowledges the financial assistance provided by the U.S. National Science Foundation through grant nos.: CAREER CHE-1004218, NSF DMR-0968937, NSF NanoEHS-1134289, and the NSF-American Competitiveness and Innovation Fellowships (NSF-ACIF) for 2010, and the accompanying research grant and NSF Creativity Award in 2011.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results and Discussion
  6. References
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