Bioresource Technology 101 (2010) 3047–3053
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Photosystem I – Based biohybrid photoelectrochemical cells Peter N. Ciesielski a,b, Frederick M. Hijazi b, Amanda M. Scott b, Christopher J. Faulkner b, Lisa Beard b, Kevin Emmett c, Sandra J. Rosenthal c, David Cliffel c, G. Kane Jennings b,* a
Interdisciplinary Materials Science Program, Vanderbilt University, Nashville, TN 37235-1604, USA Department of Chemical and Biomolecular Engineering, Vanderbilt University, Nashville, TN 37235-1604, USA c Department of Chemistry, Vanderbilt University, Nashville, TN 37235-1604, USA b
a r t i c l e
i n f o
Article history: Received 4 September 2009 Received in revised form 8 December 2009 Accepted 10 December 2009 Available online 12 January 2010 Keywords: Photocatalysis Bioelectronics Photoelectrochemical cells
a b s t r a c t Photosynthesis is the process by which Nature coordinates a tandem of protein complexes of impressive complexity that function to harness staggering amounts of solar energy on a global scale. Advances in biochemistry and nanotechnology have provided tools to isolate and manipulate the individual components of this process, thus opening a door to a new class of highly functional and vastly abundant biological resources. Here we show how one of these components, Photosystem I (PSI), is incorporated into an electrochemical system to yield a stand-alone biohybrid photoelectrochemical cell that converts light energy into electrical energy. The cells make use of a dense multilayer of PSI complexes assembled on the surface of the cathode to produce a photocatalytic effect that generates photocurrent densities of 2 lA/cm2 at moderate light intensities. We describe the relationship between the current and voltage production of the cells and the photoinduced interactions of PSI complexes with electrochemical mediators, and show that the performance of the present device is limited by diffusional transport of the electrochemical mediators through the electrolyte. These biohybrid devices display remarkable stability, as they remain active in ambient conditions for at least 280 days. Even at bench-scale production, the materials required to fabricate the cells described in this manuscript cost 10 cents per cm2 of active electrode area. Ó 2009 Elsevier Ltd. All rights reserved.
1. Introduction Naturally occurring photosynthesis has long been the largestscale solar energy conversion process on the planet (Bjorn and Govindjee, 2009) and is accompanied by the continual mass-production of the biochemical constituents that perform the process within green plants and certain bacteria. One of these components, a photoactive protein complex called Photosystem I (PSI), is a nanoscale optoelectronic workhorse that is located within the thylakoid membrane (Nelson and Yocum, 2006). PSI uses a system of chlorophylls oriented within its protein scaffolding to harness energy from incident photons and transfer it to a special pair of chlorophylls that make up the P700 reaction center. Upon receipt of this energy, P 700 achieves an excited state denoted P 700 and is then quickly oxidized to an electron deficient state, Pþ 700 , as it releases an electron down an intra-protein energy cascade, i.e. an electron transfer chain made up of chlorophylls, phylloquinones, and iron–sulfur clusters. The terminal electron acceptor of this chain, designated F B , is an iron–sulfur cluster located on the stromal side of the protein complex, and is reduced to F B when the electron ar* Corresponding author. Tel.: +1 615 322 2707; fax: +1 615 343 7951. E-mail address:
[email protected] (G.K. Jennings). 0960-8524/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.biortech.2009.12.045
rives (Fig. 1). In natural photosynthesis, electrons are shuttled þ away from F B by chloroplast ferredoxin, and resupplied to P 700 by another protein called plastocyanin. The natural abundance of PSI, combined with its impressive functionality and nanoscale dimensions, have prompted researchers to investigate its application to non-biological systems (Ciobanu et al., 2005; Das et al., 2004; Frolov et al., 2005, 2008a,b; Grimme et al., 2008; Kincaid et al., 2006; Lee et al., 1995, 1997; Terasaki et al., 2009). Our group has previously demonstrated how the functionality of PSI can be accessed in photoelectrochemical systems by its assembly onto gold surfaces (Ciobanu et al., 2007; Faulkner et al., 2008). Through further work, we (Ciesielski et al., 2008) and others(Terasaki et al., 2006) have shown how these strategies could be extended to systems of different geometries to achieve enhanced photocatalytic capabilities. Additional studies have demonstrated that assemblies of PSI exhibit a surface photovoltage when illuminated (Frolov et al., 2005) and have shown that this behavior can be used to control the gate in fieldeffect transistor devices (Frolov et al., 2008a,b; Terasaki et al., 2007). In this work, we report the development of a photoelectrochemical cell in which a multilayer assembly of PSI complexes collects incident photonic energy and converts it into chemical energy
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how a multilayer system may be assembled within an electrochemical cell via a simple, single-step injection process without the use of expensive platinum salts or genetic mutations. We also report a dramatic enhancement in the photocurrent produced by these PSI multilayers with respect to photocurrents previously reported for monolayers of PSI (Faulkner et al., 2008). 2. Methods 2.1. PSI extraction
Fig. 1. Structure of plant Photosystem I. Chlorophylls oriented within PSI collect photonic energy and transfer it to a special pair of chlorophylls that make up the P700 reaction center. Upon receipt of this energy, charge separation occurs rapidly at P700 as an electron is released into an electron transfer chain to eventually reduce an iron–sulfur cluster, denoted FB, that is located on the opposite side of the protein complex. Atomic coordinates used in this figure are from PDB entry 2001 (Amunts et al., 2007).
to drive an electrical current through the cell. In a recent study, Frolov and coworkers have shown that multilayers of PSI complexes can be constructed via a multi-step process that involves the genetic mutation of PSI complexes and the subsequent platinization of their iron–sulfur centers, and further demonstrated that these multilayers display an enhanced photovoltage response with respect to monolayers (Frolov et al., 2008a,b). Here, we describe
PSI complexes were extracted from commercial baby spinach as described previously (Ciesielski et al., 2008). To briefly summarize the procedure, thylakoid membranes were isolated via maceration followed by centrifugation using the method of Reeves and Hall (1980) with several adaptations (Ciobanu et al., 2005). PSI complexes were then separated from the thylakoid membranes by additional centrifugation followed by purification using a chromatographic column packed with hydroxylapatite (Lee et al., 1992; Shiozawa et al., 1974). The product was characterized via UV–VIS absorbance spectroscopy (Baba et al., 1996). 2.2. Cell fabrication A schematic of the photoelectrochemical cell is shown in Fig. 2. The base of the cell serves as the cathode and consists of a 125 nm thick gold layer (J&J Materials) which was thermally deposited onto a silicon support (Montico Silicon, h1 0 0i orientation). The anode consists of indium tin oxide (ITO)-coated polyeth-
ITO-Coated Plastic Copper Tape
PDMS Spacer Electrolyte Solution PSI Multilayer Gold Electrode Silicon Support
76.1 nm
60.9 nm
45.7 nm
30.4 nm
15.2 nm
0.0 nm Fig. 2. Schematic of a PSI-catalyzed photoelectrochemical cell. Inset: AFM image of the surface of a PSI multilayer from a disassembled cell, scale bar 500 nm.
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0.11
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Fig. 3. Photoresponses of a typical PSI-catalyzed photoelectrochemical cell at varying light intensities. (a) The open circuit potential of the cell increases when the cell is irradiated due to the change in the concentrations of electrochemical mediators at the electrode surface. (b) The photocatalytic effect of the PSI multilayer is observed as an increase in cathodic current when the cell is irradiated. The current decays with time due to the depletion of electrochemical mediators in the vicinity of the electrode surface. The magnitude of the photogenerated increase in both current and voltage is dependent upon the intensity of light irradiating the cell.
ylene terephthalate (Aldrich), and was modified with a small strip of copper tape (3 M) on the surface of the ITO to facilitate the lateral conduction of electrons across the counter electrode. A spacer layer of polydimethylsiloxane (PDMS) (Sylgard) separates the two electrodes and effectively forms a small reservoir sandwiched between the two conductive surfaces. An aqueous electrolyte solution of 5 mM dichloroindophenol (DCIP) (Aldrich), 100 mM ascorbic acid (Asc) (TCI America), and 100 mM NaCl (Fisher) in 5 mM pH 7 phosphate buffer (Fisher) was injected into the reservoir until it was approximately half-filled. The oxidized form of the reversible DCIP/DCIPH2 redox couple that is present in mixtures of DCIP and Asc (Iyanagi et al., 1985) is a known oxidant of þ F B , (Izawa, 1980) and the reduced form is known to reduce P 700 (Vassiliev et al., 1997). Next, a buffer solution containing 9 lM PSI complexes suspended by Triton-X 100 surfactant (0.05% wt./ vol., Acros), 0.14 M Na2HPO4 (Fisher), 0.14 M NaH2PO4 (Fisher) in 0.2 M pH 7 phosphate buffer (Fisher) was similarly injected into the cell until the reservoir was filled. The total volume of the reservoir of a typical cell used in this study was approximately 100 lL. Following injection, PSI complexes in solution assemble at the gold surface over a period of several days, after which the dense multilayer can be seen as a green film on the electrode surface. The inset of Fig. 2 shows an AFM image of a PSI multilayer from the surface of the cathode of a disassembled cell that was rinsed with DI water and dried with nitrogen. The roughly spherical particles shown in this image vary in diameter from 10 nm, which is similar to previously reported values of the major axis of PSI complexes (Lee et al., 1995), up to several hundred nanometers for the larger particles, which are likely protein/surfactant agglomerates that formed in solution and deposited onto the surface. The PSI multilayer films were typically 1–2 lm thick as measured by profilometry (data shown in Supplementary material, Fig. S2). We have estimated the materials cost for a cell with 1 cm2 of active electrode area as approximately 10 cents. 2.3. Atomic force microscopy The AFM image presented in the inset of Fig. 2 was obtained from the surface of a PSI multilayer that was formed on the cathode of a cell. The cell had been operational for at least 3 weeks before it was disassembled, and the cathode was washed with deionized water and dried with nitrogen prior to imaging. AFM images were collected with a JSPM-5200 scanning probe microscope operated in tapping mode. The image presented in Fig. 2
was obtained from an area of 2.0 2.0 lm at a clock speed of 166.7 ls using a feedback filter at a frequency of 1.2 Hz and a loop gain of 8. 2.4. Photoelectrochemical characterization All electrochemical measurements were taken with a CH Instruments CHI660a electrochemical workstation equipped with a Faraday cage. The working electrode clip was attached to the gold layer on the cell base, and the counter and reference electrodes were clipped to the copper strip on the ITO-coated cover. The light source employed was a Gebrauch KL 2500 LCD lamp, and the intensity output from six different settings on this lamp was measured with a Coherent Radiation 210 Power Meter by positioning the detector in front of the source at a distance of 1 cm. Samples were also positioned 1 cm away from the source during characterization to ensure consistent light intensities were reaching the devices. Chronoamperometric data were collected at zero bias between the reference and working electrodes. 3. Results and discussion 3.1. Photoelectrochemical performance The typical responses of the open circuit potential produced by the cells (i.e. the potential between the Au base electrode and the Cu/ITO counter electrode) to irradiation with light of various intensities are shown in Fig. 3a. During the measurement of the open circuit potential, the potentiostat applies a voltage opposing that supplied by the cell in order to sustain a net current of zero. Thus, the heterogeneous reactions occurring at the electrode surface have a net rate of zero, which allows for the investigation of reactions that occur between mediators and PSI complexes in the multilayer that do not involve net charge transfer across the electrode/ electrolyte interface but still affect the mediator concentration in the vicinity of the electrode surface. Assuming that the heterogeneous reactions are reversible, single-electron transfer events that occur between the working electrode and the redox couple, the electrode potential EðtÞ is related to the concentrations of reduced and oxidized mediators at the electrode surface at time t by the Nernstian expression:
EðtÞ ¼ E00 þ
RT C O ð0; tÞ ln ; F C R ð0; tÞ
ð1Þ
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where E00 is the formal potential of the working electrode at standard conditions, and CO(0, t) and CR(0, t) are the respective concentrations of the oxidized and reduced forms of the mediator at any time t and position x = 0, where the system geometry is defined such that x = 0 at the electrode surface and increases in the direction of the surface normal. When the cells are irradiated, charge separation rapidly occurs within PSI complexes in the multilayer which prompts the formation of P þ 700 and F B reaction centers as described by Eq. (2): hm
P700 þ F B ! P þ700 þ F B :
ð2Þ
The photogeneration of these reaction centers has been shown to produce an electric field at the electrode surface, (Lee et al., 2000) which may contribute to the steep initial increase in the open circuit potential in response to light as shown in Fig. 3a. As irradiation persists, redox reactions occur between these P þ 700 and F B reaction centers and electrochemical mediators as described by the chemical equations
Pþ700 þ R ! P700 þ O;
ð3Þ
F B þ O ! F B þ R;
ð4Þ
where O and R represent the oxidized and reduced states of the electrochemical mediators, respectively. The change in the surface concentration of the mediator that results from these reactions drives the change in the open circuit potential displayed in Fig. 3a. In the context of Eq. (1), an increase in the open circuit potential is consistent with the increase in the ratio of CO (0, t) to CR (0, t), which indicates that the net effect of PSI-mediator reactions occurring within the multilayer described by Eqs. (3) and (4) is the conversion of R to the O state. This production of species O creates a substantial difference between its concentration near the electrode surface and that in the bulk, and diffusion occurs in response to this concentration gradient. This process is observed as a decrease in the open circuit potential as irradiation continues. When the light is turned off, photogeneration of Pþ 700 and F B ceases, which quickly halts reactions (3) and (4), and causes the open circuit potential to return to its original value as diffusion from the bulk electrolyte restores CO (0, t) and CR (0, t) to their bulk concentrations. The chronoamperometric behavior of a typical cell is shown in Fig. 3b. In dark conditions, a small cathodic current flows from the gold electrode as electrochemical mediators are reduced at the electrode surface. The observation of this dark current confirms that electrochemical mediators in the oxidized state are initially present at the electrode surface, and further that the PSI multilayer film is permeable to these mediators from the bulk solution. Again assuming that the electrochemical reaction occurring at the electrode surface in dark conditions is a reversible, single-electron transfer event, then the chemical equation describing this reaction can be written simply as O þ e ! R. The net current produced from this reaction at time t is the sum of the cathodic and anodic currents, and is given by
inet ðtÞ ¼ FA½kred C O ð0; tÞ kox C R ð0; tÞ;
sults in a buildup of the reduction product R near the electrode surface, which causes an anodic response when the light is turned off as this surplus is oxidized by the electrode. Similar cathodic photocurrent responses have been observed previously for PSI monolayers on planar (Faulkner et al., 2008) and nanoporous (Ciesielski et al., 2008) electrodes in the same electrochemical mediator system, and are attributed to the reduction of photoxidized Pþ 700 reaction centers that are electronically accessible to the electrode surface (Ciobanu et al., 2007). For this reduction to take place, PSI complexes oriented such that their P700 reaction centers are electronically accessible to the electrode must be photoexcited to initiate charge separation. The potentiostat measures an increase in cathodic current as P þ 700 centers are reduced by electrons from the electrode surface, and electrons must be continuously shuttled away from the terminal electron acceptor F B by the electrochemical mediators in order for this event to occur repeatedly during extended periods of irradiation. Similarly, F B sites proximal to the electrode may donate photoexcited electrons into the electrode, giving rise to an anodic current; however, the observation of a net cathodic current indicates that this process occurs significantly less frequently than the heterogeneous reduction of Pþ 700 . The PSI multilayers within the cells described in this work produce cathodic photocurrents that are 10–20 times larger than those previously reported for PSI monolayers on planar electrodes, which suggests that the multilayer assembly provides photocatalytic mechanisms in addition to the reduction of P þ 700 reaction centers in PSI complexes proximal to the electrode surface. We propose that this enhancement can be primarily attributed to the conversion of reduced electrochemical mediators to the oxidized state by PSI complexes in subsequent layers, which acts to maintain a higher concentration of the oxidized mediator species in the vicinity of the electrode. This re-oxidation of reduced mediators by the Pþ 700 reaction centers of PSI complexes in subsequent layers proceeds as described by Eq. (3) and is shown schematically in Fig. 4. Unlike a monolayer system in which reduced mediators
ð5Þ
where F is the Faraday constant, A is the area of the electrode, and kred and kox are the heterogeneous rate coefficients for the reduction and oxidation reactions, respectively. When the cell is irradiated, the photocatalytic effect produced by PSI complexes immobilized near the electrode surface produces an increase in cathodic current, which is accompanied by an increased rate of consumption of species O at the electrode surface. This process prompts the formation of a gradient in the concentration of O that propagates away from the electrode surface as time progresses and causes the current to decease as t1/2 (Bard and Faulkner, 2001). Prolonged irradiation re-
Fig. 4. Electron transfer events between PSI reaction centers, electrochemical mediators, and the electrode surface. Reduced and oxidized mediators may react with PSI’s photogenerated P þ 700 and F B reaction centers, respectively, as well as the electrode surface. The reaction centers of PSI may also undergo electron transfer events with the electrode surface directly; however, the observation of a net cathodic current indicates that the dominant reactions occurring at the electrode are the reductions of P þ 700 and oxidized mediators. PSI complexes in subsequent layers contribute to the photoinduced increase in cathodic current by providing sites for the re-oxidation of reduced mediators in close proximity to the electrode, which effectively increases the concentration of oxidized species near the electrode surface and provides more opportunities for heterogeneous reduction events to occur.
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Fig. 5. (a) Comparison of photocurrent response of a typical PSI-containing cell to experimental controls. Small dark currents are observed from all cells due to the spontaneous reduction of electron acceptors by the cathode. However, in the absence of PSI and chlorophyll, the electrolyte/mediator solution displays a negligible photoresponse. A cell that contains entire PSI complexes produces 2 orders of magnitude more photocurrent than one that lacks the protein but contains the same amount of chlorophyll. These responses were generated using a light intensity of 29 mW/cm2. (b) External photoconversion efficiency. The maximum external photoconversion efficiency can be estimated by taking the product of the photoresponses of the open circuit potential and the short circuit current density. The transient behavior of the current and voltage produced by the cells imply that the efficiency of the device is largely influenced by the diffusion of electrochemical mediators through the cell.
must diffuse to the counter electrode to be re-oxidized, P þ 700 centers in the multilayer assembly provide sites for this to occur in close proximity to the electrode surface, which acts to maintain the concentration of oxidized mediator at the electrode surface and facilitates cathodic currents of greater magnitude. The photoresponse of the open circuit potential implies that CO (0, t) increases in the absence of net heterogeneous reactions, which supports the assertion that the photocurrent enhancement provided by a PSI multilayer with respect to that of a monolayer is due to production of oxidized mediators within the multilayer. This proposed mechanism is also consistent with the findings of a study by Proux-Delrouyre and colleagues in which the authors observe a similar photoinduced enhancement of cathodic current produced by PSI complexes dissolved in the electrolyte and attribute this effect to the regeneration of an oxidized form of an electrochemically mediating protein by PSI (Proux-Delrouyre et al., 2003). In order to evaluate the photoactivity of the electrochemical mediators and supporting electrolyte in the absence of PSI, a cell was fabricated in accordance with the procedure presented earlier in this manuscript; however, instead of injecting the PSI-containing buffer solution, an identical buffer solution that did not contain PSI was injected. Another cell was similarly fabricated, and a buffer solution that contained only chlorophyll a (instead of the chlorophyll-containing PSI complexes) was injected to further highlight the role of the electrochemical functionality of PSI in this photocatalytic system. The total concentration of chlorophyll in the PSI suspension was determined by visible spectroscopy (Arnon, 1949) to be 0.78 mM; thus, a concentration of 0.8 mM was employed so that the control contained roughly the same chlorophyll concentration as the typical PSI-catalyzed cells. Fig. 5a presents a comparison of the photocurrent production from these control cells to that of a typical cell in response to irradiation of 29 mW/cm2. A very small photoresponse was observed from the cell that contained only mediator and electrolyte solution as indicated by a slight change in the current baseline during the periods of illumination. The chlorophyll containing cell produced a small photocurrent density of 10) remained photoactive as long as their reservoirs contained electrolyte solution. The electrolyte refilling procedure discussed previously was employed
7 6 5
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4 3 2 1 0 0 10
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Days After Fabrication Fig. 6. Photoelectrochemical cell stability. Peak photocurrent production occurs several days after cell fabrication, after which it decreases, perhaps due to the degradation of PSI complexes that lack adequate stabilizing interactions. An air bubble gradually formed in the electrolyte reservoir of the cell used in this particular study and the reservoir was refilled on day 126, after which the photocurrent production returned to a level similar to that observed 2 weeks after its fabrication. The final data point reported in this plot was collected 281 days after the sample was fabricated.
4. Conclusions
Acknowledgements We gratefully acknowledge financial support from the National Science Foundation (DMR 0907619), and IGERT fellowship (NSF 0333392) for PNC, a Summer Undergraduate Research Experience fellowship by the Vanderbilt University School of Engineering for FMH, and an NSF-RET award for LB. Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.biortech.2009.12.045. References Amunts, A., Drory, O., Nelson, N., 2007. The structure of a plant photosystem I supercomplex at 3.4 Å resolution. Nature 447, 58–63. Arnon, D.I., 1949. Copper enzymes in isolated chloroplasts. Polyphenoloxidase in beta vulgaris. Plant Physiology 24, 1–15. Baba, K., Itoh, S., Hastings, G., Hoshina, S., 1996. Photoinhibition of photosystem I electron transfer activity in isolated photosystem I preparations with different chlorophyll contents. Photosynthesis Research 47, 121–130. Bard, A.J., Faulkner, L.R., 2001. Electrochemical Methods: Fundamentals and Applications, second ed. Wiley & Sons, New York, NY. Bjorn, L.O., Govindjee, 2009. The evolution of photosynthesis and chloroplasts. Current Science 96, 1466–1474. Ciesielski, P.N., Scott, A.M., Faulkner, C.J., Berron, B.J., Cliffel, D.E., Jennings, G.K., 2008. Functionalized nanoporous gold leaf electrode films for the immobilization of photosystem I. ACS Nano 2, 2465–2472. Ciobanu, M., Kincaid, H.A., Jennings, G.K., Cliffel, D.E., 2005. Photosystem I patterning imaged by scanning electrochemical microscopy. Langmuir 21, 692–698. Ciobanu, M., Kincaid, H.A., Lo, V., Dukes, A.D., Jennings, G.K., Cliffel, D.E., 2007. Electrochemistry and photoelectrochemistry of photosystem I adsorbed on hydroxyl-terminated monolayers. Journal of Electroanalytical Chemistry 599, 72–78. Curri, M.L., Petrella, A., Striccoli, M., Cozzoli, P.D., Cosma, P., Agostiano, A., 2003. Photochemical sensitisation process at photosynthetic pigments/Q-sized colloidal semiconductor hetero-junctions. Synthetic Metals 139, 593–596. Das, R., Kiley, P.J., Segal, M., Norville, J., Yu, A.A., Wang, L.Y., Trammell, S.A., Reddick, L.E., Kumar, R., Stellacci, F., Lebedev, N., Schnur, J., Bruce, B.D., Zhang, S.G., Baldo, M., 2004. Integration of photosynthetic protein molecular complexes in solidstate electronic devices. Nano Letters 4, 1079–1083. Faulkner, C.J., Lees, S., Ciesielski, P.N., Cliffel, D.E., Jennings, G.K., 2008. Rapid assembly of photosystem I monolayers on gold electrodes. Langmuir 24, 8409– 8412. Frolov, L., Rosenwaks, Y., Carmeli, C., Carmeli, I., 2005. Fabrication of a photoelectronic device by direct chemical binding of the photosynthetic reaction center protein to metal surfaces. Advanced Materials 17, 2434–2437. Frolov, L., Rosenwaks, Y., Richter, S., Carmeli, C., Carmeli, I., 2008a. Photoelectric junctions between GaAs and photosynthetic reaction center protein. Journal of Physical Chemistry C 112, 13426–13430. Frolov, L., Wilner, O., Carmeli, C., Carmeli, I., 2008b. Fabrication of oriented multilayers of photosystem I proteins on solid surfaces by auto-metallization. Advanced Materials 20, 263–266.
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