Photosystem I Protein Films at Electrode Surfaces for Solar Energy

Invited Feature Article pubs.acs.org/Langmuir

Photosystem I Protein Films at Electrode Surfaces for Solar Energy Conversion Gabriel LeBlanc,† Evan Gizzie,† Siyuan Yang,‡ David E. Cliffel,† and G. Kane Jennings*,‡ Departments of †Chemistry and ‡Chemical and Biomolecular Engineering, Vanderbilt University, Nashville, Tennessee 37235, United States ABSTRACT: Over the course of a few billion years, nature has developed extraordinary nanomaterials for the efficient conversion of solar energy into chemical energy. One of these materials, photosystem I (PSI), functions as a photodiode capable of generating a charge separation with nearly perfect quantum efficiency. Because of the favorable properties and natural abundance of PSI, researchers around the world have begun to study how this protein complex can be integrated into modern solar energy conversion devices. This feature article describes some of the recent materials and methods that have led to dramatic improvements (over several orders of magnitude) in the photocurrents and photovoltages of biohybrid electrodes based on PSI, with an emphasis on the research activities in our laboratory.

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INTRODUCTION Photosynthesis is the process by which plants, algae, and cyanobacteria convert our most abundant energy source (solar radiation from the sun) into stored energy in the form of reduced carbon.1 This process has supported the energy demands of the earth since the beginning of life and continues to fuel our ever-increasing consumption through the use of fossil fuels derived from ancient plant material. Unfortunately, the release of this stored energy has, in recent years, resulted in numerous problems such as climate change, environmental pollution, political unrest, and insufficient supply chains.2 Thus, tremendous research effort has been focused on the area of alternative energy in order to provide new avenues for converting and storing energy. Of the many possible routes, solar energy is promising becaues of its abundance, availability, and safety.3 Since the discovery of the photoelectric effect in 1839,4 researchers have attempted to efficiently capture and convert sunlight into usable and storable energy. Materials such as silicon, ruthenium dyes, zinc oxides, and other metal mixtures have provided the bases for state-of-the-art devices. Until recently, nature’s stunning photosynthesis process was neglected as a research avenue for achieving solar cells and devices, despite growing appreciation for its remarkable and highly efficient nanoscale, photoelectrochemical protein complexes. One of these nanoscale protein complexes is photosystem I (PSI). PSI is an ∼500 kDa membrane protein complex found in most organisms that perform oxygenic photosynthesis.5 In the process of photosynthesis, PSI operates as a photodiode, photoexciting electrons across the thylakoid membrane in roughly 1 μs with an internal quantum efficiency approaching unity.6 The speed and efficiency of this charge transfer and separation are due to the protein’s ability to move the excited electron down an internal electron-transfer chain (Figure 1). © XXXX American Chemical Society

Figure 1. Structure of PSI highlighting the bound chlorophylls in the membrane portion of the protein and the electron-transport chain beginning with the P700 reaction center and ending with the FB iron− sulfur complex. Atomic coordinates used to make this image are from PDB entry 2o01.7 Image reproduced with permission from Ciesielski.8

The energy of each step is slightly lower than that of the proceeding step, thus thermodynamically favoring a unidirectional electron flow. Once the electron reaches the terminal iron−sulfur complex (FB), it is ushered along to the next step of photosynthesis by the soluble redox protein ferredoxin. On the other side of the protein, the vacant “hole” in the reaction center (P700) is filled with an electron from the soluble copper-containing protein known as plastocyanin or a small heme protein known as cytochrome c.5 Received: January 15, 2014 Revised: February 25, 2014

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dx.doi.org/10.1021/la500129q | Langmuir XXXX, XXX, XXX−XXX

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Invited Feature Article

Because of the rapid charge separation and efficiency of PSI, researchers from around the world have investigated the incorporation of this nanophotodiode into functional devices.9 Research toward this end was first reported by Greenbaum in 1985,10 in which chloroplasts were modified with platinum for the photocatalyzed production of hydrogen. In this work, Greenbaum took advantage of the reducing power of PSI to photoreduce catalytic platinum on the surface of the chloroplast. Further illumination resulted in the production of hydrogen as the photoexcited electrons were passed directly into the platinum catalyst. Greenbaum then demonstrated how platinum-modified PSI could be immobilized on fiberglass filter paper.11 In doing so, he was able to make electrical contact with a metal electrode, thus enabling the generation of a sustained current under illumination and exposing the field to the possibility of using photosynthetic biological materials for the direct conversion of solar energy to either a fuel (hydrogen) or electricity. Since then, several groups have used PSI as a photoactive material for hydrogen production.12−15 The photoreduction of platinum on PSI has also been used to anchor PSI reaction centers onto metal surfaces16 and, more recently, for the organization of multilayer films of genetically modified PSI.17 In 1997, Greenbaum and co-workers moved away from PSI-Pt hybrid materials and reported that PSI proteins function as individual photodiodes on an electrode surface18 by using scanning tunneling spectroscopy to generate current−voltage (I−V) measurements on individual proteins. The orientation of the protein on the electrode surface was correlated with different I−V scan shapes. More recently, Gerster and co-workers used a metalized scanning near-field optical microscopy tip to measure the photocurrent of a single photosynthetic protein (10 pA).19 These single-molecule studies highlight the tremendous opportunities for incorporating PSI into functional devices. Progress toward electrochemically integrating PSI with an electrode was achieved from 2001 to 2003.20,21 In 2004, Baldo and co-workers employed PSI monolayer films as the active component in a solid-state photovoltaic device.22 Over the past 10 years, there have been numerous groups around the world, including our own, that have worked to improve the artificial electron transfer to and from PSI in biohybrid devices. Research at Vanderbilt University alone has demonstrated a photocurrent increase by over 5 orders of magnitude (Figure 2). These dramatic increases have resulted from a number of distinct methods for integrating PSI with electrode surfaces. Our first photocurrent measurements were made by physically adsorbing a sparse layer of PSI onto an electrode.23 By creating covalent attachments between PSI and the electrode materials, we found that photocurrent production increased dramatically as a result of the improved electronic interaction and higher coverage of PSI.24 To increase the light absorption of the biohybrid electrode, we increased the surface area of our underlying electrode25 and utilized thick multilayer films of PSI.26,27 Finally, we demonstrated the advantage of changing our underlying electrode material from a metal to a doped semiconductor that could direct electron flow through the system.28 The subsequent sections of this feature article describe the methods and materials that have enhanced the solar conversion performance of biohybrid devices based on PSI. A brief description of the extraction method for PSI from higher-order plants is followed by a few of the deposition strategies used to incorporate PSI with electrode materials. We then describe the

Figure 2. Reported photocurrents by the Jennings/Cliffel team at Vanderbilt University over the past 7 years. The photocurrent value is listed adjacent to each data point, as is the manuscript from which the data were obtained.

various methods for examining PSI in an electrochemical cell. The effects of altering the electrode material and the electrochemical mediator as well as the incorporation of additional materials within a film of PSI are explained. Finally, we conclude with an outlook on the direction of this field.

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EXTRACTION OF PSI PSI used as the integral component in biohybrid electrodes has been extracted from higher green plant leaves as well as cyanobacteria. PSI from higher plants is monomeric in form, existing as a complex of 17 smaller protein subunits, ∼180 chlorophylls, 2 phylloquinones, and 3 iron−sulfur complexes.29 The most common plant source for PSI in these studies has been spinach, due in part to the widely employed extraction protocols developed by Reeves and Hall.30 Our adapted version of this protocol is shown in Figure 3 where PSI is removed from the thylakoid membrane of spinach using Triton-X 100 solubilization followed by filtration and centrifugation steps as well as dialysis to remove residual salts and surfactant if needed on the basis of the end use.27 PSI concentrations from this extraction range from 0.1 to 10 μM, and the number of

Figure 3. General PSI extraction procedure for higher-order plants. The procedure follows the general methods described by Baba et al.,33 Shiozawa et al.,34 Reeves and Hall,30 and Ciesielski et al.27 This figure was reproduced with permission from Ciesielski.8 B


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an assembly process where the pressure above the aqueous PSI solution is reduced to evaporate the water rapidly and concentrate the PSI into a visibly green film of protein, surfactant, and salt on the surface.24 Subsequent rinsing removes all but the first layer of bound protein, resulting in dense monolayers that exhibit comparable photocurrents to those where PSI adsorbs from solution over 2 days. Electrophoretic deposition, in which an aqueous PSI solution is confined between two electrodes bearing an applied potential difference, is an alternative way to deposit PSI onto electrode surfaces.41,44,45 In these studies, a SAM-coated gold electrode served as the anode where a monolayer of PSI trimers was electrophoretically deposited with a potential difference of −2 V over several minutes. As compared to solution adsorption, the electrophoretic deposition provides enhanced adsorption of PSI45 and reduces aggregation to yield more uniform PSI monolayers, as evidenced by AFM images.41 Another way to deposit PSI monolayers is to exploit the insolubility of PSI in water and thus its tendency to partition to the air−water interface.46,47 A film of PSI at this interface can be compressed into a dense monolayer via a Langmuir trough and transferred onto a substrate through various approaches. This method offers key advantages, including controllable PSI coverage based on the applied 2D pressure,46 a wider selection of substrates, and the capability of forming multilayered structures with a known, precise number of layers. We recently showed that PSI monolayers transferred from the air−water interface to a hydroxyl-terminated SAM/Au substrate exhibit opposite orientations, depending on whether the transfer is by Langmuir−Blodgett (removing a preimmersed substrate, oriented perpendicular to the air−water interface, from solution) or Langmuir−Schaefer (pressing a horizontal substrate, face down, to the air−water interface).46 Under these conditions, the air−water interface was able to orient 57% of the adsorbed PSI complexes with the electron-transfer vector pointed toward the air phase. Although PSI monolayers are very useful for fundamental studies, the ability to deposit thicker, multilayer films of PSI enables increased absorption of light and vastly improved photoelectrochemical performance.26−28,48 A key to obtaining these thicker films rapidly is first to dialyze the extracted PSI solution to reduce the concentration of surfactant. Then, we employ the rapid assembly method described above where reduced pressure causes water to evaporate, concentrating the PSI into a dense film (Figure 4).27 With little surfactant remaining with the PSI after dialysis, subsequent rinsing of the visibly thick PSI film does not remove it. The PSI film thickness can be enhanced by repeating this process, demonstrating a growth of 390 nm (∼40 monolayers of PSI) per deposition based on the concentrations and conditions established in our prior work.27 Through this approach, we were able to prepare 2.6-μm-thick PSI films that exhibited photocurrents that were 100 times greater than our best PSI monolayers.27 The dialyzed PSI solution is critical to achieving this multilayer film; an undialyzed PSI solution would contain significant surfactant such that rinsing the deposited film would remove all components except the first bound layer of PSI.24 Although the multilayered PSI films described above do not likely result in preferential PSI orientation, Toporik et al.49 have provided insight as to the remarkable properties that could be achieved if assembly strategies were able to orient PSI serially in a thick film. One method of orienting PSI in three dimensions is crystallization. Recently, Toporik et al.49 prepared individual

externally bound chlorophylls per PSI complex can be varied from 180 down to ∼40. Rögner and co-workers developed a notable advance in PSI extraction in 1990 by employing βdodecylmaltoside as the surfactant in an improved process.31 Through this method, which is used by many in the biohybrid community, crystal structures of PSI at ultrahigh resolution can be obtained.32 Because PSI in higher plants is homologous,34,35 PSI extracted from different plant sources under similar conditions is expected to exhibit similar performance on an electrode. To demonstrate that PSI can be extracted from nonfood plant sources, Gunther et al.36 reported the preparation and performance of PSI films extracted from Pueraria lobata (kudzu), a rapidly growing, invasive vine that covers nearly a million hectares of the southern U.S.37 PSI complexes were extracted from kudzu leaves following the method of PSI extraction from spinach27 and then deposited onto lightly doped p-Si. Although kudzu PSI films on silicon demonstrated significant photocurrent enhancements over that of uncoated silicon, the concentration of kudzu PSI in the extract was 10fold lower than what is typically achieved with spinach. Thus, additional processing steps were required to achieve similar film thickness and performance for kudzu PSI as compared to spinach PSI. These results show the critical importance of the concentration or yield of active PSI that is extracted as well as the biomass production of the source, when considering a longterm source of PSI for scale up in potential applications. Another common source of PSI in biohybrid devices is the thermophilic cyanobacterium, Thermosynechoccus elongatus.12 A key advantage of this source is that PSI exists as a trimer that may be more thermally stable and robust for many solar applications. As an example, Iwuchukwu et al.12 compared hydrogen production from platinized PSI obtained from T. elongatus to that from mesophilic cyanobacterium Synechocystis PCC 6803. Thermophilic PSI was better able to maintain its chlorophylls as temperature was increased and its Pt-catalyzed hydrogen production increased up to 55 °C, whereas that for PCC 6803 continually decreased as the temperature was increased to above room temperature. In comparison to platinized monomeric PSI from spinach from earlier studies,38 the thermophilic PSI achieved plateau hydrogen generation at 4× greater light intensity, perhaps owing to its smaller antenna size.

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DEPOSITION OF PSI ONTO ELECTRODES PSI films are commonly deposited as (sub)monolayers for fundamental investigations into adsorption,39−41 orientation,18,42,43 or electron transfer.23 Perhaps the simplest way to form a monolayer of PSI is to allow the protein complex to adsorb onto a surface from aqueous solution, in which the extraction surfactant (e.g., Triton X-100) helps to suspend PSI in solution and inhibit the formation of multilayers on the surface.24,39 The substrate in these cases is often a metal or metal oxide that is terminated with an ultrathin self-assembled monolayer (SAM) to facilitate physical, electrostatic, or covalent interactions with the protein24 without providing an insulating barrier against electron transfer between the substrate and the protein (vide infra).23 We showed that the photocurrent for these single-layer PSI films is maximized as their coverage approaches the complete monolayer level and that long (48 h) adsorptions of PSI from solution are required to achieve these sufficiently dense monolayers.24 To greatly accelerate this process to a fraction of an hour, we introduced C


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trapping in deep centers in the vicinity of the FB acceptor to produce a very large net photoexcited dipole. The measured photovoltages gave rise to internal electric fields as large as 100 kV cm−1, which is higher than any reported inorganic material system. In addition, PSI crystals were expected to be stable for years under multiple light-induced photovoltage cycles with an approximate efficiency of 4.8−10%. The ability to orient PSI in films, and not just as single crystals, with inexpensive and rapid processing could lead to major advances in the performance of biohybrid electrodes.

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ELECTROCHEMICAL ANALYSIS PSI is an integral membrane protein with well-studied redox centers accessible on opposite sides of the supercomplex. Located on the stromal side are the iron sulfur clusters, denoted as FA and FB, and located on the luminal side is the P700 “special pair” chlorophyll dimer, which is buried within the protein and accessed only in vivo by the docking of plastocyanin. The unique accessibility of these two redox components of the protein have proven to make it quite useful as a biomolecular photodiode for use in biohybrid solar energy conversion. For the successful construction of PSI biohybrid devices, the thermodynamics and kinetics of electron transfer between biological redox centers of PSI and electrode surfaces must be understood. Through the use of electroparamagnetic resonance spectroelectrochemical measurements,50 the energetics of electron transfer in PSI has been explored. Through the use of square wave voltammetry, Ciobanu et al.23 were able to identify the presence of the stromal-side FA/FB and the luminal side P700/P700+ redox couples in a single voltammogram for the first time. Hydroxyl-terminated SAMs were used on gold electrodes to adsorb monolayers of the solubilized protein for direct electrochemical measurement. The observation of FA/FB and P700/P700+ redox couples present in a single voltammogram indicates the presence of a monolayer of PSI with mixed orientation on the SAM-modified electrode. The experimentally determined redox potentials of −0.36 V (vs NHE) and +0.51 V (vs NHE) for FA/FB and P700/P700+, respectively, are in good agreement with values from others who observed only the FA/FB and P700/P700+ redox couples separately.20,21 To determine the photocurrent production of a biohybrid electrode, a three-electrode electrochemical experiment known as photochronoamperometry is commonly employed.23−28,45 In these experiments, the working electrode is held at a constant potential (commonly the open circuit potential under dark conditions) and is eventually illuminated for a short period of time while the current change is measured. Using the open circuit potential enables the researcher to analyze the effect of illumination of the biohybrid electrode under equilibrium. In some studies, a fixed potential is chosen to favor electron flow to or from PSI. Such an overpotential would not exist under equilibrium conditions, as is the case for a stand-alone device. Nonetheless, the use of overpotentials can be an informative tool for performing more fundamental analysis of the biohybrid electrode. As shown in Figure 5, the current density under illumination decays according to the Cottrell equation,

Figure 4. General procedure for the deposition of thick “multilayer” films of PSI. As depicted, the thickness of the resulting film can be adjusted by repeating the deposition process or by using different concentrations of PSI in the solution. The bottom panel shows an SEM image of the cross section of the film following seven deposition steps. Image reproduced with permission from John Wiley and Sons. Image originally published in ref 27.

crystals of PSI and used Kelvin probe force microscopy (KPFM) to measure the photopotentials across the dry crystal on a substrate, reporting nearly 20 V under solar conditions (0.14 W/cm2) and up to 45 V at 1 W/cm2. These large photopotentials were attributed to the superposition of properly aligned individual PSI centers along with electron

i(t ) =

nFAD1/2C π 1/2t 1/2

(1)

where i is the current density, t is the time, n is the number of electrons, F is Faraday’s constant, D is the diffusion coefficient D


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species consumed at the SECM tip. On the basis of the relatively slow kinetics of the PSI film itself, the tip consumes Fe(CN)63− faster than the PSI film can regenerate it, thus a true positive feedback loop was not experimentally observed. However, using computational simulations, a rate constant for the PSI film was approximated as 0.0032 cm/s.52 SECM is also a powerful technique for its ability to image surfaces and map electrochemical activity through a series of raster scans across a substrate, as demonstrated in LeBlanc et al.48 In this study, platinum clusters were prepared on PSI films for the first time via photoreduction, which ensures that the catalytic platinum assembles on the PSI film directly coupled to the redox-active sites (FB/FB−) of the protein. As shown in Figure 6, the platinum clusters were imaged on the surface of

Figure 5. Sample photochronoamperometic analysis of a PSI-modified electrode. Here, the electrode was held at the experimentally determined open circuit potential under dark conditions and the current was measured as a function of time. The sample was illuminated for 20 s (from 20 to 40 s). Figure 6. SECM image of the catalytic activity of platinum particles photoreduced by PSI atop a PSI film. The bright colors indicate hot spots of hydrogen generation that are roughly equivalent in size to the particles imaged using SEM. Image reproduced with permission from the American Chemical Society and originally published in ref 48.

of the mediator, and C is the concentration of the mediator. Thus, according to eq 1, the current will decay as t−1/2. In practice, the values shortly after illumination are unreliable because of nonfaradaic contributions to the total current, limitations of the potentiostat, and limitations of the recording device. Additionally, at times longer than 20 s the buildup of density gradients and stray vibrations can cause disruptions to the diffusion layer, preventing the assumptions of the Cottrell equation from holding true.51 Additional assumptions required for the Cottrell equation to apply include the following: (1) mass transport of the charge carrier is limiting, (2) no charge recombination of the charge carrier takes place, and (3) no recycling of the charge carrier at the counter electrode takes place. Because of these limitations, we often report the photocurrent density after 10 s of illumination, when the values can be compared with higher accuracy (Figure 2). Following the illumination process, a current reversal can commonly be observed. This reversal indicates the flow of electrons in the opposite direction caused by the sudden change in the voltage at the biohybrid electrode after the illumination source has been removed. Thus, the electrode undergoes a second voltage pulse that can generate a short reversal in current before the system returns to the dark equilibrium conditions. Scanning electrochemical microscopy (SECM) is an electrochemical analysis technique that is useful in characterizing films of PSI. In 2013, Chen et al. utilized SECM approach curves under both light and dark conditions to evaluate the feedback loop generated between an ultramicroelectrode tip and the PSImodified substrate.52 In this study, a negative feedback loop (indicating a drop in current) was observed when PSI films were not illuminated. This observation confirms the hypothesis that PSI acts as an insulating layer on the electrode surface in the dark. Approach curves performed under illumination conditions resulted in a higher current as compared to the dark case, indicating that the PSI film is regenerating the redox

the PSI/Pt composite by raster scanning a Pt SECM tip over the surface. The “hot spots” of electrochemical activity, indicated by increased current measurements, demonstrate where the biohybrid electrode is generating H2 that can then be collected and oxidized by the SECM tip electrode to complete the H2/H+ feedback loop. To decouple and quantify the electrochemical interactions among PSI, the electrochemical mediator, and the electrode surface, Ciesielski et al. 53 combined experiments and simulations to model a PSI monolayer with mixed orientation on a gold surface prefunctionalized with an aminoethanethiol/ terephthaldialdehyde (TPDA) SAM. In this work, Ciesielski was able to derive a model from the Butler−Volmer equation describing the net photocurrent output for the randomly oriented monolayer of PSI. This model takes into account the ratios of PSI oriented upward (χup) or downward (χdown), the electron-transfer reactions between the electrode and both the P700 and FB ends of PSI, and the concentrations and heterogeneous rate constants for diffusional mediators that donate or accept electrons from the PSI monolayer and the gold electrode. Using this model, kinetic and electrochemical parameters were obtained by iteratively minimizing the residual between predicted current densities and photochronoamperometric experiments performed over a wide range of overpotentials. With the determined parameters, simulations were performed to predict that the significant photocurrent density predicted for a PSI film would be lost as a result of competing electrochemical reactions unless ∼80% of the PSI complexes in the film were oriented similarly. Thus, attachment strategies that lead to selective orientations, including but not limited to E


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Figure 7. Representation of a mixed-orientation monolayer of PSI on a gold electrode surface. The net photocurrent produced by this system is a result of several competing electrochemical reactions between the upright orientation (shown on the left) and the inverted orientation (shown on the right). Image adapted with permission from the American Chemical Society and originally published in ref 53.

Table 1. Comparison of Various Self-Assembled Monolayers (SAMs) Used to Attach PSI to Gold Electrodes SAM on gold electrode

method of attachment

PSI adsorptiona

electrochemical signala

ethanethiol hexanethiol octanethiol 2-mercapto-1-ethanol 4-mercapto-1-butanol 6-mercapto-1-hexanol 8-mercapto-1-octanol 11-mercapto-1-undecanol thioacetic acid mercaptoacetic acid 3-mercaptopropionic acid 8-mercaptooctanoic acid 2-amino-1-ethanethiol 6-amino-1-hexanethiol 8-amino-1-octanethiol 11-amino-1-undecanethiol 2-dimethylaminoethanethiol 4,4′-dithiodipyridine tiopronin terephthaldehydeb N-hydroxysuccinimidylb vitamin K wireb cytochrome c cysteine mutation

physical physical physical physical physical physical physical physical physical electrostatic electrostatic electrostatic electrostatic electrostatic electrostatic electrostatic electrostatic physical electrostatic covalent covalent reconstitution molecular relay covalent

low none low high high high high high low high high moderate low moderate high high low low high high high moderate high high

N/A N/A none low none moderate moderate none N/A high low high low high low none N/A N/A none high moderate high high N/A

reference 58 23 24, 23, 23 23 23 23 58 21, 23, 57 21, 57 57 57 58 21 23 24, 24 55 56 54,

57 58

58 24 24, 57

25

59

a

Relative levels (high, moderate, or low) are based on comparisons within a given manuscript or between manuscripts using similar methods or SAMs. bThe use of these attachments requires an underlying SAM to bind to the gold surface.

genetic mutations54 and subunit replacements,22,55 could lead to PSI films with high photoconversion performances.

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Gold has commonly been employed as an electrode material for the analysis of PSI films because it is an inert material with a relatively wide potential window for electroanalysis.16,21,23−25,38,55−57 Furthermore, gold is easily modified using self-assembled monolayers (SAMs) to change the interfacial composition and facilitate interaction with PSI.18,24,39 Many of the SAMs used to interface PSI with the gold electrode can be found in Table 1. Of these SAMs, nalkanethiols that expose dense methyl surfaces generally do not adsorb PSI because of the presence of the extraction surfactant that tends to adsorb to the low-energy surfaces in water and

ELECTRODE CHOICE AND MODIFICATION

Recent advancements in the photocurrent production from PSI-based electrodes have centered on the electrode material and modification. Here, we describe how the choice of electrode material and the modification of the electrode can have a tremendous impact on the resulting photocurrent of a biohybrid electrode. F


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fold photocurrent improvement over that of a monolayer film deposited on a similar substrate.24 The photocurrent improvement observed for films this thick suggests that the protein film is able to transport electrons. This idea has recently been supported by an SECM study that measured the kinetics of electrochemical reactions through these thick PSI films.52 Beyond the use of metal electrodes such as gold, the deposition of PSI onto semiconducting electrodes has recently led to dramatic increases in photocurrent resulting from these doped semiconductors favoring electron transfer in a single direction. For example, n-doped semiconductors favor electron conduction whereas p-doped semiconductors favor hole conduction. The advantage of this approach with PSI-based devices was first demonstrated by Carmeli and co-workers, who described the interface of PSI with GaAs.60,61 These studies describe the ability to covalently bind genetically modified PSI to GaAs to generate a dry-oriented junction with KPFM. The researchers found that they could control the photovoltage direction (positive vs negative) by changing the dopant type of the GaAs electrode.60 In a separate study, the researchers found that the electron transfer between PSI and n-doped GaAs was on the time scale of picoseconds.61 The advantage of controlling electron flow was also demonstrated by our research group using silicon.28 We found that p-doped Si has the appropriate Fermi energy to transfer electrons to the P700 reaction center of PSI, but its bandgap is too large to receive electrons from the protein, which helps to alleviate some of the issues related to the orientation of PSI observed on metal electrodes. In other words, PSI complexes that are oriented in opposite directions no longer cancel out as they would on a metal electrode because the electrode itself favors electron flow in a particular direction. Using PSI films on p-doped silicon, we have achieved a photocurrent of 0.9 mA/cm2 (Figure 2). In 2012, Mershin and co-workers reported the use of TiO2 and ZnO electrodes in conjunction with PSI.62 In this case, the intrinsic n-doping of the metal oxide favors oxidation reactions at the working electrode (opposite of p-doped silicon). To take advantage of this fact, the researchers developed unique PsaE and PsaD subunits that would bind to ZnO and facilitate the orientation of PSI. Because these subunits are located near the FB site of PSI, the electrons are shuttled from the protein to the semiconducting electrode. Furthermore, the band gap of these semiconductors not only aids in the direction of the electron flow but also allows light to pass through the electrode material, enabling PSI to absorb the incident photons before they pass through the electrochemical mediator. Integrating PSI with carbon-based electrodes provides the potential to produce an all-carbon biohybrid solar cell. Graphene, a transparent carbon-based electrode, has received much attention recently because of its unique electronic and optical characteristics.63 We have generated an ultrathin photoelectrode consisting of a single atomic layer of graphene plus a single monolayer of PSI.64 The transparent nature of this biohybrid system enables the use of an opaque redox mediator at high concentrations because the system can be illuminated through the electrode rather than through the mediator. Carbon nanotubes (CNTs), another carbon nanomaterial, were used as electrodes for PSI immobilization by researchers at Tel Aviv University.65−67 They first reported the covalent attachment of genetically modified PSI with maleimide-functionalized CNTs,65 and they were then able to measure the photoconductance of these systems by bridging gold contacts with

present an interface that inhibits protein attachment.39 Surfaces that provide hydrophilic functional groups,58 including hydroxyls that interact with PSI via hydrogen bonding and other weak physical interactions as well as carboxylic acids and amines that interact with PSI via electrostatic interactions, enable greater extents of PSI adsorption. When focusing on a common family of SAMs, the chain length of the molecular tether plays an important role in both the adsorption of PSI and electron transfer between the protein complex and the electrode (Table 1). In a study of PSI adsorbed onto hydroxyl-terminated SAMs, Ciobanu et al.23 were able to observe a significant photocurrent response only with a tether length of six or eight carbons. This ideal chain length was also observed in a separate study by Kondo and co-workers using amine-terminated SAMs.57 SAMs with shorter tethers are believed to pack poorly and not present a dense 2D surface for protein adsorption, whereas longer tethers provide too great of an electron tunneling barrier that slows electron transfer to the protein. SAMs that can covalently bind with PSI, such as those exposing terephthaldialdehyde and n-hydroxysuccinimide groups that can bind to lysine residues of PSI, tend to yield high coverages and good photocurrents.24 However, because lysine residues are abundant on both the luminal and stromal sides of PSI, these covalent approaches are not likely to yield selective orientations. More recently, methods to orient PSI selectively on gold electrodes have been investigated.24,25,54−56 In one elegant study, Terasaki and co-workers were able to “plug” a molecular wire into PSI by reconstituting the vitamin K1 in PSI isolated from T. elongatus55 to extract electrons efficiently at the A1 site rather than at the FB site and relay them to the underlying electrode. In a separate study, Frolov and coworkers were able to attach PSI directly to a gold electrode by genetically modifying amino acids on the stromal side of PSI to cysteines54 to bind PSI directly to the gold electrode through a gold−thiolate bond. After demonstrating PSI assembly on a gold electrode, they demonstrated the photoactivity of the system by measuring the photopotential with KPFM. Additional efforts to orient PSI on the surface of a gold electrode were performed by Kondo and co-workers using a polyhistidine tag.59 The researchers were able to use this tagging system to orient PSI in either the up or down position by fusing the tag to the C or N terminus, respectively, of the light-harvesting system. Using point-contact current imaging atomic force microscopy, the researchers reported up to a 63% orientation. Although planar gold electrodes provide a simple platform for electrochemical and spectroscopic analysis, the photocurrent of the system is limited by the absorption cross-section of the PSI complex (∼10 nm). Our research group has developed two methods for addressing this issue. The first was to use a nanoporous gold leaf electrode.25 When the silver is leached out of a thin gold−silver alloy, nanopores are generated in a meshlike structure with the average pore size controlled by varying the leaching time to enable an optimal pore size to be determined. We observed that large poresthose an order of magnitude larger than PSIwere required for the protein to access the entire surface area of the mesh electrode. The increased electrode surface area resulted in an 8-fold increase in photocurrent when compared to that of a planar electrode. The second method, described in a previous section, increases the absorption cross-section by simply depositing a thick multilayer film of PSI on the electrode rather than just a monolayer.27 PSI films as thick as 3 μm have been deposited, resulting in an 80G


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the PSI-modified CNTs.66 They found that the orientation of the PSI complex with respect to the carbon nanotube was dependent on the binding mechanism.67

As described above, the use of semiconductor electrodes can have a pronounced effect on the electron flow through the biohybrid system.28,62 In our work with p-doped silicon,28 we found that a mediator with a more negative formal potential, methyl viologen, greatly outperformed mediators with more positive formal potentials. This is because the p-doped silicon favors electron transfer to the P700 reaction center. Thus the mediator must efficiently shuttle electrons away from the FB site of PSI. In this case, the formal potential of FB lies much closer in energy to the formal potential of methyl viologen than to those of ruthenium hexammine and ferricyanide. Conversely, Mershin and co-workers used a cobalt-based mediator that possessed a more positive formal potential.62 This mediator worked best for their system because the underlying ZnO or TiO2 electrode is inherently n-doped and thus favors electron transfer with the FB site of PSI. Thus, the mediator in this system must shuttle electrons to the hole generated in the P700 reaction center of PSI.

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ELECTROCHEMICAL MEDIATORS An important consideration in the design of PSI-derived biohybrid solar energy conversion devices is the selection of a redox mediator to facilitate electron transfer from the protein to the electrode. In 2013, Chen et al.68 performed a systematic study of redox mediators in order to maximize the photocurrent output of PSI multilayer films on gold. According to the study, two of the most important considerations in mediator performance are the formal potential of the mediator and its optical absorbance properties. Enhanced photocurrent densities were observed in systems that utilized mediators with formal potentials near or more positive than the formal potential of P700, as shown in Figure 8. A trend of increasing photocurrent

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PSI COMPOSITES PSI-composite materials provide potential advantages over pure assemblies of the protein, including directed electron transfer from protein to electrode, enhancement of the protein lifetime, and the elimination of expensive metallic electrodes. Osmiumbased metallopolymers provide a particularly attractive means of integration with PSI because of their adaptable formal potential and high electron diffusion coefficients. A major milestone in the preparation of such composite films was achieved in 2011 by Badura et al.69 through the development of redox-active metallopolymers cross-linked with PSI. In this study, polyvinylimidazole was loaded with Os(bipy)2Cl coordination compounds, which when cross-linked with cyanobacterial PSI produced a photocurrent density of 29 μA/cm2. These osmium-containing hydrogels act to improve the electron transfer between PSI and the electrode components greatly via an electron-hopping mechanism between metal centers bound to the polymer side chains. Building upon this study, Kothe and co-workers developed a Z-scheme mimic based on PSI and photosystem II (PSII) that were embedded into osmium-based metallopolymers.70 In this study, two different metallopolymers were prepared with formal potentials of 0.395 and 0.505 V versus NHE. By using these two different polymers, the researchers were able to efficiently transport photoexcited electrons from PSII to PSI in the same way that cytrochrome b6/f and cytochrome c6 perform this task in nature. Thus, the researchers demonstrated the feasibility of connecting a PSII anode with a PSI cathode. These studies demonstrate the ability to integrate photoactive proteins into a supporting matrix to form a functional composite material. Future studies focusing on the use of supporting materials that are less expensive and easier to prepare than the osmium-based metallopolymers described in this section may provide robust systems capable of scale up. We anticipate that the use of these systems can significantly improve the integration of PSI with electrode materials, placing less emphasis on the orientation of PSI while using less of the protein.

Figure 8. Energy diagram relating the formal potential of each studied mediator couple relative to the formal potentials of FB and P700 of PSI. From the photocurrent−formal potential plot for a PSI multilayer on gold on the right, a general trend exists where mediators with more positive formal potentials perform better than those with more negative formal potentials. Image adapted with permission from The Electrochemical Society. Original image published in ref 68.

is observed as the formal potential of the redox couple becomes more positive; however, a break in the trend occurs with methylene blue (MB) and 2,6-dichlorophenolindophenol (DCPIP) at −0.2 and 0.09 V (vs Ag/AgCl), respectively. To explore this result, an absorbance study of each mediator was performed. MB and DCPIP both form dark-blue solutions in aqueous media and have strong absorbances in the same spectral region as PSI. Because of the overlap in absorbance between these mediators and PSI, the overall photocurrent output of PSI-modified electrodes becomes limited. When deposited on gold electrodes, PSI multilayer films must be illuminated through the mediator; thus, for strongly colored mediators that absorb in the same region as PSI’s Qy transition band or Soret band, a diminished photocurrent yield is observed, especially with high mediator concentrations (>20 mM). This study has concluded that for a randomly oriented PSI multilayer on gold electrodes, ferricyanide acts as the most effective electrochemical mediator, producing 900 nA/cm2 at a concentration of 200 μM. The high performance of this mediator in this study is attributed to its relatively high formal potential, 0.2 V (vs Ag/AgCl), and minimal spectral overlap with PSI’s Qy transition band. Additionally, metal-based redox mediators generally exhibit faster electron transfer with PSI’s cofactors as compared to nonmetallic, organic mediators.

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CONCLUSIONS AND OUTLOOK Although mankind has developed novel materials to convert photons into charge separation for roughly 175 years, nature has spent billions of years perfecting the photosynthesis H


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Biographies

process. PSI, a beautifully complex nanomaterial that nature produces daily in gross tonnage on a global scale, provides a unique resource to utilize in the development of affordable, safe, and efficient devices for solar energy conversion. Here, we have described some of the advances in this field over the past decade with historical scientific underpinnings dating back a quarter century. Looking to the future, we anticipate that the development of these biohybrid technologies will focus on optimally designed materials to interface with PSI to produce robust systems with synergistic properties as well as the facile assembly of PSI to achieve highly oriented and organized thin films. The selection of electrodes, mediators, and composite matrices with optimal properties (Fermi levels, formal potentials, selective conductivities, etc.) for seamless integration with PSI is required to continue the trend of exponential performance improvements over the next few years. With regard to composite materials, a focus on less expensive materials and more facile processes could have a large impact on future biohybrid systems. Special attention should be focused on the development of both solid-state and wet-based biohybrid composite materials with good long-term stabilities, expanding well beyond the >280 day activity that we have demonstrated for PSI films in a cell.26 Although solid-state devices would provide potential advantages in terms of performance and stability, challenges in forming electrical contacts to PSI without using processes that damage its secondary structure have proved difficult to overcome. Furthermore, solving the problems of mixed orientations in PSI films will be critical for integration in some solid-state systems.19 The advantage of highly oriented PSI materials was recently highlighted by the work of Toporik et al., who generated extraordinary photovoltages using crystals of PSI to surpass even the strongest ferroelectric crystals.49 The ability to achieve oriented films of PSI over larger surface areas with rapid, affordable processing would be a major breakthrough for the many energy-related applications of this system. Further efforts to capitalize on the dramatic improvements observed when PSI can be organized are currently underway in a number of research groups around the world. Building on the past 30 years of interfacing PSI with materials, our research team and others seek to preserve our natural resources by developing new energy solutions driven by the abundant materials that nature has engineered.

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Gabriel LeBlanc received his B.S. in chemistry at Lyon College in 2010. Currently he is a Ph.D. candidate in the Department of Chemistry at Vanderbilt University under the direction of Dr. David Cliffel and Dr. G. Kane Jennings. His current research concentrates on the integration of PSI with semiconducting and carbon basedelectrode materials for solar energy conversion.

Evan Gizzie studied at the University of Central Florida where he received his B.S. in chemistry in 2011. Currently he is pursuing his Ph.D. in chemistry at Vanderbilt University. Under the direction of Dr. David Cliffel and Dr. G Kane Jennings, his research focuses on the development and optimization of PSI-based photovoltaics that utilize low-cost materials for scalable biohybrid solar energy conversion.

AUTHOR INFORMATION

Corresponding Author

*Tel: +1 615 322 2707. Fax: +1 615 343 7951. E-mail: kane.g. [email protected]. Author Contributions

The manuscript was written through the contributions of all authors. All authors have given approval to the final version of the manuscript.

Siyuan Yang received his B.S. in chemical engineering from both the University of MissouriColumbia and East China University of Science and Technology in 2012. Currently he is pursuing his Ph.D. in chemical engineering at Vanderbilt University under the direction of Dr. G. Kane Jennings through collaboration with Dr. David E. Cliffel.

Notes

The authors declare no competing financial interest. I


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Corporation for Science Advancement. G.L. was supported in part by an ACS DAC summer fellowship.

His current research focuses on the fabrication of robust solar conversion devices by stabilizing photosystem I films on electrode substrates.

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ABBREVIATIONS PSI, photosystem I; FB, terminal iron−sulfur complex of PSI; P700, reaction center of PSI; I−V, current−voltage; NHE, normal hydrogen electrode; kudzu, Pueraria lobata; KPFM, Kelvin probe force microscopy; TPDA, terephthaldialdehyde; (Fe(CN)63−/4−, ferricyanide/ferricyanide; χup, orientation factor; SAM, self-assembled monolayer; MV2+, methyl viologen; AQS, anthraquinone-2-sulfonate; HNQ, 2-hydroxy-1,4-maphathoquinone; MB, methylene blue; Ru(NH3)6, ruthenium hexaammine; DCPIP, 2,6-dichlorophenolindophenol; Cyt C, cytochrome C; NaAsc, sodium ascorbate; FcTMA, ferrocenylmethyl-trimethylammonium hexafluorophosphate; I−/I3−, iodide/triiodide; Ag/AgCl, silver/silver chloride reference electrode; PAni, polyaniline

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David E. Cliffel is an associate professor of chemistry at Vanderbilt University. He received a B.S. in chemistry and a Bachelor of Electrical Engineering from the University of Dayton in 1992. He received his Ph.D. in chemistry in 1998 from the University of Texas at Austin under the direction of Professor Allen J. Bard and did postdoctoral work with Professor Royce W. Murray at the University of North Carolina as a postdoctoral associate working on the electrochemistry of monolayer-protected clusters. His current research concentrates on the electrochemical analysis of nanoparticles and of biological cells using scanning electrochemical microscopy and the incorporation of photosystem I into photoelectrochemical cells.

REFERENCES

(1) Hall, D.; Rao, K. Photosynthesis, 6th ed.; Cambridge University Press: Cambridge, U.K., 1999. (2) Lovins, A. Winning the Oil Endgame: Innovation for Profits, Jobs and Security; Rocky Mountian Institute: Snowmass, CO, 2004. (3) Foster, R.; Ghassemi, M.; Cota, A. Solar Energy: Renewable Energy and the Environment; CRC Press: Boca Raton, FL, 2009; p 382. (4) Becquerel, A. Recherche sur les Effets de la Radiation Chimique de la Lumière Solaire au Moyen de Courant Électrique. C. R. Acad. Sci. 1839, 9, 145−149. (5) Golbeck, J. Photosystem I: The Light-Driven Plastocyanin: Ferredoxin Oxidoreductase; Springer: Dordrecht, The Netherlands, 2006; Vol. 24, p 764. (6) Hogewoning, S. W.; Wientjes, E.; Douwstra, P.; Trouwborst, G.; van Ieperen, W.; Croce, R.; Harbinson, J. Photosynthetic Quantum Yield Dynamics: From Photosystems to Leaves. Plant Cell 2012, 24, 1921−1935. (7) Amunts, A.; Drory, O.; Nelson, N. The Structure of a Plant Photosystem I Supercomplex at 3.4Å Resolution. Nature 2007, 447, 58−63. (8) Ciesielski, P. Ph.D. Dissertation. Photosystem I-Based Systems for Photoelectrochemical Energy Conversion. Vanderbilt University, Nashville, TN, 2010. (9) Badura, A.; Kothe, T.; Schuhmann, W.; Rogner, M. Wiring Photosynthetic Enzymes to Electrodes. Energy Environ. Sci. 2011, 4, 3263−3274. (10) Greenbaum, E. Platinized Chloroplasts: A Novel Photocatalytic Material. Science 1985, 230, 1373−1375. (11) Greenbaum, E. Photobioelectronic Studies with Thylakoid Membranes. Appl. Biochem. Biotechnol. 1989, 20−21, 813−824. (12) Iwuchukwu, I. J.; Vaughn, M.; Myers, N.; O’Neill, H.; Frymier, P.; Bruce, B. D. Self-Organized Photosynthetic Nanoparticle for CellFree Hydrogen Production. Nat. Nanotechnol. 2010, 5, 73−79. (13) Evans, B. R.; O’Neill, H. M.; Hutchens, S. A.; Bruce, B. D.; Greenbaum, E. Enhanced Photocatalytic Hydrogen Evolution by Covalent Attachment of Plastocyanin to Photosystem I. Nano Lett. 2004, 4, 1815−1819. (14) Utschig, L. M.; Dimitrijevic, N. M.; Poluektov, O. G.; Chemerisov, S. D.; Mulfort, K. L.; Tiede, D. M. Photocatalytic Hydrogen Production from Noncovalent Biohybrid Photosystem I/Pt Nanoparticle Complexes. J. Phys. Chem. Lett. 2011, 2, 236−241. (15) Krassen, H.; Schwarze, A.; Friedrich, B.; Ataka, K. Photosynthetic Hydrogen Production by a Hybrid Complex of Photosystem I and Hydrogenase. ACS Nano 2009, 3, 4055−4061. (16) Lee, J. W.; Lee, I.; Greenbaum, E. Platinization: a Novel Technique to Anchor Photosystem I Reaction Centers onto a Metal Surface at Biological Temperature and pH. Biosens. Bioelectron. 1996, 11, 375−387.

Professor G. Kane Jennings received his B.S. in chemical engineering from Auburn University in 1993, his M.S. in chemical engineering practice from the Massachusetts Institute of Technology in 1996, and his Ph.D. in chemical engineering from the Massachusetts Institute of Technology in 1998. Professor Jennings joined Vanderbilt University as an assistant professor in the Department of Chemical Engineering in 1998 and was promoted to associate professor in 2005. He was promoted to professor in 2011 and became chair of the department in 2013. He has published over 70 papers in the area of organic thin films and interfacial science/engineering. His research interests include biohybrid and bioinspired approaches to the design of materials and surfaces.

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ACKNOWLEDGMENTS We gratefully acknowledge the financial support of the National Science Foundation (DMR 0907619), the NSF EPSCoR (EPS 1004083), the United States Department of Agriculture (201367021-21029 USDA), the Environmental Protection Agency (SU-83528701), and the Scialog Program of the Research J


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