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3D Graphene Matrix Supported and Thylakoid Membranes Based High-Performance Bioelectrochemical Solar Cell Galina Pankratova, Dmitry Pankratov, Chiara Di Bari, Asier Goñi-Urtiaga, Miguel Duarte Toscano, Qijin Chi, Marcos Pita, Lo Gorton, and Antonio L. De Lacey ACS Appl. Energy Mater., Just Accepted Manuscript • DOI: 10.1021/acsaem.7b00249 • Publication Date (Web): 01 Feb 2018 Downloaded from http://pubs.acs.org on February 3, 2018

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ACS Applied Energy Materials

3D Graphene Matrix Supported and Thylakoid Membranes Based High-Performance Bioelectrochemical Solar Cell

Galina Pankratova,† Dmitry Pankratov,‡ Chiara Di Bari,§ Asier Goñi-Urtiaga,∥ Miguel D. Toscano,⊥ Qijin Chi,‡ Marcos Pita,§ Lo Gorton,* † Antonio L. De Lacey*§ †

Department of Biochemistry and Structural Biology, Lund University, P.O. Box 124, SE-22100 Lund, Sweden ‡

Department of Chemistry, Technical University of Denmark, DK-2800 Kongens Lyngby, Denmark

§

Instituto de Catálisis y Petroleoquímica, CSIC, c/ Marie Curie 2, L10, 28049 Madrid, Spain

∥

Nanoinnova Technologies SL, c/ Faraday 7, 28049 Madrid, Spain

⊥

Protein Diversity, Novozymes A/S, Krogshojvej 36, 2880 Bagsvaerd, Denmark

* Corresponding Authors. E-mail addresses: [email protected] (L. Gorton), [email protected] (A.L. De Lacey). Abstract Combination of thylakoid membranes (TMs) as photobiocatalysts with high surface area electroactive materials could hold great potential for sustainable “green” solar energy conversion. We have studied the orientated immobilization of TMs on high surface area graphene electrodes, which were fabricated by electroreduction of graphene oxide and simultaneous electrodeposition with further aminoaryl functionalization. We have achieved the up-to-date highest performance under direct electron transfer conditions through a biocompatible “wiring” of TMs to graphene sheets. The photobiocurrent density generated by the optimized mediator-free TMbased bioanodes yielded up to 5.24±0.50 µA cm-2. The photo-bioelectrochemical cell integrating the photobioanode in combination with an oxygen reducing enzymatic biocathode delivered a maximum power output of 1.79±0.19 µW cm-2. Our approach ensures a simplified cell design, a greater load of photosynthetic units, a minimized overpotential loss and an enhanced overall performance. Keywords: thylakoid membrane, graphene, direct electron transfer, photobioelectrochemical cell, solar energy conversion.

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Currently most of the world’s electricity is still produced from non-renewable fossil fuels [1], which deepens the damaging environmental effect due to mining and combustion. In view of this problem today’s society meets the growing needs for alternative cheap and clean energy production [2]. Solar radiation is the ubiquitous primary energy source, which can be converted directly into electricity using semiconductor-based photovoltaics known as solar cells; which have undergone a rapid progress in the last decades [3]. Similarly, photo-bioelectrochemical cells (PBCs) employing the natural photosynthetic apparatus keep high promising possibilities for sustainable energy production. PBCs show potential advantages such as their high quantum efficiency, low cost, simple function and low negative environmental impact [4, 5]. Photosynthesis is the fundamental process of solar energy conversion into chemical energy with oxygen evolution as byproduct. A wide range of light-capturing biocatalysts have been applied for solar energy conversion: whole photosynthetic microorganisms such as cyanobacteria [6] and algae [7], plants [8], components of the cellular or the subcellular photosynthetic machinery such as isolated chloroplasts [9], thylakoid membranes (TMs) [10], photosystems I [11] and II [12] (PSI and PSII). Light absorption takes place at the photosynthetic pigments embedded in the TMs: its four major protein complexes (PSII, cytochrome protein complex, PSI, and ATP synthase) carry out the transfer of the released electrons and protons followed by the oxidation of water. Such a multi-redox protein structure along the electron transport chain makes possible multipath electron transfer (ET) delivery to the electrode surface. Additionally, the absence of any outer membrane and a higher loading of photoactive material per surface unit allow a higher energetic yield compared to use of entire cells and chloroplasts. The use of the intact photosynthetic apparatus of TMs in photoelectrochemical devices leads to a potentially greater stability, as opposed to isolated PSs, because the protein complexes retain their native environment [4, 5]. Furthermore, the procedure of extraction and purification of TMs is cheap, fast and simple to perform. These advantages have promoted TMs to consider as a promising photobiocatalyst for development of PBCs. These photo-bioelectrochemical devices may not meet real-life applications, however, unless the performance of TM-based photobioanodes is significantly improved. Such improvement may be achieved by (i) an increase in the 2 ACS Paragon Plus Environment

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electrochemically active electrode surface area and (ii) a proper orientation of the immobilized bioelement to facilitate an efficient direct electron transfer (DET) reaction between the TMs and the photobiocurrent collector [4]. Drawing on the criteria described above, we have fabricated and optimized the configuration of mediatorless photo-bioanodes and PBC based on TMs directly bound on functionalized graphene electrodes with a highly developed surface. In the past ten years there has been a great technological and scientific interest in graphene-based materials, due to their unique properties like high specific surface area [13], excellent electrical conductivity [14], and good mechanical strength [15]. Furthermore, the industrial production of graphene is low-priced compared e.g., to multi-walled carbon nanotubes (MWCNTs) [16, 17], another carbon material with a high roughness factor, reported to be suitable to achieve a high photo-electrochemical activity of TMs [18, 19]. However, the above notwithstanding, graphene has never been employed in TMbased PBCs as a support for photo-biocatalyst immobilization, to the best of our knowledge. An expanded three-dimensional (3D) graphene surface has been prepared according to the recently reported method of simultaneous electrodeposition-electroreduction of graphene oxide (GO) by cyclic voltammetry (CV) [20]. Electrodeposition was carried out on a glassy carbon (GC) electrode in presence of a 0.5 mg mL-1 aqueous dispersion of GO containing 150 mM NaCl under deoxygenated and continuous stirring conditions. The number of reduced GO (rGO) layers on the GC surface depends on the number of CV scans performed (Fig. S1A). This electrode fabrication method is easy to scale up and does not need any toxic chemicals, which can offer a biocompatible platform for further immobilization of biomaterial. An additional advantage is its good uniformity, reproducibility and controllability of cover thickness. One major concern is, however, that both rGO and TMs are negatively charged [17], which may have a negative influence on the ET rate due to electrostatic repulsion. It has recently been shown that amidation and carboxylation of a carbon based surface facilitates covalent binding of the TMs [19, 21]. However, amidated MWCNTs ensure a better electrochemical communication between the TMs and the electrode surface compared to carboxylated MWCNTs [19]. Furthermore, oxygen-containing functional groups on graphene were shown to contribute to oxidative stress of the membrane [22]. For this reason the graphene electrodes were functionalized with 3 ACS Paragon Plus Environment


aminoaryl groups following a previously described procedure [23] to diminish the negative charge on the surface, to eliminate the access of functional oxygen-based groups, and thereby improve the electrochemical connection of the TMs to the conductive support. Four types of graphene-modified electrodes were prepared by applying 30, 60, 80 or 100 cyclic voltammograms (CVs) at a scan rate of 10 mV s-1 (these electrodes are denoted as E30, E60, E80 and E100) in an aqueous GO dispersion, which resulted in capacitance values of 10.1±0.7, 41.2±3.3, 48.5±5.1 and 57.3±3.4 mF cm-2, respectively. The capacitance was calculated from CVs of non-biomodified rGO electrodes (Fig. S1B). The rGO electrodes were modified with 4 µL of a Spinacia oleracea TM suspension (3.2 mg mL-1 chlorophyll content). Note that the loaded amount of the TM suspension was optimized (Fig. S2). Detailed information on the bioelectrode preparation and the experimental setups is provided in the Supporting Information (SI). A detectable photo-bioelectrochemical response from the immobilized TMs was registered only for those electrodes prepared by 60 and 80 CV scans, with no difference between them in terms of photobiocurrent density (Fig. S3). This observation can be explained by a similar surface area of these electrodes, proportional to their capacitance, leading to a similar photobiocatalyst loading. For this reason, our following studies are only focused on the three types of electrodes, i.e. E30, E60 and E100. Scanning electron microscopy (SEM) shows that the E30 electrodes had an underdeveloped 3D surface morphology (Fig. S4A) non-suitable to host massive TM units, which also rapidly leaked from the electrode surface into the buffer solution when they were tested. The E60 electrodes showed a highly developed 3D structure (Fig. 1A), favorable for an enhanced loading of TMs. Fig. 1B shows immobilized TMs appearing in a disk-like shape of about 0.45 µm in diameter uniformly spread over the rGO surface. It is noted that the presence of the photosynthetic membranes resulted in a decrease in the electrode capacitance compared to non-biomodified graphene from 41.2±3.3 to 30.3±2.1 mF cm-2 (Fig. 2A). Previous studies on DET TM-based systems found an additional pseudocapacitive input [19, 24] attributed to the appearance of redox compounds diffusing out of the membranes. In the present case, however, there is no evidence of any leakage of intermembrane content, i.e. the absence of any membrane disruption. It should be emphasized that graphene is considered to have bactericidal activity by damaging the


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cell membrane [25, 26], therefore hindering the challenging integration and application of graphene-based materials into microbial fuel cells. However, the extent of damage drastically depends on the size of the graphene sheets [17]. The porous pattern demonstrated herein holds a microstructure close to being planar comparable with the size of the immobilized bioelement (Fig. 1), which allows adhesion of the biocatalyst with no destruction while keeping an extended surface area. The E100 electrodes have a well-developed 3D structure similar to those fabricated through 60 CV cycles (Fig. S4B, C in SI), however, the loaded TMs could not be observed by SEM. We assume that the electrodeposited graphene layer was too thick and the biomaterial went through the porous coating staying in the depth with poor access of the light, since no leakage of the photosynthetic layer from the electrode surface into the buffer was observed. Furthermore, the overall conductivity of the graphene layer was low due to its massiveness and its occasional detachment from the GC support. For this reason, all further experiments were performed using electrodes prepared by running 60 CV scans. The photocurrent generation was investigated by continuous amperometric measurements at a constant potential of 0.6 V vs. the standard hydrogen electrode (SHE) upon light on/off conditions. A relatively high potential was applied in order (i) to allow comparing the present results with those previously reported for mediatorless investigations of TMs immobilized on CNTs [19] and (ii) to avoid any possible oxygen electroreduction, which takes place on carbonaceous electrodes at lower potentials [19, 20]. Control experiments on non-biomodified rGO electrodes under the same experimental conditions were performed. A significant photocurrent of 1.02±0.14 µA cm-2 was registered, which is attributed to the photoelectrochemical activity of rGO [27]. The background current contribution of rGO electrodes was subtracted from the amperograms displaying the photobioelectrocatalytic behavior of the TM-modified rGO electrodes under illumination of 400 W m-2 (Fig. 2B). Under this intensity the maximum photobio-current density from the TMs immobilized on the rGO was 5.24±0.50 µA cm-2, which is more than 2.5 times higher compared to the latest study on TMs directly immobilized on amide-modified MWCNT [19]. Therefore, the employment of the functionalized high surface area graphene electrodes allows achieving the highest DET photo-biocurrent density output from 5 ACS Paragon Plus Environment


TMs reported so far. The residual stability after five light on/off steps (500 s of lighting in full) was as high as 64% (Fig. 2B). Such a stability level remains similar for other TM-based anodes of different designs [10, 18, 19, 28], suggesting that the decrease in photocurrent is due to an internal processes occurring inside the membranes but not to their leaking from the electrode surface or a damaging effect of graphene on the integrity of the membranes. Long-term stability experiments indicated an overall decrease down to 18% of residual activity in approximately one hour of illumination, although after that a continued steady photocurrent generation by TMs was measured for at least 1 h (Fig. S5). A previous study of the stability trend of TMs [10] demonstrated a remaining activity of only ca. 13% of the initial activity after one hour of illumination with a further decay of the photocurrent. The obtained results allow us to conclude that the 3D graphene support contributes to a higher operational stability of the TMs-based electrodes than previously studied support materials. The open-circuit potential (OCP) of the photobioanode is a significant parameter to monitor in view of the output voltage for an assembled PBC. In the absence of light the rGO electrodes both bare and TMs-loaded displayed a similar OCP value of 0.262±0.011 V. When illuminated the bare rGO graphene electrode showed negligible changes (Fig. 2C), but the bio-modified rGO anode showed a slight potential shift to 0.256±0.009 V under light-on conditions (Fig. 2C). This small OCP change is attributed to the high electrode capacitance [19]. However, the overall OCP of the anodes was lower than those for similar TM anodes both based on DET [19] and on mediator-based systems [28]. This lower OCP of the bioanode is favorable for PBC applications. To construct a complete PBC, the photobioanode was connected to an oxygen reducing enzyme-based cathode fabricated by dropcasting 5 µL of a Myrothecium verrucaria bilirubin oxidase (BOx, 4 mg mL-1) solution on low density graphite rods. Due to the lower current output of the photobioanodes than that of the biocathodes (Fig. S6) any further optimization of the biocathode was not needed. Under illumination and in the presence of an air saturated phosphate buffer (10 mM Na2HPO4, 10 mM NaH2PO4, 10 mM NaCl, 5 mM MgCl2, pH 7.0), the open circuit voltage (OCV) registered for such a PBC was 0.500±0.015 V (Fig. 3). Due to the relatively high capacitance of the rGO-based anode, the performance of the assembled 6 ACS Paragon Plus Environment

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biodevice was evaluated by applying step potentials from the OCV to 0 V; the equilibrium-resulting steady-state current for each applied voltage was recorded [29]. A current-voltage plot for the assembled PBC was obtained in air-saturated buffer under illumination (Fig. 3). Additional control measurements were performed in either the absence of light (Fig. 3) or oxygen (Fig. S7). A maximum power density of 1.79±0.19 µW cm-2 was achieved at 0.3 V. The power output is 2.7-fold higher than that for the recently reported analogous PBC, where the TMs were directly immobilized on MWCNTs [19] and more than 350 times greater compared to the TM-based conventional PBC employing nanostructured indium tin oxide as the electrode support [24]. In conclusion, the present study has shown the feasibility of TMs electrochemically connected to a highly developed graphene surface for the first time. The fabrication method comprised GO electroreduction and electrodeposition by cyclic voltammetry followed by electrochemical functionalization of the reduced and deposited GO with aminoaryl groups. This strategy allows orientated immobilization of the photosynthetic membranes and prevents leakage of the TMs from the 3D electrode surface. The obtained graphene surface has a highly porous conformation, but at the same time a close-to-planar microstructure. Such an advantageous combination assures a high load of the photoactive biocatalytic units combined with a nondisruptive effect on the biomaterial, which results in the highest current density output compared with those previously reported for TMs under DET conditions. The PBC employing such advanced graphene-based high surface area photo-bioanodes for light energy harvest has potentially wide applications due to their simple design, sustainability, and low cost. The constructed mediator-less PBC in this present study, which includes the developed photosynthetic energy conversion bioanode and the oxygen reducing biocathode, displays to the best of our knowledge the highest power density compared to other reported analogous DET-based systems. We believe the current findings have significant implications for photosynthetic energy conversion technology, where the issue of electrode-biocatalyst interaction is one of the important factors determining the overall performance [30].

Acknowledgements



The authors thank the following agencies for financial support: the European Commission (”Bioenergy” FP7-PEOPLE-2013-ITN-607793) and the ØrstedCOFUND Postdoc fellowship at DTU (Agreement No. 2014-5908) and the Swedish Research Council (project 2014-5908), and Independent Research Fund DenmarkNature Sciences (DFF-FNU, Project No. DFF-7014-00302).

ASSOCIATED CONTENT Supporting information available: Experimental details, cyclic voltammograms of electrodeposition/electroreduction of GO and rGO electrodes including values of capacitance, optimization of amounts of immobilized TMs on rGO electrodes by amperometry, amperograms for TMs immobilized on rGO electrodes of different capacitance values, SEM images of rGO electrodes of different capacitance values, photobiocurrent stability trend of TMs immobilized on rGO electrodes, current response from photobioanode and biocathode at 0.6 V, current-voltage and powervoltage characteristics of PBC in argon saturated solution under illumination. References (1)

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Figures

Figure 1. SEM images of electrodeposited rGO on GC rods fabricated by CV (60 cycles): (A) pristine rGO; (B) rGO with immobilized TMs. Magnification: ×45000 and ×25000, respectively.



Figure 2. (A) Representative cyclic voltammograms for rGO electrodes: nonbiomodified (black line) and modified with TMs (red line). Scan rate 10 mV s-1. (B) Representative background-subtracted amperogram for TMs immobilized on a rGO electrode under ”light on“ and “light off” conditions at an applied potential of 0.6 V. (C) OCP of pristine rGO electrodes (black line) and rGO with immobilized TMs (red line). Green and black arrows represent “light on” and “light off” conditions, respectively. Illumination intensity was 400 W m-2. All potentials are given versus SHE.


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Figure 3. Polarization (black) and power density (red) curves for the PBC employing a TM-based photobioanode and an enzymatic BOx-based biocathode in air saturated buffer under illumination (solid lines) and in the absence of light (dashed lines).

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