Using a simple membrane extract from spinach leaves, researchers from the Technion-Israel Institute of Technology have developed a bio-photo-electro-chemical (BPEC) cell that produces electricity and hydrogen from water using sunlight. The raw material of the device is water, and its products are electric current, hydrogen and oxygen. The findings were published in the August 23 online issue of Nature Communications.
The unique combination of a man-made BPEC cell and plant membranes, which absorb sunlight and convert it into a flow of electrons highly efficiently, paves the way for the development of new technologies for the creation of clean fuels from renewable sources: water and solar energy.
The BPEC cell developed by the researchers is based on the naturally occurring process of photosynthesis in plants, in which light drives electrons that produce storable chemical energetic molecules, that are the fuels of all cells in the animal and plant worlds.
In order to utilize photosynthesis for producing electric current, the researchers added an iron-based compound to the solution. This compound mediates the transfer of electrons from the biological membranes to the electrical circuit, enabling the creation of an electric current in the cell.
The electrical current can also be channeled to form hydrogen gas through the addition of electric power from a small photovoltaic cell that absorbs the excess light. This makes possible the conversion of solar energy into chemical energy that is stored as hydrogen gas formed inside the BPEC cell. This energy can be converted when necessary into heat and electricity by burning the hydrogen, in the same way hydrocarbon fuels are used.
However, unlike the combustion of hydrocarbon fuels – which emit greenhouse gases (carbon dioxide) into the atmosphere and pollute the environment – the product of hydrogen combustion is clean water. Therefore, this is a closed cycle that begins with water and ends with water, allowing the conversion and storage of solar energy in hydrogen gas, which could be a clean and sustainable substitute for hydrocarbon fuel.
The study was conducted by doctoral students Roy I. Pinhassi, Dan Kallmann and Gadiel Saper, under the guidance of Prof. Noam Adir of the Schulich Faculty of Chemistry, Prof. Gadi Schuster of the Faculty of Biology and Prof. Avner Rothschild of the Faculty of Material Science and Engineering.
“The study is unique in that it combines leading experts from three different faculties, namely three disciplines: biology, chemistry and materials engineering,” said Prof. Rothschild. “The combination of natural (leaves) and artificial (photovoltaic cell and electronic components), and the need to make these components communicate with each other, are complex engineering challenges that required us to join forces.”
The study was conducted at the Nancy and Stephen Grand Technion Energy Program (GTEP) and carried out at the Technion’s Hydrogen Lab, which was established under the auspices of the Adelis Foundation and GTEP. It was funded by the I-CORE (Israeli Centers of Research Excellence) program of the Council for Higher Education’s Planning and Budgeting Committee, the National Science Foundation (Grant No. 152/11), a special grant from the United States – Israel Binational Science Foundation (BSF), and the German-Israeli Project Cooperation Program (DIP).
Significant photocurrent from spinach thylakoids
Under solar-simulated illumination, water oxidation is catalysed by the PSII complex embedded in the thylakoids, releasing O2 and protons. A mediated photocurrent is obtained in the system by use of the redox couple ferri/ferrocyanide (Fe(III)/Fe(II)CN) that extracts electrons from the photosynthetic membranes and transfers them to the anode. The photocurrent dependence on the applied potential is presented in Fig. 2a, showing saturation of 450±50 μA cm−2 at an anode potential of 0.5 VAg/AgCl. The measurements were carried out in buffer A solution with a thylakoid content of 0.1 mg Chl and a Fe(III)CN concentration of 3 mM. The dependencies of the photocurrent, measured at 0.5 VAg/AgCl, on the Fe(III)CN concentration (at a thylakoid content of 0.1 mg Chl) and thylakoid content (at a Fe(III)CN concentration of 3 mM) are presented in Fig. 2b,c, respectively. A maximal photocurrent density of ca. 0.5 mA cm−2 was obtained using 3 mM Fe(III)CN and thylakoid content of 0.1 mg Chl.
Previous reports have shown photo-induced electron transfer from PSII and PSI15 and the production of photocurrent from spinach thylakoids utilizing Fe(III)CN as electron shuttle, as well as using other thylakoid sources, different types of electron mediators, and a variety of electrode compositions. For example, Calkins et al.16 immobilized spinach thylakoids onto multi-walled carbon nanotubes, and achieved a maximal photocurrent of 68 μA using Fe(III)CN as the electron mediator. We have previously reported a photocurrent density of 100 μA cm−2 using a graphite electrode and DCBQ as an electron shuttle17. Hasan et al.18 reported a maximal photocurrent density of 130 μA cm−2using a gold electrode and para-benzoquinone electron transfer mediator. Thylakoids have also been used without an electron mediator19,20, though the reported photocurrents were lower compared with reports with an electron mediator. Larom et al.21 reported the production of an unmediated photocurrent density of 16 μA cm−2 using crude Synechocystis membranes and N-acetyl cysteine-modified gold electrode. A photocurrent density of 42 μA cm−2 was reported by Hamidi et al.22, using immobilized spinach thylakoids in osmium polymer network on a graphite electrode. Other studies reported high photocurrents using purified PSI or PSII. A solid state electrochemical device23 that combines purified photosynthetic complexes with a transparent electrode coated with a sandwich of metallic nanolayers reached a photocurrent density of 120 μA cm−2. This study is mentioned in a recent review article on photosynthetic protein based PV devices24as setting the record for these devices. Isolated PSII membranes were also employed by Mersch et al.13, reporting photocurrent densities as high as 930 μA cm−2 at an applied potential of 0.5 V versus the normal hydrogen electrode (NHE). However, the photocurrent in this study was measured under red light illumination (λ=679 nm, 10 mW cm−2), which makes it difficult to compare with our results that were measured under solar-simulated white light illumination. Hence, the photocurrent density reported here sets a new record for solar-simulated measurements of BPEC cells utilizing any photosynthetic membranes, crude or purified ones. Furthermore, the preparation of isolated reaction centers is expensive, time and energy consuming and requires the use of polluting detergents, and the photocurrent quickly decays due to irreversible degradation of the reaction centers13,16,18,19,22. Our approach alleviates these drawbacks by using crude thylakoids that can be readily replaced by fresh ones, as demonstrated below.
To estimate the efficiency of the charge transfer from the thylakoids to the electric circuit we calculated the ratio between the total photo-induced charge, Qphoto, measured by integrating the photocurrent (Iphoto) over time, , and the amount of O2 that evolved by the photosynthetic membranes, ΔO2 (measured in (mol O2)). Thus, the charge transfer efficiency (ηct) was calculated according to equation (1):
where F is the Faraday constant. In order to calculate ΔO2 we measured the increase in oxygen concentration after 10 min of illumination using a Clark electrode (see Supplementary Fig. 1a). The charge transfer efficiency was (94±11)% (Supplementary Fig. 1b). This value indicates that under these conditions almost all of the electrons derived from water photo-oxidation were successfully transferred to the electric circuit.
Hybrid bio-photo-electro-chemical cells for solar water splitting
Photoelectrochemical water splitting uses solar power to decompose water to hydrogen and oxygen. Here we show how the photocatalytic activity of thylakoid membranes leads to overall water splitting in a bio-photo-electro-chemical (BPEC) cell via a simple process. Thylakoids extracted from spinach are introduced into a BPEC cell containing buffer solution with ferricyanide. Upon solar-simulated illumination, water oxidation takes place and electrons are shuttled by the ferri/ferrocyanide redox couple from the thylakoids to a transparent electrode serving as the anode, yielding a photocurrent density of 0.5 mA cm−2. Hydrogen evolution occurs at the cathode at a bias as low as 0.8 V. A tandem cell comprising the BPEC cell and a Si photovoltaic module achieves overall water splitting with solar to hydrogen efficiency of 0.3%. These results demonstrate the promise of combining natural photosynthetic membranes and man-made photovoltaic cells in order to convert solar power into hydrogen fuel.
The need for cost effective and sustainable solutions for storing intermittent solar power has spurred a growing interest in artificial photosynthesis and solar fuels1,2,3. The most elementary solar fuel production process relies on the water–hydrogen cycle, . The forward reaction is work-consuming (endergonic). Under standard conditions it requires a minimum input of 237 kJ of entropy-free energy (that is, work) to dissociate one mole of water, which is the standard Gibbs free energy of the reaction (ΔG0). The reaction products, H2 and O2 gases, serve as fuel that can be stored in separate vessels and converted back into power by the reverse reaction. Thus, H2 can be produced sustainably by water electrolysis using renewable power sources such as solar power. Replacement of the entire worldwide primary energy consumption (12,910 million tons oil equivalent in 2014; ref. 4) by solar H2 produced at an average solar to hydrogen (STH) conversion efficiency of 1%, equivalent to the solar to biomass conversion efficiency of high efficiency crop plants5, would demand a net area of 9.7 million km−2 of solar collectors. This accounts for 6.5% of the total land area or 70.3% of the estimated arable land area on earth, a scenario which is not very practical6.
This limitation motivates research on other routes to store solar energy as chemical bonds in fuel products, for example through biotechnological or artificial photosynthesis processes. Bio-processes for renewable H2 production have been explored using fermentative and photosynthetic organisms as cellular factories for H2 production. Traditionally, these bio-processes are categorized into: (i) dark fermentation, (ii) photo-fermentation and (iii) biophotolysis7. Through the fermentative processes, protons serve as electron acceptors from catabolized organic compounds, while H2 production by biophotolytic processes make use of organisms capable of oxygenic photosynthesis, for example, green microalgae or cyanobacteria. For the latter, sunlight drives the oxidation of water molecules that serve as the electron donor, and protons generated are subsequently reduced to molecular hydrogen. A major barrier to commercialization of these technologies is the necessity to impose substantial restrictions on the bioreactor operating conditions in order to generate significant quantities of H2; H2 production with green algae occurs only under near anaerobic conditions, as the primary catalytic enzyme involved ((Fe–Fe)-hydrogenase) is inhibited by oxygen. Sustained H2 production using algae can be achieved only when photosynthetic O2 evolution is severely inhibited by sulfur deprivation, to such an extent that it equals the O2 consumption in the cellular respiration. Similarly, H2 production from filamentous or unicellular cyanobacteria requires the removal of O2 from the growth medium8.
The work described here puts forward a different approach that brings together light and photosynthetic membranes in a bio-photo-electro-chemical (BPEC) cell that generates, under illumination, an electromotive force that facilitates the water splitting reaction and funnels electrons and protons for the generation of H2. The operation of the BPEC cell requires the concerted operation of three components: (i) a photochemical module that captures light and produces separated charge carriers with excess chemical potential, (ii) a catalytic module that employs the photo-excited charge carriers to carry out endergonic oxidative or reductive chemistry, and (iii) an efficient method for transferring the charge carriers between the two modules while keeping as much of their excess free energy as possible8. In previous studies, photosystem I (PSI) complexes isolated from thermophilic cyanobacteria and tethered to either Pt nanoparticle catalyst9 or [NiFe]-hydrogenase10 were reported to produce up to 170 mol H2 (mol PSI min)−1, under illumination, in the presence of sacrificial electron donor (sodium ascorbate). McCormick et al.11 reported a BPEC cell that uses a two-step process to produce H2 at a rate of 2.4 μmol H2 (mg Chlh)−1, using live culture of the cyanobacteria Synechocystis PCC 6803, electron mediator (ferricyanide, Fe(III)CN), and a Pt cathode. Recently, Wang et al.12 reported the overall water splitting by self-assembled photosystem II (PSII) membranes on artificial catalysts, achieving H2production rate of 9.1 μmol H2 (mg Chlh)−1. In this system, the PSII membranes were irreversibly attached to particles containing ruthenium or rhodium, along with other inorganic components, in the presence of Fe(III)CN. In another recent study, Mersch et al.13 presented a BPEC cell that couples PSII membranes and hydrogenase to mesoporous transparent electrodes, using 2,6-dichloro-1,4-benzoquinone (DCBQ) as an electron mediator. A benchmark water splitting photocurrent of 450 μA cm−2 was obtained at an applied bias of 0.9 V under red light illumination (λ=660 nm) at an intensity of 10 mW cm−2, corresponding to a light-to-hydrogen conversion efficiency of (1.5±0.1)%.
Unlike conventional (first generation) biofuel production technologies from crop plants, a process that has been reported to work at an average efficiency of up to 1% and creates a serious competition for food5, BPEC cells make use of leaves, and are not limited to a particular plant species. Leaves of most crops do not have high commercial value, being mostly used as feedstock. We envision the utilization of crop leaves for green and benign H2 production, as an intermediate step after the crop plant has given its fruits, and before being fed to animals. Thus, in this work we present a BPEC cell that produces H2 gas using crude thylakoid membranes (henceforth called thylakoids) extracted from spinach, which is used here as a plant model. The thylakoids are extracted with minimal preparatory effort and then applied simply by letting them settle onto the surface of a transparent electrode, thereby enabling easy replacement of photodamaged thylakoids by fresh ones. Under illumination, a photocurrent is produced, mediated by Fe(III)CN, and channelled to evolve H2 at the cathode at applied bias far below the reversible voltage of water electrolysis (1.23 V in standard conditions). Furthermore, we present a stand-alone mode of operation, wherein the BPEC cell is coupled in tandem to a Si photovoltaic (PV) module that provides the bias required to produce H2. Thus, H2 is produced by this hybrid tandem cell from oxidized water molecules without any external power source or sacrificial electron donors.