From natural to artificial photosynthesis

Abstract

Demand for energy is projected to increase at least twofold by mid-century relative to the present global consumption because of predicted population and economic growth. This demand could be met, in principle, from fossil energy resources, particularly coal. However, the cumulative nature of carbon dioxide (CO(2)) emissions demands that stabilizing the atmospheric CO(2) levels to just twice their pre-anthropogenic values by mid-century will be extremely challenging, requiring invention, development and deployment of schemes for carbon-neutral energy production on a scale commensurate with, or larger than, the entire present-day energy supply from all sources combined. Among renewable and exploitable energy resources, nuclear fusion energy or solar energy are by far the largest. However, in both cases, technological breakthroughs are required with nuclear fusion being very difficult, if not impossible on the scale required. On the other hand, 1 h of sunlight falling on our planet is equivalent to all the energy consumed by humans in an entire year. If solar energy is to be a major primary energy source, then it must be stored and despatched on demand to the end user. An especially attractive approach is to store solar energy in the form of chemical bonds as occurs in natural photosynthesis. However, a technology is needed which has a year-round average conversion efficiency significantly higher than currently available by natural photosynthesis so as to reduce land-area requirements and to be independent of food production. Therefore, the scientific challenge is to construct an 'artificial leaf' able to efficiently capture and convert solar energy and then store it in the form of chemical bonds of a high-energy density fuel such as hydrogen while at the same time producing oxygen from water. Realistically, the efficiency target for such a technology must be 10 per cent or better. Here, we review the molecular details of the energy capturing reactions of natural photosynthesis, particularly the water-splitting reaction of photosystem II and the hydrogen-generating reaction of hydrogenases. We then follow on to describe how these two reactions are being mimicked in physico-chemical-based catalytic or electrocatalytic systems with the challenge of creating a large-scale robust and efficient artificial leaf technology.

Figure 1.

A diagrammatic representation of energy flow in biology. The light reactions of photosynthesis (light absorption, charge separation, water splitting, electron/proton transfer) provides the reducing equivalents in the form of energized electrons (e) and protons (H⁺) to convert carbon dioxide (CO₂) into carbohydrates (CH₂O) and other organic molecules which make up living organisms (biomass), including those that provide humankind with food. The same photosynthetic reactions gave rise to the fossil fuels formed millions of years ago. The burning of these organic molecules either by respiration (controlled oxidation within our bodies) or by combustion of biomass and fossil fuels to power our technologies, is the reverse to photosynthesis, releasing CO₂ and combining the stored ‘hydrogen’ back with oxygen to form water. In so doing energy, which is originated from sunlight, is released.

Figure 2.

A simplified Z-scheme of the light reactions of photosynthesis taken from http://en.wikipedia.org/wiki/photosynthesis. For every electron extracted from water and transferred to CO₂, the energy of two photons of light is required. One is absorbed by photosystem II (PSII) that generates a strong oxidizing species (P680⁺), able to drive the water-splitting reaction and a reduction of pheophytin (Pheo) and then plastoquionel (Q) to plastoquinol (QH₂). The other photosystem, photosystem I (PSI) generates a strong reducing species, NADPH, which donates reducing equivalents to CO₂ to produce sugars and other organic molecules, and a weak oxidant P700⁺. Electron and proton flow from QH₂ to P700⁺ is aided by the cytochrome b₆f (Cyt b₆f) complex and plastocyanin (PC) and results in the release of energy to convert ADP to ATP. The ATP produced is required, along with NADPH, to convert CO₂ to sugars. Because the production of O₂ requires the splitting of two water molecules, the overall process involves the removal of two electrons per water molecule as shown and therefore four photons per PSII and PSI reaction centre. The reduction of oxidized nicotinamide adenine dinucleotide phosphate (NADP⁺) by PSI is facilitated by membrane bound iron sulfur proteins (F_x, F_A and F_B) and soluble ferredoxin (F_D).

Figure 3.

Schematic of the electron–proton transport chain of oxygenic photosynthesis in the thylakoid membrane, showing how photosystem I (PSI) and photosystem II (PSII) work together to use absorbed light to oxidize water and reduce NADP⁺, in an alternative representation to the Z-scheme shown in figure 2. The diagram also shows how the vectorial flow of electrons across the membrane generates a proton gradient which is used to power the conversion of ADP to ATP at the ATP synthase complex (CF_oCF₁) which is also embedded in the thylakoid membrane (not shown). In both PSI and PSII, the redox-active cofactors are arranged around a pseudo-twofold axis. In PSII, primary charge separation and subsequent electron flow occurs along one branch of the reaction centre. However, in the case of PSI, electron flow occurs up both branches as shown. Electron flow through the cytochrome b₆ f complex also involves a cyclic process known as the Q cycle. Y_Z = tyrosine; P680 = primary electron donor of PSII composed of chlorophyll (Chl); Pheo = pheophytin; Q_A and Q_B = plastoquinone; Cyt b₆f = cytochrome b₆f complex, consisting of an Fe–S Rieske centre, cytochrome f (Cyt f), cytochrome b low- and high-potential forms (Cyt b_LP and Cyt b_HP), plastoquinone binding sites, Q₁ and Q₀; PC = plastocyanin; P700 = primary electron Chl donor of PSI; A₀ = Chl; A₁[Q] = phylloquinone; F_x, F_A and F_B = Fe–S centres, F_D = ferredoxin; FNR = ferredoxin NADP reductase; NADP⁺ = oxidized nicotinamide adenine dinucleotide phosphate. Y_D = symmetrically related tyrosine to Y_z but not directly involved in water oxidation, and QH₂ = reduced plastoquinone (plastoquinol), which acts as a mobile electron/proton carrier from PSII to the cytochrome b₆f complex. With the exception of the mobile electron carriers Q/QH₂, PC and F_D, the remaining redox-active cofactors are bound to multisubunit protein complexes that span the membrane depicted as coloured boxes.

Figure 4.

(a) Structure of the Mn₄CaO₅ cluster and (b) its ligand environment as determined at a resolution of 1.9 Å by Umena et al. [32].

Figure 5.

Two different mechanisms for the final step of the S-state cycle when the dioxygen bond of O₂ is formed. (a) Mechanism 1. The very high oxidation state of the Mn-cluster, particularly the Mn ion outside the Mn₃CaO₄-cubane, leads to a high electron deficient oxo (after deprotonation of water molecules during the S-state cycle). Nucleophilic attack by the hydroxide of the second substrate water within the coordination sphere of Ca²⁺ leads to O₂ formation. (b) Mechanism 2. The formation of an oxo-radical within the Mn₃CaO₄-cubane attacks a bridging oxo species to form the O–O bond. (Online version in colour.)

Figure 6.

Catalytic active sites of [FeFe]- and [NiFe]-hydrogenases (a); schematized structure and function of [FeFe]-hydrogenase for hydrogen evolution reaction (b). Schematized electron, proton and hydrogen transfer pathways are included.

Figure 7.

Proposed activation of [FeFe]-hydrogenase and catalytic cycle for hydrogen evolution reaction [–59].

Figure 8.

Schematic of how semiconducting materials can be used as photocatalysts for water oxidation and hydrogen generation. Large band gap semiconductors can be used without (a) or with electrocatalysts Cat1 and Cat2 (b). Two narrow band gap semiconductors could be wired in a Z-scheme tandem configuration (c).

Figure 9.

Selected synthetic electrocatalysts that mimic the [Mn₄Ca]-cluster and the active sites of hydrogenases. Synthetic [Mn₃CaO₄]-clusters designed by Agapie and co-workers (a) [87] and Christou and co-workers (b) [88]; Co₄O₁₆ core stabilized within [PW₉O₃₄] ligand synthesized by Hill and co-workers (c) [89]; Nocera CoPi solid catalyst and its proposed atomic structure (d) [90]; synthetic [FeFe] and [NiFe] models designed by Pickett and co-workers [91] and Ogo and co-workers [92] (e) and (f); bioinspired model designed by Dubois and co-workers (g) [93].

Figure 10.

Selected hybrid photocatalysts/photoelectrodes engineered by assembling an OEC or a HER catalyst with a semiconductor. Ir-molecular OEC catalyst covalently grafted onto a dye-sensitized TiO₂ electrode (a) [102,103]; Co₃O₄ OEC within α-Fe₂O₃ nanowires photoanode (b) [104]; immobilization of a [NiFeSe]-hydrogenase onto dye-sensitized TiO₂ nanoparticles (c) [105]; immobilization of a synthetic FeFe-molecular HER catalyst within a mesoporous InP electrode (d) [106]; Si/MoS₂ photocathode (e) [107].

Figure 11.

Selected complete devices for the overall water-splitting process. A PEC consisted of a dye-sensitized TiO₂ photoanode and a hydrogenase cathode (a) [119]; a PEC with two photoelectrodes in the tandem configuration (b) [120]; the artificial leaf constructed from an amorphous Si triple junction solar cell and appropriate OEC and HER catalysts (c) [121,122].