Artificial Photosynthesis at Efficiencies Greatly Exceeding That of Natural Photosynthesis.

Abstract

Sunlight is an abundant energy source for a sustainable society. Indeed, photosynthetic organisms harness solar radiation to build the world around us by synthesizing energy-rich compounds from water and CO2. However, numerous energy conversion bottlenecks in the natural system limits the overall efficiency of photosynthesis; the most efficient plants do not exceed solar storage efficiencies of 1%. Artificial photosynthetic solar-to-fuels cycles may occur at higher intrinsic efficiencies, but they typically terminate at hydrogen, with no process installed to complete the cycle for carbon fixation. This limitation may be overcome by interfacing solar-driven water splitting to H2-oxidizing microorganisms. To this end, hybrid biological-inorganic constructs have been created to use sunlight, air, and water as the only starting materials to accomplish carbon fixation in the form of biomass and liquid fuels. This artificial photosynthetic cycle begins with the Artificial Leaf, which accomplishes the solar process of natural photosynthesis-the splitting of water to hydrogen and oxygen using sunlight-under ambient conditions. To create the Artificial Leaf, an oxygen evolving complex of Photosystem II was mimicked, the most important property of which was the self-healing nature of the catalyst. Self-healing catalysts permit water splitting to be accomplished using any water source, which is the critical development for (1) the Artificial Leaf, as it allows for the facile interfacing of water splitting catalysis to materials such as silicon, and (2) the hybrid biological-inorganic construct, called the Bionic Leaf, as it allows for the facile interfacing of water splitting catalysis to bioorganisms. Hydrogenases in the bioorganism allow the hydrogen to be coupled to NADPH and ATP production, thus allowing the solar energy from water splitting to be converted into cellular energy to drive cellular biosynthesis. In the design of the hybrid system, water splitting catalysts must be designed that support hydrogen generation at low applied potential to ensure a high energy efficiency while avoiding reactive oxygen species. Using the tools of synthetic biology, a bioengineered bacterium, Ralstonia eutropha, converts carbon dioxide from air, along with the hydrogen produced from such catalysts of the Artificial Leaf, into biomass and liquid fuels, thus closing an entire artificial photosynthetic cycle. The Bionic Leaf operates at solar-to-biomass and solar-to-liquid fuels efficiencies that greatly exceed the highest solar-to-biomass efficiencies of natural photosynthesis.