The solar-to-biomass conversion efficiency of natural photosynthesis is between 2.9 and 4.3% for most crops. Improving the efficiency of photosynthesis could help increase the appeal of biologically derived fuels and chemicals in comparison with traditional petrochemical processes. One approach to make photosynthesis more efficient is to build hybrid systems that combine inorganic and microbial components to produce specific chemicals. Such hybrid bioinorganic systems lead to improved efficiency and specificity and do not require processed vegetable biomass. They thus prevent harmful competition between biotechnology and the food industry and avoid the environmental perturbation caused by intensive agriculture.

Durable artificial photosynthetic apparatuses that are completely inorganic have been developed for the production of simple chemicals such as carbon monoxide, methane, and methanol. Alternatively, the artificial photosynthesis apparatus can be a bioinorganic hybrid that contains a microbial catalyst. Yang and co-workers have recently reported the use of this type of system for the production not only of simple compounds like methane but also of multicarbon chemicals including acetate, n-butanol, polyhydroxybutyrate polymer, and isoprenoids. This greater repertoire of products is possible because bioinorganic hybrid artificial photosynthesis can take advantage of the opportunities created by synthetic biology and by the metabolic plasticity of microbial cells.

In a bioinorganic artificial photosynthesis apparatus, an inorganic photoanode and photocathode harvest solar energy to split water into molecular oxygen (O₂), protons, and electrons and generate reducing equivalents that will be used by a microbial catalyst to reduce carbon dioxide (CO₂). In the first of their two studies, Yang and co-workers coupled a TiO₂/Si photoanode with a photocathode in which the acetogen Sporomusa ovata was grown directly within a silicone nanowire array. In this system, S. ovata accepts electrons directly from the photocathode to reduce CO₂ to acetate. The latter was activated to acetyl-coenzyme A in a second reactor by genetically engineered Escherichia coli before being converted into various multicarbon products. In their second study, they combined a n-TiO₂-based photoanode oxidizing water with a p-Inp/Pt photocathode to generate H2 that is then used by the methanogen Methanosarcina barkerii for converting CO₂ to methane.

In the apparatus described in, the conversion efficiency of solar energy to acetate was 0.38% over a period of 200 hours. Because of their relative simplicity compared to natural photosynthesis, artificial photosynthesis systems should be easier to improve. A rational strategy for identifying the best combination of components can readily be established. This would include engineering optimal microbial catalysts, determining the best culture-medium composition and reactor design, and improving photocathode and photoanode for higher conversion efficiency of solar energy into reducing equivalents.

Bioinorganic artificial photosynthesis can also be achieved by using a photovoltaic (PV) cell to convert solar energy into electricity, which is then used to power a separate microbial electrosynthesis (MES) reactor. This approach is different from that described by Yang and co-workers because light harvesting is carried in a compartment separated from the MES reactor where electrons are delivered to the microbial catalyst. This strategy allows the use of PV cells exclusively dedicated to light harvesting, without having to consider their compatibility with living cells.

In its most basic form, an MES system consists of an inorganic anode that oxidizes water and a cathode that delivers reducing equivalents to an autotrophic microbial catalyst. MES has been improved in the past 5 years to achieve high electron recovery into chemicals and high production rates from CO₂.

Furthermore, MES production is not limited to acetate; MES systems have been used for the electrosynthesis of longer carboxylic acids, acetone, and alcohols. With current technology, connecting an acetate-producing MES system to a commercially available PV cell with a solar-to-electrical efficiency of 20% should result in an artificial photosynthesis apparatus capable of converting about 10% of the solar energy into acetate. More efficient PV cells and MES systems could push the efficiency of artificial photosynthesis into a range where industrial applications become possible.

The efficiency of bioinorganic hybrid artificial photosynthesis for converting solar energy to chemicals has the potential to go well beyond 11 to 12%, the theoretical maximum solar energy-to-biomass conversion efficiency of natural photosynthesis. Recent advances clearly illustrate that this approach could, in a relatively short time, significantly improve the sustainability of the chemical and energy industries. Hybrid bioinorganic photosynthesis could bring multiple benefits to society by recycling the greenhouse gas CO₂ into useful products with energy from the Sun while avoiding conflicts with food production.

Science 13 November 2015:
Vol. 350 no. 6262 pp. 738-739
DOI: 10.1126/science.aad6452

http://www.sciencemag.org/content/350/6262/738.full