The launch of the space adventure has put the spotlight on artificial photosynthesis. Sustaining life in space is dependent on oxygen, water and energy sources, so attention turns to the age-old photosynthesis process to solve these challenges. The intensive research during decades focused on unravelling the biological, chemical and physical keys that make the photosynthetic process highly efficient have inspired artificial and semi-artificial in vitro technologies. In particular, the photosynthetic water-splitting reaction (water oxidation by sunlight), discovered fifty-five years ago, has inspired materials and technologies focused in molecular oxygen and hydrogen production.

It is well-known that oxygenic photosynthesis is a biological process that only occurs in green organisms – it is a process that animals, and therefore humans, cannot perform – and that it sustains aerobic life on Earth by producing molecular oxygen from sunlight and water. It emerged from ancestral anoxygenic phototrophs, likely between 3.4 and 2.9 billion years ago. Subsequently, the coevolution and rapid diversification of major cyanobacterial lineages, together endosimbiosis, dramatically expanded this biological process. Oxygenic photosynthesis is the main source of oxygen in the atmosphere and biomass but let us not forget that providing oxygen to the environment is not a main task of the photosynthetic process. Oxygen is only a by-product of the initial stages of photosynthesis. It is released from the water-splitting induced by light in the donor side of Photosystem II (PSII), a multi-subunit membrane protein-pigment complex embedded into the thylakoid membrane.

Shining light on photosynthesis

The light-induced oxidation of water by PSII has captivated the attention of numerous researchers since the middle of the 20th Century. In 1969, fifty-five years ago, Pierre Joliot discovered the mechanism of the period of four oscillations induced by light-flash for oxygen evolution in the donor side of PSII at the lumen of thylakoid membranes. One year later, Bessel Kok (1970) introduced the concept of S-states of the oxygen-evolving complex, indicating the cooperation of four flash-induced oxidizing chemical species (S-states) to yield molecular oxygen, where each S-state has a different number of oxidizing equivalents. This is named the Kok-Joliot cycle model for photosynthetic oxygen-evolving mechanism. But up to 2006 the identity of the oxidizing chemical species (S-states) was not known. Knowledge of the manganese oxidation states of the oxygen-evolving complex and the structure of the manganese-calcium cluster in PSII was crucial for understanding the mechanism of biological water oxidation. The 1.9 Å resolution crystal structure of PSII published in 2011 revealed the water splitting site in atomic detail, which had remained elusive. This structure removed previous uncertainties. Since catalysis is essential for the water splitting mechanism, the structure of the inorganic Mn₄CaO₅ cluster, which is ligated to PSII by one histidine, six carboxylate ligands, and four water-derived terminal ligands, was an important step towards developing artificial catalysts that oxidizes water to molecular oxygen (O₂) and hydrogen equivalents, which could yield hydrogen (H₂) production.

2H₂O (lumen) + 4hv (440-680 nm) → O₂ + 4H⁺ (lumen) + 4e⁻

2H⁺ + 2e⁻ → H₂

Making artificial photosynthetic devices

From then on, what had been a subject of interest only to biochemists and biophysicists in understanding the complexity of this biological system, became of interest to other disciplines and applications. From 1970, FEBS Letters and The FEBS Journal have contributed to diffusion of part of these basic investigations. The findings promoted a race to create artificial photosynthetic devices. There has been five decades of long debate on this topic for the development of multicomponent systems and bio-inspired catalysts. The former studies were mainly focused on covalently linked systems combining organized aggregates of photosensitizers and catalysts in solution. Metalloporphyrins and metal dendrimers (i.e., Ru₄ or OsRu₉) complexes as photosensitizers, catalysts based on metal complexes (i.e., Ru₄POM) and electron mediators based on cobalt or copper complexes, among others, have been extensively investigated. Persulfate anions as electron acceptors (Ru₄POM/Ru₄/S₂O₈^2-) have been looked into as well, and either non-aggregates or self-assembly systems have also been investigated. In the last decade, other strategies have emerged, such as the use of hydrogels instead of aqueous/solvent solution to mimic the internal structure of plant chloroplasts, which co-localize the molecular components for water oxidation. For that, nickel-based catalysts and other organometallic complexes have been proposed. Hardware and devices with improved components are being designed, and stability and efficiency under different temperature, pressure and gravity conditions, are tested.

The lack of oxygen and fuel constraints in space limit the duration of long-term missions or future permanent human presence on the Moon and Mars. Currently, these limitations are promoting an exciting competition to develop space technology for oxygen production and secure supply of fuel in space. In this sense, devices based on artificial photosynthesis are being proposed as a solution to colonize space. Although there are technologies to produce oxygen – electrolysis is the chemical reaction most commonly used to produce oxygen from water – they require electricity as an energy source. By contrasts, efficient bio-inspired systems based on natural photosynthesis do not require a source of electricity; this technology bypasses the need for it.

Alternative devices produce oxygen and hydrogen from water and light using semiconductor materials coated with metallic catalysts. With these and the use of solar radiation, astronauts could breathe oxygen without limitations on space missions and there would be no need for resupply from Earth. Research by the European Spatial Agency (ESA) suggests that given the conditions on the Moon, this strategy could work, and even on Mars, where sunlight is less intense, it could work by using solar mirrors to concentrate the sunlight received. It is argued that artificial photosynthesis could operate at room temperature and at pressures found on the Moon and Mars, and the different gravity conditions, would not be a limitation. This could be an advantage to be used directly in those habitats with water as the main resource. In the Moon a widespread presence of water ice has been detected, which would be a valuable resource of oxygen and hydrogen for life support and fuel.

“In 2020, NASA announced the discovery of water on the sunlit surface of the Moon. In 2023, a new map of water distribution on the Moon provided hints about how water may be moving across the Moon’s surface”. NASA Science

Photosynthesis with an App in Virtual Reality!

If you would like to use photosynthesis in your education or outreach activities, check out the Virtual Reality App "Photosystem II: assembly and function in virtual reality" on this other post from the author. It is an educational tool for teachers and students that allows the viewer to immerse themselves in the first stages of photosynthesis inside plant cells, showing the activity of the biomolecules involved and the water-splitting reaction.

Top image from Inmaculada Yruela.