Using the SLAC National Accelerator Laboratory’s Linac Coherent Light Source – the world’s most powerful X-ray laser, a multinational group of scientists was able to take detailed snapshots of photosynthesis in action as it splits water into oxygen, protons and electrons.

Photosynthesis, a process catalyzed by plants, algae and cyanobacteria, is one of the fundamental processes of life on Earth. It converts sunlight to energy thus sustaining all higher life on Earth.

Two large protein complexes, called photosystem I and II, act in series to catalyze the light-driven reactions in photosynthesis.

Photosystem II produces the oxygen we breathe, which ultimately keeps us alive.

The revealing of the mechanism of this process is essential for the development of artificial systems that mimic and surpass the efficiency of natural systems.

“Photosynthetic organisms already know how to do this, and we need to know the details of how photosynthesis carries out the process using abundant manganese and calcium,” said Prof Devens Gust of Arizona State University, who was not involved in the research.

In photosynthesis, oxygen is produced at a special metal site containing four manganese atoms and one calcium atom, connected together as a metal cluster.

This oxygen-evolving cluster is bound to photosystem II that catalyzes the light-driven process of water splitting. It requires four light flashes to extract one molecule of oxygen from two water molecules bound to the metal cluster.

There are two major drawbacks to obtaining structural and dynamical information on this process by a traditional technique called X-ray crystallography: (i) the pictures one can obtain with standard structural determination methods are static; (ii) the quality of the structural information is adversely affected by X-ray damage.

“The trick is to use the world’s most powerful X-ray laser, SLAC’s Linac Coherent Light Source. Extremely fast femtosecond pulses record snapshots of the photosystem II crystals before they explode in the X-ray beam, a principle called diffraction before destruction. In this way, snapshots of the process of water splitting are obtained damage-free. The ultimate goal of the work is to record molecular movies of water splitting,” explained Prof Petra Fromme of Arizona State University, the senior author of the paper published in the journal Nature.

Prof Fromme and her colleagues performed the time-resolved femtosecond crystallography experiments on photosystem II nanocrystals, which are so small that you can hardly see them, even under a microscope.

The crystals are hit with two green laser flashes before the structural changes are elucidated by the femtosecond X-ray pulses.

The team discovered large structural changes of the protein and the metal cluster that catalyzes the reaction.

The cluster significantly elongates, thereby making room for a water molecule to move in.

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Christopher Kupitz et al. Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser. Nature, published online July 09, 2014; doi: 10.1038/nature13453