Postcards from the photosynthetic edge

Photosytem II utilizes a water-splitting manganese-calcium enzyme that when energized by sunlight catalyzes a four photon-step cycle of oxidation states (S0-to-S3). When S3 absorbs a photon, molecular oxygen (O2) is released and S0 is generated. S4 is a transient state on the way to S0. Image: SLAC National Accelerator LaboratoryA crucial piece of the puzzle behind nature’s ability to split the water molecule during photosynthesis that could help advance the development of artificial photosynthesis for clean, green and renewable energy has been provided by an international collaboration of scientists led by researchers with the Lawrence Berkeley National Laboratory (Berkeley Lab) and the SLAC National Accelerator Laboratory. Working at SLAC’s Linac Coherent Light Source (LCLS), a powerful x-ray laser, the researchers were able to take detailed “snapshots” of the four photon-step cycle for water oxidation in photosystem II, a large protein complex in green plants. Photosystem II is the only known biological system able to harness sunlight for the oxidation of water into molecular oxygen. “An effective method of solar-based water-splitting is essential for artificial photosynthesis to succeed but developing such a method has proven elusive,” says Vittal Yachandra, a chemist with Berkeley Lab’s Physical Biosciences Div. and one of the leaders of this study. “Using femtosecond x-ray pulses for the simultaneous collection of both x-ray diffraction (XRD) and x-ray emission spectroscopy (XES) data at room temperature, we have gone around the four-step catalytic cycle of photosynthetic water oxidation in photosystem II. This represents a major advance towards the real time characterization of the formation of the oxygen molecule in photosystem II, and has yielded information that should prove useful for designing artificial solar-energy based devices to split water.” Photo-oxidation of water by photosystem II is responsible for most of the oxygen in Earth’s atmosphere. At the core of photosystem II is a manganese-calcium (Mn4Ca) metalloenzyme complex that when energized by solar photons catalyzes a four photon-step cycle of oxidation states (S0-to-S3) that ultimately yields molecular oxygen. Scientists need to observe intact x-ray crystallography of the Mn4Ca ion in action but the molecule is highly sensitive to radiation. The LCLS is the world’s only source of x-rays capable of providing femtosecond pulses at the high intensities that allow intact photosystem II crystals to be imaged before they are destroyed by exposure to the x-ray beams. “In an earlier study at the LCLS, we reported combined XRD and XES data from photosystem II samples in the dark S1state and the one visible-flash illuminated S2(1-flash) state,” says Junko Yano, a chemist also with Berkeley Lab’s Physical Biosciences Div. and also a leader of this research. “In this new study we report data from the S3(2-flash) and S0(3-flash) states, which are the intermediate states directly before and after the evolution of the oxygen molecule. In addition, we report data for the first time from a light-induced transient state between the S3and S0states, which opens the window for elucidating the mechanism of oxygen-oxygen bond formation that occurs between these two states.”