Two teams of researchers have revealed microscopic details of how oxygen is formed during photosynthesis, the process by which plants, algae and some bacteria harness sunlight to create the energy they need to grow. Understanding photosynthesis at this level could advance the development of clean fuels.
Researchers previously knew that just four consecutive particles of light, or photons, hitting a molecular structure within a plant are required to kick-start photosynthesis. These photons are absorbed by a cluster of manganese, calcium and oxygen atoms, which then break apart the plant’s water molecules, releasing the oxygen bound up in the water. But the details of what exactly happens after the fourth photon hits this cluster have eluded researchers for decades. Two experiments have now filled some of them in.
Jan Kern at Lawrence Berkeley National Laboratory in California and his colleagues captured the microscopic particulars of photosynthesis using pulses of high-energy X-rays. They arranged clusters of molecules extracted from blue-green algae on a conveyor belt, so that they were first illuminated with pulses of visible light that gave them the photons needed to start splitting water. Then the X-rays captured the arrangements of atoms during the process.
After being hit by the fourth photon, a protein complex known as Photosystem II (PSII) breaks down water molecules within a few millionths of a second. The X-rays were fast enough to show a time delay between the water splitting and the formation of a type of oxygen molecule that could eventually be released into the atmosphere – the two did not coincide. But the X-ray images taken between those two steps weren’t sharp enough to show the exact configuration of oxygen atoms.
However, the arrangement of other parts of PSII molecules around those oxygen atoms indicated that the oxygen formed some new structure. In this phase, oxygen atoms weren’t bound to hydrogen as they would be in water or gathered together in a larger oxygen molecule, but were probably briefly bound to another part of PSII. This step of the photosynthetic process has previously only been theorised, says Kern.
Holger Dau at the Free University of Berlin and his colleagues also focused on the tail end of the water-splitting process, but instead of taking X-ray images of atoms they used infrared light to determine how electrons and protons move between the atoms. They extracted PSII from 40 kilograms of fresh spinach and, after hitting it with photons of visible light, illuminated it with infrared light.
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When PSII absorbed infrared radiation, each wavelength correlated with vibrations of a specific bond. The researchers combined these measurements with computer simulations of how electrons and protons move during photosynthesis conducted by Leonardo Guidoni and his team at the University of L’Aquila in Italy. This uncovered a crucial new step in the process, where three protons are exchanged for one electron between oxygen atoms and the rest of PSII.
Philipp Simon, also at Lawrence Berkeley National Laboratory, says that some X-ray snapshots even imply that this proton motion may happen twice during the very end of the water-splitting process. Both teams want to uncover even more detail in the future by using faster X-rays, cleaner PSII samples and more infrared light. Guidoni says that these approaches to studying photosynthesis are complementary. “The more data we have from all experiments, the closer we’ll get to filling in every small step of the process,” he says.
Understanding water-splitting during photosynthesis is also important for developing devices that turn water into hydrogen fuel, says Dimitrios Pantazis at the Max Planck Institute for Coal Research in Germany. “We cannot replicate the biological system directly, but it is the only system we know that splits water so efficiently. So, we need to uncover all water-splitting tricks that evolved over billions of years,” he says.
Journal reference:
Nature DOI: 10.1038/s41586-023-06038-z, DOI: 10.1038/s41586-023-06008-5