|This image portrays the water-splitting catalytic cycle with the Mn4Ca structure in the middle.|
An international team of researchers has derived the precise structure of a catalyst composed of four manganese atoms and one calcium atom (Mn4Ca) that drives the sunlight-powered water-splitting reaction that is the cornerstone of photosynthesis.
Their work, detailed in the 3 Nov 2006 issue of Science, could help researchers synthesize molecules that mimic this catalyst and thereby support the development of clean energy technologies that rely on sunlight to split water and form hydrogen to feed fuel cells or other non-polluting power sources.
Specifically, an international team led by scientists from the Lawrence Berkeley National Laboratory (Berkeley Lab) pieced together high-resolution (approximately 0.15 Ångstrom) structures of a Mn4Ca cluster found in a photosynthetic protein complex (one Ångstrom equals one ten-billionth of a meter).
The team, which includes scientists from Germany’s Technical and Free Universities in Berlin, the Max Planck Institute in Mülheim, and the Stanford Synchrotron Radiation Laboratory, used an innovative combination of x-ray spectroscopy and protein crystallography to yield the highest-resolution structures yet of the metal catalyst.
This is the first study to combine x-ray absorption spectroscopy and crystallography in such a detailed manner to determine the structure of an active metal site in a protein, especially something as complicated as the photosynthetic Mn4Ca cluster.—Junko Yano, Berkeley Lab
The metal catalyst resides in a large protein complex, called photosystem II, found in plants, green algae, and cyanobacteria. The system drives one of nature’s most efficient oxidizing reactions by using light energy to split water into oxygen, protons, and electrons. Because of its efficiency and reliance on nothing more than the sun, the catalyst has become a target of scientists working to develop carbon-neutral sources of energy.
Until now, the precise structure of the catalyst has eluded all attempts of determination by x-ray diffraction and various spectroscopic techniques. Even a 3.0-Ångstrom-resolution structure obtained by the Berkeley Lab group’s collaborators at the Technical and Free Universities in Berlin using x-ray diffraction didn’t allow the researchers to pinpoint the exact positions of the cluster’s manganese and calcium atoms and its surrounding ligands. Part of the problem is the fact that the metal catalyst is highly susceptible to radiation damage, which rules out extremely high-resolution x-ray diffraction studies.
To minimize radiation damage, Yano and colleagues combined x-ray absorption fine structure spectroscopy measurements with x-ray diffraction data from crystallographic studies, which were obtained at the Stanford Synchrotron Radiation Laboratory, where the techniques used in this study were developed in collaboration with the Berkeley Lab scientists. This technique exposes the Mn4Ca cluster to much lower doses of radiation, and enabled the team to obtain three similar structures at a resolution much higher than previously possible.
These three structures shed new light on how the catalyst fits within the much larger photosystem II protein complex. The x-ray diffraction structures at a medium resolution are sufficient to determine the overall shape and placement of the catalyst within the protein complex, and the spectroscopy measurements provide high-resolution information about the distances and orientation of the catalyst.
We have a real structure now. It’s not just guesswork anymore. Before, there were a lot of disparate pieces and scientists were forced to speculate on the catalyst’s structure. Now, we can begin to infer how the energy of sunlight is used to oxidize water to molecular oxygen.—Vittal Yachandra, Berkeley Lab
Scientists already know that the catalyst goes through four steps as it oxidizes water to oxygen, with each step triggered by the absorption of a photon. Now, they can learn how individual bonds are broken and formed, and how the water molecule splits apart, step by step. The group’s high-resolution structure is already yielding clues.
We found that our structure is unlike the 3.0 Ångstrom-resolution x-ray structure and other previously proposed models. The higher-resolution structures are likely to be important in gaining a mechanistic understanding of water oxidation.—Junko Yano
This work is part of Berkeley Lab’s Helios program, which seeks to develop abundant and inexpensive solar-based energy technologies. The research was supported by the US Department of Energy, Office of Basic Energy Sciences, the National Institutes of Health, the Deutsche Forschungsgemeinschaft, and the Max-Planck-Gesellschaft. Synchrotron facilities were provided by the Stanford Synchrotron Radiation Laboratory operated by DOE.
“Where Water Is Oxidized to Dioxygen: Structure of the Photosynthetic Mn4Ca Cluster”; Junko Yano, Jan Kern, Kenneth Sauer, Matthew J. Latimer, Yulia Pushkar, Jacek Biesiadka, Bernhard Loll, Wolfram Saenger, Johannes Messinger, Athina Zouni, Vittal K. Yachandra; Science 3 November 2006: Vol. 314. no. 5800, pp. 821 - 825 DOI: 10.1126/science.1128186