The Role of Calcium in Photosynthetic Water Oxidation Studied by X-Ray Absorption Spectroscopy
Rosalie Tran1, Emily Tsui2, Jacob Kanady2, Jan Kern1,3, Benedikt Lassalle1, Sheraz Gul1, Guangye Han1, Ruchira
Chatterjee1, Alain Boussac4, Theodor Agapie2, Vittal Yachandra1, and Junko Yano1.
1
Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
Department of Chemistry and Chemical Engineering, California Institute of Technology, Pasadena, CA 91125,
USA.
3
SLAC National Accelerator Laboratory, Menlo Park, CA 94025, USA.
4
iBiTec-S, URA CNRS 2096, CEA Saclay, 91191 Gif sur Yvette, France.
2
The oxygen-evolving complex (OEC) is a Mn4CaO5 cluster located within the Photosystem II (PSII) membrane
complex, and catalyzes the light-driven conversion of water to oxygen during photosynthesis. During the
catalytic (Kok) cycle, the OEC undergoes transition through five structurally and electronically distinct Si-states (i
= 0-4), coupling the one-electron photochemistry of the reaction center with the four-electron chemistry of water
oxidation. Calcium is an essential cofactor for water oxidation, with previous studies on the photoactivation and
assembly of the OEC implicating the requirement of this ion for S-state advancement and enzymatic activity [1,2].
Despite extensive studies on the Mn4CaO5 cluster, a more comprehensive understanding of how calcium is
involved in photosynthetic water oxidation remains incomplete. One of the intriguing results from electron
paramagnetic resonance (EPR) and X-ray absorption spectroscopy (XAS) studies is that depletion of Ca does not
significantly perturb the core geometry of the Mn4 cluster [3-5]. Thus, to investigate the role of calcium in this
catalytic reaction, Ca K-edge XAS was used to directly probe the OEC of PSII from Thermosynechococcus
elongatus (T. elongatus). This approach focuses on the native cofactor, avoiding the use of biosynthetically
prepared 1-Sr PSII or treatments involving Ca depletion and Sr substitution. In XAS, X-ray absorption near edge
spectroscopy (XANES) can provide insight into the electronic structure and symmetry of the Ca site, whereas
Extended X-ray Absorption Fine Structure (EXAFS) presents details on the numbers, types, and distances to
ligands and neighboring atoms from the absorbing element. Additionally, the XANES pre-edge feature may
reveal information on the metal-ligand interactions since this formally forbidden transition [from 1s to (n-1)d] can
gain intensity when the metal-ligand environment is distorted from a centro-symmetric to a non-centro-symmetric
coordination [6]. Ca XANES were measured for these 1-Ca PSII complexes to examine the S-states of the Kok
cycle. To better understand the Ca XANES pre-edge features and elucidate the structural and electronic changes
occurring throughout the S-states, a series of inorganic Ca/Mn model complexes were also systematically studied
via Ca K-edge XAS. Ca XANES and EXAFS results from these studies on 1-Ca PSII will be presented, and
discussed together with the series of inorganic Ca/Mn model complexes.
References:
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[4] Latimer MJ, DeRose VJ, Yachandra VK, Sauer K, Klein MP. (1998) J Phys Chem B, 102, 8257-8265.
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complex of Photosystem II (Master’s thesis). University of Konstanz, Baden-Württemberg, Germany.
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