Where water is oxidized to dioxygen:: Structure of the photosynthetic Mn4Ca cluster from X-ray spectroscopy

被引:128
作者
Yano, Junko [1 ]
Yachandra, Vittal K. [1 ]
机构
[1] Univ Calif Berkeley, Lawrence Berkeley Lab, Phys Biosci Div, Berkeley, CA 94720 USA
关键词
D O I
10.1021/ic7016837
中图分类号
O61 [无机化学];
学科分类号
070301 ; 081704 ;
摘要
Light-driven oxidation of water to dioxygen in plants, algae, and cyanobacteria is catalyzed within photosystem II (PS II) by a Mn4Ca cluster. Although the cluster has been studied by many different methods, its structure and mechanism have remained elusive. X-ray absorption and emission spectroscopy and extended X-ray absorption fine structure studies have been particularly useful in probing the electronic and geometric structures and the mechanism of the water oxidation reaction. Recent progress, reviewed here, includes polarized X-ray absorption spectroscopy measurements of PS II single crystals. Analysis of those results has constrained the Mn4Ca cluster geometry to a set of three similar high-resolution structures. The structure of the cluster from the present study is unlike either the 3.0- or 3.5-angstrom-resolution X-ray structures or other previously proposed models. The differences between the models derived from X-ray spectroscopy and crystallography are predominantly because of damage to the Mn4Ca cluster by X-rays under conditions used for the structure determination by X-ray crystallography. X-ray spectroscopy studies are also used for studying the changes in the structure of the Mn4Ca catalytic center as it cycles through the five intermediate states known as the S-i states (i = 0-4). The electronic structure of the Mn4Ca cluster has been studied more recently using resonant inelastic X-ray scattering spectroscopy (RIXS), in addition to the earlier X-ray absorption and emission spectroscopy methods. These studies are revealing that the assignment of formal oxidation states is overly simplistic. A more accurate description should consider the charge density on the Mn atoms, which includes the covalency of the bonds and delocalization of the charge over the cluster. The geometric and electronic structures of the Mn4Ca cluster in the S states derived from X-ray spectroscopy are leading to a detailed understanding of the mechanism of O-O bond formation during the photosynthetic watersplitting process.
引用
收藏
页码:1711 / 1726
页数:16
相关论文
共 107 条
[1]   The S0 state EPR signal from the Mn cluster in photosystem II arises from an isolated S=1/2 ground state [J].
Åhrling, KA ;
Peterson, S ;
Styring, S .
BIOCHEMISTRY, 1998, 37 (22) :8115-8120
[2]   Molecular and electronic structure of nitridocyanometalates of chromium(V) and manganese(V):: A combined experimental and DFT study [J].
Bendix, J ;
Deeth, RJ ;
Weyhermüller, T ;
Bill, E ;
Wieghardt, K .
INORGANIC CHEMISTRY, 2000, 39 (05) :930-938
[3]   A high-resolution large-acceptance analyzer for X-ray fluorescence and Raman spectroscopy [J].
Bergmann, U ;
Cramer, SP .
CRYSTAL AND MULTILAYER OPTICS, 1998, 3448 :198-209
[4]   Crystal structure of cyanobacterial photosystem II at 3.2 Å resolution:: a closer look at the Mn-cluster [J].
Biesiadka, J ;
Loll, B ;
Kern, J ;
Irrgang, KD ;
Zouni, A .
PHYSICAL CHEMISTRY CHEMICAL PHYSICS, 2004, 6 (20) :4733-4736
[5]   EPR study of the oxygen evolving complex in His-tagged photosystem II from the cyanobacterium Synechococcus elongatus [J].
Boussac, A ;
Sugiura, M ;
Inoue, Y ;
Rutherford, AW .
BIOCHEMISTRY, 2000, 39 (45) :13788-13799
[6]   High-spin states (S≥5/2) of the photosystem II manganese complex [J].
Boussac, A ;
Un, S ;
Horner, O ;
Rutherford, AW .
BIOCHEMISTRY, 1998, 37 (12) :4001-4007
[7]  
Brudvig GW, 1995, ADV CHEM SER, V246, P249
[8]   Parallel polarization EPR detection of an S1-state "multiline" EPR signal in photosystem II particles from Synechocystis sp. PCC 6803 [J].
Campbell, KA ;
Peloquin, JM ;
Pham, DP ;
Debus, RJ ;
Britt, RD .
JOURNAL OF THE AMERICAN CHEMICAL SOCIETY, 1998, 120 (02) :447-448
[9]   An evaluation of structural models for the photosynthetic water-oxidizing complex derived from spectroscopic and X-ray diffraction signatures [J].
Carrell, TG ;
Tyryshkin, AM ;
Dismukes, GC .
JOURNAL OF BIOLOGICAL INORGANIC CHEMISTRY, 2002, 7 (1-2) :2-22
[10]   ELECTRON-PARAMAGNETIC-RES DETECTION OF A CRYOGENICALLY PHOTOGENERATED INTERMEDIATE IN PHOTOSYNTHETIC OXYGEN EVOLUTION [J].
CASEY, JL ;
SAUER, K .
BIOCHIMICA ET BIOPHYSICA ACTA, 1984, 767 (01) :21-28