Revealing the structure of the oxygen-evolving core dimer of photosystem II by cryoelectron crystallography

Here we present cryoelectron crystallographic analysis of an isolated dimeric oxygen-evolving complex of photosystem II (at a resolution of ~0.9 nm), revealing that the D1–D2 reaction center (RC) proteins are centrally located between the chlorophyll-binding proteins, CP43 and CP47. This conclusion supports the hypothesis that photosystems I and II have similar structural features and share a common evolutionary origin. Additional density connecting the two halves of the dimer, which was not observed in a recently described CP47–RC complex that did not include CP43, may be attributed to the small subunits that are involved in regulating secondary electron transfer, such as PsbH. These subunits are possibly also required for stabilization of the dimeric photosystem II complex. This complex, containing at least 29 transmembrane helices in its asymmetric unit, represents one of the largest membrane protein complexes studied at this resolution.

[1]  É. Hideg,et al.  Further characterization of the psbH locus of Synechocystis sp. PCC 6803: inactivation of psbH impairs QA to QB electron transport in photosystem 2. , 1993, Biochemistry.

[2]  Donald R. Ort,et al.  Oxygenic Photosynthesis: The Light Reactions , 1996, Advances in Photosynthesis and Respiration.

[3]  P. Fromme,et al.  Photosystem I at 4 Å resolution represents the first structural model of a joint photosynthetic reaction centre and core antenna system , 1996, Nature Structural Biology.

[4]  P. Fromme,et al.  A common ancestor for oxygenic and anoxygenic photosynthetic systems: a comparison based on the structural model of photosystem I. , 1998, Journal of molecular biology.

[5]  G. Garab,et al.  Photosynthesis: Mechanisms and Effects , 1998, Springer Netherlands.

[6]  J. Lepault,et al.  Structure of purple membrane from halobacterium halobium: recording, measurement and evaluation of electron micrographs at 3.5 Å resolution , 1986 .

[7]  J. Barber,et al.  Localization of the 23-kDa subunit of the oxygen-evolving complex of photosystem II by electron microscopy. , 1998, European journal of biochemistry.

[8]  J. Barber.  The Light reactions , 1987 .

[9]  M van Heel,et al.  A new generation of the IMAGIC image processing system. , 1996, Journal of structural biology.

[10]  J. Barber,et al.  The structure, function and dynamics of photosystem two , 1997 .

[11]  P. Fromme,et al.  Structure of Photosystem I at 4.5 Å resolution: A short review including evolutionary aspects , 1996 .

[12]  James Barber,et al.  Three-dimensional structure of the plant photosystem II reaction centre at 8 Å resolution , 1998, Nature.

[13]  J. Deisenhofer,et al.  Relevance of the photosynthetic reaction center from purple bacteria to the structure of photosystem II , 1988 .

[14]  G. Friso,et al.  The three-dimensional structure of a photosystem II core complex determined by electron crystallography. , 1997, Structure.

[15]  R. Henderson,et al.  Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. , 1990, Journal of molecular biology.

[16]  D. Mastronarde,et al.  Two-dimensional crystals of photosystem II: biochemical characterization, cryoelectron microscopy and localization of the D1 and cytochrome b559 polypeptides , 1996, Journal of Cell Biology.

[17]  W. Kühlbrandt,et al.  Two-dimensional structure of plant photosystem II at 8-Å resolution , 1997, Nature.

[18]  N. K. Packham.  Is the 9 kDa thylakoid membrane phosphoprotein functionally and structurally analogous to the ‘H’ subunit of bacterial reaction centres? , 1988, FEBS letters.

[19]  P. Fromme,et al.  Photosystem I of Synechococcus elongatus at 4 A resolution: comprehensive structure analysis. , 1997, Journal of molecular biology.

[20]  G. Giacometti,et al.  Investigation of the neighbour relationships between photosystem II polypeptides in the two types of isolated reaction centres (D1/D2/cytb 559 and CP47/D1/D2/cyt b 559 complexes) , 1992, FEBS letters.

[21]  G. Friso,et al.  Structural changes and lateral redistribution of photosystem II during donor side photoinhibition of thylakoids , 1992, The Journal of cell biology.

[22]  U. K. Laemmli,et al.  Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4 , 1970, Nature.

[23]  J. Barber,et al.  Isolation and biochemical characterisation of monomeric and dimeric photosystem II complexes from spinach and their relevance to the organisation of photosystem II in vivo. , 1997, European journal of biochemistry.