Abstract
In order to investigate oxygen binding and hydrophobic cavities in photosystem II (PSII), we have introduced xenon under pressure into crystals of PSII isolated from Thermosynechococcus elongatus and used X-ray anomalous diffraction analyses to identify the xenon sites in the complex. Under the conditions employed, 25 Xe-binding sites were identified in each monomer of the dimeric PSII complex. The majority of these were distributed within the membrane spanning portion of the complex with no obvious correlation with the previously proposed oxygen channels. One binding site was located close to the haem of cytochrome b559 in a position analogous to a Xe-binding site of myoglobin. The only Xe-binding site not associated with the intrinsic subunits of PSII was within the hydrophobic core of the PsbO protein.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.Abbreviations
- CP43:
-
Chlorophyll-binding PsbC protein
- D1:
-
Reaction centre PsbA protein
- PSII:
-
Photosystem II
References
Anderson JM (2001) Does functional photosystem II complex have an oxygen channel? FEBS Lett 488:1–4. doi:10.1016/S0014-5793(00)02358-9
Barber J, Rutherford AW (2007) Revealing how nature uses sunlight to split water. Philos Trans R Soc Lond B Biol Sci 363:1123–1303
Clausen J, Junge W (2004) Detection of an intermediate of photosynthetic water oxidation. Nature 430:480–483. doi:10.1038/nature02676
Clausen J, Junge W, Dau H, Haumann M (2005) Photosynthetic water oxidation at high O2 backpressure monitored by delayed chlorophyll fluorescence. Biochemistry 44:12775–12779. doi:10.1021/bi051183a
De Las Rivas J, Barber J (2004) Analyses of the structure of the PsbO protein and its implications. Photosynth Res 81:329–343. doi:10.1023/B:PRES.0000036889.44048.e4
DeLano WL (2002) The PyMOL molecular graphics system. DeLano Scientific, San Carlos, CA, USA. http://www.pymol.org
Diederichs K, Karplus PA (1997) Improved R-factors for diffraction data analysis in macromolecular crystallography. Nat Struct Biol 4:269–275. doi:10.1038/nsb0497-269
Doukov TI, Blasiak LC, Seravalli J, Ragsdale SW, Drennan CL (2008) Xenon in and at the end of the tunnel of bifunctional carbon monoxide dehydrogenase/acetyl-CoA synthase. Biochemistry 47:3474–3483. doi:10.1021/bi702386t
Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60:2126–2132. doi:10.1107/S0907444904019158
Haumann M, Grundmeier A, Zaharieva I, Dau H (2008) Photosynthetic water oxidation an evoluted dioxygen partial pressure monitored by time-resolved X-ray absorption measurements. Proc Natl Acad Sci USA (in press)
Ho FM, Styring S (2007) Access channels and methanol binding site to CaMn(4) cluster in photosystem II based on solvent accessibility simulations, with implications for substrate water access. Biochim Biophys Acta 1777:140–153
Kabsch WJ (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J Appl Crystallogr 26:795–800. doi:10.1107/S0021889893005588
Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438:1040–1044. doi:10.1038/nature04224
McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ (2005) Phaser crystallographic software. J Appl Crystallogr 40:658–674. doi:10.1107/S0021889807021206
Murray JW, Barber J (2007) Structural characteristics of channels and pathways in photosystem II including the identification of an oxygen channel. J Struct Biol 159:228–237. doi:10.1016/j.jsb.2007.01.016
Murray JW, Maghlaoui K, Kargul J, Ishida N, Lai T-LA, Rutherford AW et al (2008) X-ray crystallography identifies two chloride binding sites in the oxygen evolving centre of photosystem II. Energy Environ Sci 1:161–166. doi:10.1039/b810067p
Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53:240–255. doi:10.1107/S0907444996012255
Nienhaus K, Knapp JE, Palladino P, Royer WE, Nienhaus GU (2007) Ligand migration and binding in the dimeric hemoglobin of Scapharca inaequivalvis. Biochemistry 46(49):14018–14031. doi:10.1021/bi7016798
Petřek M, Otyepka M, Banáš P, Košinová P, Koča J, Damborský J (2006) CAVER: a new tool to explore routes from protein clefts, pockets and cavities. BMC Bioinformatics 7:316–324. doi:10.1186/1471-2105-7-316
Petřek M, Košinová P, Koča J, Otyepka M (2007) MOLE: a Voronoi diagram-based explorer of molecular channels, pores, and tunnels. Structure 15:1357–1363. doi:10.1016/j.str.2007.10.007
Riistama S, Puustinen A, Garca-Horsman A, Iwata S, Michel H, Wikstrom M (1996) Channelling of dioxygen into the respiratory enzyme. Biochim Biophys Acta 1275:1–4. doi:10.1016/0005-2728(96)00040-0
Schiltz M, Fourme R, Prangé T (2003) Use of noble gases xenon and krypton as heavy atoms in protein structure determination. Methods Enzymol 374:83–199. doi:10.1016/S0076-6879(03)74004-X
Schoenborn BP, Watson HC, Kendrew JC (1965) Binding of xenon to sperm whale myoglobin. Nature 207:28–30. doi:10.1038/207028a0
Svensson-Ek M, Abramson J, Larsson G, Trnroth S, Brzezinski P, Iwata S (2002) The X-ray crystal structure of wild-type and EQ (I-286) mutant cytochrome c oxidase from Rhodobacter sphaeroides. J Mol Biol 321:329–339. doi:10.1016/S0022-2836(02)00619-8
Wydrzynski TJ, Satoh K (2005) Photosystem II: the light-driven water: plastoquinone oxidoreductase. In: Wydrzynski TJ, Satoh K (eds) Advances in photosynthesis and respiration, vol 22. Springer, Dordrecht, The Netherlands, pp 1–76
Acknowledgments
We thank Elspeth Garman for the generous loan of a xenon cylinder and the pressurisation cell. We acknowledge financial support for this work from the Biotechnology and Biological Science Research Council (BBSRC) and from The Royal Society UK–Japan exchange programme. Preliminary data were collected at the Diamond synchrotron. We wish to acknowledge our access to the facilities and staff of the Swiss Light Source, particularly Clemens Schulze-Briese.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
These files are unfortunately not in the Publisher's archive anymore:
-
(PDB 1 kb)
-
(CIF 4866 kb)
-
(MTZ 4543 kb)
Rights and permissions
About this article
Cite this article
Murray, J.W., Maghlaoui, K., Kargul, J. et al. Analysis of xenon binding to photosystem II by X-ray crystallography. Photosynth Res 98, 523–527 (2008). https://doi.org/10.1007/s11120-008-9366-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-008-9366-2