Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1995 Apr 11;92(8):3209–3213. doi: 10.1073/pnas.92.8.3209

Detection of one slowly exchanging substrate water molecule in the S3 state of photosystem II.

J Messinger 1, M Badger 1, T Wydrzynski 1
PMCID: PMC42135  PMID: 11607525

Abstract

The exchangeability of the substrate water molecules at the catalytic site of water oxidation in photosystem II has been probed by isotope-exchange measurements using mass spectrometric detection of flash-induced oxygen evolution. A stirred sample chamber was constructed to reduce the lag time between injection of H2(18)O and the detecting flash by a factor of more than 1000 compared to the original experiments by R. Radmer and O. Ollinger [(1986) FEBS Lett. 195, 285-289]. Our data show that there is a slow (t1/2 approximately 500 ms, 10 degrees C) and a fast (t1/2 <25 ms, 10 degrees C) exchanging substrate water molecule in the S3 state of photosystem II. The slow exchange is coupled with an activation energy of about 75 kJ/mol and is discussed in terms of a terminal manganese oxo ligand, while the faster exchanging substrate molecule may represent a water molecule not directly bound to the manganese center.

Full text

PDF
3209

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Babcock G. T., Blankenship R. E., Sauer K. Reaction kinetics for positive charge accumulation on the water side of chloroplast photosystem II. FEBS Lett. 1976 Jan 15;61(2):286–289. doi: 10.1016/0014-5793(76)81058-7. [DOI] [PubMed] [Google Scholar]
  2. Babcock G. T., Wikström M. Oxygen activation and the conservation of energy in cell respiration. Nature. 1992 Mar 26;356(6367):301–309. doi: 10.1038/356301a0. [DOI] [PubMed] [Google Scholar]
  3. Brudvig G. W., Crabtree R. H. Mechanism for photosynthetic O2 evolution. Proc Natl Acad Sci U S A. 1986 Jul;83(13):4586–4588. doi: 10.1073/pnas.83.13.4586. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Debus R. J. The manganese and calcium ions of photosynthetic oxygen evolution. Biochim Biophys Acta. 1992 Oct 16;1102(3):269–352. doi: 10.1016/0005-2728(92)90133-m. [DOI] [PubMed] [Google Scholar]
  5. Hashimoto S., Tatsuno Y., Kitagawa T. Resonance Raman evidence for oxygen exchange between the FeIV = O heme and bulk water during enzymic catalysis of horseradish peroxidase and its relation with the heme-linked ionization. Proc Natl Acad Sci U S A. 1986 Apr;83(8):2417–2421. doi: 10.1073/pnas.83.8.2417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Kambara T., Govindjee Molecular mechanism of water oxidation in photosynthesis based on the functioning of manganese in two different environments. Proc Natl Acad Sci U S A. 1985 Sep;82(18):6119–6123. doi: 10.1073/pnas.82.18.6119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Kok B., Forbush B., McGloin M. Cooperation of charges in photosynthetic O2 evolution-I. A linear four step mechanism. Photochem Photobiol. 1970 Jun;11(6):457–475. doi: 10.1111/j.1751-1097.1970.tb06017.x. [DOI] [PubMed] [Google Scholar]
  8. MEHLER A. H., BROWN A. H. Studies on reactions of illuminated chloroplasts. III. Simultaneous photoproduction and consumption of oxygen studied with oxygen isotopes. Arch Biochem Biophys. 1952 Jul;38:365–370. doi: 10.1016/0003-9861(52)90042-8. [DOI] [PubMed] [Google Scholar]
  9. Malmström B. G. Enzymology of oxygen. Annu Rev Biochem. 1982;51:21–59. doi: 10.1146/annurev.bi.51.070182.000321. [DOI] [PubMed] [Google Scholar]
  10. Messinger J., Renger G. Analyses of pH-induced modifications of the period four oscillation of flash-induced oxygen evolution reveal distinct structural changes of the photosystem II donor side at characteristic pH values. Biochemistry. 1994 Sep 13;33(36):10896–10905. doi: 10.1021/bi00202a008. [DOI] [PubMed] [Google Scholar]
  11. Messinger J., Renger G. Generation, oxidation by the oxidized form of the tyrosine of polypeptide D2, and possible electronic configuration of the redox states S0, S-1, and S-2 of the water oxidase in isolated spinach thylakoids. Biochemistry. 1993 Sep 14;32(36):9379–9386. doi: 10.1021/bi00087a017. [DOI] [PubMed] [Google Scholar]
  12. Messinger J., Renger G. The reactivity of hydrazine with photosystem II strongly depends on the redox state of the water oxidizing system. FEBS Lett. 1990 Dec 17;277(1-2):141–146. doi: 10.1016/0014-5793(90)80829-8. [DOI] [PubMed] [Google Scholar]
  13. Messinger J., Schröder W. P., Renger G. Structure-function relations in photosystem II. Effects of temperature and chaotropic agents on the period four oscillation of flash-induced oxygen evolution. Biochemistry. 1993 Aug 3;32(30):7658–7668. doi: 10.1021/bi00081a009. [DOI] [PubMed] [Google Scholar]
  14. Nordblom G. D., White R. E., Coon M. J. Studies on hydroperoxide-dependent substrate hydroxylation by purified liver microsomal cytochrome P-450. Arch Biochem Biophys. 1976 Aug;175(2):524–533. doi: 10.1016/0003-9861(76)90541-5. [DOI] [PubMed] [Google Scholar]
  15. Ono T. A., Noguchi T., Inoue Y., Kusunoki M., Matsushita T., Oyanagi H. X-ray Detection of the Period-Four Cycling of the Manganese Cluster in Photosynthetic Water Oxidizing Enzyme. Science. 1992 Nov 20;258(5086):1335–1337. doi: 10.1126/science.258.5086.1335. [DOI] [PubMed] [Google Scholar]
  16. Radmer R., Ollinger O. Do the higher oxidation states of the photosynthetic O2-evolving system contain bound H2O? FEBS Lett. 1986 Jan;195(1-2):285–289. doi: 10.1016/0014-5793(86)80178-8. [DOI] [PubMed] [Google Scholar]
  17. Rutherford A. W. Photosystem II, the water-splitting enzyme. Trends Biochem Sci. 1989 Jun;14(6):227–232. doi: 10.1016/0968-0004(89)90032-7. [DOI] [PubMed] [Google Scholar]
  18. Vass I., Styring S. pH-dependent charge equilibria between tyrosine-D and the S states in photosystem II. Estimation of relative midpoint redox potentials. Biochemistry. 1991 Jan 22;30(3):830–839. doi: 10.1021/bi00217a037. [DOI] [PubMed] [Google Scholar]
  19. Winget G. D., Izawa S., Good N. E. The stoichiometry of photophosphorylation. Biochem Biophys Res Commun. 1965 Dec 9;21(5):438–443. doi: 10.1016/0006-291x(65)90401-8. [DOI] [PubMed] [Google Scholar]
  20. Yachandra V. K., DeRose V. J., Latimer M. J., Mukerji I., Sauer K., Klein M. P. Where plants make oxygen: a structural model for the photosynthetic oxygen-evolving manganese cluster. Science. 1993 Apr 30;260(5108):675–679. doi: 10.1126/science.8480177. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES