Skip to main content
SpringerLink
Log in

EPR and ENDOR studies of the water oxidizing complex of Photosystem II

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

A comparative study of X-band EPR and ENDOR of the S2 state of photosystem II membrane fragments and core complexes in the frozen state is presented. The S2 state was generated either by continuous illumination at T=200 K or by a single turn-over light flash at T=273 K yielding entirely the same S2 state EPR signals at 10 K. In membrane fragments and core complex preparations both the multiline and the g=4.1 signals were detected with comparable relative intensity. The absence of the 17 and 23 kDa proteins in the core complex preparation has no effect on the appearance of the EPR signals. 1H-ENDOR experiments performed at two different field positions of the S2 state multiline signal of core complexes permitted the resolution of four hyperfine (hf) splittings. The hf coupling constants obtained are 4.0, 2.3, 1.1 and 0.6 MHz, in good agreement with results that were previously reported (Tang et al. (1993) J Am Chem Soc 115: 2382–2389). The intensities of all four line pairs belonging to these hf couplings are diminished in D2O. A novel model is presented and on the basis of the two largest hfc's distances between the manganese ions and the exchangeable protons are deduced. The interpretation of the ENDOR data indicates that these hf couplings might arise from water which is directly ligated to the manganese of the water oxidizing complex in redox state S2.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

cw:

continuous wave

ENDOR:

electron nuclear double resonance

EPR:

electron paramagnetic resonance

hf:

hyperfine

hfc:

hyperfine coupling

MLS:

multiline signal

PS II:

Photosystem II

rf:

radio frequency

WOC:

water oxidizing complex

References

  • Adir N, Okamura MY and Feher G (1992) Cristallization of the PSII-reaction center. In: Murata N (ed) Research in Photosynthesis, Vol II, pp 195–198. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Åhrling KA and Pace RJ (1995) Simulation of the S2 state multiline electron paramagnetic resonance signal of Photosystem II: A multifrequency approach. Biophys J 68: 2081–2090

    PubMed  Google Scholar 

  • Babcock GT (1987) The photosynthetic oxygen-evolving process. In: Amesz J (ed) Photosynthesis, New Comprehensive Biochemistry, Vol 15, pp 125–158. Elsevier, Amsterdam

    Google Scholar 

  • Berthold DA, Babcock GT and Yocum CF (1981) A highly resolved, oxygen-evolving Photosystem II preparation from spinach thylakoid membranes. FEBS Lett 134: 231–234

    Article  Google Scholar 

  • Bittl R (1993) Matrix elements of spin operators in exchange coupled tetrameric metal clusters. Chem Phys Lett 215: 279–284

    Article  Google Scholar 

  • Bonvoisin J, Blondin G, Gired J-J and Zimmermann J-L (1992) Theoretical study of the multiline EPR signal from the S2 state of the oxygen evolving complex of Photosystem II. Biophys J 61: 1076–1086

    Google Scholar 

  • Britt RD, Lorigan GA, Sauer K, Klein MP and Zimmermann J-L (1992) The g=2 multiline EPR signal of the S2 state of the photosynthetic oxygen-evolving complex originates from a ground spin state. Biochim Biophys Acta 1140: 95–101

    PubMed  Google Scholar 

  • Brudvig GW, Casey JL and Sauer K (1983) The effect of temperature on the formation and decay of the nultiline EPR signal species associated with photosynthetic oxygen evolution. Biochim Biophys Acta 723: 366–371

    Google Scholar 

  • de Paula JC, Li PM, Miller A-F, Wu BW and Brudvig GW (1986) Effect of the 17- and 23-kilodalton polypeptides, calcium, and chloride on electron transfer in Photosystem II. Biochemistry 25: 6487–6494

    PubMed  Google Scholar 

  • de Paula JC, Beck WF, Miller A-F, Wilson RB and Brudvig GW (1987) Studies of the manganese site of Photosystem II by electron spin resonance spectroscopy. J Chem Soc Faraday Trans 1 83: 3635–3651

    Article  Google Scholar 

  • Debus RJ (1992) The manganese and calcium ions of photosynthetic oxygen evolution. Biochim Biophys Acta 1102: 269–352

    PubMed  Google Scholar 

  • Debus RJ, Barry BA, Sithole I, Babcock GT and McIntosh L (1988a) Directed mutagenesis indicates that the donor to P680 + in Photosystem II is tyrosine-161 of the D1 polypeptide. Biochemistry 27: 9071–9074

    PubMed  Google Scholar 

  • Debus RJ, Barry AB, Babcock GT and McIntosh L (1988b) Sitedirected mutagenesis identifies a tyrosine radical involved in the photosynthetic oxygen-evolving system. Proc Natl Acad Sci USA 85: 427–430

    PubMed  Google Scholar 

  • Dismukes GC and Siderer Y (1980) EPR spectroscopic observations of a manganese center associated with water oxidation in spinach chloroplasts. FEBS Lett 121: 78–80

    Article  Google Scholar 

  • Fiege R, Zweygart W, Irrgang KD, Adir N, Geiken B, Renger G and Lubitz W (1995) EPR/ENDOR studies of the water oxidizing complex in Photosystem II. In: Mathis P (ed) Proceedings Xth Congress of Photosynthesis. Kluwer Academic Publishers, Dordrecht, The Netherlands (in press)

    Google Scholar 

  • Haag E, Irrgang KD, Boekema EJ and Renger G (1990) Functional and structural analysis of Photosystem II core complexes from spinach with high oxygen evolution capacity. Eur J Biochem 189: 47–53

    PubMed  Google Scholar 

  • Haddy A, Aasa R and Hansson Ö (1990) Low frequency (3.9 GHz) studies of the S2-state EPR signals from the O2-evolving complex, In: Baltscheffsky M (ed) Current Research in Photosynthesis, Vol I, pp 777–780. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Joliot P and Joliot A (1973) Different types of quenching involved in Photosystem II centers. Biochim Biophys Acta 305: 302–316

    Google Scholar 

  • Kawamori A, Inui T, Ono T and Inoue Y (1989) ENDOR study on the position of hydrogens close to the manganese cluster in S2 state of Photosystem II. FEBS Let 254: 219–224

    Article  Google Scholar 

  • Khangulov S, Sivaraja M, Barynin VV and Dismukes GC (1993) The dimanganese(III,IV) oxidation state of catalase from Thermus thermophilus: Electron nuclear double resonance analysis of water and protein ligands in the active site. Biochemistry 32: 4912–4924

    PubMed  Google Scholar 

  • Koike H and Inoue Y (1987) Temperature dependence of the S-state transition in a thermophilic cyanobacterium measured by thermoluminescence. In: Biggins J (ed) Progress in Photosynthesis Research, Vol I, pp 645–648. Martinus Nijhoff Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Kurreck H, Kirste B and Lubitz W (1988) Electron Nuclear Double Resonance Spectroscopy in Solution. VCH, Weinheim

    Google Scholar 

  • Kusunoki M (1992) A new paramagnetic hyperfine structure effect in manganese tetramers. The origin of ‘multiline’ EPR signals from an S2 state of a photosynthetic water-splitting enzyme. Chem Phys Lett 197: 108–116

    Article  Google Scholar 

  • MacMillan F, Lendzian F, Renger G and Lubitz W (1995) EPR and ENDOR investigation of the primary electron acceptor radical anion QA •- in iron-depleted Photosystem II membrane fragments. Biochemistry 34: 8144–8156

    PubMed  Google Scholar 

  • McDermott AE, Yachandra VK, Guiles RD, Cole JL, Dexheimer SL, Britt RD, Sauer K and Klein MP (1988) Characterization of the manganese O2-evolving complex and the iron-quinone acceptor complex in Photosystem II from a thermophilic cyanobacterium by electron paramagnetic resonance and X-ray absorption spectroscopy. Biochemistry 27: 4021–4031

    PubMed  Google Scholar 

  • Messinger J and Renger G (1993) 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 32: 9379–9386

    PubMed  Google Scholar 

  • Messinger J, Schröder WP and Renger G (1993) Structure-function relations in Photosystem II. Effects of temperature and chaotropic agents on the period four oscillation of flash-induced oxygen evolution. Biochemistry 32: 7658–7668

    PubMed  Google Scholar 

  • Metz JG, Nixon PJ, Rögner M, Brudvig GW and Diner BA (1989) Direct alteration of the D1 polypeptide of Photosystem II: Evidence that tyrosine-161 is the redox component, Z, connecting the oxygen-evolving complex to the primary electron donor, P680. Biochemistry 28: 6960–6969

    PubMed  Google Scholar 

  • Miller A-F and Brudvig GW (1991) A guide to electron paramagnetic resonance spectroscopy of Photosystem II membranes. Biochim Biophys Acta 1056: 1–18

    PubMed  Google Scholar 

  • Mukerji I, Andrews JC, DeRose VJ, Latimer MJ, Yachandra VK, Sauer K and Klein MP (1994) Orientation of the oxygen-evolving manganese complex in a Photosystem II membrane preparation: An X-ray absorption spectroscopy study. Biochemistry 33: 9712–9721

    PubMed  Google Scholar 

  • Nugent JHA, Diner BA and Evans MCW (1981) Direct detection of the electron acceptor of Photosystem II. FEBS Lett 124: 241–244

    Article  Google Scholar 

  • Ono TA, Kusunoki M, Matsushita T, Oyanagi H and Inoue Y (1991) Structural and functional modifications of the manganese cluster in Ca2+-depleted S1 and S2 states: Electron paramagnetic resonance and X-ray absorption spectroscopy studies. Biochemistry 30: 6836–6841

    PubMed  Google Scholar 

  • Pace RJ, Smith P, Bramley R and Stehlik D (1991) EPR saturation and temperature dependence studies on signals from the oxygen-evolving centre of Photosystem II. Biochim Biophys Acta 1058: 161–170

    Google Scholar 

  • Renger G (1987) Mechanistic aspects of photosynthetic water cleavage. Photosynthetica 21: 203–224

    Google Scholar 

  • Renger G (1992) Energy transfer and trapping in Photosystem II. In: Barber J (ed) The Photosystems: Structure, Function and Molecular Biology, pp 45–99. Elsevier, Amsterdam

    Google Scholar 

  • Renger G (1993) Water cleavage by solar radiation—an inspiring challange of photosynthesis research. Photosynthe Res 38: 229–247

    Google Scholar 

  • Renger G, Gleiter HM, Haag E and Reifarth F (1993) Photosystem II: thermodynamics and kinetics of electron transport from QA − to QB(QB −) and deleterious effects of copper(II). Z Naturforsch 48c: 234–240

    Google Scholar 

  • Rutherford AW and Zimmermann JL (1984) A new EPR signal attributed to the primary plastoquinone aceptor in Photosystem II. Biochim Biophys Acta 767: 168–175

    Google Scholar 

  • Shuvalov VA, Fiege R, Schreiber U, Lendzian F and Lubitz W (1995) EPR study of cytochrome in the D1D2 Cyt b-559 complex. Biochim Biophys Acta 1228: 175–180

    Google Scholar 

  • Sivaraja M and Dismukes GC (1988) A comparison of the manganese center responsible for photosynthetic water oxidation in O2-evolving core particles and Photosystem II enriched membranes: EPR of the S2 state. Isr J Chem 28: 103–108

    Google Scholar 

  • Smith P, Ahrling KA and Pace RJ (1993) Nature of the S2 state electron paramagnetic resonance signals from the oxygen-evolving complex of Photosystem II: Q-band and oriented X-band studies. J Chem Soc Faraday Trans 89: 2863–2868

    Article  Google Scholar 

  • Tang X-S and Diner BA (1994) Biochemical and spectroscopic characterization of a new oxygen-evolving Photosystem II core complex from the cyanobacterium synechocystis PCC 6803. Biochemistry 33: 4594–4603

    PubMed  Google Scholar 

  • Tang XS, Sivaraja M and Dismukes GC (1993) Protein and substrate coordination to the manganese cluster in the photosynthetic water oxidizing complex: 15N and 1H ENDOR spectroscopy of the S2 state multiline signal in the thermophilic cyanobacterium synechococcus elongatus. J Am Chem Soc 115: 2382–2389

    Google Scholar 

  • Vermaas WFJ, Rutherford AW and Hansson Ö (1988) Site-directed mutagenesis in Photosystem II of the cyanobacterium Synechocystis sp. PCC 6803: Donor D is a tyrosine residue in the D2 protein. Proc Natl Acad Sci USA 85: 8477–8481

    Google Scholar 

  • Völker M, Ono T, Inoue Y and Renger G (1985) Effect of trypsin on PS-II particles. Correlation between Hill-activity, Mn-abundance and peptide pattern. Biochim Biophys Acta 806: 25–34

    Google Scholar 

  • Weyhermüller T (1994) Synthese und Charakterisierung oxoverbrückter Mangankomplexe mit Azamakrozyklen-Modelle für das Photosystem II? Doctoral Thesis, Ruhr-Universität Bochum, Germany

    Google Scholar 

  • Zheng M and Dismukes GC (1992) Photosynthetic water oxidation: What have we learned from the multiline EPR signals? In: Murata N (ed) Research in Photosynthesis, Vol II, pp 305–308. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Zweygart W (1995) ESR und ENDOR-Untersuchungen an mehrkernigen gemischtvalenten Mangankomplexen als Modelle für das wasseroxidierende Enzymsystem im Photosystem II. Doctoral Thesis, Technische Universität Berlin, Germany

    Google Scholar 

  • Zweygart W, Weyhermüller T, Renger G, Wieghardt K and Lubitz W (1992) EPR and ENDOR studies of manganese clusters in the water-oxidizing complex. In: Murata N (ed) Research in Photosynthesis, Vol II, pp 289–292. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Zweygart W, Thanner R and Lubitz W (1994) An improved TM110 ENDOR cavity for the investigation of transition metal complexes. J Magn res, ser A 109: 172–176

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Max Volmer-Institut für Biophysikalische und Physikalische Chemie, Technische Universität Berlin, Str. des 17. Juni 135, D-10623, Berlin, Germany

    Robert Fiege, Wolfgang Zweygart, Robert Bittl, Gernot Renger & Wolfgang Lubitz

  2. Department of Physics, University of California, San Diego, 92093-0319, La Jolla, CA, USA

    Noam Adir

Authors
  1. Robert Fiege
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wolfgang Zweygart
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Robert Bittl
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Noam Adir
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gernot Renger
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wolfgang Lubitz
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fiege, R., Zweygart, W., Bittl, R. et al. EPR and ENDOR studies of the water oxidizing complex of Photosystem II. Photosynth Res 48, 227–237 (1996). https://doi.org/10.1007/BF00041013

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00041013

Key words

Search

Navigation