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Reconstitution of the water-oxidizing complex in manganese-depleted photosystem II preparations using synthetic binuclear Mn(II) and Mn(IV) complexes: production of hydrogen peroxide

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Abstract

Reconstitution of Mn-depleted PSII particles with synthetic binuclear Mn complexes (one Mn(II)2 complex and one Mn(IV)2 complex) was examined. In both cases the electron-transfer rates in the reconstituted systems were found to be up to 75–82% of that measured in native PSII but the oxygen evolution activity remained lower (<5–40%). However, hydrogen peroxide was also produced by the reconstituted samples. These samples therefore represent a new type of reconstituted PSII that generates hydrogen peroxide as the final product in reconstituted PSII centers.

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References

  • Allakhverdiev SI, Shafiev MA, Klimov VV (1986) Effect of reversible extraction of manganese on photooxidation of chlorophyll P680 in photosystem II preparations. Photobiochem Photobiophys 12:62–65

    Google Scholar 

  • Allakhverdiev SI, Karacan MS, Somer G, Karacan N, Khan EM, Rane SY, Padhye S, Klimov VV, Renger G (1994a) Reconstitution of the water-oxidizing complex in manganese-depleted photosystem II complexes by using synthetic binuclear manganese complexes. Biochemistry 33:12210–12214

    Article  CAS  PubMed  Google Scholar 

  • Allakhverdiev SI, Karacan MS, Somer G, Karacan N, Khan EM, Rane SY, Padhye S, Klimov VV, Renger G (1994b) Binuclear manganese (III) complexes as electron donors in D1/D2/cytochrome b559 preparations isolated from spinach photosystem II membrane fragments. Z Naturforsh 49c:587–592

    Google Scholar 

  • Allakhverdiev SI, Yruela I, Picorel R, Klimov VV (1997) Bicarbonate is an essential constituent of the water-oxidizing complex of photosystem II. Proc Natl Acad Sci USA 94:5050–5054

    Article  CAS  PubMed  Google Scholar 

  • Allakhverdiev SI, Ozdemir U, Harnois J, Karacan N, Hotchandani S, Klimov VV, Murata N, Carpentier R (1999) Reconstruction of the water-oxidizing complex in manganese-depleted photosystem II preparations using mononuclear manganese complexes. Photochem Photobiol 70:57–63

    Article  CAS  Google Scholar 

  • Allakhverdiev SI, Mohanty P, Murata N (2003) Dissection of photodamage at low temperature and repair in darkness suggests the existence of an intermediate form of photodamaged photosystem II. Biochemistry 42:14277–14283

    Article  CAS  PubMed  Google Scholar 

  • Ananyev G, Nguyen T, Putnam-Evans C, Dismukes GC (2005) Mutagenesis of CP43-arginine-357 to serine reveals new evidence for (bi)carbonate functioning in the water oxidizing complex of photosystem II. Photochem Photobiol Sci 4:991–998

    Article  CAS  PubMed  Google Scholar 

  • Baranov SV, Tyryshkin AM, Katz D, Dismukes GC, Ananyev GM, Klimov VV (2004) Bicarbonate is a native cofactor for assembly of the manganese cluster of the photosynthetic water oxidizing complex. Kinetics of reconstitution of O2 evolution by photoactivation. Biochemistry 43:2070–2079

    Article  CAS  PubMed  Google Scholar 

  • Berthold DA, Babcock GT, Yocum CF (1981) A highly resolved oxygen-evolving photosystem II preparation from spinach thylakoid membranes. FEBS Lett 27:231–234

    Article  Google Scholar 

  • Debus RJ (1992) The manganese and calcium ions in photosynthetic O2 evolution. Biochim Biophys Acta 1102:269–352

    Article  CAS  PubMed  Google Scholar 

  • Ferreira KN, Iverson TM, Maghlaoui L, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838

    Article  CAS  PubMed  Google Scholar 

  • Fine PL, Frasch WD (1992) The oxygen-evolving complex requires chloride to prevent hydrogen peroxide formation. Biochemistry 31:12204–12210

    Article  CAS  PubMed  Google Scholar 

  • Iikura H, Nagata T (1998) Structural variation in manganese complexes: synthesis and characterization of manganese complexes from carboxylate-containing chelating ligands. Inorg Chem 37:4702–4711

    Article  CAS  PubMed  Google Scholar 

  • Kamiya N, Shen JR (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-Å resolution. Proc Natl Acad Sci USA 100:98–103

    Article  CAS  PubMed  Google Scholar 

  • Klimov VV, Allakhverdiev SI, Shuvalov VA, Krasnovsky AA (1982) Effect of extraction and readdition of manganese on light reactions of photosystem II preparations. FEBS Lett 148:307–312

    Article  CAS  Google Scholar 

  • Klimov VV, Ananyev GM, Allakhverdiev SI, Zharmukhamedov SK, Mulay M, Hedge U, Padhye S (1990) Photoreaction and photoinactivation of photosystem II after a complete removal of manganese from pea subchloroplast particles. In: Baltscheffsky M (ed) Current research in photosynthesis. Kluwer Academic Publishers, Dordrecht, pp 247–254

    Google Scholar 

  • Klimov V, Ananyev G, Zastryzhnaya O, Wydrzynski T (1993) Photoproduction of hydrogen peroxide in photosystem II membrane fragments: a comparison of four signals. Photosynth Res 38:409–416

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Mukhopadhyay S, Mandal SK, Bhaduri S, Armstrong WH (2004) Manganese clusters with relevance to photosystem II. Chem Rev 104:3981–4026

    Article  CAS  PubMed  Google Scholar 

  • Nagata T, Ikawa Y, Maruyama K (1994) Effect of the ligating anion on the catalase activity of dinuclear manganese(II) complexes of Schiff-base macrocycles. J Chem Soc Chem Commun 1994:471–472

    Article  Google Scholar 

  • Peloquin JM, Britt RD (2001) EPR/ENDOR characterization of the physical and electronic structure of the OEC Mn cluster. Biochim Biophys Acta 1503:95–111

    Google Scholar 

  • Radmer R, Cheniae GM (1977) Mechanisms of oxygen evolution. In: Barber J (ed) Primary processes of photosynthesis, vol 2. Elsevier, Amsterdam, pp 303–348

  • Rosenberg C, Christian J, Bricker TM, Putnam-Evans C (1999) Site-directed mutagenesis of glutamate residues in the large extrinsic loop of the photosystem II protein CP43 affects oxygen-evolving activity and PS II assembly. Biochemistry 38:15994–16000

    Article  CAS  PubMed  Google Scholar 

  • Tamura N, Cheniae GM (1987) Photoactivation of the water-oxidizing complex in photosystem II membranes depleted of Mn and extrinsic proteins: I. Biochemical and kinetic characterization. Biochim Biophys Acta 890:179–194

    Article  CAS  Google Scholar 

  • Seidler A (1996) The extrinsic polypeptides of photosystem II. Biochim Biophys Acta 1277:35–60

    Article  PubMed  Google Scholar 

  • Wydrzynski T, Aangstroem J, Vaenngaard T (1989) Hydrogen peroxide formation by photosystem II. Biochim Biophys Acta 973:23–28

    Article  CAS  Google Scholar 

  • Wydrzynski T, Hillier W, Messinger J (1996) On the functional significance of substrate accessibility in the photosynthetic water oxidation mechanism. Physiol Plant 96:342–350

    Article  CAS  Google Scholar 

  • Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W, Orth P (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409:739–743

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to Professors Jim Barber and Julian Eaton-Rye for carefully reading this manuscript and for valuable comments and discussion. This work was financially supported in part by Institute for Molecular Science (Japan), by a Grant-in-Aid for Scientific Research (No: 15655053 to TN) from JSPS, and by a grant from Russian Foundation for Basic Research (No: 05-04-49672) and by the program PCB RAS (to ASI).

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Authors and Affiliations

  1. Research Center for Molecular-scale Nanoscience, Institute for Molecular Science (IMS), National Institutes for Natural Sciences (NINS), 5-1 Higashiyama, Myodaiji, Okazaki, 444-8787, Japan

    Toshi Nagata, Takayuki Nagasawa & Suleyman I. Allakhverdiev

  2. Department of Structural Molecular Science, Graduate University for Advanced Studies (Sokendai), 5-1 Higashiyama, Myodaiji, Okazaki, 444-8787, Japan

    Toshi Nagata & Takayuki Nagasawa

  3. Institute of Basic Biological Problems, RAS, Pushchino, Moscow Region, 142290, Russia

    Sergei K. Zharmukhamedov, Vyacheslav V. Klimov & Suleyman I. Allakhverdiev

Authors
  1. Toshi Nagata
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  2. Takayuki Nagasawa
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  3. Sergei K. Zharmukhamedov
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  4. Vyacheslav V. Klimov
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  5. Suleyman I. Allakhverdiev
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Correspondence to Toshi Nagata.

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Nagata, T., Nagasawa, T., Zharmukhamedov, S.K. et al. Reconstitution of the water-oxidizing complex in manganese-depleted photosystem II preparations using synthetic binuclear Mn(II) and Mn(IV) complexes: production of hydrogen peroxide. Photosynth Res 93, 133–138 (2007). https://doi.org/10.1007/s11120-007-9161-5

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  • DOI: https://doi.org/10.1007/s11120-007-9161-5

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