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Oxidation state changes of the Mn4Ca cluster in Photosystem II

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Abstract

A detailed electronic structure of the Mn4Ca cluster is required before two key questions for understanding the mechanism of photosynthetic water oxidation can be addressed. They are whether all four oxidizing equivalents necessary to oxidize water to O2 accumulate on the four Mn ions of the oxygen-evolving complex, or do some ligand-centered oxidations take place before the formation and release of O2 during the S3 → [S4] → S0 transition, and what are the oxidation state assignments for the Mn during S-state advancement. X-ray absorption and emission spectroscopy of Mn, including the newly introduced resonant inelastic X-ray scattering spectroscopy have been used to address these questions. The present state of understanding of the electronic structure and oxidation state changes of the Mn4Ca cluster in all the S-states, particularly in the S2 to S3 transition, derived from these techniques is described in this review.

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Abbreviations

PS II:

Photosystem II

OEC:

oxygen-evolving complex

EPR:

electron paramagnetic resonance

ENDOR:

Electron-Nuclear Double Resonance

XAS:

X-ray absorption spectroscopy

EXAFS:

extended X-ray absorption fine structure

XANES:

X-ray absorption near-edge spectroscopy

MLS:

multiline EPR signal

NIR:

near infra-red

IPE:

Inflection point energy

XES:

X-ray emission spectroscopy

RIXS:

resonant inelastic X-ray scattering

CIE:

constant incident energy

CET:

constant energy transfer

References

  • Åhrling KA, Peterson S, Styring S (1998) The S0 state EPR signal from the Mn cluster arises from an isolated ground state. In: Garab G (ed) Photosynthesis: mechanisms and effects. Kluwer Academic Publishers, Dordrecht, pp 1291–1294

    Google Scholar 

  • Bergmann U, Grush MM, Horne CR, DeMarois P, Penner-Hahn JE, Yocum CF, Wright DW, Dubé CE, Armstrong WH, Christou G, Eppley HJ, Cramer SP (1998) Characterization of the Mn oxidation states in Photosystem II by Kß X-ray fluorescence spectroscopy. J Phys Chem B 102:8350–8352

    Article  CAS  Google Scholar 

  • Bonvoisin J, Blondin G, Girerd JJ, Zimmermann JL (1992) Theoretical study of the multiline EPR signal from the S2 state of the oxygen evolving complex of Photosystem-II – evidence for a magnetic tetramer. Biophys J 61:1076–1086

    Article  CAS  PubMed  Google Scholar 

  • Boussac A, Girerd J-J, Rutherford AW (1996) Conversion of the spin state of the manganese complex in Photosystem II induced by near-infrared light. Biochemistry 35:6984–6989

    Article  PubMed  CAS  Google Scholar 

  • Boussac A, Kuhl H, Un S, Rögner M, Rutherford AW (1998a) Effect of near-infrared light on the S2-state of the manganese complex of Photosystem II from Synechococcus elongatus. Biochemistry 37:8995–9000

    Article  CAS  Google Scholar 

  • Boussac A, Un S, Horner O, Rutherford AW (1998b) High-spin states (S ≥ 5/2) of the Photosystem II manganese complex. Biochemistry 37:4001–4007

    Article  CAS  Google Scholar 

  • Boussac A, Sugiura M, Kirilovsky D, Rutherford AW (2005) Near-infrared-induced transitions in the manganese cluster of Photosystem II: action spectra for the S2 and S3 redox states. Plant Cell Physiol 46:837–842

    Article  PubMed  CAS  Google Scholar 

  • Brudvig GW (1995) Structure and function of manganese in Photosystem II. Adv Chem Ser 246:249–263

    Article  CAS  Google Scholar 

  • Campbell KA, Peloquin JM, Pham DP, Debus RJ, Britt RD (1998) Parallel polarization EPR detection of an S1-state “multiline” EPR signal in Photosystem II particles from Synechocystis sp. PCC 6803. J Am Chem Soc 120:447–448

    Article  CAS  Google Scholar 

  • Carrell TG, Tyryshkin AM, Dismukes GC (2002) An evaluation of structural models for the photosynthetic water-oxidizing complex derived from spectroscopic and X-ray diffraction signatures. J Biol Inorg Chem 7:2–22

    Article  PubMed  CAS  Google Scholar 

  • Casey JL, Sauer K (1984) EPR detection of a cryogenically photogenerated intermediate in photosynthetic oxygen evolution. Biochim Biophys Acta 767:21–28

    Article  CAS  Google Scholar 

  • Chu H-A, Hillier W, Law NA, Babcock GT (2001) Vibrational spectroscopy of the oxygen-evolving complex and of manganese model compounds. Biochim Biophys Acta 1503:69–82

    Article  PubMed  CAS  Google Scholar 

  • Chu HA, Hillier W, Debus RJ (2004) Evidence that the C-terminus of the D1 polypeptide of Photosystem II is ligated to the manganese ion that undergoes oxidation during the S1 to S2 transition: an isotope-edited FTIR study. Biochemistry 43:3152–3166

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Debus RJ, Strickler MA, Walker LM, Hillier W (2005) No evidence from FTIR difference spectroscopy that aspartate-170 of the D1 polypeptide ligates a manganese ion that undergoes oxidation during the S0 to S1, S1 to S2, or S2 to S3 transitions in photosystem II. Biochemistry 44:1367–1374

    Article  PubMed  CAS  Google Scholar 

  • Dekker JP (1992) Optical studies on the oxygen-evolving complex of Photosystem II. In: Pecoraro VL (ed) Manganese redox enzymes. VCH Publishers, New York, pp 85–103

    Google Scholar 

  • Dexheimer SL, Klein MP (1992) Detection of a paramagnetic intermediate in the S1 state of the photosynthetic oxygen-evolving complex. J Am Chem Soc 114:2821–2826

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Dismukes GC, Ferris K, Watnick P (1982) EPR spectroscopic evidence for a tetranuclear manganese cluster as the site for photosynthetic oxygen evolution. Photobiochem Photobiophys 3:243–256

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Glatzel P, Bergmann U (2005) High resolution 1s core hole X-ray spectroscopy in 3d transition metal complexes – electronic and structural information. Coord Chem Rev 249:65–95

    Article  CAS  Google Scholar 

  • Glatzel P, Bergmann U, Yano J, Visser H, Robblee JH, Gu WW, de Groot FMF, Christou G, Pecoraro VL, Cramer SP, Yachandra VK (2004) The electronic structure of Mn in oxides, coordination complexes, and the oxygen-evolving complex of Photosystem II studied by resonant inelastic X-ray scattering. J Am Chem Soc 126:9946–9959

    Article  PubMed  CAS  Google Scholar 

  • Glatzel P, Yano J, Bergmann U, Visser H, Robblee JH, Gu WW, de Groot FMF, Cramer SP, Yachandra VK (2005) Resonant inelastic X-ray scattering (RIXS) spectroscopy at the MnK absorption pre-edge – a direct probe of the 3d orbitals. J Phys Chem Solids 66:2163–2167

    Article  CAS  Google Scholar 

  • Hansson Ö, Andréasson LE (1982) EPR-detectable magnetically interacting manganese ions in the photosynthetic oxygen-evolving system after continuous illumination. Biochim Biophys Acta 679:261–268

    Article  CAS  Google Scholar 

  • Hasegawa K, Ono T-A, Inoue Y, Kusunoki M (1999) Spin-exchange interactions in the S2-state manganese tetramer in photosynthetic oxygen-evolving complex deduced from g = 2 multiline EPR signal. Chem Phys Lett 300:9–19

    Article  CAS  Google Scholar 

  • Haumann M, Muller C, Liebisch P, Iuzzolino L, Dittmer J, Grabolle M, Neisius T, Meyer-Klaucke W, Dau H (2005) Structural and oxidation state changes of the photosystem II manganese complex in four transitions of the water oxidation cycle (S0 → S1, S1 → S2, S2 → S3, and S3, S4 → S0) characterized by X-ray absorption spectroscopy at 20 K and room temperature. Biochemistry 44:1894–1908

    Article  PubMed  CAS  Google Scholar 

  • Horner O, Rivière E, Blondin G, Un S, Rutherford AW, Girerd JJ, Boussac A (1998) SQUID magnetization study of the infrared-induced spin transition in the S2 state of Photosystem II: spin value associated with the g = 4.1 EPR signal. J Am Chem Soc 120:7924–7928

    Article  CAS  Google Scholar 

  • Ioannidis N, Schansker G, Barynin VV, Petrouleas V (2000) Interaction of nitric oxide with the oxygen evolving complex of Photosystem II and manganese catalase: a comparative study. JBIC, J Biol Inorg Chem 5:354–363

    Article  CAS  Google Scholar 

  • Ioannidis N, Nugent JHA, Petrouleas V (2002) Intermediates of the S3 state of the oxygen-evolving complex of Photosystem II. Biochemistry 41:9589–9600

    Article  PubMed  CAS  Google Scholar 

  • Iuzzolino L, Dittmer J, Dörner W, Meyer-Klaucke W, Dau H (1998) X-ray absorption spectroscopy on layered Photosystem II membrane particles suggests manganese-centered oxidation of the oxygen-evolving complex for the S0-S1, S1-S2, and S2-S3 transitions of the water oxidation cycle. Biochemistry 37:17112–17119

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kimura Y, Mizusawa N, Ishii A, Nakazawa S, Ono T (2005a) Changes in structural and functional properties of oxygen-evolving complex induced by replacement of D1-glutamate 189 with glutamine in Photosystem II – ligation of glutamate 189 carboxylate to the manganese cluster. J Biol Chem 280:37895–37900

    Article  CAS  Google Scholar 

  • Kimura Y, Mizusawa N, Ishii A, Ono T (2005b) FTIR detection of structural changes in a histidine ligand during S-state cycling of photosynthetic oxygen-evolving complex. Biochemistry 44:16072–16078

    Article  CAS  Google Scholar 

  • Kimura Y, Mizusawa N, Yamanari T, Ishii A, Ono T (2005c) Structural changes of D1 C-terminal alpha-carboxylate during S-state cycling in photosynthetic oxygen evolution. J Biol Chem 280:2078–2083

    Article  CAS  Google Scholar 

  • Kulik LV, Epel B, Lubitz W, Messinger J (2005) Mn-55 pulse ENDOR at 34 GHz of the S0 and S2 states of the oxygen-evolving complex in Photosystem II. J Am Chem Soc 127:2392–2393

    Article  PubMed  CAS  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  CAS  Google Scholar 

  • Kuzek D, Pace RJ (2001) Probing the Mn oxidation states in the OEC. Insights from spectroscopic, computational and kinetic data. Biochim Biophys Acta 1503:123–137

    Article  PubMed  CAS  Google Scholar 

  • Liang W, Roelofs TA, Cinco RM, Rompel A, Latimer MJ, Yu WO, Sauer K, Klein MP, Yachandra VK (2000) Structural change of the Mn cluster during the S2 → S3 state transition of the oxygen-evolving complex of Photosystem II. Does it reflect the onset of water/substrate oxidation? Determination by Mn X-ray absorption spectroscopy. J Am Chem Soc 122:3399–3412

    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  PubMed  CAS  Google Scholar 

  • Matsukawa T, Mino H, Yoneda D, Kawamori A (1999) Dual-mode EPR study of new signals from the S3-state of oxygen-evolving complex in Photosystem II. Biochemistry 38:4072–4077

    Article  PubMed  CAS  Google Scholar 

  • Messinger J (2004) Evaluation of different mechanistic proposals for water oxidation in photosynthesis on the basis of Mn4OxCa structures for the catalytic site and spectroscopic data. Phys Chem Chem Phys 6:4764–4771

    Article  CAS  Google Scholar 

  • Messinger J, Nugent JHA, Evans MCW (1997a) Detection of an EPR multiline signal for the S0 state in Photosystem II. Biochemistry 36:11055–11060

    Article  CAS  Google Scholar 

  • Messinger J, Robblee J, Yu WO, Sauer K, Yachandra VK, Klein MP (1997b) The S0 state of the oxygen-evolving complex in photosystem II is paramagnetic: detection of an EPR multiline signal. J Am Chem Soc 119:11349–11350

    Article  CAS  Google Scholar 

  • Messinger J, Robblee JH, Bergmann U, Fernandez C, Glatzel P, Visser H, Cinco RM, McFarlane KL, Bellacchio E, Pizarro SA, Cramer SP, Sauer K, Klein MP, Yachandra VK (2001) Absence of Mn-centered oxidation in the S2 to S3 transition: implications for the mechanism of photosynthetic water oxidation. J Am Chem Soc 123:7804–7820

    Article  PubMed  CAS  Google Scholar 

  • Ort DR, Yocum CF (eds) (1996) Oxygenic photosynthesis: the light reactions. Kluwer Academic Publishers, Dordrecht

  • Peloquin JM, Britt RD (2001) EPR/ENDOR characterization of the physical and electronic structure of the OEC Mn cluster. Biochim Biophys Acta 1503:96–111

    Article  PubMed  CAS  Google Scholar 

  • Peloquin JM, Campbell KA, Randall DW, Evanchik MA, Pecoraro VL, Armstrong WH, Britt RD (2000) 55Mn ENDOR of the S2-state multiline EPR signal of Photosystem II: implications on the structure of the tetranuclear cluster. J Am Chem Soc 122:10926–10942

    Article  CAS  Google Scholar 

  • Pizarro SA, Glatzel P, Visser H, Robblee JH, Christou G, Bergmann U, Yachandra VK (2004) Mn oxidation states in tri- and tetra-nuclear Mn compounds structurally relevant to Photosystem II: Mn K-edge X-ray absorption and Kβ X-ray emission spectroscopy studies. Phys Chem Chem Phys 6:4864–4870

    Article  CAS  Google Scholar 

  • Pushkar Y, Yano J, Glatzel P, Messinger J, Lewis A, Sauer K, Bergmann U, Yachandra VK (2007) Structure and orientation of the Mn4Ca cluster in plant Photosystem II membranes studied by polarized range-extended X-ray absorption spectroscopy. J Biol Chem 282:7198–7208

    Article  PubMed  CAS  Google Scholar 

  • Robblee JH, Messinger J, Cinco RM, McFarlane KL, Fernandez C, Pizarro SA, Sauer K, Yachandra VK (2002) The Mn cluster in the S0 state of the oxygen-evolving complex of Photosystem II studied by EXAFS spectroscopy: are there three di-μ-oxo-bridged Mn2 moieties in the tetranuclear Mn complex? J Am Chem Soc 124:7459–7471

    Article  PubMed  CAS  Google Scholar 

  • Roelofs TA, Liang MC, Latimer MJ, Cinco RM, Rompel A, Andrews JC, Sauer K, Yachandra VK, Klein MP (1996) Oxidation states of the manganese cluster during the flash-induced S-state cycle of the photosynthetic oxygen-evolving complex. Proc Natl Acad Sci USA 93:3335–3340

    Article  PubMed  CAS  Google Scholar 

  • Rutherford AW, Zimmermann J-L, Boussac A (1992) Oxygen evolution. In: Barber J (ed) The photosystems: structure, function, molecular biology. Elsevier, Amsterdam, pp 179–229

    Google Scholar 

  • Sarangi R, Aboelella N, Fujisawa K, Tolman WB, Hedman B, Hodgson KO, Solomon EI (2006) X-ray absorption edge spectroscopy and computational studies on LCuO2 species: superoxide-Cu-II versus peroxide-Cu-III bonding. J Am Chem Soc 128:8286–8296

    Article  PubMed  CAS  Google Scholar 

  • Siegbahn PEM (2006) O-O bond formation in the S4 state of the oxygen-evolving complex in Photosystem II. Chem Eur J 12:9217–9227

    Article  CAS  Google Scholar 

  • Strickler MA, Hillier W, Debus RJ (2006) No evidence from FTIR difference spectroscopy that glutamate-189 of the D1 polypeptide ligates a Mn ion that undergoes oxidation during the S0 to S1, S1 to S2, or S2 to S3 transitions in Photosystem II. Biochemistry 45:8801–8811

    Article  PubMed  CAS  Google Scholar 

  • Styring SA, Rutherford AW (1988) The microwave power saturation of SIIslow varies with the redox state of the oxygen-evolving complex in Photosystem II. Biochemistry 27:4915–4923

    Article  CAS  Google Scholar 

  • Visser H, Anxolabéhère-Mallart E, Bergman U, Glatzel P, Robblee JH, Cramer SP, Girerd J-J, Sauer K, Klein MP, Yachandra VK (2001) Mn K-edge XANES and Kβ XES studies of two Mn-oxo binuclear complexes. Investigation of three different oxidation states relevant to the oxygen-evolving complex of PhotosystemII. J Am Chem Soc 123:7031–7039

    Article  PubMed  CAS  Google Scholar 

  • Wydrzynski T, Satoh S (eds) (2005) Photosystem II: the light-driven water: plastoquinone oxidoreductase, Springer, Dordrecht

  • Yachandra VK (2005) The catalytic manganese-cluster: organization of the metal ions. In: Wydrzynski T et al (eds) Photosystem II: the light-driven water: plastoquinone oxidoreductase. Springer, Dordrecht, pp 235–260

    Google Scholar 

  • Yachandra VK, Klein MP (1996) X-Ray absorption spectroscopy: determination of transition metal site structures in photosynthesis. In: Amesz J et al (eds) Biophysical techniques in photosynthesis. Kluwer Academic Publishers, Dordrecht, Netherlands, pp 337–354

    Google Scholar 

  • Yachandra VK, Sauer K, Klein MP (1996) Manganese cluster in photosynthesis: where plants oxidize water to dioxygen. Chem Rev 96:2927–2950

    Article  PubMed  CAS  Google Scholar 

  • Yamauchi T, Mino H, Matsukawa T, Kawamori A, Ono T (1997) Parallel polarization electron paramagnetic resonance studies of the S1-state manganese cluster in the photosynthetic oxygen-evolving system. Biochemistry 36:7520–7526

    Article  PubMed  CAS  Google Scholar 

  • Yano J, Kern J, Irrgang K-D, Latimer MJ, Bergmann U, Glatzel P, Pushkar Y, Biesiadka J, Loll B, Sauer K, Messinger J, Zouni A, Yachandra VK (2005a) X-ray damage to the Mn4Ca complex in Photosystem II crystals: a case study for metallo-protein X-ray crystallography. Proc Natl Acad Sci USA 102:12047–12052

    Article  CAS  Google Scholar 

  • Yano J, Pushkar Y, Glatzel P, Lewis A, Sauer K, Messinger J, Bergmann U, Yachandra VK (2005b) High-resolution Mn EXAFS of the oxygen-evolving complex in Photosystem II: structural implications for the Mn4Ca Cluster. J Am Chem Soc 127:14974–14975

    Article  CAS  Google Scholar 

  • Yano J, Kern J, Sauer K, Latimer M, Pushkar Y, Biesiadka J, Loll B, Saenger W, Messinger J, Zouni A, Yachandra VK (2006) Where water is oxidized to dioxygen: structure of the photosynthetic Mn4Ca cluster. Science 314:821–825

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann J-L, Rutherford AW (1984) EPR studies of the oxygen-evolving enzyme of photosystem II. Biochim Biophys Acta 767:160–167

    Article  CAS  Google Scholar 

  • Zouni A, Witt H-T, 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  PubMed  CAS  Google Scholar 

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Acknowledgments

The research from our group presented in this review was supported by the NIH grant (GM 55302), and the DOE, Director, Office of Science, Office of Basic Energy Sciences, Chemical Sciences, Geosciences, and Biosciences Division, under Contract DE-AC02-05CH11231. Synchrotron radiation facilities were provided by SSRL, APS, and ALS, which are supported by DOE, Office of Basic Energy Sciences. The SSRL Biotechnology Program is supported by NIH, National Center of Research Resources, Biomedical Technology Program, and by DOE, Office of Health and Environmental Research. BioCAT at the APS is a NIH-supported Research Center RR-08630. We thank John Robblee, Johannes Messinger, Uwe Bergmann, Pieter Glatzel, Henk Visser, Carmen Fernandez, Shelly Pizarro, Elodie Anxolabéhère-Mallart, Wen Liang, Theo Roelofs, Yulia Pushkar, and Ken Sauer for contributing to much of the work presented in this review and for many helpful discussions over the years. We dedicate this review to the memory of Ron Guiles (1951–2005), who was a key person in the early development of X-ray spectroscopy techniques as applied to Photosystem II.

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  1. Melvin Calvin Laboratory, Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA, 94720, USA

    Junko Yano & Vittal K. Yachandra

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  1. Junko Yano
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Correspondence to Junko Yano or Vittal K. Yachandra.

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Yano, J., Yachandra, V.K. Oxidation state changes of the Mn4Ca cluster in Photosystem II. Photosynth Res 92, 289–303 (2007). https://doi.org/10.1007/s11120-007-9153-5

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