Abstract
The S2 state of the oxygen-evolving Mn-cluster of Photosystem II (PS II) is known to have different forms that exhibit the g =2 multiline and g = 4.1 EPR signals. These two spin forms are interconvertible at > 200 K and the relative amplitudes of the two signals are dependent on the species of cryoprotectant and alcohol contained in the medium. Also, it was recently found that the mutiline form can be converted to the g = 4.1 form by absorption of near-infrared light by the Mn-cluster itself at around 150 K [Boussac et al. (1996) Biochemistry 35: 6984–6989]. We have used light-induced Fourier transform infrared (FTIR) difference spectroscopy to study the structural difference in these two S2 forms. FTIR difference spectra for S2/S1 as well as for S2QA -/S1QA measured at cryogenic temperatures using PS II membranes in the presence of various cryoprotectants, and monohydric alcohols did not show any specific differences except for intensities of amide I bands, which were larger when ethylene glycol or glycerol was present in addition to sucrose. This result was interpreted due to more flexible movement of the protein backbones upon S2 formation with a higher cryoprotectant content. Light-induced difference spectra measured at 150 K using either blue light without near-infrared light or red plus near-infrared light also did not show any detectable difference. In addition, a different spectrum upon near-infrared illumination at 150 K of the PS II sample in which the S2 state had been photogenerated at 200 K exhibited no meaningful signals. These results indicate that the two S2 forms that give rise to the multiline and g = 4.1 signals have only minor differences, if any, in the structures of amino-acid ligands and polypeptide backbones. This conclusion suggests that conversion between the two spin states is caused by a spin-state transition in the Mn(III) ion rather than valence swapping within the Mn-cluster that would considerably affect the vibrations of ligands.
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References
Beck WF and Brudvig GW (1986) Binding of amines to the O2-evolving center of Photosystem II. Biochemistry 25: 6479–6486
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
Berthomieu C, Nabedryk E, Mäntele W and Breton J (1990) Characterization by FTIR spectroscopy of the photoreduction of the primary quinone acceptor QA inPhotosystem II. FEBS Lett 269: 363–367
Bishop DM (1993) The vibrational Stark effect. J Chem Phys 98: 3179–3184
Boussac A (1997) Inhomogeneity of the EPR multiline signal from the S2-state of the Photosystem II oxygen-evolving enzyme. J Biol Inorg Chem 2: 580–585
Boussac A and Rutherford AW (1988) Nature of the inhibition of the oxygen-evolvingenzyme of Photosystem II induced by NaCl washing and reversed by the addition of Ca2+ or Sr2+. Biochemistry 27: 3476–3483
Boussac A, Girerd J-J and Rutherford AW(1996) Conversion of the spin state of the manganese complex in Photosystem II induced by near-infrared light. Biochemistry 35: 6984–6989
Boussac A, Un S, Horner O and Rutherford AW (1998) Highspin state (S ? 5/2) of the Photosystem II manganese complex. Biochemistry 37: 4001–4007
Breton J and Nabedryk E (1993) S0 ? T1 infrared difference spectrum of the triplet state of the primary electron donor in Rb. sphaeroides photosynthetic bacterial reactioncenters. Chem Phys Lett 213: 571–575
Britt RD (1996) Oxygen evolution. In: Ort DR and Yocum CF (eds) Oxygenic Photosynthesis: The Light Reactions, pp 137–164. Kluwer Academic Publishers, Dordrecht, The Netherlands
Casey J and Sauer K (1984) EPR detection of a cryogenically photogenerated intermediate in photosynthetic oxygen evolution. Biochim Biophys Acta 767: 21–28
Chu H-A, Gardner MT, O'Brien JP and Babcock GT (1999) Low frequency Fourier transform infrared spectroscopy of the oxygen evolving and quinone acceptor complexes in Photosystem II. Biochemistry 38: 4533–4541
Debus RJ (1992) Themanganese and calcium ions of photosynthetic oxygen evolution. Biochim Biophys Acta 1102: 269–352
de Paula JC, Innes JB and Brudvig GW (1985) Electron transfer in Photosystem II at cryogenic temperatures. Biochemistry 24: 8114–8120
Dismukes GC and Siderer Y (1981) Intermediates of a polynuclear manganese center involved in photosynthetic oxidation of water. Proc Natl Acad Sci USA 78: 274–278
Hienerwadel R, Boussac A, Breton J and Berthomieu C (1996) Fourier transform infrared difference study of tyrosineD oxidation and plastoquinone QA reduction in Photosystem II. Biochemistry 35: 15447–15460
Liang W, Latimer MJ, Dau H, Roelofs TA, Yachandra VK, Sauer K and Klein MP (1994) Correlation between structure and magnetic spin state of the manganese cluster in the oxygen-evolving complex of Photosystem II in the S2 state: Determination by X-ray absorption spectroscopy. Biochemistry 33: 4923–4932
Mäntele W (1995) Infrared vibrational spectroscopy of reaction centers. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 627–647. Kluwer Academix Publishers, Dordrecht, The Netherlands
Nabedryk E (1996) Light-induced Fourier transform infrared difference spectroscopy of the primary electron donor in photosynthetic reaction centers. In: Mantsch HH and Chapman D (eds) Infrared Spectroscopy of Biomolecules, pp 39–81. Wiley-Liss, New York
Noguchi T and Inoue Y (1995) Identification of Fourier transform infrared signals from the non-heme iron in Photosystem II. J Biochem 118: 9–12
Noguchi T, Ono T and Inoue Y (1992) Detection of structural changes upon S1-to-S2 transition in the oxygen-evolving manganese cluster in Photosystem II by light-induced Fourier transform infrared difference spectroscopy. Biochemistry 31: 5953–5956
Noguchi T, Ono T and Inoue Y (1993a) Temperature dependence of the S1 ? S2 transition in the oxygen-evolving complex of Photosystem II studied by FT-IRspectroscopy. Biochim Biophys Acta 1143: 333–336
Noguchi T, Inoue Y and Satoh K (1993b) FT-IR studies on the triplet state of P680 in the Photosystem II reaction center: triplet equilibrium within a chlorophyll dimer. Biochemistry 32: 7186–7195
Noguchi T, Ono T and Inoue Y (1995a) Direct detection of a carboxylate bridge between Mn and Ca2+ in the photosynthetic oxygen-evolving center by means of Fourier transform infrared spectroscopy. Biochim Biophys Acta 1228: 189–200
Noguchi T, Ono T and Inoue Y (1995b) A carboxylate ligand interacting with water in the oxygen-evolving center of Photosystem II as revealed by Fourier transform infrared spectroscopy. Biochim Biophys Acta 1232: 59–66
Noguchi T, Ono T and Inoue Y (1995c) FTIR studies on the structure and reactions of theoxygen-evolving center in Photosystem II. In: Mathis P (ed) Photosynthesis: from Light to Biosphere, Vol. II, pp 235–240. Kluwer Academic Publishers, Dordrecht, The Netherlands
Noguchi T, Inoue Y and Tang X-S (1997) Structural coupling between the oxygen-evolving Mn cluster and a tyrosine residue in Photosystem II as revealed by Fourier transform infrared spectroscopy. Biochemistry 36: 14705–14711
Noguchi T, Inoue Y and Tang X-S (1999) Hydrogen bonding interaction between the primary quinone acceptor QA and a histidine side chain in Photosystem II as revealed by Fourier transform infrared spectroscopy. Biochemistry 38: 399–403
Ono T and Inoue Y (1986) Effects of removal and reconstitution of the extrinsic 33, 24 and 16 kDa proteins on flash oxygen yield in Photosystem II particles. Biochim Biophys Acta 850: 380–389
Ono T, Nakayama H, Gleiter H, Inoue Y and Kawamori A (1987) Modification of the properties of S2 state in photosynthetic O2-evolving center by replacement of chloride with other anions. Arch Biochem Biophys 256: 618–624
Pace RJ, Smith P, Bramley R and Stehlik D (1991) EPR saturation and temperature dependence studies on signals from the oxygenevolving centre of photosystem II. Biochim Biophys Acta 1058: 161–170
Renger G (1997) Mechanistic and structural aspects of photosynthetic water oxidation. Physiol Plant 100: 824–841
Steenhuis JJ and Barry BA (1996) A difference infrared study of protein structural changes in the photosynthetic water-oxidizing complex. J Am Chem Soc 118: 11927–11932
Steenhuis JJ and Barry BA (1997) Protein and ligand environments of the S2 state in photosynthetic oxygen evolution: A difference FT-IR study. J Phys Chem B 101: 6652–6660
Tommos C and Babcock GT (1998) Oxygen production in nature: A light-driven metalloradical enzyme process. Acc Chem Res 31: 18–25
Van Vliet P and Rutherford W (1996) Properties of the chloridedepleted oxygen-evolving complex of Photosystem II studied by electron paramagnetic resonance. Biochemistry 35: 1829–1839
Yachandra VK, Sauer K and Klein MP (1996) Manganese cluster in photosynthesis: Where plants oxidize water to dioxygen. Chem Rev 96: 2927–2950
Zhang H, Fischer G and Wydrzynski T (1998) Room-temperature vibrational difference spectrum for S2QB¯/S1QB of Photosystem II determined by time-resolved Fourier transform infrared spectroscopy. Biochemistry 37: 5511–5517
Zimmermann J-L and Rutherford AW (1984) EPR studies of the oxygen-evolving enzyme of Photosystem II. Biochim Biophys Acta 767: 160–167
Zimmermann J-L and Rutherford AW (1986) Electron paramagnetic resonance propertiesof the S2 state of the oxygen-evolving complex of Photosystem II. Biochemistry 25: 4609–4615
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Onoda, K., Mino, H., Inoue, Y. et al. An FTIR study on the structure of the oxygen-evolving Mn-cluster of Photosystem II in different spin forms of the S2 state. Photosynthesis Research 63, 47–57 (2000). https://doi.org/10.1023/A:1006362118267
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DOI: https://doi.org/10.1023/A:1006362118267