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The Cl− Requirement for Oxygen Evolution by Photosystem II Explored Using Enzyme Kinetics and EPR Spectroscopy

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Photosynthesis: Structures, Mechanisms, and Applications

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Summary

Chloride is a well-known activator of oxygen evolution activity in photosystem II. Its effects have been characterized over several decades of research, as methods have developed and improved. By replacing chloride with other small anions with a range of chemical properties, a picture of the requirements of a successful anion activator can be formulated. In this review, the results of experiments on the chloride effect using enzyme kinetics methods and electron paramagnetic resonance spectroscopy are described, with summaries for the major anion activators and inhibitors that have been studied.

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References

  • Andersson, B., C. Critchley, I. J. Ryrie, C. Jansson, C. Larsson and J. M. Anderson (1984). “Modification of the chloride requirement for photosynthetic O2 evolution. The role of the 23 kDa polypeptide.” FEBS Letters 168: 113–117.

    Article  CAS  Google Scholar 

  • Andréasson, L.-E. and K. Lindberg (1992). “The inhibition of photosynthetic oxygen evolution by ammonia probed by EPR.” Biochimica et Biophysica Acta 1100: 177–183.

    Article  Google Scholar 

  • Andréasson, L.-E., Ö. Hansson and K. von Schenck (1988). “The interaction of ammonia with the photosynthetic oxygen-evolving system.” Biochimica et Biophysica Acta 936: 351–360.

    Article  Google Scholar 

  • Arnon, D. I. and F. R. Whatley (1949). “Is chloride a coenzyme of photosynthesis?“ Science 110: 554–556.

    Article  CAS  PubMed  Google Scholar 

  • Baumgarten, M., J. S. Philo and G. C. Dismukes (1990). “Mechanism of photoinhibition of photosynthetic water oxidation by Cl− depletion and F− substitution: Oxidation of a protein residue.” Biochemistry 29: 10814–10822.

    Article  CAS  PubMed  Google Scholar 

  • Beck, W. F. and G. W. Brudvig (1986a). “Ammonia binds to the manganese site of the O2-evolving complex of photosystem II in the S2 state.” Journal of the American Chemical Society 108: 4018–4022.

    Article  CAS  Google Scholar 

  • Beck, W. F. and G. W. Brudvig (1986b). “Binding of amines to the O2-evolving center of Photosytem II.” Biochemistry 25: 6479–6486.

    Article  CAS  PubMed  Google Scholar 

  • Berthold, D. A., G. T. Babcock and C. F. Yocum (1981). “A highly resolved, oxygen-evolving photosystem II preparation from spinach thylakoid membranes.” FEBS Letters 134: 231–234.

    Article  CAS  Google Scholar 

  • Boussac, A. (1995). “Exchange of chloride by bromide in the manganese Photosystem-II complex studied by cw- and pulsed-EPR.” Chemical Physics 194: 409–418.

    Article  CAS  Google Scholar 

  • Boussac, A. and A. W. Rutherford (1994). “Electron transfer events in chloride-depleted photosystem II.” Journal of Biological Chemistry 269: 12462–12467.

    CAS  PubMed  Google Scholar 

  • Boussac, A., J.-L. Zimmermann and A. W. Rutherford (1989). “EPR signals from modified charge accumulation states of the oxygen evolving enzyme in Ca2+-deficient Photosystem II.” Biochemistry 28: 8984–8989.

    Article  CAS  PubMed  Google Scholar 

  • Boussac, A., A. W. Rutherford and S. Styring (1990a). “Interaction of ammonia with the water splitting enzyme of photosystem II.” Biochemistry 29: 24–32.

    Article  CAS  PubMed  Google Scholar 

  • Boussac, A., J.-L. Zimmermann and A. W. Rutherford (1990b). “Factors influencing the formation of modified S2 EPR signal and the S3 EPR signal in Ca2+-depleted photosystem II.” FEBS Letters 277: 69–74.

    Article  CAS  PubMed  Google Scholar 

  • Boussac, A., M. Sugiura, Y. Inoue and A. W. Rutherford (2000). “EPR study of the oxygen evolving complex in His-tagged photosystem II from the cyanobacterium Synechococcus elongatus.” Biochemistry 39: 13788–13799.

    Article  CAS  PubMed  Google Scholar 

  • Boussac, A., N. Ishida, M. Sugiura and F. Rappaport (2012). “Probing the role of chloride in photosystem II from Thermosynechococcus elongatus by exchanging chloride for iodide.” Biochimica et Biophysica Acta 1817: 802–810.

    Article  CAS  PubMed  Google Scholar 

  • Bricker, T. M., J. L. Roose, R. D. Fagerlund, L. K. Frankel and J. J. Eaton-Rye (2012). “The extrinsic proteins of photosystem II.” Biochimica et Biophysica Acta 1817: 121–142.

    Article  CAS  PubMed  Google Scholar 

  • Britt, R. D., J.-L. Zimmermann, K. Sauer and M. P. Klein (1989). “Ammonia binds to the catalytic Mn of the oxygen evolving complex of photosystem II: Evidence by electron spin echo envelope modulation spectroscopy.” Journal of the American Chemical Society 111: 3522–3532.

    Article  CAS  Google Scholar 

  • Broser, M., C. Glöckner, A. Gabdulkhakov, A. Guskov, J. Buchta, J. Kern, F. Müh, H. Dau, W. Saenger and A. Zouni (2011). “Structural basis of cyanobacterial photosystem II inhibition by the herbicide terbutryn.” Journal of Biological Chemistry 286: 15964–15972.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brudvig, G. W., J. L. Casey and K. Sauer (1983). “The effect of temperature on the formation and decay of the multiline EPR signal species associated with photosynthetic oxygen evolution.” Biochimica et Biophysica Acta 723: 366–371.

    Article  CAS  Google Scholar 

  • Brynda, M. and R. D. Britt (2010). The manganese-calcium cluster of the oxygen-evolving system: Synthetic models, EPR studies, and electronic structure calculations. Metals in Biology: Applications of High-Resolution EPR. G. Hanson and L. Berliner, Springer Science: 203–271.

    Google Scholar 

  • Bryson, D. I., N. Doctor, R. Johnson, S. Baranov and A. Haddy (2005). “Characteristics of iodide activation and inhibition of oxygen evolution by photosystem II.” Biochemistry 44: 7354–7360.

    Article  CAS  PubMed  Google Scholar 

  • Casey, J. L. and K. Sauer (1984). “EPR detection of a cryogenically photogenerated intermediate in photosynthetic oxygen evolution.” Biochimica et Biophysica Acta 767: 21–28.

    Article  CAS  Google Scholar 

  • Chen, X. (2008). Mathematical models for the pH dependence of oxygen evolution under fluoride inhibition and effects of nitrite on oxygen evolution in photosystem II, Master’s Thesis, UNC-Greensboro.

    Google Scholar 

  • Clemens, K. L., D. A. Force and R. D. Britt (2002). “Acetate binding at the Photosystem II oxygen evolving complex: An S2-state multiline signal ESEEM study.” Journal of the American Chemical Society 124: 10921–10933.

    Article  CAS  PubMed  Google Scholar 

  • Damoder, R., V. V. Klimov and G. C. Dismukes (1986). “The effect of Cl− depletion and X− reconstitution on the oxygen-evolution rate, the yield of the multiline manganese EPR signal and EPR Signal II in the isolated photosystem-II complex.” Biochimica et Biophysica Acta 848: 378–391.

    Article  CAS  PubMed  Google Scholar 

  • de Paula, J. C., P. M. Li, A.-F. Miller, B. W. Wu and G. W. Brudvig (1986). “Effect of the 17- and 23-kilodalton polypeptides, calcium, and chloride on electron transfer in photosystem II.” Biochemistry 25: 6487–6494.

    Article  PubMed  Google Scholar 

  • Debus, R. J. (2014). “Evidence from FTIR difference spectroscopy that D1-Asp61 influences the water reactions of the oxygen-evolving Mn4CaO5 cluster of photosystem II.” Biochemistry 53: 2941–2955.

    Article  CAS  PubMed  Google Scholar 

  • DeRose, V. J., M. J. Latimer, J.-L. Zimmermann, I Mukerji, V. K. Yachandra, K. Sauer and M. P. Klein (1995). “Fluoride substitution in the Mn cluster from photosystem II: EPR and X-ray absorption spectroscopy studies.” Chemical Physics 194: 443–459.

    Article  CAS  Google Scholar 

  • Dilbeck, P. L., H. J. Hwang, I. Zaharieva, L. Gerencser, H. Dau and R. L. Burnap (2012). “The D1-D61N mutation in Synechocystis sp. PCC 6803 allows the observation of pH-sensitive intermediates in the formation and release of O2 from photosystem II.” Biochemistry 51: 1079–1091.

    Article  CAS  PubMed  Google Scholar 

  • Dismukes, G. C. and Y. Siderer (1980). “EPR spectroscopic observations of a manganese center associated with water oxidation in spinach chloroplasts.” FEBS Letters 121: 78–80.

    Article  CAS  Google Scholar 

  • Dismukes, G. C. and Y. Siderer (1981). “Intermediates of a polynuclear manganese center involved in photosynthetic oxidation of water.” Proceedings of the National Academy of Science 78: 274–278.

    Article  CAS  Google Scholar 

  • Dorlet, P., M. Di Valentin, G. T. Babcock and J. L. McCracken (1998). “Interaction of YZ• with its environment in acetate-treated photosystem II membranes and reaction center cores.” Journal of Physical Chemistry B 102: 8239–8247.

    Article  CAS  Google Scholar 

  • Enami, I., S. Kikuchi, T. Fukuda, H. Ohta and J.-R. Shen (1998). “Binding and functional properties of four extrinsic proteins of photosystem II from a red alga, Cyanidium caldarium, as studied by release-reconstitution experiments.” Biochemistry 37: 2787–2793.

    Article  CAS  PubMed  Google Scholar 

  • Force, D. A., D. W. Randall and R. D. Britt (1997). “Proximity of acetate, manganese, and exchangeable deuterons to Tyrosine YZ-dot in acetate-inhibited Photosystem II membranes: Implications for the direct involvement of YZ-dot in water-splitting.” Biochemistry 36: 12062–12070.

    Article  CAS  PubMed  Google Scholar 

  • Ford, R. C. and M. C. W. Evans (1983). “Isolation of a photosystem 2 preparation from higher plants with highly enriched oxygen evolution activity.” FEBS Letters 160: 159–164.

    Article  CAS  Google Scholar 

  • Fork, D. C. (1972). “Oxygen electrode.” Methods in Enzymology 24: 113–122.

    Article  CAS  PubMed  Google Scholar 

  • Ghanotakis, D. F., G. T. Babcock and C. F. Yocum (1984a). “Calcium reconstitutes high rates of oxygen evolution in polypeptide depleted Photosystem II preparations.” FEBS Letters 167: 127–130.

    Article  CAS  Google Scholar 

  • Ghanotakis, D. F., J. N. Topper, G. T. Babcock and C. F. Yocum (1984b). “Water-soluble 17 and 23 kDa polypeptides restore oxygen evolution activity by creating a high-affinity binding site for Ca2+ on the oxidizing side of Photosystem II.” FEBS Letters 170: 169–173.

    Article  CAS  Google Scholar 

  • Ghanotakis, D. F., G. T. Babcock and C. F. Yocum (1985). “On the role of water-soluble polypeptides (17, 23 kDa), Fcalcium and chloride in photosynthetic oxygen evolution.” FEBS Letters 192: 1–3.

    Article  CAS  Google Scholar 

  • Gorham, P. R. and K. A. Clendenning (1952). “Anionic stimulation of the Hill reaction in isolated chloroplasts.” Archives of Biochemistry and Biophysics 37: 199–223.

    Article  CAS  PubMed  Google Scholar 

  • Grundmeier, A. and H. Dau (2012). “Structural models of the manganese complex of photosystem II and mechanistic implications.” Biochimica et Biophysica Acta 1817: 88–105.

    Article  CAS  PubMed  Google Scholar 

  • Guskov, A., J. Kern, A. Gabdulkhakov, M. Broser, A. Zouni and W. Saenger (2009). “Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride.” Nature Structural and Molecular Biology 16: 334–342.

    Article  CAS  PubMed  Google Scholar 

  • Haddy, A. (2007). “EPR spectroscopy of the manganese cluster of photosystem II.” Photosynthesis Research 92: 357–368.

    Article  CAS  PubMed  Google Scholar 

  • Haddy, A., W. R. Dunham, R. H. Sands and Roland Aasa (1992). “Multifrequency EPR investigations into the origin of the S2-state signal at g = 4 of the O2-evolving complex.” Biochimica et Biophysica Acta 1099: 25–34.

    Article  CAS  PubMed  Google Scholar 

  • Haddy, A., J. A. Hatchell, R. A. Kimel and R. Thomas (1999). “Azide as a competitor of chloride in oxygen evolution by photosystem II.” Biochemistry 38: 6104–6110.

    Article  CAS  PubMed  Google Scholar 

  • Haddy, A., R. A. Kimel and R. Thomas (2000). “Effects of azide on the S2 state EPR signals from photosystem II.” Photosynthesis Research 63: 35–45.

    Article  CAS  PubMed  Google Scholar 

  • Hallahan, B. J., J. H. A. Nugent, J. T. Warden and M. C. W. Evans (1992). “Investigation of the origin of the “S3” EPR signal from the oxygen-evolving complex of Photosystem 2: The role of Tyrosine Z.” Biochemistry 31: 4562–4573.

    Article  CAS  PubMed  Google Scholar 

  • Hasegawa, K., Y. Kimura and T.-a. Ono (2002). “Chloride cofactor in the photosynthetic oxygen-evolving complex studied by Fourier transform infrared spectroscopy.” Biochemistry 41: 13839–13850.

    Article  CAS  PubMed  Google Scholar 

  • Haumann, M., M. Barra, P. Loja, S. Löscher, R. Krivanek, A. Grundmeier, L.-E. Andreasson and H. Dau (2006). “Bromide does not bind to the Mn4Ca complex in its S1 state in Cl−-depleted and Br−-reconstituted oxygen-evolving photosystem II: Evidence from X-ray absorption spectroscopy at the Br K-edge.” Biochemistry 45: 13101–13107.

    Article  CAS  PubMed  Google Scholar 

  • Homann, P. H. (1985). “The association of functional anions with the oxygen-evolving center of chloroplasts.” Biochimica et Biophysica Acta 809: 311–319.

    Article  CAS  Google Scholar 

  • Homann, P. H. (1988a) “Structural effects of Cl− and other anions on the water oxidizing complex of chloroplast photosystem II”. Plant Physiology 88, 194–199.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Homann, P. H. (1988b). “The chloride and calcium requirement of photosynthetic water oxidation: effects of pH.” Biochimica et Biophysica Acta 934: 1–13.

    Article  CAS  Google Scholar 

  • Homann, P. H. (2002). “Chloride and calcium in Photosystem II: from effects to enigma.” Photosynthesis Research 73: 169–175.

    Article  CAS  PubMed  Google Scholar 

  • Ikeuchi, M. and Y. Inoue (1987). “Specific125I labeling of D1 (herbicide-binding protein).” FEBS Letters 210: 71–76.

    Article  CAS  Google Scholar 

  • Ikeuchi, M., H. Koike and Y. Inoue (1988). “Iodination of D1 (herbicide-binding protein) is coupled with photooxidation of125I− associated with Cl−-binding site in Photosystem-II water-oxidation system.” Biochimica et Biophysica Acta 932: 160–169.

    Article  CAS  Google Scholar 

  • Imaoka, A., K. Akabori, M. Yanagi, K. Izumi, Y. Toyoshima, A. Kawamori, H. Nakayama and J. Sato (1986). “Roles of three lumen-surface proteins in the formation of S2 state and 02 evolution in Photosystem II particles from spinach thylakoid membranes.” Biochimica et Biophysica Acta 848: 201–211.

    Article  CAS  Google Scholar 

  • Inoue-Kashino, N., Y. Kashino, K. Satoh, I. Terashima and H. B. Pakrasi (2005). “PsbU provides a stable architecture for the oxygen-evolving system in cyanobacterial photosystem II.” Biochemistry 44: 12214–12228.

    Article  CAS  PubMed  Google Scholar 

  • Itoh, S. and S. Uwano (1986). “Characteristics of the Cl− action site in the O2 evolving reaction in PS II particles: Electrostatic interaction with ions.” Plant and Cell Physiology 27: 25–36.

    CAS  Google Scholar 

  • Itoh, S., C. T. Yerkes, Y. Koike, H. H. Robinson and A. R. Crofts (1984). “Effects of chloride depletion on electron donation from the water-oxidizing complex to the photosystem II reaction center as measured by the microsecond rise of chlorophyll fluorescence in isolated pea chloroplasts.” Biochimica et Biophysica Acta 766: 612–622.

    Article  CAS  Google Scholar 

  • Izawa, S., R. L. Heath and G. Hind (1969). “The role of chloride ion in photosynthesis. III. The effect of artificial electron donors upon electron transport.” Biochimica et Biophysica Acta 180: 388–398.

    Article  CAS  PubMed  Google Scholar 

  • Katoh, H., S. Itoh, J.-R. Shen and M. Ikeuchi (2001). “Functional analysis of psbV and a novel c-type cytochrome gene psbV2 of the thermophilic cyanobacterium Thermosynechococcus elongatus strain BP-1.” Plant and Cell Physiology 42: 599–607.

    Article  CAS  PubMed  Google Scholar 

  • Katoh, S. (1972). “Inhibitors of electron transport associated with photosystem II in chloroplasts.” Plant and Cell Physiology 13: 273–286.

    Article  CAS  Google Scholar 

  • Kawakami, K., Y. Umena, N. Kamiya and J.-R. Shen (2009). “Location of chloride and its possible functions in oxygen-evolving photosystem II revealed by X-ray crystallography.” Proceedings of the National Academy of Sciences of the United States of America 106: 8567–8572.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawakami, K., Y. Umena, N. Kamiya and J.-R. Shen (2011). “Structure of the catalytic, inorganic core of oxygen-evolving photosystem II at 1.9 A resolution.” Journal of Photochemistry and Photobiology, B: Biology 104: 9–18.

    Article  CAS  Google Scholar 

  • Kawamoto, K., J. Mano and K. Asada (1995). “Photoproduction of the azidyl radical from the azide anion on the oxidizing side of Photosytem II and suppression of photooxidation of Tyrosine Z by the azidyl radical.” Plant and Cell Physiology 36: 1121–1129.

    Article  CAS  Google Scholar 

  • Kelley, P. and S. Izawa (1978). “The role of chloride ion in photosystem II: I. Effects of chloride ion on photosystem II electron transport and on hydroxylamine inhibition.” Biochimica et Biophysica Acta 502: 198–210.

    Article  CAS  PubMed  Google Scholar 

  • Kirilovsky, D., M. Roncel, A. Boussac, A. Wilson, J. L. Zurita, J.-M. Ducruet, H. Bottin, M. Sugiura, J. M. Ortega and A. W. Rutherford (2004). “Cytochrome c550 in the cyanobacterium Thermosynechococcus elongatus.” Journal of Biological Chemistry 279: 52869–52880.

    Article  CAS  PubMed  Google Scholar 

  • Klein, M. P., K. Sauer and V. K. Yachandra (1993). “Perspectives on the structure of the photosynthetic oxygen evolving manganese complex and its relation to the Kok cycle.” Photosynthesis Research 38: 265–277.

    Article  CAS  PubMed  Google Scholar 

  • Kühne, H., V. A. Szalai and G. W. Brudvig (1999). “Competitive binding of acetate and chloride in Photosystem II.” Biochemistry 38: 6604–6613.

    Article  PubMed  Google Scholar 

  • Kuntzleman, T. S. and A. Haddy (2009). “Fluoride inhibition of photosystem II and the effect of removal of the PsbQ subunit.” Photosynthesis Research 102: 7–19.

    Article  CAS  PubMed  Google Scholar 

  • Kuwabara, T. and N. Murata (1982). “Inactivation of photosynthetic oxygen evolution and concomitant release of three polypeptides in the photosystem II particles of spinach chloroplasts.” Plant and Cell Physiology 23: 533–539.

    Article  CAS  Google Scholar 

  • Kuwabara, T. and N. Murata (1983). “Quantitative analysis of the inactivation of photosynthetic oxygen evolution and the release of polypeptides and manganese in the photosystem II particles of spinach chloroplast.” Plant and Cell Physiology 24: 741–747.

    Article  CAS  Google Scholar 

  • Lakshmi, K. V., S. S. Eaton, G. R. Eaton, H. A. Frank and G. W. Brudvig (1998). “Analysis of dipolar and exchange interactions between manganese and Tyrosine Z in the S2YZ-dot state of acetate-inhibited Photosystem II via EPR spectral simulations at X- and Q-bands.” Journal of Physical Chemistry B 102: 8327–8335.

    Article  CAS  Google Scholar 

  • Lakshmi, K. V., M. J. Reifler, D. A. Chisholm, J. Y. Wang, B. A. Diner and G. W. Brudvig (2002). “Correlation of the cytochrome c550 content of cyanobacterial Photosystem II with the EPR properties of the oxygen-evolving complex.” Photosynthesis Research 72: 175–189.

    Article  CAS  PubMed  Google Scholar 

  • Lindberg, K. and L.-E. Andréasson (1996). “A one-site, two-state model for the binding of anions in photosystem II.” Biochemistry 35: 14259–14267.

    Article  CAS  PubMed  Google Scholar 

  • Lindberg, K., T. Wydrzynski, T. Vänngård and L.-E. Andréasson (1990). “Slow release of chloride from36Cl-labeled photosystem II membranes.” FEBS Letters 264: 153–155.

    Article  CAS  Google Scholar 

  • Lindberg, K., T. Vänngård and L.-E. Andréasson (1993). “Studies of the slowly exchanging chloride in photosystem II of higher plants.” Photosynthesis Research 38: 401–408.

    Article  CAS  PubMed  Google Scholar 

  • MacLachlan, D. J. and J. H. A. Nugent (1993). “Investigation of the S3 electron paramagnetic resonance signal from the oxygen-evolving complex of Photosystem 2: Effect of inhibition of oxygen evolution by acetate.” Biochemistry 32: 9772–9780.

    Article  CAS  PubMed  Google Scholar 

  • Mavankal, G., D. C. McCain and T. M. Bricker (1986). “Effects of chloride on paramagnetic coupling of manganese in calcium chloride-washed photosystem II preparations.” FEBS Letters 202: 235–239.

    Article  CAS  Google Scholar 

  • McDermott, A. E., V. K. Yachandra, R. D. Guiles, J. L. Cole, S. L. Dexheimer, R. D. Britt, K. Sauer and M. P. Klein (1988). “Characterization of the manganese 02-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

    Article  CAS  PubMed  Google Scholar 

  • Miyao, M. and N. Murata (1983). “Partial disintegration and reconstitution of the photosynthetic oxygen evolution system.” Biochimica et Biophysica Acta 725: 87–93.

    Article  CAS  Google Scholar 

  • Miyao, M. and N. Murata (1984). “Calcium ions can be substituted for the 24-kDa polypeptide in photosynthetic oxygen evolution.” FEBS Letters 168: 118–120.

    Article  CAS  Google Scholar 

  • Miyao, M. and N. Murata (1985). “The Cl− effect on photosynthetic oxygen evolution: interaction of Cl− with 18-kDa, 24-kDa and 33-kDa proteins.” FEBS Letters 180: 303–308.

    Article  CAS  Google Scholar 

  • Morgan, T. R., J. A. Shand, S. M. Clarke and J. J. Eaton-Rye (1998). “Specific requirements for cytochrome c-550 and the manganese-stabilizing protein in photoautotrophic strains of Synechocystis sp. PCC 6803 with mutations in the domain Gly-351 to Thr-436 of the chlorophyll-binding protein CP47.” Biochemistry 37: 14437–14449.

    Article  CAS  PubMed  Google Scholar 

  • Murray, J. W., K. Maghlaoui, J. Kargul, N. Ishida, T.-L. Lai, A. W. Rutherford, M. Sugiura, A. Boussac and J. Barber (2008). “X-ray crystallography identifies two chloride binding sites in the oxygen evolving centre of photosystem II.” Energy and Environmental Science 1: 161–166.

    Article  CAS  Google Scholar 

  • Olesen, K. and L.-E. Andréasson (2003). “The function of the chloride ion in photosynthetic oxygen evolution.” Biochemistry 42: 2025–2035.

    Article  CAS  PubMed  Google Scholar 

  • Ono, T.-A. and Y. Inoue (1986). “Effects of removal and reconstitution of the extrinsic 33, 24 and 16 kDa proteins on flash oxygen yield in Photosystem II particles.” Biochimica et Biophysica Acta 850: 380–389.

    Article  CAS  Google Scholar 

  • Ono, T.-A. and Y. Inoue (1988). “Abnormal S-state turnovers in NH3-binding Mn centers of photosynthetic O2 evolving system.” Archives of Biochemistry and Biophysics 264: 82–92.

    Article  CAS  PubMed  Google Scholar 

  • Ono, T.-A. and Y. Inoue (1990). “Abnormal redox reactions in photosynthetic O2-evolving centers in NaCl/EDTA-washed PS II. A dark-stable EPR multiline signal and an unknown positive charge accumulator.” Biochimica et Biophysica Acta 1020: 269–277.

    Article  CAS  Google Scholar 

  • Ono, T.-A., J. L. Zimmermann, Y. Inoue and A. W. Rutherford (1986). “EPR evidence for a modified S-state transition in chloride-depleted photosystem II.” Biochimica et Biophysica Acta 851: 193–201.

    Article  CAS  Google Scholar 

  • Ono, T.-A., H. Nakayama, H. Gleiter, Y. Inoue and A. Kawamori (1987). “Modification of the properties of S2 state in photosynthetic O2-evolving center by replacement of chloride with other anions.” Archives of Biochemistry and Biophysics 256: 618–624.

    Article  CAS  PubMed  Google Scholar 

  • Papageorgiou, G. C. and T. Lagoyanni (1991). “Interactions of iodide ions with isolate photosystem 2 particles.” Archives of Biochemistry and Biophysics 285: 339–343.

    Article  CAS  PubMed  Google Scholar 

  • Peloquin, J. M. and R. D. Britt (2001). “EPR/ENDOR characterization of the physical and electronic structure of the OEC Mn cluster.” Biochimica et Biophysica Acta 1503: 96–111.

    Article  CAS  PubMed  Google Scholar 

  • Peloquin, J. M., K. A. Campbell and R. D. Britt (1998). “55Mn pulsed ENDOR demonstrates that the Photosystem II “split” EPR signal arises from a magnetically-coupled mangano-tyrosyl complex.” Journal of the American Chemical Society 120: 6840–6841.

    Article  CAS  Google Scholar 

  • Philbrick, J. B., B. A. Diner and B. A. Zilinskas (1991). “Construction and characterization of cyanobacterial mutants lacking the manganese-stabilizing polypeptide of photosystem II.” Journal of Biological Chemistry 266:13370–13376

    CAS  PubMed  Google Scholar 

  • Pokhrel, R. and G. W. Brudvig (2013). “Investigation of the inhibitory effect of nitrite on photosystem II.” Biochemistry 52: 3781–3789.

    Article  CAS  PubMed  Google Scholar 

  • Pokhrel, R., I. L. McConnell and G. W. Brudvig (2011). “Chloride regulation of enzyme turnover: Application to the role of chloride in photosystem II.” Biochemistry 50: 2725–2734.

    Article  CAS  PubMed  Google Scholar 

  • Pokhrel, R., R. J. Service, R. J. Debus and G. W. Brudvig (2013). “Mutation of Lysine 317 in the D2 subunit of photosystem II alters chloride binding and proton transport.” Biochemistry 52: 4758–4773.

    Article  CAS  PubMed  Google Scholar 

  • Popelkova, H. and C. F. Yocum (2007). “Current status of the role of Cl− ion in the oxygen-evolving complex.” Photosynthesis Research 93: 111–121.

    Article  CAS  PubMed  Google Scholar 

  • Popelkova, H., S. D. Betts, N. Lydakis-Symantiris, M. M. Im, E. Swenson and C. F. Yocum (2006). “Mutagenesis of basic residues R151 and R161 in manganese-stabilizing protein of photosystem II causes inefficient binding of chloride to the oxygen-evolving complex.” Biochemistry 45: 3107–3115.

    Article  CAS  PubMed  Google Scholar 

  • Popelkova, H., A. Commet and C. F. Yocum (2009). “Asp157 is required for th function of PsbO, the photosystem II manganese stabilizing protein.” Biochemistry 48, 11920–11928.

    Article  CAS  PubMed  Google Scholar 

  • Rachid, A. and P. H. Homann (1992). “Properties of iodide-activated photosynthetic water-oxidizing complexes.” Biochimica et Biophysica Acta 1101: 303–310.

    Article  Google Scholar 

  • Rivalta, I., M. Amin, S. Luber, S. Vassiliev, R. Pokhrel, Y. Umena, K. Kawakami, J.-R. Shen, N. Kamiya, D. Bruce, G. W. Brudvig, M. R. Gunner and V S. Batista (2011). “Structural-functional role of chloride in photosystem II.” Biochemistry 50: 6312–6315.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roose, J. L., K. M. Wegener and H. B. Pakrasi (2007). “The extrinsic proteins of photosystem II.” Photosynthesis Research 92: 369–387.

    Article  CAS  PubMed  Google Scholar 

  • Sanakis, Y., D. Petasis, V. Petrouleas and M Hendrich (1999). “Simultaneous binding of fluoride and NO to the nonheme iron of photosystem II: Quantitative EPR evidence for a weak exchange interaction between the semiquinone QA − and the iron-nitrosyl complex.” Journal of the American Chemical Society 121: 9155–9164.

    Article  CAS  Google Scholar 

  • Sandusky, P. O. and C. F. Yocum (1983). “The mechanism of amine inhibition of the photosynthetic oxygen evolving complex.” FEBS Letters 162: 339–343.

    Article  CAS  Google Scholar 

  • Sandusky, P. O. and C. F. Yocum (1984). “The chloride requirement for photosynthetic oxygen evolution: analysis of the effects of chloride and other anions on amine inhibition of the oxygen-evolving complex.” Biochimica et Biophysica Acta 766: 603–611.

    Article  CAS  Google Scholar 

  • Sandusky, P. O. and C. F. Yocum (1986). “The chloride requirement for photosynthetic oxygen evolution: factors affecting nucleophilic displacement of chloride from the oxygen-evolving complex.” Biochimica et Biophysica Acta 849: 85–93.

    Article  CAS  Google Scholar 

  • Sauer, K., J. Yano and V. K. Yachandra (2008). “X-ray spectroscopy of the photosynthetic oxygen-evolving complex.” Coordination Chemistry Reviews 252: 318–335.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saygin, Ö., S. Gerken, B. Meyer and H. T. Witt (1986). “Total recovery of O2 evolution and nanosecond reduction kinetics of chlorophyll-aII + (P-680+) after inhibition of water cleavage with acetate.” Photosynthesis Research 9: 71–78.

    Article  CAS  PubMed  Google Scholar 

  • Shen, J.-R. and Y. Inoue (1993). “Binding and functional properties of two new extrinsic components, cytochrome c-550 and a 12-kDa protein, in cyanobacterial photosystem II.” Biochemistry 32: 1825–1832.

    Article  CAS  PubMed  Google Scholar 

  • Shen, J.-R., M. Ikeuchi and Y. Inoue (1992). “Stoichiometric association of extrinsic cytochrome c550 and 12 kDa protein with a highly purified oxygen-evolving photosystem II core complex from Synechococcus vulcanus.” FEBS Letters 301: 145–149.

    Article  CAS  PubMed  Google Scholar 

  • Shen, J.-R., M. Ikeuchi and Y. Inoue (1997). “Analysis of the psbU gene encoding the 12-kDa extrinsic protein of photosystem II and studies on its role by deletion mutagenesis in Synechocystis sp. PCC 6803.” Journal of Biological Chemistry 272: 17821–17826.

    Article  CAS  PubMed  Google Scholar 

  • Shen, J.-R., M. Qian, Y. Inoue and R. L. Burnap (1998). “Functional characterization of Synechocystis sp. PCC 6803 del-psbU and del-psbV mutants reveals important roles of cytochrome c-550 in cyanobacterial oxygen evolution.” Biochemistry 37: 1551–1558.

    Article  CAS  PubMed  Google Scholar 

  • Shoji, M., H. Isobe, S. Yamanaka, Y. Umena, K. Kawakami, N. Kamiya, J.-R. Shen, T. Nakajima and K. Yamaguchi (2015). “Theoretical modelling of biomolecular systems I. Large-scale QM/MM calculations of hydrogen bonding networks of the oxygen evolving complex of photosystem II.” Molecular Physics 113: 359–384.

    Article  CAS  Google Scholar 

  • Sinclair, J. (1984). “The influence of anions on oxygen evolution by isolated spinach chloroplasts.” Biochimica et Biophysica Acta 764: 247–252.

    Article  CAS  Google Scholar 

  • Sivaraja, M., J. Tso and G. C. Dismukes (1989). “A calcium-specific site influences the structure and activity of the manganese cluster responsible for photosynthetic water oxidation.” Biochemistry 28: 9459–9464.

    Article  CAS  PubMed  Google Scholar 

  • Stemler, A. and J. B. Murphy (1985). “Bicarbonate-reversible and irreversible inhibition of photosystem II by monovalent anions.” Plant Physiology 77: 974–977.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strickler, M. A., L. M. Walker, W. Hillier and R. J. Debus (2005). “Evidence from biosynthetically incorporated strontium and FTIR difference spectroscopy that the C-terminus of the D1 polypeptide of photosystem II does not ligate calcium.” Biochemistry 44: 8571–8577.

    Article  CAS  PubMed  Google Scholar 

  • Styring, S., M. Miyao and A. W. Rutherford (1987). “Formation and flash-dependent oscillation of the S2-state multiline EPR signal inan oxygen-evolving photosystem-ll preparation lacking the three extrinsic proteins in the oxygen-evolving system.” Biochimica et Biophysica Acta 890: 32–38.

    Article  CAS  Google Scholar 

  • Suga, M., F. Akita, K. Hirata, G. Ueno, H. Murakami, Y. Nakajima, T. Shimizu, K. Yamashita, M. Yamamoto, H. Ago and J.-R. Shen (2015). “Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses.” Nature (London) 517: 99–103.

    Article  CAS  Google Scholar 

  • Summerfield, T. C., J. A. Shand, F. K. Bentley and J. J. Eaton-Rye (2005a). “PsbQ (Sll1638) in Synechocystis sp. PCC 6803 is required for photosystem II activity in specific mutants and in nutrient-limiting conditions.” Biochemistry 44: 805–815.

    Article  CAS  PubMed  Google Scholar 

  • Summerfield, T. C., R. T. Winter and J. J. Eaton-Rye (2005b). “Investigation of a requirement for the PsbP-like protein in Synechocystis sp. PCC 6803.” Photosynthesis Research 84: 263–268.

    Article  CAS  PubMed  Google Scholar 

  • Suzuki, H., J. Yu, T. Kobayashi, H. Nakanishi, P. J. Nixon and T. Noguchi (2013). “Functional roles of D2-Lys317 and the interacting chloride ion in the water oxidation reaction of photosystem II as revealed by Fourier transform infrared analysis.” Biochemistry 52: 4748–4757.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szalai, V. A. and G. W. Brudvig (1996a). “Formation and decay of the S3 EPR signal species in acetate-inhibited photosystem II.” Biochemistry 35: 1946–1953.

    Article  CAS  PubMed  Google Scholar 

  • Szalai, V. A. and G. W. Brudvig (1996b). “Reversible binding of nitric oxide to tyrosyl radicals in photosystem II. Nitric oxide quenches formation of the S3 EPR signal species in acetate-inhibited photosystem II.” Biochemistry 35: 15080–15087.

    Article  CAS  PubMed  Google Scholar 

  • Szalai, V. A., H. Kühne, K. V. Lakshmi and G. W. Brudvig (1998). “Characterization of the interaction between manganese and tyrosine Z in acetate-inhibited photosystem II.” Biochemistry 37: 13594–13603.

    Article  CAS  PubMed  Google Scholar 

  • Takahashi, Y. and S. Styring (1987). “A comparative study of the reduction of EPR signal IIslow by iodide and the iodo-labeling of the D2-protein in photosystem II.” FEBS Letters 223: 371–375.

    Article  CAS  Google Scholar 

  • Takahashi, Y., M.-a. Takahashi and K. Satoh (1986). “Identification of the site of iodide photooxidation in the photosystem II reaction center complex.” FEBS Letters 208: 347–351.

    Article  CAS  Google Scholar 

  • Tang, X.-S., D. W. Randall, D. A. Force, B. A. Diner and R. D. Britt (1996). “Manganese-tyrosine interaction in the Photosystem II oxygen-evolving complex.” Journal of the American Chemical Society 118: 7638–7639.

    Article  CAS  Google Scholar 

  • Theg, S. M., P. A. Jursinic and P. H. Homann (1984). “Studies on the mechanism of chloride action on photosynthetic water oxidation.” Biochimica et Biophysica Acta 766: 636–646.

    Article  CAS  Google Scholar 

  • Thornton, L. E., H. Ohkawa, J. L. Roose, Y. Kashino, N. Keren and H. B. Pakrasi (2004). “Homologs of plant PsbP and PsbQ proteins are necessary for regulation of photosystem II activity in the cyanobacterium Synechocystis 6803.” Plant Cell 16: 2164–2175.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Umena, Y., K. Kawakami, J.-R. Shen and N. Kamiya (2011). “Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å.” Nature (London) 473: 55–59.

    Article  CAS  Google Scholar 

  • van Gorkom, H. J. and C. F. Yocum (2005). The calcium and chloride cofactors. Photosystem II: The light-driven water: plastoquinone oxidoreductase. T. Wydrzynski and K. Satoh. The Netherlands, Springer: 307–327.

    Google Scholar 

  • van Vliet, P. and A. W. Rutherford (1996). “Properties of the chloride-depleted oxygen-evolving complex of photosystem II studied by electron paramagnetic resonance.” Biochemistry 35: 1829–1839.

    Article  PubMed  Google Scholar 

  • Velthuys, B. R. (1975). “Binding of the inhibitor NH3 to the oxygen-evolving apparatus of spinach chloroplasts.” Biochimica et Biophysica Acta 396: 392–401.

    Article  CAS  PubMed  Google Scholar 

  • Vogt, L., D. J. Vinyard, S. Khan and G. W. Brudvig (2015). “Oxygen-evolving complex of Photosystem II: An analysis of second-shell residues and hydrogen-bonding networks.” Current Opinion in Chemical Biology 25: 152–158.

    Article  CAS  PubMed  Google Scholar 

  • Warburg, O. and W. Lüttgens (1944). “Weitere experimente zur kohlensaureassimilation.” Naturwissenschaften 40: 301.

    Article  Google Scholar 

  • Wincencjusz, H., H. J. van Gorkom and C. F. Yocum (1997). “The photosynthetic oxygen evolving complex requires chloride for its redox state S2-to-S3 and S3-to-S0 transitions but not for S0-to-S1 or S1-to-S2 transitions.” Biochemistry 36: 3663–3670.

    Article  CAS  PubMed  Google Scholar 

  • Wincencjusz, H., C. F. Yocum and H. J. van Gorkom (1998). “S-state dependence of chloride binding affinities and exchange dynamics in the intact and polypeptide-depleted O2 evolving complex of photosystem II.” Biochemistry 37: 8595–8604.

    Article  CAS  PubMed  Google Scholar 

  • Wincencjusz, H., C. F. Yocum and H. J. van Gorkom (1999). “Activating anions that replace Cl− in the O2-evolving complex of photosystem II slow the kinetics of the terminal step in water oxidation and destabilize the S2 and S3 states.” Biochemistry 38: 3719–3725.

    Article  CAS  PubMed  Google Scholar 

  • Yachandra, V. K., R. D. Guiles, K. Sauer and M. P. Klein (1986). “The state of manganese in the photosynthetic apparatus. 5. The chloride effect in photosynthetic oxygen evolution.” Biochimica et Biophysica Acta 850: 333–342.

    Article  CAS  Google Scholar 

  • Yachandra, V. K., K. Sauer and M. P. Klein (1996). “Manganese cluster in photosynthesis: Where plants oxidize water to dioxygen.” Chemical Reviews 96: 2927–2950.

    Article  CAS  PubMed  Google Scholar 

  • Yano, J. and V. K. Yachandra (2009). “X-ray absorption spectroscopy.” Photosynthesis Research 102: 241–254.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yocum, C. F. (2008). “The calcium and chloride requirements of the O2 evolving complex.” Coordination Chemistry Reviews 252: 296–305.

    Article  CAS  Google Scholar 

  • Yu, H., C. P. Aznar, X. Xu and R. D. Britt (2005). “Evidence that azide occupies the chloride binding site near the manganese cluster in photosystem II.” Biochemistry 44: 12022–12029.

    Article  CAS  PubMed  Google Scholar 

  • Zimmermann, J.-L. and A. W. Rutherford (1984). “EPR studies of the oxygen-evolving enzyme of Photosystem II.” Biochimica et Biophysica Acta 767: 160–167.

    Article  CAS  Google Scholar 

  • Zimmermann, J.-L. and A. W. Rutherford (1986). “Electron paramagnetic resonance properties of the S2 state of the oxygen-evolving complex of photosystem II.” Biochemistry 25: 4609–4615.

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by grants from the National Science Foundation, the Camille and Henry Dreyfus Foundation, and the UNCG Office of Research. Many thanks to Sergei Baranov, David Bryson, and Hong Qian for technical assistance.

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  1. Department of Chemistry and Biochemistry, University of North Carolina at Greensboro, Greensboro, NC, 27402, USA

    Alice Haddy, Vonda Sheppard, Rachelle Johnson & Eugene Chen

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Correspondence to Alice Haddy .

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  1. Department of Physical Sciences, Alabama State University, Montgomery, Alabama, USA

    Harvey J.M. Hou

  2. Center for Research in Climate Change and Global Warming, Institute for Advanced Studies in Basic Sciences, Zanjan, Iran

    Mohammad Mahdi Najafpour

  3. School of Molecular Sciences, Center for Applied Structural Discovery at the Biodesign Institute, Arizona State University, Tempe, Arizona, USA

    Gary F. Moore

  4. Institute of Plant Physiology, Russian Academy of Sciences, Moscow, Russia

    Suleyman I. Allakhverdiev

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Haddy, A., Sheppard, V., Johnson, R., Chen, E. (2017). The Cl− Requirement for Oxygen Evolution by Photosystem II Explored Using Enzyme Kinetics and EPR Spectroscopy. In: Hou, H., Najafpour, M., Moore, G., Allakhverdiev, S. (eds) Photosynthesis: Structures, Mechanisms, and Applications. Springer, Cham. https://doi.org/10.1007/978-3-319-48873-8_5

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