Abstract
PsbP is an extrinsic protein of PSII having a function of Ca2+ and Cl− retention in the water-oxidizing center (WOC). In order to understand the mechanism how PsbP regulates the Cl− binding in WOC, we examined the effect of PsbP depletion on the protein structures around the Cl− sites using Fourier transform infrared (FTIR) spectroscopy. Light-induced FTIR difference spectra upon the S1→S2 transition were obtained using Cl−-bound and NO3−-substituted PSII membranes in the presence and absence of PsbP. A clear difference in the amide I band changes by PsbP depletion was observed between Cl−-bound and NO3−-substituted PSII samples, indicating that PsbP binding perturbed the protein conformations around the Cl−ion(s) in WOC. It is suggested that PsbP stabilizes the Cl− binding by regulating the dissociation constant of Cl− and/or an energy barrier of Cl− dissociation through protein conformational changes around the Cl− ion(s).
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- DCMU:
-
3-(3,4-dichlorophenyl)-1,1-dimethylurea
- FTIR:
-
Fourier transform infrared
- Mes:
-
2-(N-morpholino) ethanesulfonic acid
- PMS:
-
phenazine methosulfate
- WOC:
-
water-oxidizing center
References
Ashizawa R., Noguchi T.: Effects of hydrogen bonding interactions on the redox potential and molecular vibrations of plastoquinone as studied by density functional theory calculations.–Phys. Chem. Chem. Phys. 16: 11864–11876, 2014.
Berthomieu C., Nabedryk E., Mäntele W. et al.: Characterization by FTIR spectroscopy of the photoreduction of the primary quinone acceptor QA in photosystem II.–FEBS Lett. 269: 363–367, 1990.
Bricker T.M., Roose J.L., Fagerlund R.D. et al.: The extrinsic proteins of Photosystem II.–Biochim. Biophys. Acta 1817: 121–142, 2012.
Bricker T.M., Roose J.L., Zhang P. et al.: The PsbP family of proteins.–Photosynth. Res. 116: 235–250, 2013.
Chu H.-A.: Fourier transform infrared difference spectroscopy for studying the molecular mechanism of photosynthetic water oxidation.–Front. Plant Sci. 4: 146, 2013.
Debus R.J.: FTIR studies of metal ligands, networks of hydrogen bonds, and water molecules near the active site Mn4CaO5 cluster in Photosystem II.–BBA-Bioenergetics 1847: 19–34, 2015.
Enami I., Okumura A., Nagao R. et al.: Structures and functions of the extrinsic proteins of photosystem II from different species.–Photosynth. Res. 98: 349–363, 2008.
Fagerlund R.D., Eaton-Rye J.J.: The lipoproteins of cyanobacterial photosystem II.–J. Photoch. Photobio. B 104: 191–203, 2011.
Grundmeier A., Dau H.: Structural models of the manganese complex of photosystem II and mechanistic implications.–Biochim. Biophys. Acta 1817: 88–105, 2012.
Hasegawa K,. Kimura Y., Ono T.: Chloride cofactor in the photosynthetic oxygen-evolving complex studied by Fourier transform infrared spectroscopy.–Biochemistry 41: 13839–13850, 2002.
Hasegawa K., Kimura Y., Ono T.: Oxidation of the Mn cluster induces structural changes of NO3− functionally bound to the Cl− site in the oxygen-evolving complex of photosystem II.–Biophys. J. 86: 1042–1050, 2004.
Ido K., Kakiuchi S., Uno C. et al.: The conserved His-144 in the PsbP protein is important for the interaction between the PsbP N-terminus and the Cyt b559 subunit of photosystem II.–J. Biol. Chem. 287: 26377–26387, 2012.
Ifuku K., Ishihara S., Shimamoto R. et al.: Structure, function, and evolution of the PsbP protein family in higher plants.–Photosynth. Res. 98: 427–437, 2008.
Ifuku K., Ido K., Sato F.: Molecular functions of PsbP and PsbQ proteins in the photosystem II supercomplex.–J. Photoch. Photobio. B 104: 158–164, 2011.
Ifuku K., Noguchi T.: Structural coupling of extrinsic proteins with the oxygen-evolving center in photosystem II.–Front. Plant Sci. 7: 84, 2016.
Joliot P., Barbieri G., Chabaud R.: Model of the System II photochemical centers.–Photochem. Photobiol. 10: 309–329, 1969.
Kakiuchi S., Uno C., Ido K. et al.: The PsbQ protein stabilizes the functional binding of the PsbP protein to photosystem II in higher plants.–Biochim. Biophys. Acta 1817: 1346–1351, 2012.
Kok B., Forbush B., McGloin M.: Cooperation of charges in photosynthetic O2 evolution-I. A linear four step mechanism.–Photochem. Photobiol. 11: 457–475, 1970.
Messinger J., Noguchi T., Yano J.: Photosynthetic O2 evolution. Chapter 7.–In: Wydrzynski T., Hillier W. (ed.): Molecular Solar Fuels. Pp. 163–207. Royal Society of Chemistry, Cambridge 2012.
Miyao M., Fujimura Y., Murata N.: Partial degradation of the extrinsic 23-kDa protein of the Photosystem II complex of spinach.–BBA-Bioenergetics 936: 465–474, 1988.
Nagao R., Tomo T., Noguchi T.: Effects of extrinsic proteins on the protein conformation of the oxygen-evolving center in cyanobacterial photosystem II as revealed by Fourier transform infrared spectroscopy.–Biochemistry 54: 2022–2031, 2015.
Nakamura S., Noguchi T.: Quantum mechanics/molecular mechanics simulation of the ligand vibrations of the wateroxidizing Mn4CaO5 cluster in photosystem II.–P. Natl. Acad. Sci. USA 113: 12727–12732, 2016.
Nishimura T., Nagao R., Noguchi T. et al.: The N-terminal sequence of the extrinsic PsbP protein modulates the redox potential of Cyt b559 in photosystem II.–Sci. Rep. 6: 21490, 2016.
Nishimura T., Uno C., Ido K. et al.: Identification of the basic amino acid residues on the PsbP protein involved in the electrostatic interaction with photosystem II.–Biochim. Biophys. Acta 1837: 1447–1453, 2014.
Noguchi T.: Fourier transform infrared difference and timeresolved infrared detection of the electron and proton transfer dynamics in photosynthetic water oxidation.–BBABioenergetics 1847: 35–45, 2015.
Noguchi T., Berthomieu C.: Molecular analysis by vibrational spectroscopy.–In: Wydrzynski T., Satoh K. (ed.): Photosystem II: The Light-Driven Water:Plastoquinone Oxidoreductase. Pp. 367–387. Springer, Dordrecht 2005.
Noguchi T., Ono T., Inoue Y.: Direct detection of a carboxylate bridge between Mn and Ca2+ in the photosynthetic oxygenevolving center by means of Fourier transform infrared spectroscopy.–BBA-Bioenergetics 1228: 189–200, 1995.
Noguchi T., Sugiura M.: Flash-induced Fourier transform infrared detection of the structural changes during the S-state cycle of the oxygen-evolving complex in photosystem II.–Biochemistry 40: 1497–1502, 2001.
Noguchi T., Sugiura M.: Analysis of flash-induced FTIR difference spectra of the S-state cycle in the photosynthetic water-oxidizing complex by uniform 15N and 13C isotope labeling.–Biochemistry 42: 6035–6042, 2003.
Ono T., Inoue Y.: Effects of removal and reconstitution of the extrinsic 33, 24 and 16 kDa proteins on flash oxygen yield in photosystem II particles.–BBA-Bioenergetics 850: 380–389, 1986.
Petrouleas V., Crofts A.R.: The quinone iron acceptor complex.–In: Wydrzynski T., Satoh K. (ed.): Photosystem II: The Light-Driven Water:Plastoquinone Oxidoreductase. Pp. 177–206. Springer, Dordrecht 2005.
Roose J.L., Frankel L.K., Mummadisetti M.P. et al.: The extrinsic proteins of photosystem II: update.–Planta 243: 889–908, 2016.
Seidler A.: The extrinsic polypeptides of Photosystem II.–Biochim. Biophys. Acta 1277: 35–60, 1996.
Shen J.-R.: The structure of photosystem II and the mechanism of water oxidation in photosynthesis.–Annu. Rev. Plant Biol. 66: 23–48, 2015.
Sinclair J.: The influence of anions on oxygen evolution by isolated spinach chloroplasts.–Biochim. Biophys. Acta 764: 247–252, 1984.
Suga M., Akita F., Hirata K. et al.: Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses.–Nature 517: 99–103, 2015.
Suzuki H., Sugiura M., Noguchi T.: Determination of the miss probabilities of individual S-state transitions during photosynthetic water oxidation by monitoring electron flow in photosystem II using FTIR spectroscopy.–Biochemistry 51: 6776–6785, 2012.
Suzuki H., Yu J., Kobayashi T. et al.: 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, 2013.
Tomita M., Ifuku K., Sato F. et al: FTIR evidence that the PsbP extrinsic protein induces protein conformational changes around the oxygen-evolving Mn cluster in photosystem II.–Biochemistry 48: 6318–6325, 2009.
Uno C., Nagao R., Suzuki H. et al.: Structural coupling of extrinsic proteins with the oxygen-evolving center in red algal photosystem II as revealed by light-induced FTIR difference spectroscopy.–Biochemistry 52: 5705–5707, 2013.
Umena Y., Kawakami K., Shen J.-R. et al.: Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å.–Nature 473: 55–60, 2011.
Vinyard D.J., Ananyev G.M., Dismukes G.C.: Photosystem II: The reaction center of oxygenic photosynthesis.–Annu. Rev. Biochem. 82: 577–606, 2013.
Wei X.P., Su X.D., Cao P. et al.: Structure of spinach photosystem II-LHCII supercomplex at 3.2 Å resolution.–Nature 534: 69–74, 2016.
Wincencjusz H., Yocum C.F., van Gorkom H.J.: 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, 1999.
Author information
Authors and Affiliations
Corresponding author
Additional information
Acknowledgments: This study was supported by the Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology (17H03662 to T.N.).
Rights and permissions
About this article
Cite this article
Kondo, J., Noguchi, T. PsbP-induced protein conformational changes around Cl− ions in the water oxidizing center of photosystem II. Photosynthetica 56, 178–184 (2018). https://doi.org/10.1007/s11099-017-0749-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11099-017-0749-5