Abstract
The effect of hydration on protein dynamics in photosystem II (PS II) membrane fragments from spinach has been investigated by using the method of quasielastic neutron scattering (QENS) at room temperature. The QENS data obtained indicate that the protein dynamics is strongly dependent on the extent of hydration. In particular, the hydration-induced activation of localized diffusive protein motions and Q −A reoxidation by QB in PS II appear to be correlated in their onset at a hydration value of about 45% relative humidity (r.h.). These findings underline the crucial functional relevance of localized diffusive protein motions on the picosecond-timescale for the reactions of light-induced photosynthetic water splitting under formation of plastoquinol and molecular oxygen in PS II of green plants.
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References
Baxter RHG, Ponomarenko N, Srajer V, Pahl R, Moffat K, Norris JR (2004) Time-resoved crystallographic studies of light-induced structural changes in the photosynthetic reaction center. Proc Natl Acad Sci USA 101:5982–5987
Bee M (1988) Quasielastic neutron scattering: principles and applications in solid state chemistry, biology, materials science. Adam & Hilger, Philadelphia
Bernarding J, Eckert H-J, Eichler H-J, Napiwotzki A, Renger G (1994) Kinetic studies on the stabilization of the primary radical pair P680+Pheo− in different photosystem II preparations from higher plants. Photochem Photobiol 59:566–573
Berthold DA, Babcock GT, Yocum CF (1981) A highly resolved, oxygen-evolving photosystem II preparation from spinach thylakoid membranes: EPR and electron-transport properties. FEBS Lett 134:231–234
Breton J (2004) Absence of large-scale displacement of quinone QB in bacterial photosynthetic reaction centers. Biochemistry 43:3318–3326
Christen G, Renger G (1999) The role of hydrogen bonds for the multiphasic P680+ reduction by YZ in photosystem II with intact oxygen evolution capacity. Analysis of kinetic H/D isotope exchange effects. Biochemistry 38:2068–2077
Christen G, Seeliger A, Renger G (1999) P680+ reduction kinetics and redox transition probability of the water oxidising complex as a function of pH and H/D isotope exchange in spinach thylakoids. Biochemistry 38:6082–6092
Cordone L, Ferrand M, Vitrano E, Zaccai G (1999) Harmonic behavior of trehalose-coated carbon-monoxy-myoglobin at high temperature. Biophys J 76(2):1043–1047
Curtis JE, Tarek M, Tobias DJ (2004) Methyl group dynamics as a probe of the protein dynamical transition. J Am Chem Soc 126:15928–15929
Doster W, Settles M (2005) Protein–water displacement distributions. Biochim Biophys Acta 1749:173–186
Doster W, Cusack S, Petry W (1989) Dynamical transition of myoglobin revealed by inelastic neutron scattering. Nature 337:754–756
Ferrand M, Dianoux AJ, Petry W, Zaccaı G (1993) Thermal motions and function of bacteriorhodopsin in purple membranes: effects of temperature and hydration studied by neutron scattering. Proc Natl Acad Sci USA 90:9668–9672
Ferreira K, Iverson TM, Maghlouni K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838
Fitter J (1999) The temperature dependence of internal molecular motions in hydrated and dry alpha-amylase: the role of hydration water in the dynamical transition of proteins. Biophys J 76(2):1034–1042
Fitter J, Lechner RE, Bueldt G, Dencher NA (1996) Internal molecular motions of bacteriorhodopsin: hydration-induced flexibility studied by quasielastic incoherent neutron scattering using oriented purple membranes. Proc Natl Acad Sci USA 93:7600–7605
Fitter J, Verclas SAW, Lechner RE, Seelert H, Dencher NA (1998) Function and picosecond dynamics of bacteriorhodopsin in purple membrane at different lipidation and hydration. FEBS Lett 433:321–325
Fitter J, Lechner RE, Dencher NA (1999) Interactions of hydration water and biological membranes studied by neutron scattering. J Phys Chem B 103:8036–8050
Gabel F, Bicout D, Lehnert U, Tehei M, Weik M, Zaccai G (2002) Protein dynamics studied by neutron scattering. Q Rev Biophys 35:327–367
Garbers A, Kurreck J, Reifarth F, Renger G, Parak F (1998) Correlation between protein flexibility and electron transfer from Q •−A to QB in PS II membrane fragments from spinach. Biochemistry 37:11399–11404
Hughes JL, Smith P, Pace R, Krausz E (2006) Charge separation in photosystem II core complexes induced by 690–730 nm excitation at 1.7 K. Biochim Biophys Acta 1757(7):841–851
Joliot P, Joliot A (1973) Different types of quenching involved in photosystem II centers. Biochim Biophys Acta 305:302–316
Kaminskaya O, Renger G, Shuvalow VA (2003) Effect of dehydration on light induced reactions in photosystem II: photoreactions of cytochrome b559. Biochemistry 42:8119–8132
Ke B (2001) Photosynthesis: photobiochemistry and photobiophysics. Kluwer, Dordrecht
Kneller G (2005) Quasielastic neutron scattering and relaxation processes in proteins: analytical and simulation-based models. Phys Chem Chem Phys 7:2641–2655
Koike H, Inoue Y (1987) Temperature dependence of the S-state transitions in a thermophilic cyanobacterium measured by thermoluminescence. In: Biggins J (ed) Progress in photosynthesis research, vol I. Martinus Nijhoff, Dordrecht, pp 645–648
Kok B, Forbush B, McGloin M (1970) Cooperation of charges in photosynthetic O2 evolution. I. A linear four step mechanism. Photochem Photobiol 11:457–476
Lancaster CRD (2007) Structures of reaction centers in anoxygenic bacteria. In: Renger G (ed) Primary processes of photosynthesis: basic principles and apparatus, vol II. Reaction centers/photosystems, electron transport chains, photophosphorylation and evolution. Royal Society of Chemistry, Cambridge, pp 5–56
Lechner RE, Riekel C (1983) Neutron scattering and muon spin rotation. Springer, Heidelberg
Lechner RE, Melzer R, Fitter J (1996) First QINS results from the TOF-spectrometer NEAT. Physica B 226:86–91
Lehnert U, Reat V, Weik M, Zaccai G, Pfister C (1998) Thermal motions in bacteriorhodopsin at different hydration levels studied by neutron scattering. Biophys J 75:1945–1952
Loll B, Kern J, Sänger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438:1040–1044
Marconi M, de Francesco A, Cornicchi E, Onori G, Paciaroni A (2005) Hydration and temperature dependent dynamics of lysozyme in glucose–water matrices. A neutron scattering study. Chem Phys 317:274–281
Mulkidjanian AY, Kozlova MA, Cherepanov DA (2005) Ubiquinone reduction in the photosynthetic reaction centre of Rhodobacter sphaeroides: interplay between electron transfer, proton binding and flips of the quinone ring. Biochem Soc Trans 33(4):845–850
Natali F, Relini A, Gliozzi A, Rolandi R, Cavatorta P, Deriu A, Fasano A, Riccio P (2004) The influence of the lipid–protein interaction on the membrane dynamics. Physica B 350:623–626
Noguchi T, Sugiura M (2002) Flash-induced FTIR difference spectra of the water oxidizing complex in moderately hydrated photosystem II core films: effect of hydration extent on S-state transitions. Biochemistry 41:2322–2330
Paciaroni A, Orecchini A, Cinelli S, Onori G, Lechner RE, Pieper J (2003) Protein dynamics on the picosecond timescale as affected by the environment: a quasielastic neutron scattering study. Chem Phys 292:397–404
Parak F, Frolov EN, Kononenko AA, Mössbauer R, Goldansky VI, Rubin AB (1980) Evidence for a correlation between the photoinduced electron transfer and dynamic properties of the chromatophore membranes from Rhodospirillum rubrum. FEBS Lett 17:368–372
Petrouleas V, Crofts AR (2005) The iron–quinone acceptor complex. In: Wydrzynski T, Satoh K (eds) Photosystem II: the water/plastoquinone oxido-reductase in photosynthesis. Kluwer, Dordrecht, pp 177–206
Pieper J, Hauß T, Buchsteiner A, Baczynski K, Adamiak K, Lechner RE, Renger G (2007) Temperature- and hydration-dependent protein dynamics in photosystem II of green plants studied by quasielastic neutron scattering. Biochemistry 46(40):11398–11409
Reifarth F, Renger G (1998) Indirect evidence for structural changes coupled with Q •−B formation in photosystem II. FEBS Lett 428:123–126
Remy A, Gerwert K (2003) Coupling of light-induced electron transfer to proton uptake in photosynthesis. Nat Struct Biol 10:637–644
Renger G, Gleiter HM, Haag E, Reifarth F (1993) Photosystem II: thermodynamics and kinetics of electron transport from Q a to Q b and deleterious effects of copper (II). Z Naturforsch 48c:234–240
Renger G (2001) Photosynthetic water oxidation to molecular oxygen: apparatus and mechanism. Biochim Biophys Acta 1503:210–228
Renger G (2007) Functional pattern of photosystem II in oxygen evolving organisms. In: Renger G (ed) Primary processes of photosynthesis: basic priniciples and apparatus, vol II. Reaction centers/photosystems, electron transport chains, photophosphorylation and evolution. Royal Society of Chemistry, Cambridge, pp 237–290
Renger G, Holzwarth AR (2005) Primary electron transfer. In: Wydrzynski T, Satoh K (eds) Photosystem II: the water/plastoquinone oxido-reductase in photosynthesis. Kluwer, Dordrecht, pp 139–175
Renger G, Eckert H-J, Bergmann A, Bernarding J, Liu B, Napiwotzki A, Reifahrt F, Eichler H-J (1995) Fluorescence and spectroscopic studies of exciton trapping and electron transfer in photosystem II of higher plants. Aust J Plant Physiol 22:167–181
Roh JH, Novikov VN, Gregory RB, Curtis JE, Chowdhuri Z, Sokolov AP (2005) Onsets of anharmonicity in protein dynamics. Phys Rev Lett 95:038101
Rufflè B (2000) Fitmo user manual. Hahn-Meitner-Institut Berlin, Germany
Sears VF (1967) Cold neutron scattering by a molecular liquid. III. Methane. Can J Phys 45:237–254
Smith JC, (1991) Protein dynamics: comparison of simulations with inelastic neutron scattering experiments. Q Rev Biophys 24:1–65
Stowell MHB, McPhilips TM, Rees DC, Soltis SM, Abresch E, Feher G (1997) Light-induced structural changes in photosynthetic reaction center: implications for mechanism of electron–proton transfer. Science 276:812–816
Styring S, Rutherford AW (1988) Deactivation kinetics and temperature dependence of the S-state transitions in the oxygen-evolving system of photosystem II measured by EPR spectroscopy. Biochim Biophys Acta 933:378–387
Völker M, Ono T, Inoue Y, Renger G (1985) Effect of trypsin on PS II particles. Correlation between Hill-activity, Mn-abundance and peptide pattern. Biochim Biophys Acta 767:548–556
Xu Q, Baciou L, Sebban P, Gunner MR (2002) Exploring the energy landscape for Q −A to QB electron transfer in bacterial photosynthetic reaction centers. Biochemistry 41:10021–10025
Acknowledgments
Financial support by Deutsche Forschungsgemeinschaft (SFB 429, TP A1) is gratefully acknowledged. We are also grateful to S. Kussin and M. Weß (TU Berlin) for their help in sample preparation as well as to G. Steiner and B. Urban (HMI Berlin) for technical assistance during the neutron scattering experiments.
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Advanced neutron scattering and complementary techniques to study biological systems. Contributions from the meetings, “Neutrons in Biology”, STFC Rutherford Appleton Laboratory, Didcot, UK, 11–13 July and “Proteins At Work 2007”, Perugia, Italy, 28–30 May 2007.
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Pieper, J., Hauß, T., Buchsteiner, A. et al. The effect of hydration on protein flexibility in photosystem II of green plants studied by quasielastic neutron scattering. Eur Biophys J 37, 657–663 (2008). https://doi.org/10.1007/s00249-008-0297-9
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DOI: https://doi.org/10.1007/s00249-008-0297-9