Temperature- and hydration-dependent protein dynamics in photosystem II of green plants studied by quasielastic neutron scattering

Biochemistry

Volumn 46, Issue 40, 2007, Pages 11398-11409

  Pieper, Jörg ^a   Hauss, Thomas ^b   Buchsteiner, Alexandra ^c   Baczyński, Krzysztof ^d   Adamiak, Karolina ^d   Lechner, Ruep E ^b   Renger, Gernot ^a  

^a TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

^b DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^c HAHN MEITNER INSTITUT   (Germany)

^d ADAM MICKIEWICZ UNIVERSITY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

ELECTRON TRANSPORT PROPERTIES; HYDRATION; NEUTRON SCATTERING; PLANTS (BOTANY); THERMAL EFFECTS; VIBRATION ANALYSIS;

PROTEIN DYNAMICS; TEMPERATURE RANGE; VIBRATIONAL MOTIONS; WATER-OXIDIZING COMPLEX;

PROTEINS;

ARTICLE; ELECTRON TRANSPORT; HYDRATION; NEUTRON SCATTERING; NONHUMAN; OXIDATION; PHOTOSYSTEM II; PLANT; PRIORITY JOURNAL; QUASIELASTIC NEUTRON SCATTERING; SPINACH; TEMPERATURE DEPENDENCE; WATER CONTENT;

KINETICS; NEUTRONS; PHOTOSYSTEM II PROTEIN COMPLEX; PLANT PROTEINS; SCATTERING, RADIATION; SPINACIA OLERACEA; TEMPERATURE; THERMODYNAMICS; WATER;

SPINACIA OLERACEA; VIRIDIPLANTAE;

EID: 35048839174     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi700179s     Document Type: Article

References (92)

1. Ke, B. (2001) Photosynthesis: Photobiochemistry and Photobiophysics, Kluwer Academic Publishers, Dordrecht, The Netherlands.
2. Renger, G., and Holzwarth, A.R. (2005) Primary Electron Transfer, in Photosystem II: The Water/Plastoquinone Oxido-Reductase in Photosynthesis (Wydrzynski, T., and Satoh, K., Eds.) pp 139-175, Kluwer Academic Publishers, Dordrecht, The Netherlands.
3. - in different photosystem II preparations from higher plants, Photochem. Photobiol. 59, 566-573.
4. Petrouleas, V., and Crofts, A.R. (2005) The Iron-Quinone Acceptor Complex, in Photosystem II: The Water/Plastoquinone Oxido-Reductase in Photosynthesis (Wydrzynski, T., and Satoh, K., Eds.) pp 177-206, Kluwer Academic Publishers, Dordrecht, The Netherlands.
5. 2 evolution. I. A linear four step mechanism, Photochem. Photobiol. 11, 457-476.
6. Ferreira, K., Iverson, T. M., Maghlouni, K., Barber, J., and Iwata, S. (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303, 1831-1838.
7. Loll, B., Kern, J., Sänger, W., Zouni, A., and Biesiadka, J. (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II, Nature 438, 1040-1044.
8. Hughes, J. L., Smith, P., Pace, R., and Krausz, E. (2006) Charge separation in photosystem II core complexes induced by 690-730 nm excitation at 1.7 K, Biochim. Biophys. Acta 1757, 841-851.
9. Joliot, P., and Joliot, A. (1973) Different types of quenching involved in Photosystem II centers, Biochim. Biophys. Acta 305, 302-316.
10. Renger, G. (1993) Water cleavage by solar radiation: an inspiring challenge of photosynthesis research, Photosynth. Res. 38, 229-247.
11. B in PS II membrane fragments from spinach, Biochemistry 37, 11399-11404.
12. -• formation in Photosystem II, FEBS Lett. 428, 123-126.
13. Koike, H., and Inoue, Y. (1987) Temperature Dependence of the S-State Transitions in a Thermophilic Cyanobacterium Measured by Thermoluminescence, in Progress in Photosynthesis Research (Biggins, J., Ed.) Vol. I, pp 645-648, Martinus Nijhoff, Dordrecht, The Netherlands.
14. Styring, S., and Rutherford, A. W. (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.
15. Gleiter, H. M., Haag, E., Inoue, Y., and Renger, G. (1993) New results on the functional properties of a photosystem II core complex preparation from spinach, Photosynth. Res. 35, 41-53.
16. Kaminskaya, O., Renger, G., and Shuvalow, V. A. (2003) Effect of dehydration on light induced reactions in Photosystem II: photoreactions of cytochrome b559, Biochemistry 42, 8119-8132.
17. Noguchi, T., and 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.
18. Clayton, R. K. (1978) Effects of dehydration on reaction centers from Rhodopseudomonas sphaeroides, Biochim. Biophys. Acta 504, 255-264.
19. Nikolaev, G. M., Knox, P. P., Kononenko, A. A., Grishanova, N. P., and Rubin, A. B. (1980) Photo-induced electron transport and water state in Rhodospirillum rubrum chromatophores, Biochim. Biophys. Acta 590, 194-201.
20. Palazzo, G., Mallardi, A., Hochkoeppler, A., Cordone, L., and Venturoli, G. (2002) Electron transfer kinetics in photosynthetic reaction centers embedded in trehalose glasses: trapping of conformational substates at room temperature, Biophys. J. 82, 558-568.
21. Berg, A. I., Knox, P. P., Kononenko, A. A., Frolov, E. N.., Khrymova, I. N., Rubin, A. B., Likhtenstein, G. I., Goldansky, V. I., Parak, F., Bukl, M., and Mössbauer, R. (1979) Conformational regulation of the functional activity of photosynthetic membranes of purple bacteria, Mol. Biol. 13, 81-89.
22. Parak, F., Frolov, E. N., Kononenko, A. A., Mössbauer, R., Goldansky, V. I., and Rubin, A. B. (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.
23. Mc Mahon, B. H., Müller, J. D., Wraight, C. A., and Nienhaus, G. U. (1998) Electron transfer and protein dynamics in the photosynthetic reaction center, Biophys. J. 74, 2567-2587.
24. Fitter, J., Lechner, R. E., and Dencher, N. A. (1999) Interactions of hydration water and biological membranes studied by neutron scattering, J. Phys. Chem. B 103, 8036-8050.
25. Gabel, F., Bicout, D., Lehnert, U., Tehei, M., Weik, M., and Zaccai, G. (2002) Protein dynamics studied by neutron scattering, Q. Rev. Biophys. 35, 327-367.
26. Kneller, G. (2005) Quasielastic neutron scattering and relaxation processes in proteins: analytical and simulation-based models, Phys. Chem. Chem. Phys. 7, 2641-2655.
27. Smith, J. C. (1991) Protein dynamics: comparison of simulations with inelastic neutron scattering experiments, Q. Rev. Biophys. 24, 1-65.
28. Middendorf, H. D., Hayward, R. L., Parker, S. F., Bradshaw, J., and Miller, A. (1995) Vibrational neutron spectroscopy of collagen and model polypeptides. Biophys. J. 69, 660-673.
29. Doster, W., Cusack, S., and Petry, W. (1989) Dynamical transition of myoglobin revealed by inelastic neutron scattering, Nature 337, 754-756.
30. Natali, F., Relini, A., Gliozzi, A., Rolandi, R., Cavatorta, P., Deriu, A., Fasano, A., and Riccio, P. (2004) The influence of the lipid-protein interaction on the membrane dynamics, Physica B 350, 623-626.
31. Paciaroni, A., Orecchini, A., Cinelli, S., Onori, G., Lechner, R. E., and Pieper, J. (2003) Protein dynamics on the picosecond timescale as affected by the environment: a quasielastic neutron scattering study, Chem. Phys. 292, 397-404.
32. 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, 1034-1042.
33. Cordone, L., Ferrand, M., Vitrano, E., and Zaccai, G. (1999) Harmonic behavior of trehalose-coated carbon-monoxy-myoglobin at high temperature, Biophys. J. 76, 1043-1047.
34. Tsai, A. M., Neumann, D. A., and Bell, L. N. (2000) Molecular dynamics of solid-state lysozyme as affected by glycerol and water: a neutron scattering study, Biophys. J. 79, 2728-2732.
35. Paciaroni, A., Cinelli, S., and Onori, G. (2002) Effect of the environment on the protein dynamical transition: a neutron scattering study, Biophys. J. 83, 1157-1164.
36. Marconi, M., de Francesco, A., Cornicchi, E., Onori, G., and Paciaroni, A. (2005) Hydration and temperature dependent dynamics of lysozyme in glucose-water matrices. A neutron scattering study, Chem. Phys. 317, 274-281.
37. Caliskan, G., Briber, R. M., Thirumalai, D., Garcia-Sakai, V., Woodson, S. A., and Sokolov, A. P. (2006) Dynamic transition in tRNA is solvent induced, J. Am. Chem. Soc. 128, 32-33.
38. Dellerue, S., and Bellissent-Funel, M.-C. (2000) Relaxational dynamics of water molecules at protein surfaces, Chem. Phys. 258, 315-325.
39. Pieper, J., Charalambopoulou, G., Steriotis, T., Vasenkov, S., Desmedt, A., and Lechner, R. E. (2003) Water diffusion in fully hydrated porcine stratum corneum, Chem. Phys. 292, 465-471.
40. Teixeira, J., Bellissent-Funel, M.-C., Chen., S. H., and Dianoux, A. J. (1985) Experimental determination of the nature of diffusive motions of water molecules at low temperatures, Phys. Rev. A 31, 1913-1917.
41. Lechner, R. E., Fitter, J., Dencher, N. A., and Hauss, T. Low-energy dynamics and biological function, Physica B, 385-386, 835-837.
42. Berthold, D. A., Babcock, G. T., and Yocum, C. F. (1981) A highly resolved, oxygen-evolving photosystem II preparation from spinach thylakoid membranes: EPR and electron-transport properties, FEBS Lett. 134, 231-234.
43. Völker, M., Ono, T., Inoue, Y., and 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.
44. + 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.
45. Z in photosystem II with intact oxygen evolution capacity. Analysis of kinetic H/D isotope exchange effects, Biochemistry 38, 2068-2077.
46. Renger, G., Eckert, H.-J., Bergmann, A., Bernarding, J., Liu, B., Napiwotzki, A., Reifahrt, F., and 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.
47. Lechner, R. E. (1992) Optimization of the chopper system for the cold-neutron time-of-flight spectrometer NEAT at the HMI-Berlin. Physica B 180-181, 973-977.
48. Lechner, R. E., Melzer, R., and Fitter, J. (1996) First QINS results from the TOF-spectrometer NEAT, Physica B 226, 86-91.
49. Rufflè, B. (2000) Fitmo User Manual, Hahn-Meitner-Institut Berlin, Germany.
50. Lechner, R. E., and Riekel, C. (1983) Neutron Scattering and Muon Spin Rotation, Springer-Verlag, Berlin, Germany.
51. Bee, M. (1988) Quasielastic Neutron Scattering: Principles and Applications in Solid State Chemistry, Biology Materials Science, Adam & Hilger, Philadelphia, PA.
52. -1.
53. Sears, V. F. (1967) Cold neutron scattering by a molecular liquid. III.-Methane, Can. J. Phys. 45, 237-254.
54. Volino, F., and Dianoux, A. (1980) Neutron incoherent scattering law for diffusion in a potential of spherical symmetry, Mol. Phys. 41, 271-279.
55. Williams, G., and Watts, D. (1969) Non-symmetrical dielectric relaxation behavior arising from a simple empirical decay function, Trans. Faraday. Soc. 66, 80-85.
56. Metzler, R., and Klafter, J. (2000) The random walks guide to anomalous diffusion: a fractional dynamics approach, Phys. Rep. 339, 1-77.
57. Hinsen, K., Petrescu, A.-J., Dellerue, S., Bellissent-Funel, M.-C., and Kneller, G. R. (2000) Harmonicity in slow protein dynamics, Chem. Phys. 261, 25-37.
58. Kneller, G. R. (2000), Inelastic neutron scattering from damped collective vibrations of macromolecules, Chem. Phys. 261, 1-24.
59. Lovesey, S. (1984) in Theory of Neutron Scattering from Condensed Matter, p 301, Clarendon Press, Oxford, U.K.
60. 4He, Phys. Rev. B 19, 1458-1462.
61. Teixeira, J., Bellissent-Funel, M.-C., Chen, S. H., and Dorner, B. (1985), Observation of new short-wavelength collective excitations in heavy water by coherent inelastic neutron scattering, Phys. Rev. Lett. 54, 2681-2683.
62. Longeville, S., and Lechner, R. E. (2000) Light- and heavy-water dynamics, Physica B 276-278, 183-184.
63. Dunahay, T. G., Staehelin, L. A., Seibert, M., Ogilvie, P. D., and Berg, S. P. (1984) Structural, biochemical and biophysical characterization of four oxygen-evolving photosystem II preparations from spinach, Biochim. Biophys. Acta 764, 179-193.
64. Shi, L.-X., and Schröder, W. P. (2004) The low molecular mass subunits of the photosynthetic supracomplex, photosystem II. Biochim. Biophys. Acta 1608, 75-96.
65. Dekker, J. P., and Boekema, E. J. (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim. Biophys. Acta 1706, 12-39.
66. Lehnert, U., Reat, V., Weik, M., Zaccai, G., and Pfister, C. (1998) Thermal motions in bacteriorhodopsin at different hydration levels studied by neutron scattering, Biophys. J. 75, 1945-1952.
67. Fitter, J., Lechner, R. E., Bueldt, G., and Dencher, N. A. (1996) Internal molecular motions of bacteriorhodopsin: hydrationinduced flexibility studied by quasielastic incoherent neutron scattering using oriented purple membranes, Proc. Natl. Acad. Sci. U.S.A. 93, 7600-7605.
68. Pieper, J., Irrgang, K.-D., Renger, G., and Lechner, R. E. (2004) Density of vibrational states of the light-harvesting complex II of green plants studied by inelastic neutron scattering, J. Phys. Chem. B 108, 10556-10565.
69. Pieper, J., Voigt, J., and Small, G. J. (1999) Chlorophyll a Franck-Condon factors and excitation energy transfer, J. Phys. Chem. B 103, 2319-2322.
70. Diehl, M., Doster, W., Petry, W., and Schober, H. (1997) Water-coupled low-frequency modes of myoglobin and lysozyme observed by inelastic neutron scattering, Biophys. J. 73, 2726-2732.
71. Orecchini, A., Paciaroni, A., Bizzani, A. R., and Cannistraro, S. (2002) Low-frequency vibrational anomalies in β-lactoglobulin: contribution of different hydrogen classes revealed by inelastic neutron scattering, J. Phys. Chem. B 106, 12150-12156.
72. Kurkal, V., Daniel, R. M., Finney, J. L., Tehei, M., Dunn, R. V., and Smith, J. C. (2005) Low-frequency enzyme dynamics as a function of temperature and hydration: a neutron scattering study, Chem. Phys. 317, 267-273.
73. Hayward, J. A., Daniel, R. M., Finney, J. L., and Smith, J. C. (2003) Use of computer simulation in the interpretation of elastic neutron scattering in complex molecular systems: a small protein in various environments, Chem. Phys. 292, 389-396.
74. Steinbach, P. J., Loncharich, R. J., and Brooks, B. R. (1991) The effects of environment and hydration on protein dynamics: a simulation study of myoglobin, Chem. Phys. 158, 383-394.
75. Kurkal, V., and Smith, J. C. (2006) Low-temperature protein dynamics: a simulation analysis of interprotein vibrations and the boson peak at 150 K, J. Am. Chem. Soc. 128, 2356-2364.
76. Roh, J. H., Novikov, V. N., Gregory, R. B., Curtis, J. E., Chowdhuri, Z., and Sokolov, A. P. (2005) Onsets of anharmonicity in protein dynamics, Phys. Rev. Lett. 95, 038101.
77. Curtis, J. E., Tarek, M., and Tobias, D. J. (2004) Methyl group dynamics as a probe of the protein dynamical transition, J. Am. Chem. Soc. 126, 15928-15929.
78. Pieper, J., Schödel, R., Irrgang, K.-D., Voigt, J., and Renger, G. (2001) Electron-phonon coupling in solubilized LHC II complexes of green plants investigated by line-narrowing and temperature dependent fluorescence spectroscopy, J. Phys. Chem. B 105, 7115-7124.
79. y-level structure and dynamics of solubilized light-harvesting complex II of green plants: pressure and hole burning studies, J. Phys. Chem. A 103, 2412-2421.
80. Rogl, H., Schödel, R., Lokstein, H., Kühlbrandt, W., and Schubert, A. (2002) Assignment of spectral substructures to pigment-binding sites in higher plant light-harvesting complex LHC-II, Biochemistry 41, 2281-2287.
81. Wu, H.-M., Rätsep, M., Jankowiak, R., Cogdell, R. J., and Small, G. J. (1997) Comparison of the LH2 antenna complexes of Rhodopseudomonas acidophila (Strain 10050) and Rhodobacter sphaeroides by high-pressure absorption, high-pressure hole burning, and temperature-dependent absorption spectroscopies, J. Phys. Chem. B 101, 7641-7653.
82. Hayes, J. M., and Small, G. J. (1978) Non-photochemical hole burning and impurity site relaxation processes in organic glasses, Chem. Phys. 27, 151-157.
83. Reddy, N. R. S., Lyle, P. A., and Small, G. J. (1992) Applications of spectral hole burning spectroscopies to antenna and reaction center complexes, Photosynth. Res. 31, 167-194.
84. Tietz, C., Jelezko, F., Gerken, U., Schuler, S., Schubert, A., Rogl, H., and Wrachtrup, J. (2001) Single molecule spectroscopy on the light-harvesting complex II of higher plants, Biophys. J. 81, 556-562.
85. Zanotti, J.-M., Bellissent-Funel, M.-C., and Parello, J. (1999) Hydration-coupled dynamics in proteins studied by neutron scattering and NMR: the case of the typical EF-hand calcium-binding parvalbumin, Biophys. J. 76, 2390-2411.
86. Stowell, M. H. B., McPhilips, T. M., Rees, D. C., Soltis, S. M., Abresch, E., and Feher, G. (1997) Light-induced structural changes in photosynthetic reaction center: implications for mechanism of electron-proton transfer, Science 276, 812-816.
87. B electron transfer in bacterial photosynthetic reaction centers, Biochemistry 41, 10021-10025.
88. Remy, A., and Gerwert, K. (2003) Coupling of light-induced electron transfer to proton uptake in photosynthesis, Nature Struct. Biol. 10, 637-644.
89. Breton, J. (2004) Absence of large-scale displacement of quinone QB in bacterial photosynthetic reaction centers, Biochemistry 43, 3318-3326.
90. Baxter, R. H. G., Ponomarenko, N., Srajer, V., Pahl, R., Moffat, K., and Norris, J. R. (2004) Time-resoved crystallographic studies of light-induced structural changes in the photosynthetic reaction center, Proc. Natl. Acad. Sci. U.S.A. 101, 5982-5987.
91. Mulkidjanian, A. Y., Kozlova, M. A., and Cherepanov, D. A. (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, 845-850.
92. Lancaster, C. R. D. (2007) Structures of Reaction Centers in Anoxygenic Bacteria, in Primary Processes of Photosynthesis: Basic Principles and Apparatus, Part 2: Reaction Centers/Photosystems, Electron Transport Chains, Photophosphorylation and Evolution (Renger, G., Ed.) pp 5-57, Royal Society of Chemistry, Cambridge, U.K.