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Temperature dependence of cytochrome photooxidation and conformational dynamics of Chromatium reaction center complexes

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Abstract

A temperature dependence of multiheme cytochrome c oxidation induced by a laser pulse was studied in photosynthetic reaction center preparations from Chromatium minutissimum. Absorbance changes and kinetic characteristics of the reaction were measured under redox conditions where one or all of the hemes of the cytochrome subunit are chemically reduced (E h =+300 mV or E h =−20 to -60 mV respectively). In the first case photooxidation is inhibited at temperatures lower than 190–200 K with the rate constant of the photooxidation reaction being practically independent on temperature over the range of 300 to 190 K (k=2.2×105 s-1). Under reductive conditions (E h =−20 to -60 mV) lowering the temperature to 190–200 K causes the reaction to slow from k=8.3×105 s-1 to 2.1×104 s-1. Under further cooling down to the liquid nitrogen temperature, the reaction rate changes negligibly. The absorption amplitude decreases by 30–40% on lowering the temperature. A new physical mechanism of the observed critical effects of temperature on the rate and absorption amplitude of the multiheme cytochrome c oxidation reaction is proposed. The mechanism suggests a close interrelation between conformational mobility of the protein and elementary electron tunneling act. The effect of “freezing” conformational motion is described in terms of a local diffusion along a random rough potential.

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References

  • Bartsch RG (1978) Cytochromes in the photosynthetic bacteria. In: Clayton RK and Sistrom WR (eds) The Photosynthetic Bacteria, pp 249–279. New York: Plenum Press

    Google Scholar 

  • Basovets SK, Uporov IV, Shaitan KV, Krupyanskii YuF, Kurinov IV, Suzdalev IP, Rubin AB and Goldanskii VI (1988) A method of Mössbauer Fourier spectroscopy for determination of the biopolimer coordinate correlation functions. Hyperfine Interactions 39: 369–378

    Google Scholar 

  • Basovets SK, Uporov IV, Shaitan KV, Krupyanskii YuF and Rochev VYa (1989) Estimation of spatial and temporary characteristics of motion in macromolecular systems from Mössbauer spectra over a wide range of times. Khim fizica 8, N5: in press (in Russian)

  • Bauminger ER, Cohen SG, Nowik I, Ofer S and Yariv J (1983) Dynamics of heme iron in crystals of metmyoglobin and deoxymyoglobin. Proc Natl Acad Sci USA 80: 736–740

    Google Scholar 

  • Bixon M and Jortner J (1986) On the mechanism of cytochrome oxidation in bacterial photosynthesis. FEBS Lett 200: 303–308

    Google Scholar 

  • Case GD, Parson WW and Thornber JP (1970) Photo-oxidation of cytochromes in reaction center preparations from C. vinosum and Rps. viridis. Biochim Biophys Acta 223: 122–128

    Google Scholar 

  • Case PA and Karplus M (1979) Dynamics of ligand binding to heme proteins. J Mol Biol 135: 343–368

    Google Scholar 

  • Chamorovsky SK, Pyt'eva NF and Rubin AB (1977) Lightinduced electron transport reactions in C. minutissimum chromatophores poised at different redox potentials. Studia biophysica 66: 129–143

    Google Scholar 

  • Chamorovsky SK, Kononenko AA, Remennikov SM and Rubin AB (1980) The oxidation rate of high-potential c-type cytochrome in the photochemical reaction is temperature independent. Biochim Biophys Acta 589: 151–155

    Google Scholar 

  • Chamorovsky SK, Kononenko AA, Petrov EG, PottosinII and Rubin AB (1986) Effects of dehydration and low temperatures on the oxidation of high-potential cytochrome c by photosynthetic, reaction centers in Ectothiorhodospira shaposhnikovii. Biochim Biophys Acta 849: 402–410

    Google Scholar 

  • Chamorovsky SK, Sabo Ya and Brown L (1989) The automation pulsed laser spectrophotometer to investigate processes of a photoinduced charge transfer in photosynthesis. Biol Nauki (USSR) 6

  • Chance B (1974) The function of cytochromes. Ann NY Acad Sci 222: 613–626

    Google Scholar 

  • Chance B and Nishimura M (1960) On the mechanism of chlorophyll cytochrome interaction: The temperature insensitivity of light-induced cytochrome oxidation in C. vinosum. Proc Natl Acad Sci USA 46: 19–24

    Google Scholar 

  • Deisenhofer J, Epp O, Miki K, Huber R and Michel H (1984) X-ray structure analysis of a membrane protein complex. Electron density map at 3 Å resolution and a model of the chromophores of the photosynthetic reaction center from Rhodopseudomonas viridis. J Mol Biol 180: 385–398

    Google Scholar 

  • Deisenhofer J, Epp O, Miki K, Huber R and Michel H (1985) Structure of the protein subunits in the photosynthetic reaction center from Rhodopseudomonas viridis at 3 Å resolution. Nature 318: 618–624

    Google Scholar 

  • DeVault D and Chance B (1966) Studies of photosynthesis using a pulsed laser. I. Temperature dependence of cytochrome oxidation rate in Chr. vinosum. Evidence for tunneling. Biophys J 6: 825–847

    Google Scholar 

  • Dogonadze RR and Kuznetsov AM (1973) Electron-transfer reactions in polar solvents. Itogi nauki, Ser Fiz Chim Kinetika Vol 2, p. 209. Moscow: VINITI (in Russian)

    Google Scholar 

  • Dracheva SM, Drachev LA, Konstantinov AA, Semenov A Yu, Skulachev VP, Arutjunjan AM, Shuvalov VA and Zaberezhnaya SM (1988) Electrogenic steps in the redox reactions catalysed by photosynthetic reaction centre complex from Rhodopseudomonas viridis. Eur J Biochem 171: 253–264

    Google Scholar 

  • Dutton PL (1971) Oxidation-reduction potential dependence of the interactions of cytochromes, bacteriochlorophyll and carotenoides at 77 K in chromatophores of C. vinosum and Rps. gelatinosa. Biochim Biophys Acta 226: 63–80

    Google Scholar 

  • Dutton PL, Kihara T, McCray JA and Thornber JP (1971) Cytochrome c 553 and bacteriochlorophyll interaction at 77 K in chromatophores and sub-chromatophore preparation in C. vinosum. Biochim Biophys Acta 226: 81–87

    Google Scholar 

  • Dutton PL and Prince RC (1978) Reaction center-driven cytochrome interactions in electron and proton translocation and energy coupling. In: Clayton RK and Sistrom WR (eds) The Photosynthetic Bacteria, pp 525–570. New York: Plenum Press

    Google Scholar 

  • Frauenfelder H, Petsko GA and Tsernoglou D (1979) Temperature dependent X-ray diffraction as a probe of protein structural dynamics. Nature 280: 558–563

    Google Scholar 

  • Gardiner CW (1985) Handbook of Stochastic Methods. Berlin, Heidelberg: Springer-Verlag

    Google Scholar 

  • Gavish B and Werber MM (1979) Viscosity dependent structural fluctuations in enzyme catalysis. Biochemistry 18: 1269–1275

    Google Scholar 

  • Hales BJ (1976) Temperature dependence of the rate of electron transport as a monitor of protein motion. Biophysical J 16: 471–480

    Google Scholar 

  • Himmelblau D (1973) Statistical Analysis of Processes. Moscow: MIR Publishers (in Russian)

    Google Scholar 

  • Jortner J (1980) Dynamics of electron transfer in bacterial photosynthesis. Biochim Biophys Acta 594: 193–230

    Google Scholar 

  • Jortner J and Bixon M (1987) Charge exchange between localized sites. In: Austin R, Bunks E, Chance B, DeVault D, Dutton PL, Frauenfelder H and Goldanskii VI (eds) Protein Structure. Molecular and Electronic Reactivity, pp 277–308. New York: Springer-Verlag

    Google Scholar 

  • Kaminskaya OP, Shkuropatova VA, Shuvalov VA and Konstantinov AA (1989) Biol Nauki (USSR) (in press)

  • Kestner NR, Logan J and Jortner J (1974) Thermal electron transfer reactions in polar solvents. J Phys Chem 78: 2148–2166

    Google Scholar 

  • Kihara T and Chance B (1969) Cytochrome photooxidation at liquid nitrogen temperature in photosynthetic bacteria. Biochim Biophys Acta 189: 116–124

    Google Scholar 

  • Knapp EW, Fischer SF and Parak F (1983) The influence of protein dynamics on Mössbauer spectra. J Chem Phys 78: 4701–4711

    Google Scholar 

  • Knapp EW and Fischer SF (1987) Electron transfer and protein dynamics. J Chem Phys 87: 3880–3887

    Google Scholar 

  • Krupyanskii YuF, Bade D, Sharkevich IV, Uspenskaya NYa, Kononenko AA, Suzdalev IV, Parak F, Goldanskii VI, Mössbauer PL and Rubin AB (1985) The mobility of chromatophore membranes from Ectothiorhodospira shaposhnikovii revealed by Rayleigh scattering of Mössbauer radiation (RSMR) experiments. Eur Biophys J 12: 107–114

    Google Scholar 

  • Krupyanskii YuF, Shaitan KV, Goldanskii VI, Kurinov IV, Rubin AB and Suzdalev IP (1987) Study of protein dynamics by Mössbauer spectroscopy methods. Biofizika 32: 761–774

    Google Scholar 

  • Kuhn H (1986) Electron transfer mechanism in the reaction center of photosynthetic bacteria. Phys Rev A 34: 3409–3425

    Google Scholar 

  • Kuznetsov AM, Sondergard NC and Ulstrup J (1978) Lowtemperature electron transfer in bacterial photosynthesis. Chem Phys 29: 383–390

    Google Scholar 

  • Marcus RA and Sutin N (1985) Electron transfer in chemistry and biology. Biochim Biophys Acta 811: 265–322

    Google Scholar 

  • Michel-Beyerle ME, Plato M, Deisenhofer J, Michel H, Bixon M and Jortner J (1988) Unidirectionality of charge separation in reaction centers of photosynthesis bacteria. Biochim Biophys Acta 932: 52–70

    Google Scholar 

  • Nitscke W and Rutherford AW (1989) The tetraheme cytochrome c subunit of Rhodopseudomonas viridis characterised by EPR. Biochemistry (in press)

  • Rips I and Jortner J (1987) Dynamic solvent effects on outersphere electron transfer. J Chem Phys 87: 2090–2104

    Google Scholar 

  • Rubin AB, Kononenko AA and Shaitan KV (1987) The electron-conformation interactions in photosynthesis. Itogi nauki, Ser Biofizika Vol 21, 160 p. Moscow: VINITI (in Russian)

    Google Scholar 

  • Sabo Ya, Zakharova NI, Chamorovsky SK, Uspenskaya NYa and Kononenko AA (1989) Isolation procedure and characteristics of cytochrome c containing photosynthetic reaction center complexes from chromatophores of Chromatium minutissimum. Dokl AN USSR (in Russian) 305, N 3: 732–735

    Google Scholar 

  • Sarai A and De Vault D (1983) Temperature dependence of high-potential cytochrome photo-oxidation in C. vinosum. In: Abstr of 6th Intern Congr on Photosynthesis, Vol 2, p 430, Brussels

  • Seibert M and DeVault D (1970) Relationship between the laser-induced oxidation of the high and low potential cytochromes of C. vinosum. Biochim Biophys Acta 205: 222–231

    Google Scholar 

  • Seibert M (1971) Spectral, kinetic and potentiometric studies of the laser induced primary photochemical reactions in the photosynthetic bacterium C. vinosum. PhD thesis, Univ. Pennsylvania, Philadelphia

  • Shaitan KV and Rubin AB (1980) Conformational mobility and Mössbauer effects in biological system. Brownian motion damped oscillator for conformation modes. Mol Biol 14: 1046–1058

    Google Scholar 

  • Shaitan KV and Rubin AB (1982) Conformon equation and primitive molecular machines for electron transport in biological objects. Mol Biol 16: 794–807

    Google Scholar 

  • Shaitan KV and Uporov IV (1986) Stochastic dynamics of a system of N-bound Brownian oscillators and Mössbauer effect in proteins. Khim fizika 5: 8–12 (in Russian)

    Google Scholar 

  • Shopes RJ, Levine LM, Holten D and Wraight CA (1987) Kinetics of oxidation of the bound cytochromes in reaction centers from Rhodopseudomonas viridis. Photosynth Res 12: 165–180

    Google Scholar 

  • Uporov IV, Basovets SK, Shaitan KV, Makarov EF and Rochev VYa (1989) Dynamic properties of human serum albumin over a wide range of temperatures, as determined by Mössbauer Fourier spectroscopy. Khim fizika 8 (in press) (in Russian)

  • Vredenberg WY and Duysens LNM (1964) Light induced oxidation of cytochromes in photosynthetic bacteria between 20° and -170°. Biochim Biophys Acta 76: 456–463

    Google Scholar 

  • Welch GR, Somogyi B and Damjanovich S (1982) The role of protein fluctuations in enzyme action. Progr Biophys Mol Biol 39: 109–146

    Google Scholar 

  • Weyer KA, Lottspeich F, Shafer W and Michel H (1987) The fatty acid-anchored four heme cytochrome of the photosynthetic reaction center from the purple bacterium Rhodospeudomonas viridis. In: Papa S, Chance B, Ernster L (eds) Cytochrome Systems. Molecular Biology and Bioenergetics, pp 325–331. New York: Plenum Press

    Google Scholar 

  • Zusman LD (1988) The theory of electron transfer reactions in solvents with two characteristic relaxation times. Chem Phys 119: 51–61

    Google Scholar 

  • Zwanzig R (1988) Diffusion in a rough potential. Proc Natl Acad Sci USA 85: 2029–2030

    Google Scholar 

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Authors and Affiliations

  1. Department of Biophysics, Faculty of Biology, M.V. Lomonosov State University, 119899, Moscow, U.S.S.R.

    Andrew B. Rubin, Konstantin V. Shaitan, Alexander A. Kononenko & Sergey K. Chamorovsky

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  1. Andrew B. Rubin
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  2. Konstantin V. Shaitan
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  3. Alexander A. Kononenko
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  4. Sergey K. Chamorovsky
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Rubin, A.B., Shaitan, K.V., Kononenko, A.A. et al. Temperature dependence of cytochrome photooxidation and conformational dynamics of Chromatium reaction center complexes. Photosynth Res 22, 219–231 (1989). https://doi.org/10.1007/BF00048301

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  • DOI: https://doi.org/10.1007/BF00048301

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