Abstract
Persistent photochemical hole burned profiles are reported for the primary electron donor state P700 of the reaction center of PS I. The hole profiles at 1.6 K for a wide range of burn wavelengths (λB) are broad (FWHM∼310 cm-1) and for the 45:1 enriched particles studied exhibit no sharp zero-phonon hole feature coincident with λB. The λB hole profiles are analyzed using the theory of Hayes et al. [J Phys Chem 1986, 90: 4928] for hole burning in the presence of arbitrarily strong linear electron-phonon coupling. A Huang-Rhys factor S in the range 4–6 and a corresponding mean phonon frequency in the range 35–50 cm-1 together with an inhomogeneous line broadening of∼100 cm-1 are found to provide good agreement with experiment. The zero-point level of P700* is predicted to lie at∼710 nm at 1.6K with an absorption maximum at∼702 nm. The hole spectra are discussed in the context of the hole spectra for the primary electron donor states of PS II and purple bacteria.
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Abbreviations
- NPHB:
-
nonphotochemical hole burning
- O.D.:
-
optical density
- PSBH:
-
phonon sideband hole
- PS I:
-
Photosystem I P680
- P700, P870, P960:
-
the primary electron donors of Photosystem II, Photosystem I, Rhodobacter sphaeroides, Rhodopseudomonas viridis
- PED:
-
primary electron donor
- RC:
-
reaction center
- ZPH:
-
zero-phonon holes
References
Allen JP, Feher G, Yeates TO, Rees DC, Deisenhofer J, Michel H and Huber R (1986) Structural homology of reaction centers from Rhodopseudomonas sphaeroides and Rhodopseudomonas viridis as determined by X-ray diffraction. Proc Natl Acad Sci USA 83: 8589–8593
Allen JP, Feher G, Yeates TO, Komiya H and Rees DC (1987a) Structure of the reaction center from Rhodobacter sphaeroides R-26: the cofactors. Proc Natl Acad Sci USA 84: 5730–5734
Allen JP, Feher G, Yeates TO, Komiya H and Rees DC (1987b) Structure of the reaction center from Rhodobacter sphaeroides R-26: the protein subunits. Proc Natl Acad Sci USA 84: 6161–6166
Allen JP, Feher G, Yeates TO, Komiya H and Rees DC (1988) Structure of the reaction center from Rhodobacter sphaeroides R-26: protein-cofactor (quinones and Fe2+) interactions. Proc Natl Sci USA 85: 8487–8491
Bearden AJ and Malkin R (1972) Quantitative EPR studies of the primary reaction of photosystem I in chloroplasts. Biochim Biophys Acta 283: 456–468
Boxer SG, Lockhart DJ and Middendorf TR (1986a) Photochemical hole burning in photosynthetic reaction centers. Chem Phys Lett 123: 476–482
Boxer SG, Middendorf TR and Lockhart DJ (1986b) Reversible photochemical hole burning in Rhodopseudomonas viridis reaction centers. FEBS Lett 200: 237–241
Braun HP, Michel-Beyerle ME, Breton J, Buchanan S and Michel H (1987) Electric field effect on absorption spectra of reaction centers of Rb. sphaeroides and Rps. viridis. FEBS Lett 221: 221–225
Breton J, Martin J-L, Fleming GR and Lambry J-C (1988) Low-temperature femtosecond spectroscopy of the initial steps of electron transfer in reaction centers from photosynthetic purple bacteria. Biochemistry 27: 8276–8284
Chang CH, Tiede D, Tang J, Smith U, Norris J and Schiffer M (1986) Structure of Rhodopseudomonas sphaeroides R-26 reaction center. FEBS Lett 205: 82–86
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
Deisenhofer J, Epp O, Miki K, Huber R and Michel H (1985) Structure of the protein subunits in the photosynthetic reaction center of Rhodopseudomonas viridis. Nature (London) 318: 618–624
Fenton JM, Pellin MJ, Govindjee and Kaufmann KJ (1979) Primary photochemistry of the reaction center of photosystem I. FEBS Lett 100: 1–4
Fearey BL, Carter TP and Small GJ (1983) Efficient nonphotochemical hole burning of dye molecules in polymers. J Phys Chem 87: 3590–3592
Friedrich J, Swalen JD and Haarer D (1980) Electron-phonon coupling in amorphous organic host materials as investigated by photochemical hole burning. J Phys Chem 73: 705–711
Friedrich J and Haarer D (1984) Photochemical hole burning: a spectroscopic study of relaxation processes in polymers and glasses. Angew Chem Int Ed Engl 23: 113–140
Gillie JK, Fearey BL, Hayes JM, Small GJ and Golbeck JH (1987a) Persistent hole burning of the primary donor state of photosystem I: strong linear electron-phonon coupling. Chem Phys Lett 134: 316–322
Gillie JK, Hayes JM, Small GJ and Golbeck JH (1987b) Hole burning spectroscopy of a core antenna complex. J Phys Chem 91: 5524–5527
Gillie JK, Small GJ and Golbeck JH (1989) Nonphotochemical hole burning of the native complex of photosystem I (PSI-200). J Phys Chem 93: 1620–1627
Golbeck JH (1980) Subchloroplast particle enriched in P700 and iron-sulfur protein. In: San Pietro A (ed) Methods in Enzymology, vol 69, pp 129–141. New York: Academic Press
Golbeck JH (1987) Structure, function, and organization of the Photosystem I reaction center complex. Biochim Biophys Acta 895: 167–204
Hayes JM and Small GJ (1986) Photochemical hole burning and strong electron-phonon coupling: primary donor states of reaction centers of photosynthetic bacteria. J Phys Chem 90: 4928–4931
Hayes JM, Gillie JK, Tang DT and Small GJ (1988) Theory for spectral hole burning of the primary electron donor state of photosynthetic reaction centers. Biochim Biophys Acta 932: 287–305
Hayes JM and Small GJ (1978) Nonphotochemical hole burning and impurity site relaxation processes in organic glasses. Chem Phys 27: 151–157
Jankowiak R, Tang D, Small GJ and Seibert M (1989) Transient and persistent hole burning of the reaction center of photosystem II. J Phys Chem 93: 1649–1654
Jankowiak R and Small GJ (1987a) Hole burning spectroscopy and relaxation dynamics of amorphous solids at low temperatures. Science 237: 618–625
Jankowiak R, Shu L, Kenney MJ and Small GJ (1987b) Dispersive kinetic processes, optical linewidths and dephasing in amorphous solids. J Lumin 36: 293–305
Johnson SG and Small GJ (1989) Spectral hole burning of a strongly excitonic coupled bacteriochlorophyll a antenna complex. Chem Phys Lett 155: 371–375
Johnson SG, Tang D, Jankowiak R, Hayes JM, Small GJ and Tiede, DM (accepted) Structure and marker mode of the primary electron donor state absorption of photosynthetic bacteria: hole burned spectra. J Phys Chem
Ke B, Demeter S, Zamaraea KI and Khairutdimov RF (1978) Charge recombination in photosystem I at low temperatures. Biochim Biophys Acta 545: 265–284
Köhler W, Friedrich J, Fischer R and Scheer H (1988a) Siteselective spectroscopy and level ordering in c-phycocyanine. Chem Phys Lett 143: 169–173
Köhler W, Friedrich J, Fischer R and Scheer H (1988b) High resolution frequency selective photochemistry of phycobilisomes at cryogenic temperatures. J Chem Phys 89: 871–874
Lee IJ, Hayes JM and Small GJ (accepted) Hole and anti-hole profiles in non-photochemical hole burned spectra. J Chem Phys
Lockhart DJ and Boxer SG (1987) Magnitude and direction of the change in dipole moment associated with excitation of the primary electron donor in Rhodopseudomonas sphaeroides reaction centers. Biochemistry 26: 664–668
Lockhart DJ and Boxer SG (1988) Stark effect spectroscopy of Rhodobacter sphaeroides and Rhodopseudomonas viridis reaction centers. Proc Natl Acad Sci USA 85: 107–111
Lösche M, Feher G and Okamura MY (1987) The stark effect in reaction centers from Rhodobacter sphaeroides R-26 and Rhodopseudomonas viridis. Proc Natl Acad Sci USA 84: 7537–7541
Martin J-L, Breton J, Hoff AJ, Migus A and Antonetti A (1986) Femtosecond spectroscopy of electron transfer in the reaction center of the photosynthetic bacterium Rhodopseudomonas sphaeroides R-26: direct electron transfer from the dimeric bacteriochlorophyll primary donor to the bacteriopheophytin acceptor with a time constant of 2.8±0.2 ps. Proc Natl Acad Sci USA 83: 957–961
Meech SR, Hoff AJ and Wiersma DA (1985) Evidence for a very early intermediate in bacterial photosynthesis. A photon-echo and hole-burning study of the primary donor band in Rhodopseudomonas sphaeroides. Chem Phys Lett 121: 287–292
Meech SR, Hoff AJ and Wiersma DA (1986) Role of chargetransfer states in bacterial photosynthesis. Proc Natl Acad Sci USA 83: 9464–9468
Michel H, Epp O and Deisenhofer J (1986) Pigment-protein interactions in the photosynthetic reaction center from Rhodopseudomonas viridis. EMBO J 5: 2445–2451
Michel H and Deisenhofer P (1986) X-ray diffraction studies on a crystalline bacterial photosynthetic reaction center: a progress report and conclusions on the structure of photosystem II reaction centers. In: Staehelin AC and Arntzen CJ (eds) Encylopedia of Plant Physiology: Photosynthesis III, pp 371–381. Berlin: Springer-Verlag
Michel H and Deisenhofer J (1987) The photosynthetic reaction center from the purple bacterium Rhodopseudomonas viridis. Chemica Scripta 27B: 173–180
Moerner WE (ed) (1988) Persistent spectral hole-burning: science and applications. Berlin: Springer-Verlag
Mullet JE, Burke JJ, Arntzen CJ (1980) Chlorophyll proteins of Photosystem I. Plant Physiol 65: 814–822
Nanba O and Satoh K (1987) Isolation of a photosystem II reaction center consisting of D-1 and D-2 polypeptides and cytochrome b-559. Proc Natl Acad Sci USA 84: 109–112
Owens TG, Webb SP, Mets L, Alberts RS and Fleming GR (1987) Antenna size dependence of fluorescence decay in the core antenna of photosystem I: estimates of charge separation and energy transfer rates. Proc Natl Acad Sci USA 84: 1532–1536
Renge I, Mauring K and Avarmaa R (1987) Site-selection optical spectra of bacteriochlorophyll and bacteriopheophytin in frozen solutions. J Lumin 37: 207–214
Renge I, Mauring K and Vladkova R (1988) Zero-phonon transitions of chlorophyll a in mature plant leaves revealed by spectral hole-burning method at 5 K. Biochim Biophys Acta 935: 333–336
Schaffernicht H and Junge W (1981) Analysis of the complex band spectrum of P700 based on photoselection studies with photosystem I particles. Photochem Photobiol 34: 223–232
Sétif P, Mathis P and Vänngård T (1984) Photosytem I photochemistry at low temperature: heterogeniety in pathways for electron transfer to the secondary acceptors and for recombination processes. Biochim Biophys Acta 767: 404–414
Small GJ (1983) Persistent nonphotochemical hole burning and the dephasing of impurity electronic transitions in organic glasses. In: Agranovich VM and Hochstrasser RM (eds) Spectroscopy and excitation dynamics of condensed molecular systems, pp 515–554. Amsterdam: North-Holland
Small GJ (1970) Multiplet and phonon structure in mixed crystal spectra: anthacene in p-terphenyl. J Chem Phys 52: 656–673
Tang D, Jankowiak R, Gillie JK, Small GJ and Tiede DM (1988) Structured hole-burned spectra of reaction centers of Rhodopseudomonas viridis. J Phys Chem 92: 4012–4015
Tang D, Jankowiak R, Small GJ and Tiede DM (1989) Structured hole-burned spectra of the primary donor state absorption region of Rhodopseudomonas viridis. Chem Phys 131: 99–113
Tang D, Johnson SG, Jankowiak RJ, Hayes JM, Small GJ and Tiede DM (accepted) Structure and marker mode of the primary electron donor state absorption of photosynthetic bacteria: hole burned spectra. In: Jortner J and Pullman B (eds) Twenty-Second Jerusalem Symposium Quantum Chemistry and Biochemistry: Perspectives in Photosynthesis. Kluwer Academic: Dordrecht, to be published
Trebst A (1986) The topology of the plastoquinone and herbicide binding peptides of photosystem II in the thylakoid membrane. Z Naturforsch 41C: 240–245
Wasielewski MR, Johnson DG, Seibert M and Govindjee (1989) Determination of the primary charge separation rate in isolated photosystem II reaction centers with 500-fs time resolution. Proc Natl Acad Sci USA 86: 524–528
Wasielewski MR, Fenton JM and Govindjee (1987) The rate of formation of P700+-A0 - in photosystem I particles from spinach as measured by picosecond transient absorption spectroscopy. Photosyn Res 12: 181–190
Won Y and Friesner RA (1988a) Theoretical studies of photochemical hole burning in photosynthetic bacterial reaction centers. J Phys Chem 92: 2214–2219
Won Y and Friesner RA (1988b) On the viability of the superexchange mechanism in the primary charge separation step of bacterial photosynthesis. Biochim Biophys Acta 935: 9–18
Won Y and Friesner RA (1989) Comment: theoretical studies of photochemical hole burning in photosynthetic bacterial reaction centers. J Phys Chem 93: 1007
Yeates TO, Komiya H, Chirino A, Rees DC, Allen JP and Feher G (1988) Structure of the reaction center from Rhodobacter sphaeroides R-26 and 2.4.1:protein-cofactor (bacteriochlorophyll, bacteriopheophytin, and carotenoid) interactions. Proc Natl Acad Sci USA 85: 7993–7997
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Gillie, J.K., Lyle, P.A., Small, G.J. et al. Spectral hole burning of the primary electron donor state of Photosystem I. Photosynth Res 22, 233–246 (1989). https://doi.org/10.1007/BF00048302
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DOI: https://doi.org/10.1007/BF00048302