The effect of very high magnetic fields on the delayed fluorescence from oriented bacterial reaction centers

doi:10.1016/S0005-2728(89)80010-6

Biochimica et Biophysica Acta (BBA) - Bioenergetics

Volume 977, Issue 1, 26 October 1989, Pages 70-77

https://doi.org/10.1016/S0005-2728(89)80010-6 Get rights and content

Delayed fluorescence is observed from quinone-depleted Rhodobacter sphaeroides reaction centers due to re-formation of the excited state of the special pair electron donor from the initially formed radical-pair state. Theoretical calculations based on the currently accepted scheme for the initial reaction dynamics predict quantum beats in the delayed fluorescence time evolution at very high magnetic field for oriented reaction centers. The delayed fluorescence was observed at magnetic fields from 1 kG to 150 kG using time-resolved single-photon counting. The reaction centers were oriented by insertion into phosphatidylcholine vesicles that were subsequently air-dried. Quantum beats were not observed, indicating that the reaction scheme may need revision. Saturation of the magnetic field effect on the delayed fluorescence lifetime was observed above 100 kG. The decay rate above saturation permits the first direct measurement of k_T, the rate of radical pair decay to the triplet state of the electron donor. We obtain a value for k_T of (4.0±0.3)·10⁸ s⁻¹. The implications of this value of k_T and the absence of quantum beats at high field are discussed further in the accompanying manuscript. (Biochim. Biophys. Acta 977 (1989) 78–86).

References (35)

WernerH. et al.
Biochim. Biophys. Acta
(1978)
HaberkornR. et al.
Biophys. J.
(1979)
ShuvalovV.A. et al.
Biochim. Biophys. Acta
(1976)
GodikV.I. et al.
Biochim. Biophys. Acta
(1980)
WoodburyN.W. et al.
Biochim. Biophys. Acta
(1984)
SchenckC.C. et al.
Biochim. Biophys. Acta
(1982)
TangJ. et al.
Chem. Phys. Lett.
(1982)
ChidseyC.E.D. et al.
Biochim. Biophys. Acta
(1984)
HörberJ.K.H. et al.
FEBS Lett.
(1986)
WoodburyN.W. et al.
Biochim. Biophys. Acta
(1986)

GoldsteinR.A. et al.

Biochim. Biophys. Acta

(1989)

VeselovA.V. et al.

Chem. Phys. Lett.

(1987)

GoldsteinR.A. et al.

Biophys. J.

(1987)

LerschW. et al.

Chem. Phys.

(1983)

GoldsteinR.A. et al.

Biochim. Biophys. Acta

(1988)

HunterD.A. et al.

Chem. Phys. Lett.

(1987)

NabedrykE. et al.

Biochim. Biophys. Acta

(1982)

Cited by (21)

Photon statistics as an experimental test discriminating between theories of spin-selective radical-ion-pair reactions
2012, Chemical Physics Letters
Radical–ion-pair reactions were recently shown to represent a rich biophysical laboratory for the application of quantum measurement theory methods and concepts. We here propose a concrete experimental test that can clearly discriminate among the fundamental master equations currently attempting to describe the quantum dynamics of these reactions. The proposed measurement based on photon statistics of fluorescing radical pairs is shown to be molecular-model-independent and capable of elucidating the singlet–triplet decoherence inherent in the radical–ion-pair recombination process.
The importance of a hot-sequential mechanism in triplet-state formation by charge recombination in reaction centers of bacterial photosynthesis
2006, Chemical Physics
Citation Excerpt :
If the broadening originated only from the lifetime due to recombination of 3[P+H−], the width would have enabled us to correctly determine kT. The kT thus determined had a magnitude of ∼0.4–1.1 (ns)−1, nearly independent of temperature [8,12,14]. To the broadening of the energy level, however, other factors also contribute.
In photosynthesis, pigment-excitation energies in the antenna system produced by light harvesting are transferred among antenna pigments toward the core antenna, where they are captured by the reaction center and initially fixed in the form of a charge separation. Primary charge separation between an oxidized special pair (P⁺) and a reduced bacteriopheohytin (H⁻) is occasionally intervened by recombination, and a spin-triplet state (³P*) is formed on P in the bacterial reaction center. The ³P* state is harmful to bio-organisms, inducing the formation of the highly damaging singlet oxygen species. Therefore, understanding the ³P*-formation mechanism is important. The ³P* formation is mediated by a state |m〉 of intermediate charge separation between P and the accessory chlorophyll, which is located between P and H. It will be shown theoretically in the present work that at room temperature, not only the mechanism of superexchange by quantum-mechanical virtual mediation at |m〉, but also a hot-sequential mechanism contributes to the mediation. In the latter, although |m〉 is produced as a real state, the final state ³P* is quickly formed during thermalization of phonons in the protein matrix in |m〉. In the former, the final state is formed more quickly before dephasing-thermalization of phonons in |m〉. ³P* is unistep formed from the charge-separated state in the both mechanisms.
Triplet energy transfer in bacterial photosynthetic reaction centres
1998, Biochimica et Biophysica Acta - Bioenergetics
[3-vinyl]-13²-OH-bacteriochlorophyll a has been selectively exchanged against native bacteriochlorophyll a in the monomer binding sites at the A- and B-branch of the photosynthetic reaction centre from Rhodobacter sphaeroides. Transient absorption difference measurements were performed on these samples over a temperature range from 4.2 to 300 K with 20 ns time resolution. Specifically the decay of the primary donor triplet state, ³P₈₇₀, as well as the rise and decay rates of the carotenoid triplet state, ³Car (spheroidene), were measured. The observed rates revealed a thermally activated carotenoid triplet formation corresponding to the decay of the primary donor triplet state. The activation energies for the triplet energy transfer process were 100(±10) cm⁻¹ for reaction centers from wild-type Rhodobacter sphaeroides 2.4.1, with and without exchange of the monomeric bacteriochlorophyll on the electron transfer-active branch, B_A. For reaction centers from Rhodobacter sphaeroides R26.1 with both monomers exchanged against [3-vinyl]-13²-OH-bacteriochlorophyll a, and subsequent spheroidene reconstitution the activation energy was 460(±20) cm⁻¹. These activation energies correspond to the energy difference between the triplet states of the accessory BChl monomer, B_B, and the primary donor when native BChl a or [3-vinyl]-13²-OH-BChl a is present in the B_B binding site. In all samples the ³Car formation rates were bi-phasic over a large temperature range. A fast temperature-independent rate was observed on the wavelength of the carotenoid triplet–triplet absorption which dominated at very low temperatures. Additionally, a slower temperature-independent ³Car formation rate was observed at low temperatures which could be explained with the assumption of heterogeneity in the energy barrier (³B_B) and/or the primary donor triplet state (³P₈₇₀). A tunneling mechanism as proposed earlier by Kolaczkowski (PhD thesis, Brown University, 1989) is not only unnecessary but also incompatible with the available experimental data.
Photophysics of photosynthesis. Structure and spectroscopy of reaction centers of purple bacteria
1997, Physics Report
The fundamental photochemical reaction of photosynthetic energy conversion, which transforms the photon energy of light in chemical free energy, takes places in a membrane-bound, pigmented reaction center protein (RC). We examine here the structure-function relationships of this uniquely efficient process. First, the RC is discussed in relation to the overall photosynthetic apparatus. Second, we highlight the X-ray diffraction analysis of two bacterial RCs, discussing the problems associated with the analysis of a non-water-soluble protein of molecular weight over 120 kDa. The structure of the polypeptide chains in the RC-protein, and the configuration of the cofactors non-covalently bound to the polypeptide scaffolding, is reviewed in detail. Third, we present a detailed account of investigations on the functioning of the RC with a number of optical and magnetic resonance spectroscopic techniques, with emphasis on the relation between structure and function. The results for RCs of purple bacteria, green bacteria and the two plant photosystems are compared, and discussed in the framework of current theories of photosynthetic electron transport.
Free-energy dependence of the rate of electron transfer to the primary quinone in beta-type reaction centers
1995, Chemical Physics
Reaction centers of the beta-type mutants, (M)L214H and (M)L214H/(L)E104V, which contain a bacteriochlorophyll (denoted β) in place of the photoactive bacteriopheophytin, have been depleted of the native ubiquinone and reconstituted with a number of quinones. This system has allowed investigation of the rate versus free-energy relationship for electron transfer to the primary quinone in the activationless and inverted regions. The dependence of the rate on driving force is found to be much weaker in both mutants than in wild-type RCs. Analysis of the data using electron transfer theory shows that the essentially flat dependence of rate on free energy for the quinone-reconstituted beta-type mutants cannot be explained simply on the basis of increased driving force, but additionally requires a decrease in the reorganization energy. A decreased reorganization energy most likely derives from a change in the nature of the intermediary electron carrier in the mutants compared to wild-type RCs, in particular the involvement of the accessory bacteriochlorophyll molecule BChl_L. The weak free-energy and temperature dependence of the electron transfer process are consistent with coupling to a range of high- to low-frequency vibrational modes of the cofactors and protein.
Temperature-dependent electron spin polarization of the triplet state of the primary donor in Rhodopseudomonas viridis
1994, BBA - Bioenergetics
The electron spin polarization (ESP) of the triplet of the primary donor (³P) in reaction centers of the photosynthetic bacterium Rhodopseudomonas viridis shows an anisotropic temperature dependence (Van Wijk, F.G.H. and Schaafsma, T.J. (1988) Biochim. Biophys. Acta 936, 236). The reported inversion of the initial electron spin polarization (IESP) for the canonical Y-direction of ³P at 100 K has been explained by means of coherent S-T_± mixing in the radical pair, due to a fast relaxing electron spin on the iron-quinone acceptor complex X (Hore, P.J., Hunter, D.A., Van Wijk, F.G.H., Schaafsma, T.J. and Hoff, A.J. (1988) Biochim. Biophys. Acta 936, 249). Using direct-detection EPR, we show that at 100 K the IESP in randomly oriented samples is not inverted for the canonical Y-direction of ₃P. Furthermore, in single crystals the IESP at 100 K is shown to be almost zero for the complete YZ-plane of ³P. Since X^·− shows a strong g-anisotropy, the model of Hore et al., in which polarization-inversion only occurs when the effective g-value of X^·− is around g = 2.00, is inadequate to explain the temperature-dependent changes of the IESP. Therefore, we conclude that anisotropic fast spin-lattice relaxation in the radical pair triplet state is the origin of the temperature dependence of the ESP. The inversion for the canonical Y-direction under continuous illumination is the result of the interplay of spin-lattice relaxation in ³P and its triplet decay rates, in combination with changes in the IESP.

View all citing articles on Scopus

View full text

The effect of very high magnetic fields on the delayed fluorescence from oriented bacterial reaction centers

Biochim. Biophys. Acta

Biophys. J.

Biochim. Biophys. Acta

Biochim. Biophys. Acta

Biochim. Biophys. Acta

Biochim. Biophys. Acta

Chem. Phys. Lett.

Biochim. Biophys. Acta

FEBS Lett.

Biochim. Biophys. Acta

Biochim. Biophys. Acta

Chem. Phys. Lett.

Biophys. J.

Chem. Phys.

Biochim. Biophys. Acta

Chem. Phys. Lett.

Biochim. Biophys. Acta