Formation Dynamics, Decay Kinetics, and Singlet–Triplet Splitting of the (Bacteriochlorophyll Dimer)⁺ (Bacteriopheophytin)⁻ Radical Pair in Bacterial Photosynthesis

Abstract

We explore the interrelationship between (i) the kinetic data for the primary electron transfer (ET) from the excited singlet state (1P*) of the bacteriochlorophyll dimer (P) to bacteriopheophytin (H) in the reaction centers (RCs) of purple photosynthetic bacteria and (ii) the energetics and dynamics of the primary radical pair, P+H, i.e., its singlet‐triplet splitting rate, J, and triplet recombination rate, kT. We present a critical scrutiny of the ET mechanisms with regard to the role of the accessory bacteriochlorophyll (B). On the basis of the very weak temperature dependence of J, which sets a lower limit to the energy of (hypothetic) transient short‐lived ionic intermediate states, we argue against the applicability of sequential ET mechanisms involving P+B− H or P+BH−. The nonadiabatic/adiabatic ET mechanism is fraught with difficulties pertaining to a very low medium reorganization energy for the nonadiabatic crossing and an exceedingly high rate of the adiabatic crossing, together with a predicted order‐of‐magnitude enhancement of the low‐temperature (77 K) fluorescence quantum yield in high electric fields (5–10 mV/Å) which seem not to be borne out by experiment We propose that primary ET occurs via the unistep superexchange 1P*BH r̊ P+H−, which is mediated by electronic coupling with P+B−H. The analysis of the competition between superexchange and thermally activated ET resulted in large values of the intermolecular electronic couplings at the equilibrium nuclear configuration of 1P*BH. We suggest that the structural relaxation of one of the prosthetic groups (H) accompanying the primary ET results in the decrease of the intermolecular electronic coupling at the equilibrium configuration of P+BH−. It was established that the superexchange‐predicted kinetic data are consistent with the magnetic data for the radical pair. The small value of J for P+BH− originates from the cumulative effect of: (i) an essential, model‐independent cancellation between the triplet contribution, which is related to kT by a self‐consistency relationship, and the singlet contribution; (ii) the effect of configurational relaxation on the singlet contribution. Our analysis supports the superexchange mechanism for primary ET in bacterial photosynthetic RCs.

Energetics and Mechanism of Primary Charge Separation in Bacterial Photosynthesis. A Comparative Study on Reaction Centers of Rhodobacter sphaeroides and Chloroflexus aurantiacus

“…A shift of 1 (P + H A -) of at least 10 -2 cm -1 ≈ 100 G was estimated. 2,10,12,13,16 This is much larger than the experimentally observed value of J. Two possibilities to resolve this discrepancy when assuming superexchange charge separation were discussed: (i) a fortuitous compensation of the shift of 1 (P + H A -) by an equivalently large shift of 3 (P + H A -) in the same direction; however, the maximum values of the triplet shift calculated with a more refined theoretical treatment 14,98 including the interaction with all vibronic states are not large enough to compensate the expected large values of the singlet shift; (ii) a fast decrease of the coupling between P and H A due to some conformational relaxation after charge separation.…”

“…sphaeroides. 10,16 This is larger by a factor of 20 than the electronic coupling V T between 3 (P + H A -) and 3 P*; see below. Triplet recombination from P + H A -is near the activationless case; triplet recombination from P + B A -, on the other hand, has a larger freeenergy gap, but is not expected to have a larger reorganization energy.…”

The First Picoseconds in Bacterial Photosynthesis—Ultrafast Electron Transfer for the Efficient Conversion of Light Energy

“…[46] These data were taken as an important indication for a superexchange ET as the primary charge-separation process in photosynthesis: the electron should not be transferred step by step between neighbouring chromophores as was expected from conventional Marcus- [49] Even if the superexchange model seemed to be convincingly supported by experiments and theory, [30,50,51] a number of unsolved questions or contradictory results had to be considered: Studies on the initial reaction dynamics and intended to develop a unifying view of the reaction centre, had difficulties to reconcile a superexchange forward reaction with recombination dynamics. [51][52][53][54][55] Inspecting the data of Martin and Breton, R. Marcus found that these data would not exclude the existence of an intermediate P + B A À even with a relatively long lifetime of up to 1 ps. [52] Simulations on the energetics of intermediates that considered the published structure of the reaction centre and polar molecules in the vicinity of the electron carriers indicated that the energy of intermediate P…”

Initial electron-transfer in the reaction center from Rhodobacter sphaeroides.

“…There was no generally accepted experimental evidence of an intermediate electron-carrying state B- (16)(17)(18)(19)(20)(21)(22)(23). The postulated direct electron transfer from P to H imposed numerous difficulties on the theoretical description of the charge-transfer process (24)(25)(26)(27)(28)(29)(30)(31)(32)(33)(34)(35)(36)(37)(38) …”