The Possible Existence of a Charge Transfer State which Preceeds the Formation of (BChl)₂ ⁺ BPh⁻ in Rhodobacter sphaeroides Reaction Centers

Abstract

The nature of the first electron transfer step in the photosynthetic reaction center protein is far from certain. Several investigators have considered a monomeric BChl to be important in promoting forward electron transfer from (BChl)₂* to BPh. The center of the BChl is positioned in the X-ray crystal structure 0.25nm from the center of the (BChl)₂, measured in a direction parallel with the z-axis of the protein (4,5). The monomer is displaced out of the direct line joining (BChl)₂ and BPh centers but nevertheless it remains an obvious candidate to be on the electron transfer reaction pathway. However, careful searches in the picosecond time domain for absorbance changes that may be associated with transient redox changes on the BChl have failed to demonstrate its involvment in the sequence over a wide temperature range (1–3 although see ref. 6). Instead, spectroscopic investigations with picosecond and subpicosecond resolution have revealed that the loss of the excited singlet state of the special pair of bacteriochlorophylls, (BChl)₂*, coincides with the appearance of the reduced bacteriopheophytin (BPh⁻). Thus, the formation of the state (BChl)₂ ⁺ BPh⁻, which is positioned some 0.2ev below the (BChl)₂* state appears to occur in a single step with a rate of approximately 3×10¹¹ s⁻¹ (1–3). This separates charge across the approximately 1.1 nm between the centers of the (BChl)₂ and BPh, again measured along the line parallel to the z-axis of the protein (4,5). Because of the closly matched kinetics of (BChl)₂* decay and BPh⁻ appearance, the involvement of BChl as a conventional redox carrier is cryptic and in doubt. However, it is acknowledged in these studies that, for technical reasons, levels of BChl⁺ or BChl⁻ must achieve 15% of the total reaction center population to be detected with any certainty. Thus, there are several viable models (see refs 1–3,6,7–10 for discussion) that can explain these early steps in photosynthesis leading to formation of (BChl)₂ ⁺ BPh⁻. These include:

• 1. The BChl plays no part in electron transfer from (BChl)₂ to BPh.

• 2. The BChl serves to increase the electron coupling between (BChl)₂ and BPh by the mechanism of superexchange.

• 3. The BChl is a bona fide redox agent that accepts an electron from (BChl)₂* to form (BChl)₂ ⁺ BChl⁻ which is followed by electron donation to BPh.

• 4. The BChl is a bona fide redox agent, but the reaction sequence is that singlet energy transfer from (BChl)₂* to BChl first induces an electron transfer from BChl to BPh to form BChl⁺BPh⁻. The cation BChl⁺ so formed then moves to the (BChl)₂.