Photosynthetic reaction center electron transfer cofactors

Kirmaier, C., Cua, A. He, C. Holten, D. Bocian, David F. (2002) Probing M-branch electron transfer and cofactor environment in the bacterial photosynthetic reaction center by addition of a hydrogen bond to the M-side bacteriopheophytin, Journal of Physical Chemistry B 106, 495-503. 

FIGURE 7. Two redox cofactor chains meet at the bacteriochlorophyl dimer in the photosynthetic reaction center of Rp. viridis. Electron transfer takes place by tunneling between cofactors diat are spaced by no more dian 14, assuring overall elech on transfer rates in the msec or faster range, even though a total distance of 70 is crossed by the c heme chain. 

Wamcke, K., and Dutton, P. L., 1993, Influence of QA site redox cofactor structure on equilibrium binding, in situ electrochemistry, and electron transfer performance in the photosynthetic reaction center protein Biochemistry 32 4769n4779. 

Nevertheless, other chromophores have been investigated and they have provided interesting insights, particularly porphyrin and Cso groups, since these serve as useful mimics of the cofactors present in the photosynthetic reaction center (Figure 37). Electron transfer involving porphyrins and fullerenes will be presented in more detail elsewhere in this Handbook Volume III, Part 2, Chapter 2 and Volume II, Part 1, Chapter 5 respectively), and so only a brief discussion is presented here. An excellent overview of photoinduced ET processes in Cso-based multichromophoric systems has been produced previously [116]. 

Photoinduced electron transfer reactions have been studied in the dyads 44(6), 45(9), and 46(11). The 6-bond porphyrin-quinone dyad 44(6) serves as a model for aspects of ET in the photosynthetic reaction center, since congeners of these chromophores are present in the center as cofactors (Figure 37). Photoinduced ET in... 

Figure 18. In [2]catenane 20 + [86], upon excitation of its [Rutbpy), p moiety, a very fast electron transfer process to a bipyridinium unit occurs. Owing to the catenane structure, the two bipyridinium units do not possess the same reduction potential (half-wave potential values versus SCE for the inside and outside units are indicated) such a redox asymmetry could mimic that of the cofactors in the bacterial photosynthetic reaction center.

The photosynthetic reaction center stores light energy by effecting electron transfer to reduce an electron transfer cofactor and form a proton gradient across the membrane. The arrangement of electron transfer cofactors is indicated in Figure 2 and includes a special pair of bacteriochlorophyll molecules, two accessory bacteriochloroophylls, two bacteriopheophytins, two quinone electron acceptors, and a non-henae iron. The reaction center functions... 

Figure 2. Arrangement of the electron transfer cofactors in the photosynthetic reaction center protein from the bacterium Rhodobacter sphaeroides. The figure shows the special pair of bacteriochlorophylls (top, in green and light blue), two accessory bacteriochlorophyll molecules (dark blue), two bacteriopheophytins (red), the primary quinone (Qa), the secondary quinone (Qb), and the non-heme iron.

Following the initial work of Salemme, models for other electron transfer complexes have been proposed for cytochrome c-cytochrome-c peroxidase (98), cytochrome c-flavodoxin (99), cytochrome Z>s-hemoglobin (100), cytochrome (75-myoglobin (101), cytochrome c-photosynthetic reaction center (102, 103), and ferredoxin-cytochrome C3 (104). The same general approach of identifying potential salt bridges that could stabilize a complex with approximately coplanar cofactor rings has been utilized in many of these studies. 

The bacterial photosynthetic reaction center protein (RC) catalyzes the conversion of light to electrochemical energy through a sequence of photon-initiated electron transfer reactions between redox cofactors held at fixed distances in the protein [1-4]. The primary processes are elicited by absorption of a photon by the primary donor, a dimer of bacteriochlorophyll ([BChIjg). The first excited singlet state of the dimer, [BChljg, transfers an electron over 10 A in 3 ps to a bacteriopheophytin (BPh). The BPh" in turn reduces a quinone bound at the site to form an anionic semiquinone in 0.2 ns (for a review, see [5]). Numerous experimental efforts have aimed to identify the factors which control the remarkable near unit quantum yield and temperature independence of the RC processes [6-9], often with an eye toward emulation in artificial photosynthetic devices [10]. Here, we examine the role of structural components of the quinone cofactor in determining electron transfer rates at the RC Q/y site. 

Figure 1. Location of the electron transfer cofactors in the photosynthetic reaction center of Rb. sphaeroides.

Light-induced electron transport in bacterial photosynthetic reaction centers leads to the creation of a charge-separated state stable for milliseconds to seconds. The structures provided by X-ray crystallography (Michel et aL, 1986 Allen et al., 1988 Deisenhofer Michel, 1989 El-Kabbani et al., 1991) constitute a unique guideline to address questions on how the function may be related to the arrangement of the cofactors and of specific amino acid residues in their vicinity. The sequence of electron transfer reactions, the identity of the reaction partners, and the reaction mechanisms have been characterized from static and time-resolved absorbance measurements (for a review, see Parson Ke, 1982). Transfer of the first electron to the primary (Q ) and secondary (Qg) quinone electron acceptors has received considerable attention, since it is associated with intraprotein protolytic reactions (for a recent review, see Okamura Feher, 1992), which have a potential role in electrostatic charge stabilization. 

The only known function of PhQ in cyanobacteria and plants is to function as an electron transfer cofactor in PS I. In spite of its importance in cyanobacteria, the biosynthetic route of PhQ was not previously elucidated. Many prokaryotes contain the metabolic pathway for the biosynthesis of menaquinone (MQ), a PhQ-Hke molecule (Figure 119.1). In certain bacteria, MQ is used during fumarate reduction in anaerobic respiration. - In green sulfur bacteria and in heliobacteria, MQ may function as a loosely bound secondary electron acceptor in the photosynthetic reaction center. The genes encoding enzymes involved in the conversion of chorismate to MQ were cloned in a variety of organisms. MQ differs from PhQ only in the tail portion of the molecule an unsaturated C-40 side chain is present, rather than a mostly saturated C-20 phytyl side chain. Therefore, the synthesis of the naphthalene rings in PhQ and MQ involves similar steps in both pathways. 

Chains of redox cofactors for long range electron transfer are clearly the way electrons are transferred over the tens of angstroms dimensions of membranes and their proteins. Once again, purple photosynthetic bacterial reaction centers provide an archetype for understanding electron transfer chain design and behavior. The heme chain in Rps. viridis... 

Fig. 11. Photosynthetic bacterial reaction center represented by a simplified model consisting of the reaction center and lightharvesting complexes (A), a three-dimensional model consisting of the L-, M-, H- and C-subunits (B, left) and the corresponding simplified model consisting of cofactors only (B, right). (C) illustration of the electron-transfer reactions with their associated reaction times.

The function of photosynthetic bacterial reaction centers (RCs) is closely related to their structure. In the last 15 years a wealth of structural data has been accumulated on bacterial RCs, mainly through X-ray structure analysis of three-dimensional RC crystals. In this chapter, the arrangement of protein subunits and cofactors in the RC complexes ofthe non-sulfur purple bucienn Rhodobacter (Rb.) sphaeraides mARhodopseudomonas (Rp.) viridis are delineated. A prominent feature ofthe bacterial RCs is their location in the photosynthetic membrane. Inside the RC complex, a finely tuned arrangement of amino acid residues and cofactors maintains a highly ordered system. The positions and likely functions of hydrogen bonds are described, since they play a key role in protein-cofactor interactions. Special emphasis is placed on the symmetry relations in the RC and on the functional asymmetry of electron and proton transfer that contradicts the observed pseudo two-fold structural symmetry. 

Reaction centers in photosynthetic bacteria typically contain three membrane-bound subunits (L, M, and H), and the following cofactors four bacteriochlo-rophyll (Bchl or B), two bacteriopheophytin (Bphe or 4>), two quinones (Q), and one Fe atom 28, 178). The sequence of electron transfer steps along the various cofactors has been established largely by spectroscopic methods. The primary donor, D, which initially absorbs light (creating the excited state D ) is a dimer of Bchl molecules [also designated (Bchl)2 or P]. Electron transfer proceeds from D to an intermediate acceptor (a Bphe molecule), to a primary acceptor, Qa, and finally to the secondary acceptor Qb. After these initial events, the RC... 

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