Mechanism of the initial charge separation in bacterial photosynthetic reaction centers.

Abstract

The initial electron tranfer in reaction centers from Rhodobacter sphaeroides R26 was studied by a subplcosecond transient pump-probe technique. The measured kinetics at various wavelengths were analyzed and compared with several mechanisms for electron tra er. An unambiguous determination of the initial electron transfer mechanism in reaction centers cannot be made by studying the anion absorption region (6404690 nm), due to the spectral congestion in this region. However, correlations between the stimulated emission decay of the excited state of the special pair, P*, at 926 nm and bleaching of the bacteriopheophytin Qx absorption at 545 mu suggest that the electron transfer at 283 K is dominated by a two-step sequential mechanism, whereas one-step superexchange and the two-step sequential mechanism have about equal contributions at 22 K.The highly efficient primary charge separation in photosynthesis occurs in a membrane-bound protein complex called the reaction center (RC). The x-ray crystal structure of RCs from Rhodopseudomonas (Rps.) viridis and Rhodobacter (Rb.) sphaeroides has been determined and reveals a pseudo C2 symmetry (1-3). In the RC, two strongly interacting bacteriochlorophylls form the special pair, denoted P. Along each side of the C2 axis there is a monomeric bacteriochlorophyll (BA and BB) adjacent to the special pair, followed by a bacteriopheophytin (HA and HB) and then by a quinone molecule (QA and QB). There is also a single non-heme iron on the C2 axis between the two quinones.Electron transfer could occur along either branch related by the C2 symmetry, yet it occurs only down one branch (branch A) from P* to HA in about 3 ps at room temperature. One unresolved question concerns the role of BA in the initial charge separation process between P* and HA. Early picosecond and femtosecond measurements on RCs from Rb. sphaeroides and Rps. viridis at room temperature and at 10 K (4-9) did not detect any intermediate state involving B-, and the decay of P* and the bleaching of HA had the same time constant. These observations indicated that the initial electron transfer from P*BAHA to P+BAH-occurred either by a single-step superexchange mechanism or by a two-step hopping process with the second step much faster than the first step. The one-step superexchange mechanism has been supported by measurements by Kirmaier and Holten (10,11). Using an electric field to perturb the electron transfer, Lockhart et al. (12) concluded that (at 77 K) the two-step mechanism was unlikely. The same conclusion was reached by Ogrodnik et al. (13) (19) suggests that for reasonable parameter values, the electron transfer is dominated by the two-step sequential mechanism at room temperature, while the contribution of the one-step superexchange mechanism becomes important at low temperature.In this paper, we address the mechanism of the initial electron transfer by using kinetic data for Rb. sphaeroides R26 RCs obtained at several wavelengths where the various species involved absorb. The analysis of our da...

Time-resolved spectroscopy of the primary photosynthetic processes of membrane-bound reaction centers from an antenna-deficient mutant of Rhodobacter capsulatus

“…Very recent emission experiments have shown that the 3 ps decay of P* seems to be a biphasic process with two time constants [8,9]. At all temperatures an additional subpicosecond component was detected in Rhodobacter sphaeroides having time constants of 0.3 ps to 0.9 ps for temperatures of 25 K to 300 K [10,11]. The same ultrafast component was found in RCs from Rhodopseudomonas viridis having a time constant of 0.65 ps at 300 K [5].…”

Long-time quantum simulation of the primary charge separation in bacterial photosynthesis.

“…Photoexcitation is followed by the transfer of an electron to a distant bacteriopheophytin HL (Fig. 2) with time constant equal to about 3 ps and with quantum yield that approaches unity (3)(4)(5)(6)(7). It is now accepted that this fast long-range electron transfer is mediated by an accessory bacteriochlorophyll monomer BL whose reduced state couples to those of the excited special pair and the bacteriopheophytin.…”

“…However, the energetics of the accessory chlorophyll, as well as the mechanism of the process, are still under debate . Time-resolved experiments on wild-type reaction centers (3)(4)(5)(6) have failed to detect a reduced accessory chlorophyll state and concluded that the population of this state remains small throughout the charge transfer. If the chlorophyll monomer is involved via a sequential mechanism, this behavior is possible if the second step is much faster than the first.…”

Primary electron transfer kinetics in bacterial reaction centers with modified bacteriochlorophylls at the monomeric sites BA,B.

“…The observation of an additional, subpicosecond time constant in Rhodobacter sphaeroides (16)(17)(18)(19)(20) again raised the possibility of P+B-being a real intermediate according to P .…”