Magnetic characterization of the primary state of bacterial photosynthesis

Abstract

The results of reaction yield-detected magnetic resonance (RYDMR) experiments carried out on modified bacterial photosynthetic reaction centers (RCs) are interpreted in terms of a model that assigns the initial charge-separated radical ion-pair state, pF, as the carrier of the spectrum. The radical pair theory, which has been invoked to explain magnetic field effects in RCs, was significantly expanded to take into consideration the electron dipole-dipole interaction. It is shown that this is the largest interaction between the components of the radical ion pair. Quantum statistical calculations are described simulating the RYDMR spectra and low-field effects in quinone-depleted RCs. The experimental data on which the simulations are based are (i) the magnitude of the field effect at 3,000 G, (ii) the field at which 0.5 of the maximal field effect is observed, (iii) the pF population as a function of time at zero magnetic field, (iv) the RYDMR linewidth for low microwave field strength, (v) the RYDMR intensity and width as a function of microwave field, and (vi) the maximum RYDMR intensity at HI 2jJj. With this information it was found possible to characterize pF in terms of four parameters, two containing structural information and two with kinetic implications. These are the dipole-dipole interaction, D = -47 ± 10 X 10-4 cm'; the exchange interaction, J = -7.5 + 1.9 X 10-4 cm-1; and the inverse rate constants of the decay of the radical pair states with singlet and triplet spin functions, respectively, ksl = 15 ± 4 nsec and ki' = 1.8 ± 0.2 nsec. The structural and dynamic implications of these parameters are discussed.For the last two decades, the early events of photosynthesis have been probed by magnetic techniques with the aim ofgaining structural and mechanistic insights into the initial chargeseparation steps. The existence of a short-lived paramagnetic radical pair state, pF (1, 2), in bacterial reaction centers had been predicted (3) on the basis of unusual non-Boltzman populations determined by the conventional EPR spectrum of the triplet state, pR (4). The unique features of the EPR spectrum ofthe triplet state pR were explained as arising from annihilation of charge separation within the radical ion-pair state pF. In addition, it was suggested that the short lifetime Of pF would necessitate the application ofoptical detection methods to observe its magnetic resonance spectrum (3). A recent paper from these laboratories (5) reports the optically detected EPR spectrum of pF, presumably the earliest paramagnetic state in bacterial photosynthesis. It is the purpose of this paper to report the results of a quantitative evaluation of these spectra and the associated magnetic field effects yielding structural and dynamic parameters that are of importance to the general mechanism of photosynthesis.At this point, pF is thought to contain the primary donor, special pair bacteriochlorophyll cation (P870), and the primary acceptor, bacteriopheophytin anion (6). Most recently another bacteriochlorophyll m...

Primary photochemistry of reaction centers from the photosynthetic purple bacteria

“…Subsequent electron transfer from the reduced primary quinone (Q£) to the secondary quinone (QB), leading ultimately to the formation and utilization of QB H2, has been recently reviewed [31], and will not be described here. Nor will we describe in detail the interesting and often novel photochemistry observed in reaction centers in which electron transfer to QA is prevented by its removal or chemical reduction (see [15,56,101,112] and references therein), except insofar as such experiments reveal information about the nature and energetics of states which take part in the normal sequence of events leading to P+ QA formation. This review will especially focus on progress made during the last three to five years, with the intent of highlighting current efforts to understand better the relationship between the structure of the reaction center and how, at a molecular level, it functions so efficiently.…”

Iron-depleted reaction centers from Rhodopseudomonas sphaeroides R-26.1: characterization and reconstitution with iron(2+), manganese(2+), cobalt(2+), nickel(2+), copper(2+), and zinc(2+)

“…From the quantum yield for formation of the triplet state 'DIQA-[0.1-0.2 at 20 O C (Parson et al, 1975;Parson & Monger, 1977)] and the value of klD-' (10-20 ns), one infers for native RCs a value of kIT-' -100 ns [for more detailed discussions of triplet formation in RCs see Norris et al (1982), Ogrodnik et al (1982), Schenck et al (1982), and Chidsey et al (1984)l. If klT is unaffected by removal of the Fe, this relationship implies that [krQ(2)]-1 -1 ps in Fe-depleted RCs.…”

Magnetic Interactions Between Photosynthetic Reactants

“…The value of D is considerable, but the kT rate constant used for the fit deviates rather much from that found by Ogrodnik et a f . (1982) and Norris et al (1982).…”