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Quick links to online content Ann. Rev. Biochem. 1978. 47:635-653 Copyright @ 1978 by Annual Reviews Inc. All rights reserved

THE PHOTOCHEMICAL

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Annu. Rev. Biochem. 1978.47:635-653. Downloaded from www.annualreviews.org Access provided by University of Bristol on 01/25/15. For personal use only.

ELECTRON TRANSFER REACTIONS OF PHOTOSYNTHETIC BACTERIA AND PLANTS Robert E Blankenship and William W Parson Department of Biochemistry, SJ

-

70, University of Washington,

Seattle, Washington 98195

CONTENTS PERSPECTIVES AND SUMMARY PHOTOSYNTHETIC BACTERIA

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PLANT PHOTOSYSTEM I PLANT PHOTOSYSTEM II .....

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635 637 643 646

PERSPECTIVES AND SUMMARY The essence of photosynthesis in chlorophyll-containing organisms is the use of light to generate oxidants and reductants

(1-10). Richly

pigmented

membranes in these organisms act as antennas, which absorb light and funnel energy to special "reaction centers" (RCs), where the electron trans­ fer processes begin. In the last few years, preparations of purified RCs have been isolated from a variety of bacteria, including Rhodopseudomonas spha­

eroides (11-17), Rps. ge/atinosa (18), Rps. viridis (19-22), Rhodospirillum rubrum (15, 16,23-25),and Chromatium vinosum (26). The availability of purified RCs has made it possible to use picosecond and nanosecond spec­ troscopic techniques to study the primary electron transfer reaction in detail. The primary photochemical reaction in the bacterial RC is the oxidation of a complex of bacteriochlorophyll (BChl) molecules that we call

P. (P 635

0066-4154/78/0701-0635$01.00

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frequently is given a subscript such as 870 to indicate the wavelength of the major absorption band of the complex.) When P is excited it transfers an electron to a quinone by way of an intermediate electron acceptor that appears to be a bacteriopheophytin (BPh). (BPh is BChl with two protons replacing the Mg.) This process occurs with a quantum yield near 100% (27), and it takes only about 2 X 10-10 sec. On a slower time scale, the oxidized BChl complex (P+) extracts an electron from a c-type cytochrome, the reduced quinone passes an electron on to another quinone, and further carriers return electrons from the second quinone to the cytochrome, com­ pleting a cycle eventually coupled to ATP synthesis. If the secondary reac­ tions are blocked, the primary electron transfer is fully reversible even at cryogenic temperatures. The photosynthetic apparatus of algae and green plants is considerably more complex. Plants transfer electrons over a much wider range of redox potentials, using two photosystems in series. Photosystem II (PS II) gener­ ates a weak reductant and a strong oxidant that can oxidize H20 to O2. Photosystem I (PS I) generates a weak oxidant and a strong reductant that can reduce ferredoxin and subsequently NADP. The PS II reductant and PS I oxidant are coupled by an electron transport chain. This electron transport scheme is noncyclic, in contrast to the cyclic bacterial system. Like the bacterial reactions, the electron transfer reactions of plants operate with quantum yields near 100% (28). Knowledge of the primary reactions of plants is much less detailed than that of photosynthetic bacteria. Picosecond and nanosecond absorbance measurements have not yet been reported. This is largely because purified RCs are not yet available from plants, although several preparations en­ riched in PS I to a level of one RC per 40 antenna chlorophylls have been obtained (29), and reports of more highly enriched particles have appeared (30, 31). Studies at cryogenic temperatures also are more difficult in plants than in bacteria, because their photochemical reactions usually are partly irreversible at low temperatures. Secondary electron transfer reactions with low activation energies may occur rapidly and prevent electrons from re­ turning by direct back reactions. A purified RC may lack secondary elec­ tron donors and acceptors and exhibit reversible primary reactions at low temperatures. However, some highly enriched PS I preparations are inac­ tive at low temperatures, while retaining activity at room temperature (32, 33). This could mean that the native electron acceptor is missing and that other acceptors are able to substitute at room but not at low tempera­ ture. When little information was available about the electron acceptors, PS I frequently was likened to the bacterial system. Their electron donors are indeed very similar. However, recent work suggests that the bacterial accep-

ELECTRON TRANSFER REACTIONS IN PHOTOSYNTHESIS

637

tor is more like that of PS II. Parallels do exist between bacterial and plant photosynthesis, but the situation is not so simple as it once seemed.

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PHOTOSYNTHETIC BACTERIA

RCs purified from most bacterial species contain three hydrophobic poly� peptides, with molecular weights of approximately 20,000, 24,000, and 30,000, of which only the smaller two are essential for photochemical activity (15, 34). Those from Rps. gelatinosa have only two polypeptides, with molecular weights of about 24,000 and 34,000 (18). Some of the preparations contain additional polypeptides due to tightly bound cyto­ chromes. Purified RCs from Rps. sphaeroides (13,35), Rps. viridis ( 22), and Rds. rubrum (25) have 4 molecules of BChl and 2 of BPh per functional unit. The pigment content has not been analyzed in the preparations from other species, but similarities in the optical absorption spectra indicate that the compositions are likely to be similar. RCs purified from strains that synthe­ size carotenoids also typically contain one molecule of a carotenoid ( 25,36). The BChl, BPh, and the carotenoid all reside on the lightest pair of the three polypeptides (12, 15, 36). In addition, purified RCs usually contain one or more quinones, which can be either Ubiquinone or menaquinone (18, 37, 38), and one atom of nonheme Fe (12). The Fe is missing in some prepara­ tions (21,39) and it can be removed from others or replaced by Mn without destroying photochemical activity (39-41). When the BChl complex is raised to an excited singlet state (P*), it releases an electron, which reduces another component of the RC, I. The reduced acceptor (1-) then transfers an electron to another acceptor, X, which appears to be a quinone. The identity of X was a puzzle for some time, because the electron spin resonance (ESR) spectrum of the reduced acceptor (X-) is anomalous. Rather than the sharp signal near g = 2.00 that is typical of semiquinones, X- has a very broad ESR spectrum with a principal g factor near 1. 8 (12, 41-43). The unusual spectrum evidently results from magnetic interactions between X- and the nonheme Fe of the RC, because removal of the Fe causes the spectrum to become essentially identical with that of the semiquinone of Ubiquinone in vitro (39, 40). Extraction of the quinone, on the other hand, causes the RCs to lose their photochemical activity (37, 44). The activity can be restored by reconstitut­ ing the RCs with ubiquinone or other related quinones. The discordant observation ( 45, 46) that all Ubiquinone could be extracted from C. vinosum chromatophores without affecting the photooxidation of P has been ex­ plained by the finding that a menaquinone acts as the primary acceptor in this species (38). RCs from Rps. viridis also appear to contain menaquinone

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&

PARSON

instead of ubiquinone (19). However, RCs and chromatophores of Rds. rubrum have been reported to retain activity when they contain

The photochemical electron transfer reactions of photosynthetic bacteria and plants.

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