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Review Shared Thematic Elements in Photochemical Reaction Centers (Photosynthesis/Chlorbiaceae/Heliobacteriaceae/Iron-Sulfur Clusters/Evolution) John H

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Review Shared Thematic Elements in Photochemical Reaction Centers (Photosynthesis/Chlorbiaceae/Heliobacteriaceae/Iron-Sulfur Clusters/Evolution) John H Proc. Natl. Acad. Sci. USA Vol. 90, pp. 1642-1646, March 1993 Review Shared thematic elements in photochemical reaction centers (photosynthesis/Chlorbiaceae/Heliobacteriaceae/iron-sulfur clusters/evolution) John H. Golbeck Department of Biochemistry, Center for Biological Chemistry, University of Nebraska, Lincoln, NE 68583-0718 ABSTRACT The structural, func- electron is rapidly transferred to the qui- (e.g., Heliobacterium chlorum, Helio- tional, and evolutionary relationships be- none, which acts to stabilize against the bacterium gestii, and Heliobacillus mo- tween photosystem II and the purple non- rapid charge recombination between the bilis) has further stimulated interest in sulfur bacterial reaction center have been primary reactants. these organisms as evolutionary precur- recognized for several years. These can be As depicted in Table 1, the identities of sors of PSI (ref. 7; see also ref. 8). classified as "quinone type" (type I) pho- the components and the kinetics of the PSI is considered an "iron-sulfur- tosystems because the terminal electron initial forward electron transfer reactions type" RC in which the bound primary acceptor is a mobile quinone molecule. are remarkably similar in the purple bac- quinone, A1, donates its electron to an The analogous relationship between pho- terial RC, PSII, and PSI. A further shared iron-sulfur cluster (probably Fx) instead tosystem I and the green sulfur bacterial feature is that the photoactive compo- of to the secondary quinone (reviewed in (and heliobacterial) reaction centers has nents are located on a chlorophyll- ref. 9). Fx is a rare example of an inter- only recently become dear. These can be containing, homo- or heterodimer that is polypeptide [4Fe-4S] cluster that occu- dcassified as "iron-sulfur type" (type I) predicted to possess an overall C2 axis of pies the same relative position as the photosystems because the terminal elec- symmetry (this is only known for certain non-heme iron in the purple bacterial RC tron acceptor consists of one or more in the purple bacterial RC). The differ- and in PSII. However, it may serve a bound iron-sulfur clusters. At a funda- ences between the various RCs lie largely very different function. Unlike the non- mental level, the quinone type and iron- in the details of the protein scaffold that heme iron in quinone-type RCs, Fx is sulfur type reaction centers share a com- modulates the redox potentials of the thought to undergo redox chemistry un- mon photochemical motif in the early pro- photoactive components and in the iden- der physiologically relevant conditions. cess of charge separation, leading to the tities of the secondary electron donors Its role in PSI may be to divert the speculation that al photochemical reac- and acceptors that have evolved to pro- electron out of the membrane phase and tion centers have a common evolutionary vide the specialized functions of water into the stromal phase, leading to the origin. This review summarizes the cur- oxidation in PSII and nicotinamide ade- reduction of soluble ferredoxin through rent state of knowledge in comparative nine dinucleotide phosphate (NADP+) the involvement of the bound iron-sulfur reaction center biochemistry between pro- reduction in PSI. It is the purpose of this clusters FA and FB. The function of the karyotic bacteria, cyanobacteria, and article to review recent developments in secondary quinone in PSI is not known. green plants. the area of comparative RC biochemistry PSI is a heterodimer of 82- and 83-kDa and examine the evolutionary implica- polypeptides labeled PSI-A and PSI-B. tions offound similarities in structure and These proteins are highly hydrophobic, General Features of Photochemical function. each transversing the thylakoid mem- Charge Separation brane up to 11 times. The psaA genes PSI and the Chlorobium RC predict polypeptides of 739-751 amino All known classes of photochemical re- acids, and the presence of a short N-ter- action centers (RCs)-photosystem I The functional relationship between the minal extension is the only significant (PSI) and photosystem II (PSII) in green purple bacterial RC and PSII in green difference in length between the prokary- plants and cyanobacteria and the purple plants and cyanobacteria has been appar- otic and eukaryotic sequences. The psaB non-sulfur bacterial and green sulfur bac- ent for nearly a decade: both are consid- genes predict polypeptides of 733-736 terial RC-are now recognized to share a ered "quinone-type" photosystems in amino acids that are similar in length in strikingly similar motif. This shared which the bound primary quinone, QA, prokaryotes and eukaryotes. The higher theme consists of a dimeric protein core donates its electron across the het- plant sequences are about 95% identical, that functions as a scaffold for antenna erodimeric protein boundary to a mobile and when conservative replacements are chlorophylls and a series of bound elec- secondary quinone, QB (reviewed in refs. considered, the higher plant, green algal, tron donors and acceptors that serve to 1 and 2). Due to the overwhelming sim- and cyanobacterial sequences are 95% stabilize the initial charge separation be- ilarity in structure and function, it is well similar. The psaA and psaB sequence tween primary electron donor and accep- accepted that the purple bacterial RC and classes are 45% identical in sequence to tor. A "generic" photochemical RC can PSII share a common ancestor. In con- one another and another 10% when con- be depicted with the following notation: trast, there has been no definitive bacte- servative amino acid replacements are hi. rial analog for PSI. However, a series of considered. This high degree of homol- recent publications have provided excel- PIQ hP*IQP+I-QP+I Q, ogy strongly suggests that the sequences lent evidence that the RC in green sulfur arose by duplication and divergence from where P is a chlorophyll primary electron bacteria of the genus Chlorbiaceae (e.g., a single ancestral gene. The high degree donor, I is a chlorophyll primary electron Chlorobium limicola f. thiosulfato- acceptor, and Q is a quinone secondary philum, Chlorobium phaeobacteroides, In Abbreviations: PSI, photosystem I; PSII, pho- electron acceptor. this generalized Chlorobium vibriforme) contains bound tosystem II; RC, reaction center; ESR, elec- RC, the absorption of a photon results in iron-sulfur clusters (3-6). The discovery tron spin (paramagnetic) resonance; S/N, sig- charge separation between the chloro- of iron-sulfur clusters in Gram-positive nal-to-noise; NADP+, nicotinamide adenine phyll donor and acceptor molecules. The bacteria of the genus Heliobacteriaceae dinucleotide phosphate. 1642 Downloaded by guest on September 29, 2021 Review: Golbeck Proc. Natl. Acad. Sci. USA 90 (1993) 1643 Table 1. Shared components and kinetics of photochemical charge separation tical and the cyanobacterial sequences Purple non-sulfur bacteriat are >90% identical, and virtually all P860 BPh QA h P8* BPh QA -O P860+ BPh- QA C P860+ BPh QA- amino acid substitutions are conservative Photosystem Ilt replacements. The primary sequence Phye Ph QA -Vh p* Ph QA 2 P68o+ Ph- QA C P68o+ Ph QA contains nine cysteine residues and two Photosystem I§ I<. PS CxxCxxCxxxCP motifs characteristic of P7oo Ao Al 1-SPspoo* Ao Al 10~sP7oo+ Ao- Al S20P P700+ Ao Al- proteins that contain [4Fe-4S] clusters. A very similar folding pattern is exhibited tp8w is a bacteriochlorophyll dimer, BPh is a bacteriopheophytin monomer, and QA is a bound the ferredoxin from Pepto- molecule of menaquinone in Rhodobacter sphaeroides. by 2[4Fe-4S] tP680 is a chlorophyll a monomer or dimer, Ph is a pheophytin monomer, and QA is a bound coccus aerogenes (15) and the [3Fe- molecule of plastoquinone in cyanobacteria and green plants. 4S][4Fe-4S] ferredoxin fromAzotobacter §P7oo is a chlorophyll a dimer; Ao is a chlorophyll a monomer, and A1 is a tightly bound vinelandii (16), and there are significant molecule of phylloquinone (or 5'-monohydroxyphylloquinone) in cyanobacteria and green regions of homology with ferredoxins plants. from Desulfovibrio gigas (17) and Bacil- lus thermoproteolyticus (18) that contain of primary sequence similarity between erodimer. The sequence similarities indi- a single [4Fe-4S] cluster. Although the the subunit classes also leads to the ex- cate that the divergence of the green three-dimensional structure of PSI-C is pectation that the three-dimensional sulfur bacterium from PSI occurred be- not (yet) available, there is enough se- structures of the two subunits will be fore the gene duplication event that led to quence homology with the 54-amino acid similar. the heterodimeric protein core of the PSI P. aerogenes ferredoxin and the fist 58 The recent sequencing of the RC gene RC. The strong implication is that the residues of the 106-amino acid A. vine- from C. limicola f. thiosulfatophilum heliobacterial and green sulfur bacterial landiiferredoxin to make meaningful pre- now places the green sulfur bacteria on RCs and PSI shared a common ancestor. dictions of tertiary structure. secure footing with PSI (10). The gene Gene duplication in the L and M subunits The P. aerogenes protein shows a re- encodes a protein of730 amino acids with ofbacteria and the Dl and D2 subunits of markable two-fold rotation symmetry a calculated mass of 82 kDa. The pre- PSII may have also taken place indepen- axis related to the two iron-sulfur binding dicted protein is highly hydrophobic, dently, which indicates that the purple sites (reviewed in refs. 19 and 20). When containing up to 11 transmembrane seg- bacterial and cyanobacterial precursors the protein is rotated 1800 around the ments. Although the similarity of amino also shared a single common ancestor symmetry axis, the main chain atoms acid residues is only 15% with PSI-A and (13). Accordingly, Dl did not descend approximately overlay, but the iron- 14% with PSI-B, this may not be the from L and D2 did not descend from M; sulfur clusters superimpose almost ex- problem it first appears.
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