Photosynthesis Research
1 0 : 3 3 7 - 3 4 6 (1986) © Martinus N i j h o f f Publishers, Dordrecht - Printed in the Netherlands
ELECTRON DONORS AND ACCEPTORS
IN PHOTOSYNTHETIC
337
REACTION CENTERS
J. AMESZ and L.N.M. DUYSENS Department of Biophysics, Huygens Laboratory of the State University, P.O. Box 9504, 2300 RA Leiden, The Netherlands
I. SUMMARY A review is given of primary a n d associated electron transport reactions in various divisions of photosynthetic bacteria and in the two photosystems of plant photosynthesis.Two types of electron aceeptor chains are distinguished: type 'Q', found in purple bacteria, Chloroflexus and system II of oxygenic photosynthesis and type 'F', found in green sulfur bacteria, Heliobacterium and photosystem I. Secondary donor reactions are discussed in relation to plant photosystem II. 2. INTRODUCTION There is a large body of evidence (see ref. 62 for a review) that in all photosynthetic organisms the primary photochemical reaction consists of the transfer of an electron from an excited chlorophyll (Chl) a or bacteriochlorophyll (BChl) a or b molecule (P), to an acceptor, usually called I. The electron is--subs-equently transferred from I- to other acceptors. In each electron transfer step a more stable (longer lived) charge separation is established. Additional stabilization occurs by transfer of an electron from a donor molecule (D), e.g. a cytochrome, to oxidized P, P+. These reactions thus can be written as: *
D P I X
I
+
-
> D P I X
2
+
> D P I X-
3
> D+P I X-
Reactions I, 2 and 3 occur, depending upon the species, in times of about 10 ps or less, of 50 - 600 ps, and of 0.1 - 200 ~s, respectively. The multistep electron transfer is required to transfer the electron extremely rapidly across the membrane, a relatively large distance of 5 rim. The rapidity is necessary for a good quantum yield: t h e electron transfer rate should be much higher than the decay rate of P~ which is of the order of 109 s -I. Rapid electron transfer is possible if the transferring molecules are so close to each other that the electron wavefunctions overlap. This requires three or more molecules (such as Chl) to bridge the gap across the membrane. In addition, the large transmembrane distance slows down the back transfer of the electron from X- to D +, so that these compounds have sufficient time to be restored to X and D by the subsequent dark reactions of photosynthesis. This short review will mainly deal with the characteristics of the electron acceptor chain in reaction center complexes of various photosynthetic systems and organisms, with emphasis on recent developments. Donor reactions will be only discussed in relation to photosystem II of oxygenic photosynthesis. For more extensive reviews the reader is referred to refs. 2,4,5,17,36,62,67 and 83. Dedicated to the memory of Warren L. Butler
[1911
338
[192]
3. THE TYPE Q ACCEPTOR CHAIN As will be discussed in this and the next section, the primary electron acceptor chains found in various divisions of photosynthetic bacteria and in the two photosystems of plant photosynthesis may be divided into two types, which we call Q and F, that can be distinguished on basis of the chemical nature and midpoint potentials of the electron acceptors involved. Type Q is found in purple bacteria, Chloroflexus and system II of oxygenic photosynthesis. It may be summarized by the following set of reactions +
--
+
--
+
P I QAQB ~ P I QAQB ~ P I QA QB ~ P I QAQB
)
where I is pheophytin (Pheo) a or bacteriopheophytin (BPheo a or b and QA and QB are bound quinones (u-biquinone, menaquinone or plasto--quin~ne). QA and QB together serve to reduce QB to the quinol by two one-electron transfers from I-, accompanied by the uptake of protons. Reduced QB is then restored to the oxidized state, presumably by exchange with a quinone molecule from a large pool in the membrane (19,29,88). 3.1. Purple bacteria and Chloroflexus The primary and secondary electron transport reactions have been studied much more extensively in purple bacteria than in other organisms. The main reason was the availability of isolated reaction center complexes, obtained from cytoplasmic membranes of various species of purple bacteria by means of detergents. These reaction center complexes have been characterized in terms of their chemical constituents (for reviews see refs. 32 and 58). They all contain four BChl a or b and two BPheo a or b molecules, one molecule of carotenoid (exce~ fo--r some mutant-s like Rhodobacter (Rhodopseudomonas) sphaeroides R-26) and, depending on preparation and species, one non-heme iron or manganese (68) and one or two qulnone molecules. The use of isolated reaction centers enabled the application of flash spectroscopy and various electron spin resonance techniques with better precision than with intact cells or isolated membranes. These studies need not be reviewed here; the reader is again referred to refs. 17 and 62. CYTOPLASM
PERIPLASMIC SPACE
Fe
i
Menaquinone
/'OA'
~specia|pair of B[hl
BCh[
( p)
FIGURE I. Arrangement of reaction center components as determined by X-ray diffraction analysis of a crystalline reaction center complex of Rps. vlridis. Redrawn from ref. 20. The figure was kindly provided to us by Dr. H.J. van Gorkom.
[193]
339
A new and important step in photosynthesis research is the crystallization of the reaction center complex of Rhodopseudomonas viridis (51, 52), and the subsequent X-ray analysis of its structure (20,21). Together with the primary structure of the constituent polypeptides (see 1,53), the results of the X-ray analysis provide a three-dimenslonal picture of the organization of the reaction center that rapidly becomes more detailed. The often debated (e.g. 24,61) question of whether the primary electron donor P is a (B)Chl dimer has been resolved at least for Rps. viridis by the X-ray data (20). The density distribution, at 3 A resolution, showed the location and orientation of the four BChl, two BPheo, and one menaquinone (Figure I) that are contained in the reaction center. Two BChl molecules are close together, at a center-to-center distance of 7 A, and apparently represent the P dimer. The arrangement of BChl and BPheo shows roughly a two-fold rotation symmetry about an axis perpendicular to the membrane (9) and passing through, the middle of P Presumably, electron transfer occurs from excited P, P*, via the BChl (73) and BPheo (I) at the right hand slde of Figure I to the menaquinone (QA) (66). The BChl at the left hand side can be removed or modified without affecting the quantum efficiency for electron transfer (50,74). The ubiquinone that serves as secondary electron acceptor QB is missing in the crystals. The protein moiety of the reaction center complex shows ten helical stretches of amino acid residues (21) that belong to the so-called L and M subunits (58). Recent evidence has shown that Chloroflexus aurantiacus, which was classified as a green bacterium (63) on the basis of its morphological Era(mY) -1000 -800 -600
25ns/ / /
X TeV
1.43 e~
//
-z,O0
;
ps / ,,
-200
/ g0p.s ~ /
0 II
200 400
//
II
x/
_.1
c-ss~o~
ii
/t"
/ I
/
/
13ms(SK}
//
i//
[-~'~"~ ..___---~-554
1 0 : 3 3 7 - 3 4 6 (1986) © Martinus N i j h o f f Publishers, Dordrecht - Printed in the Netherlands
ELECTRON DONORS AND ACCEPTORS
IN PHOTOSYNTHETIC
337
REACTION CENTERS
J. AMESZ and L.N.M. DUYSENS Department of Biophysics, Huygens Laboratory of the State University, P.O. Box 9504, 2300 RA Leiden, The Netherlands
I. SUMMARY A review is given of primary a n d associated electron transport reactions in various divisions of photosynthetic bacteria and in the two photosystems of plant photosynthesis.Two types of electron aceeptor chains are distinguished: type 'Q', found in purple bacteria, Chloroflexus and system II of oxygenic photosynthesis and type 'F', found in green sulfur bacteria, Heliobacterium and photosystem I. Secondary donor reactions are discussed in relation to plant photosystem II. 2. INTRODUCTION There is a large body of evidence (see ref. 62 for a review) that in all photosynthetic organisms the primary photochemical reaction consists of the transfer of an electron from an excited chlorophyll (Chl) a or bacteriochlorophyll (BChl) a or b molecule (P), to an acceptor, usually called I. The electron is--subs-equently transferred from I- to other acceptors. In each electron transfer step a more stable (longer lived) charge separation is established. Additional stabilization occurs by transfer of an electron from a donor molecule (D), e.g. a cytochrome, to oxidized P, P+. These reactions thus can be written as: *
D P I X
I
+
-
> D P I X
2
+
> D P I X-
3
> D+P I X-
Reactions I, 2 and 3 occur, depending upon the species, in times of about 10 ps or less, of 50 - 600 ps, and of 0.1 - 200 ~s, respectively. The multistep electron transfer is required to transfer the electron extremely rapidly across the membrane, a relatively large distance of 5 rim. The rapidity is necessary for a good quantum yield: t h e electron transfer rate should be much higher than the decay rate of P~ which is of the order of 109 s -I. Rapid electron transfer is possible if the transferring molecules are so close to each other that the electron wavefunctions overlap. This requires three or more molecules (such as Chl) to bridge the gap across the membrane. In addition, the large transmembrane distance slows down the back transfer of the electron from X- to D +, so that these compounds have sufficient time to be restored to X and D by the subsequent dark reactions of photosynthesis. This short review will mainly deal with the characteristics of the electron acceptor chain in reaction center complexes of various photosynthetic systems and organisms, with emphasis on recent developments. Donor reactions will be only discussed in relation to photosystem II of oxygenic photosynthesis. For more extensive reviews the reader is referred to refs. 2,4,5,17,36,62,67 and 83. Dedicated to the memory of Warren L. Butler
[1911
338
[192]
3. THE TYPE Q ACCEPTOR CHAIN As will be discussed in this and the next section, the primary electron acceptor chains found in various divisions of photosynthetic bacteria and in the two photosystems of plant photosynthesis may be divided into two types, which we call Q and F, that can be distinguished on basis of the chemical nature and midpoint potentials of the electron acceptors involved. Type Q is found in purple bacteria, Chloroflexus and system II of oxygenic photosynthesis. It may be summarized by the following set of reactions +
--
+
--
+
P I QAQB ~ P I QAQB ~ P I QA QB ~ P I QAQB
)
where I is pheophytin (Pheo) a or bacteriopheophytin (BPheo a or b and QA and QB are bound quinones (u-biquinone, menaquinone or plasto--quin~ne). QA and QB together serve to reduce QB to the quinol by two one-electron transfers from I-, accompanied by the uptake of protons. Reduced QB is then restored to the oxidized state, presumably by exchange with a quinone molecule from a large pool in the membrane (19,29,88). 3.1. Purple bacteria and Chloroflexus The primary and secondary electron transport reactions have been studied much more extensively in purple bacteria than in other organisms. The main reason was the availability of isolated reaction center complexes, obtained from cytoplasmic membranes of various species of purple bacteria by means of detergents. These reaction center complexes have been characterized in terms of their chemical constituents (for reviews see refs. 32 and 58). They all contain four BChl a or b and two BPheo a or b molecules, one molecule of carotenoid (exce~ fo--r some mutant-s like Rhodobacter (Rhodopseudomonas) sphaeroides R-26) and, depending on preparation and species, one non-heme iron or manganese (68) and one or two qulnone molecules. The use of isolated reaction centers enabled the application of flash spectroscopy and various electron spin resonance techniques with better precision than with intact cells or isolated membranes. These studies need not be reviewed here; the reader is again referred to refs. 17 and 62. CYTOPLASM
PERIPLASMIC SPACE
Fe
i
Menaquinone
/'OA'
~specia|pair of B[hl
BCh[
( p)
FIGURE I. Arrangement of reaction center components as determined by X-ray diffraction analysis of a crystalline reaction center complex of Rps. vlridis. Redrawn from ref. 20. The figure was kindly provided to us by Dr. H.J. van Gorkom.
[193]
339
A new and important step in photosynthesis research is the crystallization of the reaction center complex of Rhodopseudomonas viridis (51, 52), and the subsequent X-ray analysis of its structure (20,21). Together with the primary structure of the constituent polypeptides (see 1,53), the results of the X-ray analysis provide a three-dimenslonal picture of the organization of the reaction center that rapidly becomes more detailed. The often debated (e.g. 24,61) question of whether the primary electron donor P is a (B)Chl dimer has been resolved at least for Rps. viridis by the X-ray data (20). The density distribution, at 3 A resolution, showed the location and orientation of the four BChl, two BPheo, and one menaquinone (Figure I) that are contained in the reaction center. Two BChl molecules are close together, at a center-to-center distance of 7 A, and apparently represent the P dimer. The arrangement of BChl and BPheo shows roughly a two-fold rotation symmetry about an axis perpendicular to the membrane (9) and passing through, the middle of P Presumably, electron transfer occurs from excited P, P*, via the BChl (73) and BPheo (I) at the right hand slde of Figure I to the menaquinone (QA) (66). The BChl at the left hand side can be removed or modified without affecting the quantum efficiency for electron transfer (50,74). The ubiquinone that serves as secondary electron acceptor QB is missing in the crystals. The protein moiety of the reaction center complex shows ten helical stretches of amino acid residues (21) that belong to the so-called L and M subunits (58). Recent evidence has shown that Chloroflexus aurantiacus, which was classified as a green bacterium (63) on the basis of its morphological Era(mY) -1000 -800 -600
25ns/ / /
X TeV
1.43 e~
//
-z,O0
;
ps / ,,
-200
/ g0p.s ~ /
0 II
200 400
//
II
x/
_.1
c-ss~o~
ii
/t"
/ I
/
/
13ms(SK}
//
i//
[-~'~"~ ..___---~-554
