PhowsynthesisResearch 48: 47-53, 1996. (~) 1996KluwerAcademicPublishers. Printedin the Netherlands. Minireview

Pigment protein complexes and the concept of the photosynthetic unit: Chlorophyll complexes and phycobilisomes Elisabeth Gantt Department of Plant Biology & Maryland Experiment Station, University of Maryland, College Park, MD 20742, USA Received6 December1995;accepted 11 March 1996 Key words: light-harvesting antenna, chromophytes, chlorophytes, rhodophytes

Abstract

The photosynthetic unit includes the reaction centers (RC 1 and RC 2) and the light-harvesting complexes which contribute to evolution of one 02 molecule. The light-harvesting complexes, that greatly expand the absorptance capacity of the reactions, have evolved along three principal lines. First, in green plants distinct chlorophyll (Chl) a/b-binding intrinsic membrane complexes are associated with RC 1 and RC 2. The Chl a/b-binding complexes may add about 200 additional chromophores to RC 2. Second, cyanobacteria and red algae have a significant type of antenna (with RC 2) in the form of phycobilisomes. A phycobilisome, depending on the size and phycobiliprotein composition adds from 700 to 2300 light-absorbing chromophores. Red algae also have a sizable Chl a-binding complex associated with RC 1, contributing an additional 70 chromophores. Third, in chromophytes a variety of carotenoid-Chl-complexes are found. Some are found associated with RC 1 where they may greatly enhance the absorptance capacity. Association of complexes with RC 2 has been more difficult to ascertain, but is also expected in chromophytes. The apoprotein framework of the complexes provides specific chromophore attachment sites, which assures a directional energy transfer whithin complexes and between complexes and reaction centers. The major Chl-binding antenna proteins generally have a size of 16-28 kDa, whether of chlorophytes, chromophytes, or rhodophytes. High sequence homology observed in two of three transmembrane regions, and in putative chlorophyll-binding residues, suggests that the complexes are related and probably did not evolve from widely divergent polyphyletic lines. Abbreviations: APC - allophycocyanin; B-phycoerythrin- large bangiophycean phycoerythrin; Chl - chlorophyll; LCM - linker polypeptide in phycobilisome to thylakoid; FCP - fucoxanthin Chl a/c complex; LHC(s) - Chl-binding light harvesting complex(s); LHC I-Chl-binding complex of Photosystem I; LHC II-Chl-binding complex of Photosystem II; P C - phycocyanin; P C P - peridinin Chl-binding complex; P 7 0 0 - photochemically active Chl a of Photosystem I; PS I-Photosystem I; PS II-Photosystem II; RC 1 -reaction center core of PS I; RC 2-reaction center core of PS II; R-phycoerythrin-large rhodophycean phycoerythrin; sPCP-soluble peridinin Chl-binding complex Introduction

The idea of a photosynthetic unit originated with the Emerson and Arnold experiments published in 1932, when they obtained a maximal flash yield of about 1 02 with 2000-3100 Chl molecules. Although beyond the scope of this review, it may be mentioned here that con-

siderable work over the last 50 years has elucidated the components and functioning of the photosynthetic unit. For example, the realization that the two light reactions are interactive and connected by an electron transport chain naturally led to the search for a morphological unit and its spatial arrangement within photosynthetic membranes. Discovery of particles in freeze-fractured

48 granal membranes (Park and Biggins 1964) provided evidence for a structural unit (the 'quantasome'). Fractionation studies of the membranes showed the presence of the expected lipid composition, carotenoids, chlorophylls a and b, and cytochrome b6/f. However, the quantasome was too small to bind thousands of Chl molecules, and disappointingly did not correspond to the anticipated photosynthetic unit particle. Yet, the excitement generated subsequently led to the realization that RC 2 centers, primarily sequestered in the granal regions, are surrounded by Chl a/b-antenna complexes in green plants (Armond et al. 1977; Staehelin 1986). A particular conundrum was the location of the chlorophylls in membranes since maximal energy transfer requires close contact between the chlorophylls and the reaction centers. The idea of how the photosynthetic membrane is constructed was largely influenced by the unit membrane concept modified from the Danielli-Davson lipid bilayer model (Robertson 1966). N o w we know that photosynthetic membranes are made up of intrinsic transmembrane complexes and that chlorophyll molecules exist within an apoprotein framework (Kiihlbrandt et al. 1994). However, in the 1960s it was generally agreed that Chl existed in monolayers between two lipoprotein layers (cf. Weier et al. 1966). Almost 70 years after Engelmann's elegant experiments showed that many different wavelengths in the visible spectrum result in the release of 02 (Engelmann 1883), the role of accessory pigments was rediscovered. In the 1950s precise action spectra were made of differently pigmented algae, all of which showed that phycobiliproteins, Chls c, fucoxanthin and peridinin, in addition to Chls a and b, contributed substantially to photosynthesis. Many of these classical spectra by E T. Haxo, L. R. Blinks and colleagues are preserved in a volume by Allen (1960). An inclusive review by Green and Durnford (1996) demonstrates the extensive progress in the last thirty years.

Green algae and plants Each photosystem can be visualized as consisting of two parts: the reaction center core (RC 1 and RC 2) components, and the peripheral antenna lightharvesting complexes (LHCs) that bind chlorophylls and carotenoids (Figure 1). In green plants LHCs bind Chl a/b and xanthophylls and all are intrinsic membrane proteins. In some marine green algae siphonaxanthin and siphonein are bound together with Chl a/b

CYANOPHYTB:

LUMEN

~J'II.OROPHYTi~:

CHROMORtYT~: Typ.i

Type •

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Chla&oar Chl a/c & mlr

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Chla/b&cir PBS

Figure 1. Schematicmodelof light-harvesting compartmentsin oxygenie organisms:RC 1 (Photosystem I reaction center); RC 2 (Photosystem II reaction center); and the peripheral antenna complexes. Structurally simplest are the cyanophytes(e.g. Synechoccocus) where phycobilisomes (PBS) feed energy to RC 2. In rhodophytes (e.g. Porphyridium) a Chl a-carotenoid complex is attached to RC 1 and PBS to RC 2. In chlorophytes(e.g. Pisum, Chlamydomonas) both reaction centers ate associated with Chl a/b-carotenoid complexes. The greatest complexity is found in the chromophyteswith Chl a/b-carotenoid complexes, but where the association with the RCs is partly inferred. Type I examples include: dinoflagellates (e.g. Gonyaulax) with intrinsic Chl a/c-peridinin complexes and extrinsic Chl a-peridinin complexes; brown algae (e.g. Fucus) and diatoms (e.g. Phaeodactylura) where fucoxanthinis the predominant carotenoid; and xanthophytes (e.g. Pleurochloris) with diodinoxanthin as one of the predominant carotenoids. In Type II organisms (e.g. Cryptomonas) phycobiliproteins in the thylakoid lumen can pass their energy to RCs, which are also associated with intrinsic Chl a/c-carotenoidcomplexes.

to LHC complexes and function as significant light absorbers (cf. Anderson and Barrett 1986). Generally, the xanthophylls lutein, violaxanthin, neoxanthin and loroxanthin (in some green algae) function in protection against photodamage and in stabilizing the chlorophylls in the complexes (Plumley and Schmidt 1987).

49 Fewer accessory polypeptides and less Chl are associated with the core of Photosystem I than with that of Photosystem II in higher plants. Four LHC I polypeptide types are commonly found and typically add an additional 100-120 Chl to the reaction center core for a total of about 210 per holocomplex (Jansson 1994). In addition to binding Chl a and b they bind lutein and violaxanthin. It has been tentatively suggested by Boekema et al. (1990) that 8 LHC I monomers surround each RC 1. However, an aggregation of LHC Is into trimers is also possible (Thornber et al. 1994). LHC IIs have a greater number of polypeptide types in green plants. More energy can be funneled into the Photosystem II core by its LHCs because the LHC II complex is considerably larger and the polypeptide composition is more complex than in LHC I. Thornber and coworkers have separated the complexes of barley, and by using mild detergent treatments they have been able to retain the chlorophylls and xanthophylls. They determined that somewhat over 50% of the total chlorophyll is present in LHC II (Thornber et al. 1994). In contrast, LHC I accounts for only about 18% of the total chlorophyll, while the remainder is in the reaction center cores. About 40% of the total chlorophyll content in barley is bound to LHC IIb (Thornber et al. 1994), which consists of a group of polypeptides of similar size (25-28 kDa) with a Chl a/b ratio of ca. 1.4 and is located in the granal regions. It is a group of considerable complexity, and in fact, up to eight different apoproteins have been identified in this complex (Sigrist and Staehelin 1992). Another set of LHC IIs accounts for about 12% of the chlorophyll. The complexes of LHC II are thought to exist as trimers, and various models have been proposed on how they are associated with the reaction centers (Dreyfuss and Thornber 1994; Jansson 1994; Paulsen 1995; Thornber et al. 1994). Homo-trimers of LHC IIb were crystallized by Ktihlbrandt and have been extremely valuable for the determination of the atomic structure at high resolution (Ktihlbrandt et al. 1994). Each polypeptide binds a minimum of 12 chlorophylls (7 Chl a and 5 Chl b) and two luteins. The model proposed by Ktihlbrandt et al. (1994), based on the 2- dimensional crystal structure and on energy transfer considerations, shows that the Chls are associated with three transmembrane helices, with the Chl a molecules located nearest to the luteins (within less than 5 ,h,), and with Chls b more peripherally placed but within about 5 A of Chl a. Such close proximity of the chlorophylls allows rapid transfer of energy, and the luteins are strategically placed for photoprotection.

Chromophyte algae In chromophyte algae we find the greatest array of accessory pigment types. In addition to Chl a, several types of Chl c are found, as are numerous xanthophylls (Btichel and Wilhelm 1993; Caron et al. 1988; Hiller et al. 1988, 1993; Prezelin 1987). Some chromophytes have an LHC complex with Chl a/b/c (Schmitt et al. 1994), while cryptophytes have Chl a/c complexes in thylakoids and phycobiliproteins in the thylakoid lumen (Lichtl6 et al. 1987). In diatoms and brown algae the intrinsic pigment complexes usually consist of fucoxanthin and Chl a/c (FCP), while in dinoflagellates peridinin is the common photosynthetically active carotenoid in the complexes (PCP). The binding of fucoxanthin or peridinin extends the light harvesting capacity by about 80-100 nm toward the red region. The photosynthetic contribution is less clear for many companion carotenoids in the complexes, including diadinoxanthin, diatoxanthin, heteroxanthin, neofucoxanthin and vaucherixanthin ester. They may be involved in quenching of triplet Chl a or singlet oxygen, or in light-induced epoxidation reactions. Water-soluble peridinin-Chl a-protein complexes (sPCP) are found in many dinoflagellates in addition to intrinsic membrane peridinin Chl a/c complexes (Prezelin 1987; Ogata et al. 1994). A 37 kDa monomer from Alexandrium cohorticula binds 12 peridinin and 2 Chl a molecules (Ogata et al. 1994), which is higher than that from Gonyaulax with 9 peridinins and 2 Chls a (Haxo et al. 1976). Aggregates of sPCP have been proposed to be functionally comparable to phycobilisomes, and in a model by KnStzel and Rensing (1990) they are shown as projecting into the stroma. Whereas a close structural association between sPCP and PCPs is expected, direct visual verification has been elusive. Although photosynthetically functional in transferring energy from peridinin to Chl a, it is not clear if the sPCP is associated with specific thylakoid sites and with the reaction centers. From an analysis of a number of symbiotic dinoflagellates (Heterocapsa pyg-

maea, Symbiodinium microadriaticum, S. kawagutii, S. pilosum) Iglesias-Prieto et al. (1993) conclude that sPCP is a minor light-harvesting complex, and that an intrinsic peridinin-Chl a/c2-protein complex represents the major light-harvesting component. Such a complex contains 40% of the Chl a, 75% of the Chl c2 and 70% of the peridinin. Interestingly, the pigments are bound to a 19-20 kDa apoprotein which is not immunologically recognized by antibodies against sPCP. In Amphidinium carterae Hiller et al. (1993,

50 1995) have sequenced two distinct proteins that bind peridinin. They concluded that the PCP is a member of the universal family with 3 transmembrane helixes (as in green plants), but that the sPCP lacks obvious affinities with other proteins. FCP apoproteins in diatoms (Brown, 1988) and brown algae are reported to range from 16-20 kDa to 28 and even to 50 kDa. The higher molecular weight complexes may be aggregates of 16-20 kDa proteins. In the most widely investigated diatom Phaeodactylum tricornutum, a major FCP with 70% of the total pigment binds Chl a/c-fucoxanthin (with ratios of Chl a:cl:c2:fucoxanthin = 1.0:0.09:0.28:2.22) (Owens and Wold 1986). In brown algae evidence for an association of a fucoxanthin-Chl a/c2-protein complex with PS II, and a violaxanthin-Chl a/cl/c2-protein complex with PS I has been reported (cf. Anderson and Barrett 1986). The fucoxanthin-Chl a/c2-protein complex accounted for 60% of the total pigment, thus suggesting a substantial enhancement of PS II absorption. However, isolation of pigment complexes, especially those functionally associated with reaction centers, remains generally quite difficult, much more so than in chlorophytes and rhodophytes, where conditions are available for isolation of holocomplexes. An interesting FCP supramolecular complex from the brown alga Dictyota dichotoma has been isolated with decylsucrose (Katoh et al. 1989). Such a complex has a molecular mass of about 520 kDa with 189 chromophores. It has 7 monomers, each with 13 Chl a, 3 Chl c, 10 fucoxanthins and 1 violaxanthin. Energy transfer is from Chl c to Chl a and from fucoxanthin to Chl a, without Chl c serving as an intermediary. Similar complexes also exist in other browns, and in fact such a complex has been found associated with P S I (Katoh 1993). Photosystem I holocomplex preparations have been isolated from the xanthophyte Pleurochloris meiringensis containing 525 Chl/P700, as compared to 1750 Chl/P700 in whole cells (Btichel and Wilhelm 1993). Fucoxanthin is not present, but diadinoxanthin is the major carotenoid found in the Chl a/c complex. As in other chromophytic algae less is known about the complex(es) associated with RC 2, but LHC IIs were found in this species as in diatoms (Brown 1988). Cryptophytes, with phycobiliproteins in the thylakoid lumenal space and Chl a/c intrinsic membrane complexes, are among the most unusual members of the diverse chromophyte group. The phycobiliproteins are smaller than those in rhodophytes and cyanobacte-

ria and are devoid of the amino acid sequence stretches that are necessary for aggregation; hence phycobilisomes are absent. Either phycoerythrin or phycocyanin occur in the thylakoid lumen, and they transfer energy directly to Chl a. Lichtl6 et al. (1987) isolated complexes enriched in P700 from Cryptomonas rufescens. In addition to Chl a these complexes had a small amount of Chl c and a high amount of a-carotene, presumably in an LHC I complex. Two PS II complexes were also isolated, one with a high PS II activity contained phycoerythrin while another with low PS II activity was enriched in Chl a/c. Surprisingly both the P S I and PS II fractions were not particulate but consisted of vesicles (0.1/zm diameter), which suggests that the two photosystems have very sizeable domains but are somehow segregated from each other.

Phycobilisome algae The discovery of the participation of brightly colored phycobiliproteins in photosynthesis predated the photosynthetic unit concept by almost 5 decades (Engelmann 1883). Phycobilisomes of cyanobacteria and red algae were the first photosynthetic supramolecular complexes to be characterized (Gantt 1981; Glazer and Melis 1987). At least 2 300 chromophores are contained in one phycobilisome from a red alga like Porphyridium cruentum, while smaller ones in cyanobacteria have ca. 700 chromophores per phycobilisome. Phycobilisomes, attached to the stromal surface of thylakoids, have a central core of APC and specific linkers. The peripheral portion contains rods of phycocyanin which may, depending on the species and light conditions during growth, may have phycoerythrin or phycoerythrocyanin at the periphery and collectively greatly augment the 500 to 650 nm absorptance range. Covalently bound chromophores, stability of the chromoproteins and relative ease of crystallization, have allowed rapid advances in studies of phycobiliprotein structure. The advances in cyanobacteria have been comprehensively reviewed (Bryant 1991; Sidler 1994). The rod-core linker, and rod-rod linkers ensure the functional association between the phycobiliprotein dodecamers within the rods and the junctions of the core rods. Chromophores are generally not bound to linker polypeptides, although they are conspicuous in 3' subunits (linkers) of B- and Rphycoerythrin of red algae and some cyanobacteria (Apt et al. 1995; Glazer and Melis 1987). It is well known that Chl a is the only type of Chl in cyanobacteria and rhodophytes and that phyco-

51 bilisomes serve the light-harvesting function. In fact, phycobilisomes transfer energy directly to PS II, which has been directly verified by isolating phycobilisomePS II complexes (Gantt et al. 1986). Attachment of phycobilisomes to P S I is possible, and in fact, PC has been found to enhance PS I activity in PS Ienriched phycobilisome preparations of Synechococcus (Mullineaux 1992). However, lacking up to this time is confirmation by isolation of a functionally associated phycobilisome-PS 1-complex, similar to the phycobilisome-PS II-particle (cf. Gantt et al. 1986). It appears that in some photoautrophic species of cyanobacteria the amount of Chl associated with PS II is inadequate to provide sufficient energy for normal growth of the organism. The contribution from phycobiliproteins, or at least from partial phycobilisomes, is required. For example, a Synechococcus sp. PCC 7942 mutant that lacks peripheral PC rods, but possesses the APC core and the membrane linker (LcM), is able to survive and grow slowly, unlike the core-less mutant (deficient in PC and APC which is not capable of growth (Bhalerao et al. 1995). In cyanobacteria LHCs seem to be missing and have not been found in association with either RC 1 or RC 2. However, in the red alga Porphyridium cruentum a sizeable LHC I complex has been found. It expands the absorptance capacity of RC 1 (100 Chl a) by at least 70 Chl for a total of 170 Chl a per P700 in the P S I holocomplex (Tan et al. 1995). The red algal LHC I complex is novel in that it binds Chl a, zeaxanthin, and beta-carotene and contains more polypeptides (23.5, 23, 22.5, 22, 21, 19.5 kDa) than LHC Is of green plants. We estimate that 75-80% of the Chl a is associated with PSI and about 18-20% with PS II in P. cruentum. All red algae thus far examined have LHC I complexes (Wolfe et al. 1994a; EX. Cunningham, E. Gantt, S. Tan, unpublished). Attempts to identify LHC II-type polypeptides in red algae and cyanobacteria have been inconclusive so far. Neither immunoprobing of thylakoids, nor examination of isolated PS II preparations showed evidence of LHC IIs (Tan et al. 1995; Wolfe et al. 1994b). Evolution of phycobiliproteins has been examined by comparing amino acid alignments and phylogenetic analysis of over 100 phycobiliprotein sequences (Apt et al. 1995). They exhibit a number of highly conserved sequences, especially in the regions involved with chromophore binding, and with subunit interactions. It appears that the a- and/3-subunits formed two evolutionary groups and probably co-evolved. Interestingly, the eukaryotic phycoerythrins appear to be more

closely related to those of certain marine cyanobacteria, and phycoerythrins from cryptophytes are more closely related to those of rhodophytes than to those of extant cyanobacteria. L H C relatedness

All higher plant LHC apoproteins have sequence homology and show a number of highly conserved motifs. The greatest conservation occurs in the transmembrane helices B (1) and A (3), especially in the regions of chlorophyll binding (Green and Kiihlbrandt 1995). There is little doubt that those in green plants are derived from a common ancestral line (Green and Pichersky 1994; Jansson 1994). Initial evidence, mostly from immunoreactivity tests, also suggested common structural relationships between green plant Chl a/bbinding-proteins and Chl a/c-binding-proteins of chromophytes. This has since been confirmed by sequence comparisons (Hiller et al. 1995; Green and Pichersky 1994; Grossman et al 1990). Green and Pichersky (1994) speculate that the divergence of the LHC I-LHC II probably occurred before the separation of higher plants from the green algae. Although prochlorophytes also contain Chl a/b-binding proteins, they do not cross-react with antibodies made to green plant LHCs or to LHCs from chromophytes. It will be interesting to compare the putative LHC structure with those of other Chl a/b proteins, when the sequences from prochlorophytes become available. Since rhodophytes, like cyanobacteria, have only Chl a and phycobilisomes for light-harvesting, they were until recently considered to have originated independently of the Chl a/b-containing chlorophytes and the Chl a/ccontaining chromophytes. Nevertheless, it was recently shown that the LHC I of P. cruentum is immunologically related to those of higher-plant LHC I and to those of chromophyte fucoxanthin-Chl a/c antenna complexes (Wolfe et al. 1994a). This establishes a clear link between organisms containing phycobilisomes and the chlorophyte and chromophyte groups. We recently cloned and characterized the first red algal LHC I genes (S. Tan, A. Ducret, R. Aebersold, E. Gantt, unpublished). From the deduced amino acid sequence we can predict that the LHC I has three transmembrane helices, two of which are similar to helices B(1) and A(3), and six highly conserved residues that are putative Chl-liganding sites. The pigment content and analysis of the deduced protein structure suggest that LHCs in red algae are primitive and are probably

52 near the base of the ancestral line from which the others evolved. Collectively, the data on LHCs support the idea that the light-harvesting proteins and plastids arose through a monophyletic line (Green and Ktihlbrandt 1995; Green and Pichersky 1994) which is also supported by evidence more fully discussed by Reith (1995).

Conclusion A photosynthetic unit is not a discrete morphological unit, but rather, it is a collection of compartments as suggested in Figure 1. An understanding of the interactive compartments is one of the future challenges of photosynthesis research. We need to know not only the size and composition of each compartment, but for a meaningful understanding it is necessary to determine their spatial relationship within the thylakoid membranes. It is already clear that the RC 1 and RC 2 cores directly interact with their own type, as evidenced by the PS II dimers that have been isolated from green plants and cyanobacteria (Boekema et al. 1995), and the RC 1 trimers that have been repeatedly demonstrated in cyanobacteria. There is little question about the significance of the role of phycobilisomes and LHCs in increasing the absorptance of the RCs. However what additional roles they play in connecting the domains remains to be elucidated. Study of the involvement of LHCs in forming functional domains should be especially interesting and challenging for the chromophyte algae.

Acknowledgements

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This work was supported in part by the Maryland Agricultural Station (Scientific article No. A7835 and contribution No. 9163). The help of B. Grabowski with editing and S. Tan with the illustration is appreciated.

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Pigment protein complexes and the concept of the photosynthetic unit: Chlorophyll complexes and phycobilisomes.

The photosynthetic unit includes the reaction centers (RC 1 and RC 2) and the light-harvesting complexes which contribute to evolution of one O2 molec...
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