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THEJOURNAL OF BIOLOGICAL CHEMISTRY Minireview Vol. 264, No. 1, Iseue of January 5, pp. 1-4, 1989 0 1989 by The American Society for Biochemistry and Molecular Biology, Inc. Printed in U.S.A. complex containing hundreds of chromophores to be delivered to a reaction center with an efficiency exceeding 95%. Light Guides Bilins DIRECTIONALENERGY TRANSFERIN A PHOTOSYNTHETIC ANTENNA* Red algae and cyanobacteria may appear blue-green, purple, red, orange, or yellow in color. The pigmentation is a composite of contributions from the chlorophyll a and @-caroteneinvariably present inthese organisms and of the predominating phycobiliprotein(s) which they may contain. The distinctive colors of different phycobiliproteins are in turn dependent on the nature of the covalently attached tetrapyrrole (bilin) prostheticgroups. The structures of the bilins are shown in Fig. 1 in colors which approximate closely those of neutral solutions of the appropriate bilin peptides. Two important points emerge from examination of these structures. The compounds shown in Fig. 1 are isomers differing only in the arrangement of double bonds. The diverse colors generated in this simple manner span almost the total range of visible wavelengths from a maximum at 495 nm for phycourobilin (PUB)' to one a t 620 nm for peptidebound phycocyanobilin (PCB). The second point is that the bilins are in each instance bound to cysteinyl residues through ring A and that bilins linked through both rings A and D to cysteinyl residues 10 residues apart in the linear amino acid sequence are also present. The most important way in which the diversity of phycobiliprotein spectra is generated is by variation in the structure of the bilin prosthetic groups. Alexander N. Glazer From the Department of Microbiology and Immunology, University of California, Berkeley, California 94720 Light Harvesting in Photosynthesis The light reactions of photosynthesis begin with the absorption of a photon by a pigment-protein (antenna) complex. In a series of radiationless transfers the excitation energy is conveyed from one light-harvesting chromophore to another ending at a special pair of chlorophyll (or bacteriochlorophyll) molecules within a transmembrane reaction center complex. Its arrival promotes a separation of charge which is stabilized by several consecutive electron transfer steps within the reaction center. In general, each reaction center is associated with an antenna complex containing several hundred light-harvesting pigment molecules. The requirement for a large antenna is evident from the following considerations. The light reactions described above are s, whereas about 0.02 s are required for the complete in about completion of the dark reactions of photosynthesis. The frequency of absorption events ( n )for a molecule is determined by the equation n = 4 X lo-'' EN,,., where t is the molar extinction coefficient/molecule and Nhuis the light flux in quanta/(s .cm2). Indirect sunlight a t noon the light flux is 1017visible quanta/(s. cm2).Assuming an average of 3 X lo' for visible light for antenna pigment molecules such as chlorophylls and bilins, one molecule would absorb about 12 quantal s. Since the dark reactions of photosynthesis require 8 quanta/0.02 s (l),photosynthesis would be light-limited even under such very intense light flux unless some 34 accessory pigment molecules were able to supply a reaction center. Adaptations to low light intensity can be dramatic. Green sulfur bacteria have over 2000 antenna bacteriochlorophyll molecules associated with each reaction center. Clayton (2) noted that a culture of these organisms ". . . growing in a 30-liter jug, illuminated only by a 25-watt tungsten lamp, soon resembles liquid spinach." Different photosynthetic organisms have distinctive antenna and reaction center structures (3). Clarification of many features of the conversion of excitation energy to electron flow within reaction centers has resulted from the elegant crystallographic and spectroscopic studies of such complexes from purple bacteria (4, 5). Comparable information is now accumulating on a light-harvesting complex, the phycobilisome,present incyanobacteria ("blue-green algae") and red algae. The purple bacterial reaction center has served as a paradigm for reaction centers of higher plants (6). Inthe same manner, the understanding of the principles that govern the structure and function of the phycobilisome can guide the study of other lightharvesting assemblies. The greatest diversity of antenna pigments is seen among the marine algae (2, 3, 7). For example, phycobiliproteins play this role in red algae and in cyanobacteria, while brown algae, diatoms, and dinoflagellates utilize protein complexes with carotenoids such as fucoxanthin and peridinin. The value of these particular complexes can be readily rationalized on an ecological basis. Their absorption spectra lie in the region of maximum light transmission through seawater (7). Phycobiliprotein-containing organisms show the greatest range of spectral variation in their antenna pigments and the greatest adaptabilityto thequality and quantity of incident radiation. In this reviewwe examine the structural features that permit an excitationquantum absorbed at any location within anantenna Phycobiliproteins The majority of antenna complexes and all reaction center complexes are membrane proteins. In contrast, the phycobiliproteins are highly water-soluble. They are extraordinary in yet another respect. The chromophores of all other photosyntheticcomplexes are extractable by organic solvents, but, as noted above, those of the phycobiliproteins are covalently attached to the polypeptides. The unusual properties of these intensely colored brilliantly fluorescent proteins did not go unnoticed by early investigators. A comment made by Sorby in 1877 (11) "It would be difficult to find another series of colouring matters of greater beauty or with such remarkable and instructive chemical and physical peculiarities" has not been challenged. The phycobiliproteins are an artifact of purification. In intact cells they are components of a large macromolecular structure which breaks down as soon as the cells are ruptured unless very special precautions are taken to stabilize the phycobilisomes (12). Phycobiliproteins should therefore be regarded as highly ordered subassemblies which preserve to a varying degree the supramolecular structure which they possessed in the intact phycobilisome (8).Certain properties of these building blocks can be clearly defined. The phycobiliproteins each consist of two dissimilar polypeptide chains, a and @, of approximately 17 and 18 kDa, respectively. Each polypeptide chain carries one or more covalently attached bilins. The amino acid sequences of numerous phycobiliproteins have been determined either directly or from the DNA sequence of the relevant genes. The sequences of the a and @ subunits of a given phycobiliprotein are related to each other and to those of the corresponding subunits of other phycobiliproteins (13, 14). These proteins have all evolved from a common ancestral gene. Purification of native phycobiliproteins by conventional methods frequently leads to the isolation of either a trimeric, ((Y@)B, or hexameric, (CY&, complex. Some phycobiliproteins are isolated either as a@ or (a@)2 forms or as equilibrium mixtures of varying aggregates. The outcome depends on the purification protocol and on the organismal source of the protein (15). Certain phycoerythrins are isolated as assemblies with the composition (a@)67,where the y subunit has a molecular weight of 30,000. Phycobiliprotein trimers are disc-shaped with a thickness of 30 A and a diameter of 120 A the hexameric molecules are face-toface dimers of the trimeric assemblies. Evidence from electron microscopy and from a variety of spectroscopic studies indicates that * This work wassupported in part by National Science Foundation Grant DMB 85-18066 and National Institutes of Health Grant GM 28994. ' The abbreviations used are: PUB, phycourobilin; PCB, phycocyanobilin; PEB, phycoerythrobilin. 1 Minireview: Directional Energy Transfer in Phycobilisomes L A Peptide-linked PHYCOCYANOBILIN possible to compare the position of the bilin attachment sites in proteins with increasing numbers of bilins/subunit (see Fig. 2). Allophycocyanin has the smallest number of bilins, one PCB/subunit. These are attached a t a-84 and 8-84 (C-phycocyanin residue numbering is used throughout, see Ref. 13). The three PCBgroups in Cphycocyanin are a t a-84, 8-84, and 8-155. C-phycoerythrin carries five PEB groups a t or-84, a-l43a, 8-84, 8-155, and 8-50,61 (linked through both rings A and D) (16). The a-143a attachment site is on a short inserted sequence; the 8-50,61 site appears to have been generated by amino acid substitutions. Conservation of sites of attachmentis seen in all of the phycobiliproteins. The important finding is that the location of the bilin residue in theprimary structure is fmed whereas the chemical nature of the bilin a t a given site differs from one phycobiliprotein to another. Peptide-linked PHYCOBlLlVlOLlN C Phycobilisome Structure and Assembly )tide- 1 “ Peptide-linked PHYCl FIG. 1. Bilin structures and bilin-peptide linkages in phycobiliproteins (see Refs. 8-10 for complete references). PROTEIN TYPF OF R I U BILINS/(ap)3 PCB PEB PXB PUB I I In intact cells, phycobilisomes form regular arrays on the cytoplasmic face of the thylakoid membranes. The morphology of phycobdisomes varies with the source organism (17-20). The particles may be ellipsoidal, hemidiscoidal, or bundles of rod-shaped elements. These differences in gross morphology do not reflect fundamental differences in the placement of the major phycobiliproteins or in the functional properties of this particle. Phycobilisomes range in size from about 7 X lo6 to about 15 X lo6 daltons. The particles may be detached intact from the thylakoid membranes with detergents such as Triton X-100 in high concentrations of NaK-phosphate buffers, 0.65-1.0 M,pH 7-8, and purified by sucrose density gradient centrifugation (12). The particles are stable only in the presence of such high concentrations of NaK-phosphate or sodium sulfate. Isolated phycobilisomes retain full functional integrity as assessed by comparison of the kinetics of energy transfer from one phycobiliprotein to the next in the purified particles and in intactcells (e.g. Refs. 21 and 22). Hemidiscoidal phycobilisomes are common among cyanobacteria and one such phycobilisome, that of Synechocystis PCC6701,is described here. This phycobilisome consists of two morphologically distinct domains-a triangular core made up of three cylindrical elements from which emana? six rods (Fig. 3). Each core element is made up of four 30 X 115-A discs, whereas the rods are stacks of 60 X 120-A double discs. Detailed analyses of incomplete phycobilisomes from mutant cyanobacteria, of phycobilisome subassemblies isolated by partial dissociation, and of structures formed in in vitro reconstitution experiments have led to the picture of phycobilisome structure shown in Fig. 4, which details the correspondence between the morphological elements revealed by electron microscopy (Fig. 3) ll 6 6 0 B 8 16 BILINS/( 34 34 FIG. 2. Bilin compositionandcontent in variousphycobiliproteins. The colors in the fist column approximate closely those of dilute solutions of each of the phycobdiproteins. The number of bilins given in the vertical colored columns is per a8 monomer, except for B- and R-phycoerythrii where the numbers given are per (&)gy. Allophycocyanin B and allophycocyanin have one bilin/subunit, while C- and R-phycocyanin and phycoerythrocyanin have one bilin on the a subunit and two bilins on the 8 subunit. C-, B-, and Rphycoerythrins have two bilins on the a subunit and three on the 8 subunit. The y subunit of B- and R-phycoerythrins carries four bilins. PXB, cryptoviolin. these complexes share common structural featureswith those within phycobilisomes. Fig. 2 shows the number and type of bilins carried by various phycobiliproteins. The color of a given phycobiliprotein is not determined solely by the chemical nature of ita bilins. For example, Cphycocyanin and allophycocyanin both carry only PCB groups, yet C-phycocyanin has .a, X a t 620 nm and allophycocyanin at 650 nm. The spectroscopic properties of each bilin within a phycobiliprotein are strongly influenced by the conformation and environment imposed on the bilin by the native protein. Inter-a8 interactions also make an important contribution. For example, monomeric (a8)allophycocyanin has a, X a t 615 nm whereas, X of ab)^ lies at 650 nm. When the amino acid sequences of the polypeptide chains of the phycobiliproteins are aligned so as to maximizehomology, it is FIG. 3. Electronmicrograph of Synechocystis PCC6701 phycobilisomes negatively stainedwith uranyl formate. The width of a rod substructure is 120 A. Minireview: Directional Energy Transfer in Phycobilisomes A ' \ I I ROD COMPLEXES C is mode up of 2 copies each of FIG.5. Crystal structure of C-phycocyanin.Structure of the Mastigoclodus laminosus C-phycocyanin trimer projected down the crystallographic 3-fold axis. C" backbone (a-subunit, brown; &subunit, green) and PCB chromophores (a-84, violet; 8-84, pink; 0-155, blue) are shown (courtesy of Dr. R. Huber; see Ref. 28). CORE COMPLEXES FIG.4. Schematic representation of the phycobilisome from protein is long. In contrast, the preferred conformation of bilins in Synechocystie PCC6701. A rod is made up of hexameric bilipro- free solution is cyclohelical (8, 30). The latter conformation is chartein complexes, each of which is attached through its specific linker polypeptide to the component adjacent to it in the phycobilisome. The abbreviations A P , PC, and PE are used for allophycocyanin, p", etc. for the a and 8 phycocyanin, and phycoerythrin, and 8, subunits of these proteins. Linker polypeptides are abbreviated L, with a superscript denoting the apparent size X lo3 daltons, and a subscript that denotes the location of the polypeptide: R, rod substructure; RC, rod-core junction; C, core; CM, core-membrane region (modified from Ref. 8). and their polypeptide composition (for reviews, see Refs. 8, 14, 23, and 24). Results of analyses of phycobilisomes assembled by organisms in which individual polypeptide components have been deleted by insertional inactivation of structural genes are fully consistent with this structure (25). The assembly of the phycobilisome is mediated by a group of polypeptides named "linker" polypeptides (26, 27). As indicated in Fig. 4, each of the trimeric or hexameric subassemblies of the phycobilisome contains at least one specific linker polypeptide. Each of the four rod liiker polypeptides plays several roles. It determines the type and location of the phycobiliprotein within the rod, its aggregation state, andmodulates ita spectroscopic properties (see below). Inspection of Fig. 4 shows that the order of 565 nm), phycocythe major phycobiliproteins, phycoerythrin (X, anin (Amm 620 nm), and allophycocyanin (Arna 650 nm), corresponds to that of spontaneous excitation energy flow (from higher to lower energy transitions) with phycoerythrin a t the periphery of the rods and allophycocyanin in the core. Three-dimensionalStructure and Pathways of Energy Flow in Phycobiliproteins The determination of the crystal structure of C-phycocyanin in both the trimeric (Fig. 5) and hexameric assembly forms has provided a basis for the understanding of the functional properties of the phycobiliproteins (28, 29). An extraordinary fiiding is that each of the three bilins within an a8 monomer interacts with an aspartyl residue in an identical manner. The protein modifies the spectroscopic properties of the bilins in two ways critical to their role in light absorption and transfer: (a) the bilins in C-phycocyanin are held rigidly in extended conformations; (b)the excited state lifetime of the acterized by a strong near-UV absorption band and weaker absorption in the visible. The reverse is true for the extended conformations, such as those seen in C-phycocyanin, where the strongest absorption band is in the visible. Free bilins (and bilins in denatured phycobiliproteins) fluoresce very weakly. This indicates that the excitation energy is lost rapidly by radiationless relaxation pathways. The radiationless de-excitation pathways (twisting about bonds, photoisomerization, and intersystem crossing) are minimized by the environment and rigid framework in which the bilins are held in the native protein. In consequence, native phycobiliproteins fluoresce with high quantum yields. The energy levels of the bilins in a phycobiliprotein arenot equivalent. Consequently, whereas all of the bilins in a given phycobiliprotein absorb excitation energy, the fluorescence of the protein originates from the bilins with the longest wavelength absorption bands. Bilins which absorb light energy but transfer the excitation energy to other bilins are called donors. Those bilins that both absorb excitation energy and fluoresce are called acceptors. The intramolecular energy transfer within phycobiliprotein trimers and hexamers is very fast, and in consequence the steady state fluorescence emission originates almost exclusively from the acceptors. Synthesis of the data from chemical, crystallographic, and spectroscopic studies on numerous phycobiliproteins has led to theidentification of donor and acceptor bilins in C-phycocyanin and, by less rigorous arguments, in the various other phycobiliproteins. In C-phycocyanin, the biliis at a-84 and 8-155 are donors and the bilin a t 8-84 is the acceptor (31, 32). PCB 8-84 extends into the center of the trimeric disc (Fig. 5), whereas those a t 01-84and 8-155 lie toward the periphery. In consecutive double discs in the phycobilisome rod, the phycocyanin trimers are stacked face-to-face (29). In the stack, the 6-84 bilins of consecutive discs are arranged vertically above one anotherand ina mutual orientation that favors rapid transfer of energy from each of the three acceptor bilins in one disc to the acceptor bilins of the disc below. The phycoerythriis listed in Fig. 2 have five bilinslap. The sequences of the a and 8 subunits of B- and C-phycoerythrins and the bilin attachment sites are known. These proteins are highly homologous to each other and to C-phycocyanin. If the assumption is made that these phycoerythrins share a similar three-dimensional structure with C-phycocyanin, the location of the additional bilins can be assigned by model building. This leads to the finding that the addi- 4 Minireview: Directional Energy Transfer tional bilins lie at the periphery of the discs and to the conclusion that they function as donors. Support for this conclusion has been obtained from studies of the phycoerythrins of marine cyanobacteria Synechococcus spp. (33). These phycoerythrins are very similar to Band C-phycoerythrins but have much higher phycourobilin contents. Sequence studies on these phycoerythrins have shown that thepositions of the “additional” bilins in the phycoerythrins can be occupied at 495 nm, whereas by PUB groups (33). These groups have a, X PEB groups have Amax at 530-565 nm. Consequently, a position occupied by a PUB group in a phycoerythrin containing PEB groups as well must be a donor position. Picosecond energy transfer measurements show that theexcitation energy absorbed by any of the bilins at the periphery of the disc is rapidly localized on the centrally located acceptor bilins. The latter bilins are the way stations in the energy transfer pathway through the phycobilisome. i n Phycobilisomes bilins on the aAPB and LCM”polypeptides is complete in <8 X 10”’ s (37). In summary, the energy absorbed by any one of the bilins in the phycobilisome localizes rapidly on the four terminal acceptor bilins in the core. The emission of these bilins overlaps precisely the absorption spectrum of the reaction center of photosystem 11, believed to be the recipient of the energy harvested by the phycobilisome (38). With the radiationless transfer of energy from the terminal acceptors in the phycobilisome to the reaction center, the light guide function of the phycobilisome is completed. Acknowledgment-I am grateful to Phyllis Thompson Spowart for her assistance with the illustrations for this paper. REFERENCES 1. Duysens, L. M. N. (1964) Prog. Biophys. Mol. Biol. 14,3-104 2. Clayton, R. K. (1980) Photosynthesis: Physical Mechanism a@ Chemical Patterns, p. 48, Cambridge University Press, Cambridge, Unlted Kingdom 3. Glazer, A. N. (1983) Annu. Reu. Biochem. 52,125-157 4. Deisenhofer, J., Epp, O., Miki, K., Huber, R., and Michel, H. (1984) J. Mol. Biol. 180,385-398 5. Deisenhofer, J., Epp, O., Miki, K., Huber, R., and Michel, H. (1985) Nature 318,618-624 6. Micbel, H., and Deisenhofer, J. (1986) in Encyclopedia of Plant Physiology, Photosynthesis. III. Photosynthetic Membranes and Light Harvesting S y s t e m (Staehelin, L. A,, and Amtzen, C. J., eds) Vol. 19, pp. 371-381, Springer-Verlag, Berlin 7. Yentscb, C. S. (1980) in The PhysiologicalEcologyofPhytoplankton(Morris, I., ed) pp. 95-127, University of California Press, Berkeley, CA 8. Glazer, A. N. (1985) Annu. Reu. Biophys. Biophys. Chem. 14,47-77 9. Bishop, J. E., Rapoport, H., Klotz, A. V., Chan, C. F., Glazer, A. N., Fiiglistaller, P., and Zuber, H. (1987) J. Am. Chem. SOC.109,875-881 10. La arias, J . C., Klotz, A.V., Dallas, J. L., Glazer, A. N., Bishop, J. E., h o n n e l l , J. F., and Rapoport, H. (1988) J. Biol. Chem. 2 6 3 , 1297712985 11. Sorby, H. C. (1877) J. Linn. Soc. Land. Bot. 16,34-40 12. Gantt, E., and Lipschultz, C. A. (1972) J. CeU Biol. 54,313-324 13. Zuber, H. (1987) in The Light Reactions (Barber, J., ed) pp. 197-259, Elsevier Scientific Publishing Co., Amsterdam 14. Glazer, A. N. (1984) Biochim. Eiophys. Acta 7 6 8 , 29-51 15. Glazer, A. N. (1981) in The Biochemistry of Plants (Hatch, M. D., and Boardman, N. K., eds) Vol. 8, pp. 51-96, Academic Press, New York 16. Sidler, W., Kumpf, B., Rudiger, W., and Zuber, H. (1986) Biol. Chem. Hop e Se ler 367,627-642 17. Morscfel, Koller, K.-P., Wehrmeyer, W., andSchneider, H. (1977) Cytobiologie 16,118-129 18. Bryant, D. A,, Guglielmi, G., Tandeau de Marsac, N., Castets, A,“., and Cohen-Bazire, G. (1979) Arch. Microbiol. 1 2 3 , 113-127 19. Glazer, A. N., Williams, R. C., Yamanaka, G., and Schachman,H. K. (1979) Proc. Natl. Acad. Sci. U.S. A. 76,6162-6166 20. Gantt, E. (1980) Int. Reu. Cytol. 66,45-80 21. Porter, G.. Tredwell, C. J., Searle, G. F.W., and Barber, J. (1978) Biochim. Bioph s Acta 601,232-245 22. Searle, $.F. W., Barber, J., Porter, G., and Tredwell, C. J. (1978) Biochim. Biophys. Acta 601,246-256 23. Glazer, A. N.(1983) Annu. Reu. Microbiol. 3 6 , 173-198 24. Glazer, A. N., Lundell, D. J., Yamanaka, G., and Williams, R. C. (1983) Ann. Microbiol. Inst. Pasteur B134,159-180 25. Bryant, D. A. (1986) Can. Bull. Fish. Aqwt. Sci. 214,423-500 26. Lundell, D. J., Williams, R.C., and Glazer, A. N. (1981) J. BioI. Chem. 256,3580-3592 27. Yu, M.-H., Glazer, A. N., and Williams, R. C. (1981) J. Bid. Chem. 266, 13130-13136 28. Schirmer, T.,Bode, W., Huber, R., Sidler, W., and Zuber, H. (1985) J. Mol. B ~ O 184,257-277 L 29. Schirmer, T., Huber, R., Schneider, M., Bode, W., Miller, M., and Hackert, M. L. (1986) J. Mol. Bioi. 1 8 8 , 6 5 - 6 7 6 30. Scheer, H., and Kufer, W. (1977) 2. Naturforsch. Sect. C Biosci. 32,513- Pathway of Energy Plow in Phycobilieomes How is the excitation energy conveyed through the phycobilisome? Each of the 12 C-phycoerythrin hexamers in acomplete Synechocystis PCC 6701 phycobilisome (34) contains 30 bilins, and each of the 1 2 C-phycocyanin hexamers contains 18 bilins (Figs. 2 and 4). How is random walk of the excitation energy among the 576 bilins in the phycobilisome rods minimized and how is polarity of energy transfer achieved? The phycoerythrin and phycocyanin hexamers are assembled into six separate rods. Consequently, excitation energy absorbed by phycoerythrin, for example, is limited to a 60-PEB domain within a single rod. If all of the phycoerythrin in a phycobilisome were interconnected, the PEB domain size would be 360. Within a phycoerythrin hexamer, the transfer of energy to theacceptor bilins takes place within <8 X 10”’ s (35). The fluorescence lifetime of a phycoerythrin hexamer is 2.5 X lo-’ s, whereas the time taken for the energy absorbed by phycoerythrin to transfer to a proximal phycocyanin disc is about 2.5 X lo-” s (35). Consequently, the efficiency of transfer is 100 X ((2.5 X lo-’ - 2.5 X 10-”)/2.5 X lo-’) = 99%. Only three such transfers are needed to convey the energy to the core complexes. It is easy to see that the large energy difference between phycoerythrin and phycocyanin promotes directional energy transfer. How is preferential polarity of transfer achieved between the phycocyanin discs? As indicated above (Fig. 4), each disc contains a specific linker polypeptide. Interaction with different linker polypeptides confers distinctive spectroscopic properties on the acceptor bilins in the two phycocyanin hexamers. The absorption and emission spectra of the (~pcppc)~LRC’7complex are shifted red relative to those of (~pcflpc)&R33’6 (26,27). In consequence, the favored direction of transfer is from the distal disc to the phycocyanin disc proximal to the core. In the rods, the design of the discs ensures a rapid flow of energy from the donor bilins to the acceptor bilins. The positioning of the phycobiliproteins and the influence of the linker polypeptides contribute to rapid directional flow of the excitation energy from one acceptor bilin to theone below it toward the core. The understanding of the organization of the core is less complete, but features similar to those seen in the rods govern the polar transfer of energy. Allophycocyanin trimers form the major building blocks of the core (Fig. 31. 4). The fluorescence properties of (apcflpC)6L~cz7 and the absorption properties of allophycocyanin ensure that the latter functions as an 32. efficient acceptor. The basal core cylinders of the phycobilisome each 33. contain two copies of each of two distinct terminal energy acceptor complexes with similar spectroscopic properties, (a1APBa2APf13AP)LC10 and (aAppAp)2@’8.6LcM99 (Fig. 4). Each of the polypeptides L C Mand ~ 34. aAPB carries a single PCB group and confers a, ,X of 670 nm and a 35. fluorescence emission maximum of 680 nm on the complexes in which they are contained (8, 24, 36). Note that the same bilin (PCB) is 36. present in phycocyanin, allophycocyanin, and the terminal acceptor complexes. The spectrum of the bilins is in each instance “tuned” by 37. the protein to a different A., . In the intact phycobilisome core, the transfer of energy from allophycocyanin to the terminal acceptor 38. 2, 514 Si&;zknriibl, S., Fischer, R., and Scheer, H. (1987) 2.Naturforsch. Sect. C Biosci. 42,258-262 Schirmer, T., and Vincent, M. G. (1987) Biachim. Biophys. Acta 893,379385 Ong, L. J. (1988) Phycobiliproteins from marine cyanobacteria: Bilin Distribution and the Identificationof the Terminal Acceptor Bilin in Phycocyanins and Phycoerythrins. Ph.D. thesis, University of California, Berkeley Gingrich, J. C., Lundell, D. J., and Glazer, A. N. (1983) J. Cell. Biochem. 22, 1-14 Glazer, A. N., Yeh, S. W., Webb, S. P., and Clark, J. H. (1985) Science 227 419-423 Maxsoh, P., Sauer, K., and Glazer, A. N. (1988) in Photosynthetic 4’ ht Harvesting System. Structure and Functwn (Scheer,H.,and Schnelfer, S., eds) pp. 439-449, Walter de Gruyter,Berlin Glazer, A. N.,Chan, C., Williams, R. C., Yeh, S. W., and Clark,J. H. (1985) Science 230,1051-1053 Glazer, A. N.,and Melis, A. (1987) Annu. Reu. Plant Physiol. 3 8 , 11-45