Abstract
Phycobilisomes, supramolecular complexes of water-soluble accessory pigments, serve as the major light-harvesting antennae in cyanobacteria and red algae. Regular arrays of these organelles are found on the surface of the thylakoid membranes of these organisms. In the present study, the hemi-discoidal phycobilisomes of several species of cyanobacteria were examined in thin sections of cells and by negative staining after isolation and fixation. Their fundamental structures were found to be the same. Isolated phycobilisomes possessed a triangular core assembled from three stacks of disc-shaped subunits. Each stack contained two discs which were ∼12 nm in diameter and ∼6–7 nm thick. Each of these discs was probably subdivided into halves ∼3–3.5 nm thick. Radiating from each of two sides of the triangular core were three rods ∼12 nm in diameter. Each rod consisted of stacks of 2 to 6 disc-shaped subunits ∼6 nm thick. These discs were subdivided into halves ∼3 nm thick.
The average number of discs of ∼6 nm thickness forming the peripheral rods varied among the strains studied. For certain chromatically adapting strains, the average rod length was dependent upon the wavelength of light to which cells were exposed during growth. Analyses of phycobilisomes by spectroscopic techniques, polyacrylamide gel electrophoresis, and electron microscopy were compared. These analyses suggested that the triangular core was composed of allophycocyanin and that the peripheral rods contained phycocyanin and phycoerythrin (when present). A detailed model of the hemi-discoidal phycobilisome is proposed. This model can account for many aspects of phycobiliprotein assembly and energy transfer.
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Abbreviations
- PBS:
-
phycobilisome(s)
- PBP:
-
phycobiliprotein(s)
- AP:
-
allophycocyanin
- PC:
-
phycocyanin
- PE:
-
phycoerythrin
- PEC:
-
phycoerythrocyanin
- AP-B:
-
allophycocyanin B
- C-:
-
cyanobacterial
- R-:
-
rhodophytan
- B-:
-
Bangiophycean
- SDS:
-
sodium dodecyl sulfate
- LPP:
-
Lyngbya-Plectonema-Phormidium group
- Na-KPO4 buffers:
-
NaH2PO4 titrated with a solution of KH2PO4 of equivalent molarity to a given pH
References
Abad-Zapatero, C., Fox, J. L., Hackert, M. L.: The quarternary structure of a unique phycobiliprotein: B-phycoerythrin from Porphyridium cruentum. Biochem. Biophys. Res. Commun. 78, 266–272 (1977)
Berns, D. S., Edwards, M. R.: Electron micrographic investigations of C-phycocyanin. Arch. Biochem. Biophys. 110, 511–516 (1965)
Bennett, A., Bogorad, L.: Properties of subunits and aggregates of blue-green algal biliproteins. Biochemistry 10, 3625–3634 (1971)
Bogorad, L.: Phycobiliproteins and complementary chromatic adaptation. Ann. Rev. Plant Physiol. 26, 369–401 (1975)
Bryant, D. A.: Comparative studies on cyanobacterial and rhodophytan biliproteins. Ph. D. thesis, Los Angeles: University of California (1977)
Bryant, D. A., Glazer, A. N., Eiserling, F. A.: Characterization and structural properties of the major biliproteins of Anabaena sp. Arch. Microbiol. 110, 61–75 (1976)
Cohen-Bazire, G., Béguin, S., Rimon, S., Glazer, A. N., Brown, D. M.: Physicochemical and immunological properties of allophycocyanins. Arch. Microbiol. 111, 225–238 (1977)
Cohen-Bazire, G., Lefort-Tran, M.: Fixation of phycobiliproteins to photosynthetic membranes by glutaraldehyde. Arch. Mikrobiol. 71, 245–257 (1970)
Cosner, J. C.: Phycobilisomes in spheroplasts of Anacystis nidulans. J. bacteriol. 135, 1137–1140 (1978)
Dobler, M., Dover, S. D., Laves, K., Binder, A., Zuber, H.: Crystallization and preliminary crystal data of C-phycocyanin. J. mol. Biol. 71, 785–787 (1972)
Edwards, M. R., Gantt, E.: Phycobilisomes of the thermophilic blue-green alga Synechococcus lividus. J. Cell Biol. 50, 896–900 (1971)
Eiserling, F. A., Glazer, A. N.: Blue-green algal proteins: Assembly forms of C-phycocyanin from Synechococcus sp. J. Ultrastruct. Res. 47, 16–25 (1974)
Gantt, E.: Properties and ultrastructure of phycoerythrin from Porphyridium cruentum. Plant Physiol. 44, 1629–1638 (1969)
Gantt, E.: Phycobilisomes: Light-harvesting pigment complexes. Bioscience 25, 781–787 (1975)
Gantt, E.: Recent contributions in phycobiliproteins and phycobilisomes. Photochem. Photobiol. 26, 685–689 (1977)
Gantt, E., Conti, S. F.: Phycobiliprotein localization in algae. Brookhaven Symp. Biol. 19, 393–405 (1966)
Gantt, E., Conti, S. F.: Ultrastructure of blue-green algae. J. Bacteriol. 97, 1486–1493 (1968)
Gantt, E., Edwards, M. R., Conti, S. F.: Ultrastructure of Porphyridium aerugineum. A blue-green colored Rhodophytan. J. Phycol. 4, 65–71 (1968)
Gantt, E., Lipschultz, C. A.: Phycobilisomes of Porphyridium cruentum. I. isolation. J. Cell Biol. 54, 313–324 (1972)
Gantt, E., Lipschultz, C. A.: Energy transfer in phycobilisomes from phycoerythrin to allophycocyanin. Biochim. Biophys. Acta 292, 858–868 (1973)
Gantt, E., Lipschultz, C. A.: Phycobilisomes of Porphyridium cruentum: Pigment analysis. Biochemistry 13, 2960–2966 (1974)
Gantt, E., Lipschultz, C. A.: Probing phycobilisome structure by immuno-electron microscopy. J. Phycol. 13, 185–192 (1977)
Gantt, E., Lipschultz, C. A., Grabowski, J., Zimmermann, B. K.: Phycobilisomes from blue-green and red algae: Isolation criteria and “dissociation” characteristics. Plant Physiol. 63, 615–620 (1979)
Gantt, E., Lipschultz, C. A., Zilinskas, B.: Further evidence for a phycobilisome model from selective dissociation, fluorescence emission, immunoprecipitation, and electron microscopy. Biochim. Biophys. Acta 430, 375–388 (1976a)
Gantt, E., Lipschultz, C. A., Zilinskas, B. A.: Phycobilisomes in relation to the thylakoid membranes. Brookhaven Symp. Biol. 28, 347–357 (1976b)
Glazer, A. N.: Phycocyanins: structure and function. Photochem. Photobiol. Rev. 1, 71–115 (1976)
Glazer, A. N.: Structure and molecular organization of the photosynthetic accessory pigments of cyanobacteria and red algae. Mol. Cell. Biochem. 18, 125–140 (1977)
Glazer, A. N., Bryant, D. A.: Allophycocyanin B (λmax 671, 618nm): A new cyanobacterial phycobiliprotein. Arch. Microbiol. 104, 15–22 (1975)
Glazer, A. N., Hixson, C. S.: Characterization of R-phycocyanin. Chromophore content of R-phycocyanin and C-phycoerythrin. J. Biol. Chem. 250, 5487–5495 (1975)
Grabowsky, J., Gantt, E.: Photophysical properties of phycobiliproteins from phycobilisomes: Fluorescence lifetimes, quantum yields, and polarization spectra. Photochem. Photobiol. 28, 39–45 (1978a)
Grabowski, J., Gantt, E.: Excitation energy migration in phycobilisomes: Comparison of experimental results and theoretical predictions. Photochem. Photobiol. 28, 47–54 (1978b)
Gray, B. H., Gantt, E.: Spectral properties of phycobilisomes and phycobiliproteins from the blue-green alga Nostoc sp. Photochem. Photobiol. 21, 121–128 (1975)
Gray, B. H., Lipschultz, C. A., Gantt, E.: Phycobilisomes from a blue-green alga Nostoc species. J. Bacteriol. 116, 471–478 (1973)
Gysi, J., Zuber, H.: Allophycocyanin I — a second cyanobacterial allophycocyanin? Isolation, characterization, and comparison with allophycocyanin II from the same alga. FEBS Lett. 68, 49–54 (1976)
Hackert, M. L., Abad-Zapatero, C., Stevens, S. E., Fox, J. L.: Crystallization of C-phycocyanin from the marine blue-green alga Agmenellum quadruplicatum. J. mol. Biol. 111, 365–369 (1977)
Kao, O. H. W., Edwards, M. R., Berns, D. S.: Physical-chemical properties of C-phycocyanin isolated from an acido-thermophilic eukaryote, Cyanidium caldarium. Biochem. J. 147, 63–70 (1975)
Kessel, M., MacColl, R., Berns, D. S., Edwards, M. R.: Electron microscope and physical chemical characterization of C-phycocyanin from fresh extracts of two blue-green algae. Can. J. Microbiol. 19, 831–836 (1973)
Koller, K. P., Wehrmeyer, W., Mörschel, E.: Biliprotein assembly in the dischaped phycobilisomes of Rhodella violacea. Eur. J. Biochem. 91, 57–63 (1978)
Koller, K. P., Wehrmeyer, W., Schneider, H.: Isolation and characterization of disc-shaped phycobilisomes from the red alga Rhodella violacea. Arch Microbiol. 112, 61–67 (1977)
Lefort, M.: Sur le chromatoplasma d'une cyanophycée endosymbiotique: Glaucocystis nostochinearum Itzigs. C. r. hebd. Séanc. Acad. Sci. (Paris) 261, ser. 1, 233–236 (1965)
Lefort-Tran, M., Cohen-Bazire, G., Pouphile, M.: Les membranes photosynthétiques des algues à biliproteines observées après cryodécapage. J. Ultrastruct. Res. 44, 199–209 (1973)
Lemasson, C., Tandeau de Marsac, N., Cohen-Bazire, G.: Role of allophycocyanin as a light-harvesting pigment in cyanobacteria. Proc. nat. Acad. Sci. (Wash.) 70, 3130–3133 (1973)
Ley, A. C., Butler, W. L., Bryant, D. A., Glazer, A. N.: Isolation and function of allophycocyanin B of Porphyridium cruentum. Plant Physiol. 59, 974–980 (1977)
Lichtlé, C., Thomas, J. C.: Etude ultrastructurale des thylacoides des algues à phycobiliproteines, comparison des résultats obtenus par fixation classique et cryodécapage. Phycologia 15, 393–404 (1976)
McEwen, C. R.: Tables for estimating sedimentation through linear concentration gradients of sucrose solution. Analyt. Biochem. 20, 114–149 (1967)
Mörschel, E., Koller, K. P., Wehrmeyer, W., Schneider, H.: Biliprotein assembly in the disc-shaped phycobilisomes of Rhodella violacea. I. Electron microscopy of phycobilisomes in situ and analysis of their architecture after isolation and negative staining. Cytobiologie 16, 118–129 (1977)
Neushul, M.: A freeze-etching study of the red alga Porphyridium. Amer. J. Bot. 57, 1231–1239 (1970)
Neushul, M.: Uniformity of the thylakoid structure in a red, a brown, and two blue-green algae. J. Ultrastruct. Res. 37, 532–543 (1971)
O'Carra, P., O'hEocha, C.: Algal biliproteins and phycobilins. In: Chemistry and Biochemistry of Plant Pigments (Goodwin, T. W., ed.), 2nd edn., pp. 328–376. New York: Academic Press 1976
Porter, G., Tredwell, C. J., Searle, G. F. W., Barber, J.: Picosecond time-resolved energy transfer in Porphyridium cruentum. Part 1. In the intact alga. Biochim. Biophys. Acta 501, 232–245 (1978)
Reynolds, E. S.: The use of lead citrate at a high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963)
Rippka, R., Deruelles, J., Waterbury, J. B., Herdman, M., Stanier, R. Y.: Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J. gen. Microbiol. 111, 1–61 (1979)
Rippka, R., Waterbury, J., Cohen-Bazire, G.: A cyanobacterium which lacks thylakoids. Arch. Microbiol. 100, 419–436 (1974)
Searle, G. F. W., Barber, J., Porter, G., Tredwell, C. J.: Picosecond time-resolved energy transfer in Porphyridium cruentum. Part II. In the isolated light harvesting complex (phycobilisomes). Biochim. Biophys. Acta 501, 246–256 (1978)
Stanier, R. Y., Cohen-Bazire, G.: Phototrophic prokaryotes: The cyanobacteria. Ann. Rev. Microbiol. 31, 225–274 (1977)
Stanier, R. Y., Kunisawa, R., Mandel, M., Cohen-Bazire, G.: Purification and properties of unicellular blue-green algae (Order Chroococcales). Bact. Rev. 35, 171–205 (1971)
Sweet, R. M., Fuchs, H. E., Fisher, R. G., Glazer, A. N.: Preliminary crystallographic investigations of two phycobiliproteins. J. biol. Chem. 252, 8258–8260 (1977)
Tandeau de Marsac, N.: Occurence and nature of chromatic adaptation in cyanobacteria. J. Bacteriol. 130, 82–91 (1977)
Tandeau de Marsac, N., Cohen-Bazire, G.: Molecular composition of cyanobacterial phycobilisomes. Proc. nat. Acad. Sci. (Wash.) 74, 1635–1639 (1977)
Wehrmeyer, W.: Electronenmikroskopische Untersuchung zur Feinstruktur von Porphyridium violaceum Kornmann mit Bemerkungen über seine taxonomische Stellung. Arch. Mikrobiol. 75, 121–139 (1971)
Wildman, R. B., Bowen, C. C.: Phycobilisomes in blue-green algae. J. Bacteriol. 117, 866–881 (1974)
Yamanaka, G., Glazer, A. N., Williams, R. C.: Cyanobacterial phycobilisomes. Characterization of the phycobilisomes of Synechococcus sp. 6301. J. biol. Chem. 253, 8303–8310 (1978)
Zilinskas, B. A., Zimmermann, B. K., Gantt, E.: Allophycocyanin forms isolated from Nostoc sp. phycobilisomes. Photochem. Photobiol. 27, 587–595 (1978)
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Bryant, D.A., Guglielmi, G., de Marsac, N.T. et al. The structure of cyanobacterial phycobilisomes: a model. Arch. Microbiol. 123, 113–127 (1979). https://doi.org/10.1007/BF00446810
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DOI: https://doi.org/10.1007/BF00446810