Archives of Microbiology

, Volume 123, Issue 2, pp 113–127 | Cite as

The structure of cyanobacterial phycobilisomes: a model

  • Donald A. Bryant
  • Gérard Guglielmi
  • Nicole Tandeau de Marsac
  • Anne-Marie Castets
  • Germaine Cohen-Bazire


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.

Key words

Phycobilisomes Phycobiliproteins Cyanobacteria Chromatic adaptation Fine structure Photosynthesis Protein assembly 















allophycocyanin B








sodium dodecyl sulfate


Lyngbya-Plectonema-Phormidium group

Na-KPO4 buffers

NaH2PO4 titrated with a solution of KH2PO4 of equivalent molarity to a given pH


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  1. 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)Google Scholar
  2. Berns, D. S., Edwards, M. R.: Electron micrographic investigations of C-phycocyanin. Arch. Biochem. Biophys. 110, 511–516 (1965)Google Scholar
  3. Bennett, A., Bogorad, L.: Properties of subunits and aggregates of blue-green algal biliproteins. Biochemistry 10, 3625–3634 (1971)Google Scholar
  4. Bogorad, L.: Phycobiliproteins and complementary chromatic adaptation. Ann. Rev. Plant Physiol. 26, 369–401 (1975)Google Scholar
  5. Bryant, D. A.: Comparative studies on cyanobacterial and rhodophytan biliproteins. Ph. D. thesis, Los Angeles: University of California (1977)Google Scholar
  6. 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)Google Scholar
  7. 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)Google Scholar
  8. Cohen-Bazire, G., Lefort-Tran, M.: Fixation of phycobiliproteins to photosynthetic membranes by glutaraldehyde. Arch. Mikrobiol. 71, 245–257 (1970)Google Scholar
  9. Cosner, J. C.: Phycobilisomes in spheroplasts of Anacystis nidulans. J. bacteriol. 135, 1137–1140 (1978)Google Scholar
  10. 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)Google Scholar
  11. Edwards, M. R., Gantt, E.: Phycobilisomes of the thermophilic blue-green alga Synechococcus lividus. J. Cell Biol. 50, 896–900 (1971)Google Scholar
  12. 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)Google Scholar
  13. Gantt, E.: Properties and ultrastructure of phycoerythrin from Porphyridium cruentum. Plant Physiol. 44, 1629–1638 (1969)Google Scholar
  14. Gantt, E.: Phycobilisomes: Light-harvesting pigment complexes. Bioscience 25, 781–787 (1975)Google Scholar
  15. Gantt, E.: Recent contributions in phycobiliproteins and phycobilisomes. Photochem. Photobiol. 26, 685–689 (1977)Google Scholar
  16. Gantt, E., Conti, S. F.: Phycobiliprotein localization in algae. Brookhaven Symp. Biol. 19, 393–405 (1966)Google Scholar
  17. Gantt, E., Conti, S. F.: Ultrastructure of blue-green algae. J. Bacteriol. 97, 1486–1493 (1968)Google Scholar
  18. Gantt, E., Edwards, M. R., Conti, S. F.: Ultrastructure of Porphyridium aerugineum. A blue-green colored Rhodophytan. J. Phycol. 4, 65–71 (1968)Google Scholar
  19. Gantt, E., Lipschultz, C. A.: Phycobilisomes of Porphyridium cruentum. I. isolation. J. Cell Biol. 54, 313–324 (1972)Google Scholar
  20. Gantt, E., Lipschultz, C. A.: Energy transfer in phycobilisomes from phycoerythrin to allophycocyanin. Biochim. Biophys. Acta 292, 858–868 (1973)Google Scholar
  21. Gantt, E., Lipschultz, C. A.: Phycobilisomes of Porphyridium cruentum: Pigment analysis. Biochemistry 13, 2960–2966 (1974)Google Scholar
  22. Gantt, E., Lipschultz, C. A.: Probing phycobilisome structure by immuno-electron microscopy. J. Phycol. 13, 185–192 (1977)Google Scholar
  23. 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)Google Scholar
  24. 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)Google Scholar
  25. Gantt, E., Lipschultz, C. A., Zilinskas, B. A.: Phycobilisomes in relation to the thylakoid membranes. Brookhaven Symp. Biol. 28, 347–357 (1976b)Google Scholar
  26. Glazer, A. N.: Phycocyanins: structure and function. Photochem. Photobiol. Rev. 1, 71–115 (1976)Google Scholar
  27. Glazer, A. N.: Structure and molecular organization of the photosynthetic accessory pigments of cyanobacteria and red algae. Mol. Cell. Biochem. 18, 125–140 (1977)Google Scholar
  28. Glazer, A. N., Bryant, D. A.: Allophycocyanin B (λmax 671, 618nm): A new cyanobacterial phycobiliprotein. Arch. Microbiol. 104, 15–22 (1975)Google Scholar
  29. 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)Google Scholar
  30. Grabowsky, J., Gantt, E.: Photophysical properties of phycobiliproteins from phycobilisomes: Fluorescence lifetimes, quantum yields, and polarization spectra. Photochem. Photobiol. 28, 39–45 (1978a)Google Scholar
  31. Grabowski, J., Gantt, E.: Excitation energy migration in phycobilisomes: Comparison of experimental results and theoretical predictions. Photochem. Photobiol. 28, 47–54 (1978b)Google Scholar
  32. Gray, B. H., Gantt, E.: Spectral properties of phycobilisomes and phycobiliproteins from the blue-green alga Nostoc sp. Photochem. Photobiol. 21, 121–128 (1975)Google Scholar
  33. Gray, B. H., Lipschultz, C. A., Gantt, E.: Phycobilisomes from a blue-green alga Nostoc species. J. Bacteriol. 116, 471–478 (1973)Google Scholar
  34. 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)Google Scholar
  35. 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)Google Scholar
  36. 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)Google Scholar
  37. 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)Google Scholar
  38. Koller, K. P., Wehrmeyer, W., Mörschel, E.: Biliprotein assembly in the dischaped phycobilisomes of Rhodella violacea. Eur. J. Biochem. 91, 57–63 (1978)Google Scholar
  39. 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)Google Scholar
  40. 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)Google Scholar
  41. 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)Google Scholar
  42. 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)Google Scholar
  43. 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)Google Scholar
  44. 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)Google Scholar
  45. McEwen, C. R.: Tables for estimating sedimentation through linear concentration gradients of sucrose solution. Analyt. Biochem. 20, 114–149 (1967)Google Scholar
  46. 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)Google Scholar
  47. Neushul, M.: A freeze-etching study of the red alga Porphyridium. Amer. J. Bot. 57, 1231–1239 (1970)Google Scholar
  48. Neushul, M.: Uniformity of the thylakoid structure in a red, a brown, and two blue-green algae. J. Ultrastruct. Res. 37, 532–543 (1971)Google Scholar
  49. 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 1976Google Scholar
  50. 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)Google Scholar
  51. 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)Google Scholar
  52. 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)Google Scholar
  53. Rippka, R., Waterbury, J., Cohen-Bazire, G.: A cyanobacterium which lacks thylakoids. Arch. Microbiol. 100, 419–436 (1974)Google Scholar
  54. 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)Google Scholar
  55. Stanier, R. Y., Cohen-Bazire, G.: Phototrophic prokaryotes: The cyanobacteria. Ann. Rev. Microbiol. 31, 225–274 (1977)Google Scholar
  56. 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)Google Scholar
  57. 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)Google Scholar
  58. Tandeau de Marsac, N.: Occurence and nature of chromatic adaptation in cyanobacteria. J. Bacteriol. 130, 82–91 (1977)Google Scholar
  59. Tandeau de Marsac, N., Cohen-Bazire, G.: Molecular composition of cyanobacterial phycobilisomes. Proc. nat. Acad. Sci. (Wash.) 74, 1635–1639 (1977)Google Scholar
  60. Wehrmeyer, W.: Electronenmikroskopische Untersuchung zur Feinstruktur von Porphyridium violaceum Kornmann mit Bemerkungen über seine taxonomische Stellung. Arch. Mikrobiol. 75, 121–139 (1971)Google Scholar
  61. Wildman, R. B., Bowen, C. C.: Phycobilisomes in blue-green algae. J. Bacteriol. 117, 866–881 (1974)Google Scholar
  62. 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)Google Scholar
  63. Zilinskas, B. A., Zimmermann, B. K., Gantt, E.: Allophycocyanin forms isolated from Nostoc sp. phycobilisomes. Photochem. Photobiol. 27, 587–595 (1978)Google Scholar

Copyright information

© Springer-Verlag 1979

Authors and Affiliations

  • Donald A. Bryant
    • 1
  • Gérard Guglielmi
    • 1
  • Nicole Tandeau de Marsac
    • 1
  • Anne-Marie Castets
    • 1
  • Germaine Cohen-Bazire
    • 1
  1. 1.Unité de Physiologie Microbienne, Département de Biochimie et Génétique Microbienne, C.N.R.S.-E.R.A. 398Institut PasteurParisFrance
  2. 2.Division of Biological Sciences, Section of Botany, Genetics, and DevelopmentCornell UniversityIthacaUSA

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