Skip to main content
Log in

The structure of cyanobacterial phycobilisomes: a model

  • Published:
Archives of Microbiology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

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)

    Google Scholar 

  • Berns, D. S., Edwards, M. R.: Electron micrographic investigations of C-phycocyanin. Arch. Biochem. Biophys. 110, 511–516 (1965)

    Google Scholar 

  • Bennett, A., Bogorad, L.: Properties of subunits and aggregates of blue-green algal biliproteins. Biochemistry 10, 3625–3634 (1971)

    Google Scholar 

  • Bogorad, L.: Phycobiliproteins and complementary chromatic adaptation. Ann. Rev. Plant Physiol. 26, 369–401 (1975)

    Google Scholar 

  • Bryant, D. A.: Comparative studies on cyanobacterial and rhodophytan biliproteins. Ph. D. thesis, Los Angeles: University of California (1977)

    Google Scholar 

  • 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 

  • 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 

  • Cohen-Bazire, G., Lefort-Tran, M.: Fixation of phycobiliproteins to photosynthetic membranes by glutaraldehyde. Arch. Mikrobiol. 71, 245–257 (1970)

    Google Scholar 

  • Cosner, J. C.: Phycobilisomes in spheroplasts of Anacystis nidulans. J. bacteriol. 135, 1137–1140 (1978)

    Google Scholar 

  • 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 

  • Edwards, M. R., Gantt, E.: Phycobilisomes of the thermophilic blue-green alga Synechococcus lividus. J. Cell Biol. 50, 896–900 (1971)

    Google Scholar 

  • 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 

  • Gantt, E.: Properties and ultrastructure of phycoerythrin from Porphyridium cruentum. Plant Physiol. 44, 1629–1638 (1969)

    Google Scholar 

  • Gantt, E.: Phycobilisomes: Light-harvesting pigment complexes. Bioscience 25, 781–787 (1975)

    Google Scholar 

  • Gantt, E.: Recent contributions in phycobiliproteins and phycobilisomes. Photochem. Photobiol. 26, 685–689 (1977)

    Google Scholar 

  • Gantt, E., Conti, S. F.: Phycobiliprotein localization in algae. Brookhaven Symp. Biol. 19, 393–405 (1966)

    Google Scholar 

  • Gantt, E., Conti, S. F.: Ultrastructure of blue-green algae. J. Bacteriol. 97, 1486–1493 (1968)

    Google Scholar 

  • 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 

  • Gantt, E., Lipschultz, C. A.: Phycobilisomes of Porphyridium cruentum. I. isolation. J. Cell Biol. 54, 313–324 (1972)

    Google Scholar 

  • Gantt, E., Lipschultz, C. A.: Energy transfer in phycobilisomes from phycoerythrin to allophycocyanin. Biochim. Biophys. Acta 292, 858–868 (1973)

    Google Scholar 

  • Gantt, E., Lipschultz, C. A.: Phycobilisomes of Porphyridium cruentum: Pigment analysis. Biochemistry 13, 2960–2966 (1974)

    Google Scholar 

  • Gantt, E., Lipschultz, C. A.: Probing phycobilisome structure by immuno-electron microscopy. J. Phycol. 13, 185–192 (1977)

    Google Scholar 

  • 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 

  • 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 

  • Gantt, E., Lipschultz, C. A., Zilinskas, B. A.: Phycobilisomes in relation to the thylakoid membranes. Brookhaven Symp. Biol. 28, 347–357 (1976b)

    Google Scholar 

  • Glazer, A. N.: Phycocyanins: structure and function. Photochem. Photobiol. Rev. 1, 71–115 (1976)

    Google Scholar 

  • 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 

  • Glazer, A. N., Bryant, D. A.: Allophycocyanin B (λmax 671, 618nm): A new cyanobacterial phycobiliprotein. Arch. Microbiol. 104, 15–22 (1975)

    Google Scholar 

  • 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 

  • 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 

  • Grabowski, J., Gantt, E.: Excitation energy migration in phycobilisomes: Comparison of experimental results and theoretical predictions. Photochem. Photobiol. 28, 47–54 (1978b)

    Google Scholar 

  • 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 

  • Gray, B. H., Lipschultz, C. A., Gantt, E.: Phycobilisomes from a blue-green alga Nostoc species. J. Bacteriol. 116, 471–478 (1973)

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • McEwen, C. R.: Tables for estimating sedimentation through linear concentration gradients of sucrose solution. Analyt. Biochem. 20, 114–149 (1967)

    Google Scholar 

  • 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 

  • Neushul, M.: A freeze-etching study of the red alga Porphyridium. Amer. J. Bot. 57, 1231–1239 (1970)

    Google Scholar 

  • 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 

  • 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

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • Rippka, R., Waterbury, J., Cohen-Bazire, G.: A cyanobacterium which lacks thylakoids. Arch. Microbiol. 100, 419–436 (1974)

    Google Scholar 

  • 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 

  • Stanier, R. Y., Cohen-Bazire, G.: Phototrophic prokaryotes: The cyanobacteria. Ann. Rev. Microbiol. 31, 225–274 (1977)

    Google Scholar 

  • 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 

  • 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 

  • Tandeau de Marsac, N.: Occurence and nature of chromatic adaptation in cyanobacteria. J. Bacteriol. 130, 82–91 (1977)

    Google Scholar 

  • Tandeau de Marsac, N., Cohen-Bazire, G.: Molecular composition of cyanobacterial phycobilisomes. Proc. nat. Acad. Sci. (Wash.) 74, 1635–1639 (1977)

    Google Scholar 

  • Wehrmeyer, W.: Electronenmikroskopische Untersuchung zur Feinstruktur von Porphyridium violaceum Kornmann mit Bemerkungen über seine taxonomische Stellung. Arch. Mikrobiol. 75, 121–139 (1971)

    Google Scholar 

  • Wildman, R. B., Bowen, C. C.: Phycobilisomes in blue-green algae. J. Bacteriol. 117, 866–881 (1974)

    Google Scholar 

  • 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 

  • Zilinskas, B. A., Zimmermann, B. K., Gantt, E.: Allophycocyanin forms isolated from Nostoc sp. phycobilisomes. Photochem. Photobiol. 27, 587–595 (1978)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00446810

Key words

Navigation