Isolation, characterization and electron microscopy analysis of a hemidiscoidal phycobilisome type from the cyanobacterium Anabaena sp. PCC 7120

European Journal of Biochemistry

Volumn 236, Issue 3, 1996, Pages 1010-1024

  Ducret, Axel ^a   Sidler, Walter ^a   Wehrli, Ernst ^a   Frank, Gerhard ^a   Zuber, Herbert ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

cyanobacterium; electron microscopy; photosynthesis; phycobiliprotein; phycobilisome

Indexed keywords

ARTICLE; CELL STRUCTURE; CYANOBACTERIUM; CYTOCHEMISTRY; ELECTRON MICROSCOPY; PHOTOSYNTHESIS; PRIORITY JOURNAL;

ANABAENA SP.; ANABAENA VARIABILIS; CYANOBACTERIA; MASTIGOCLADUS LAMINOSUS; NOSTOC SP. PCC 7120; VITIS SP.;

EID: 0029994573     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.1996.01010.x     Document Type: Article

References (68)

1. Belknap, W. R. & Haselkorn, R. (1987) Cloning and regulation of expression of the phycocyanin operon of the cyanobacterium Anabaena, EMBO J. 6, 871-884.
2. Bryant, D. A. (1982) Phycoerythrocyanin and phycoerythrin: properties and occurrence in cyanobacteria, J. Gen. Microbiol. 128, 835-844.
3. Bryant, D. A. (1991) Cyanobacterial phycobilisomes: Progress toward complete structural and functional analysis via molecular genetics, Cell culture Somatic Cell Genet. Plants 7B, 257-300.
4. Bryant, D. A., Glazer, A. N. & Eiserling, F. A. (1976) Characterization and structural properties of the major phycobiliproteins of Anabaena sp., Arch. Microbiol. 110, 61-75.
5. Bryant, D. A., Hixson, C. S. & Glazer, A. N. (1978) Structural studies on phycobiliproteins. III. Comparison of bilin-containing peptides from the β subunits of C-phycocyanin, R-phycocyanin and phycoerythrocyanin, J. Biol Chem. 253, 220-225.
6. Bryant. D. A., de Lorimier, R., Guglielmi, G. & Stevens, S. E. Jr (1990) Structural and compositional analyses of the phycobilisomes of Synechococcus sp. PCC 7002. Analyses of the wild-type strain and a phycocyanin-less mutant constructed by interposon mutagenesis, Arch. Microbiol. 153, 550-560.
7. Bryant, D. A., Stirewalt, V. L., Glauser, M., Frank, G., Sidler, W. & Zuber, H. (1991) A small multigene family encodes the rod-core linker polypeptides of Anabaena sp. PCC 7120 phycobilisomes, Gene (Amst.) 107, 91-99.
8. Capuano, V., Braux, A., Tandeau de Marsac, N. & Houmard, J. (1991) The anchor polypeptide of cyanobacterial phycobilisomes, J. Biol. Chem. 266, 7239-7247.
9. De Lorimier, R., Bryant, D. A. & Stevens, S. E. Jr (1990a) Genetic analysis of a 9 kDa phycocyanin-associated linker polypeptide, Biochim. Biophys. Acta 1019, 29-41.
10. De Lorimier, R., Gulgielmi, G., Bryant, D. A. & Stevens, S. E. Jr (1990b) Structure and mutation of a gene encoding a 33 kDa phycocyanin-associated linker polypeptide, Arch. Microbiol. 153, 541-549.
11. Ducret, A., Sidler, W., Frank, G. & Zuber, H. (1994) The complete amino acid sequence of R-phycocyanin-I α and β subunits from the red alga Porphyridium cruentum. Structural and phylogenetic relationships of the phycocyanins within the phycobiliprotein families, Eur. J. Biochem. 221, 563-580.
12. Duerring, M., Huber, R., Bode, W., Rümbeli, R. & Zuber, H. (1990) Refined three-dimensional structure of phycoerythrocyanin from the cyanobacterium Mastigocladus laminosus at 2.7 Å, J. Mol. Biol. 211, 633-644.
13. Duerring, M., Schmidt, G. B. & Huber, R. (1991) Isolation, crystallization, crystal structure analysis and refinement of constitutive C-phycocyanion from the chromatically adapting cyanobacterium Fremyella diplosiphon at 1.66 Å resolution, J. Mol. Biol. 217, 577-592.
14. Esteban, M. A. (1993) Sequenzierung, Klonierung und Charakterisierung der Gene von Core-Polypeptiden aus dem Cyanobakterium Mastigocladus laminosus, PhD dissertation No.10040, Eidgenössische Technische Hochschule, Zürich, Switzerland.
15. Ficner, R., Lobeck, K., Schmidt, G. & Huber, R. (1992) Isolation, crystallization, crystal structure analysis and refinement of B-phycoerythrin from the red alga Porphyridium sordidum at 2.2 Å resolution, J. Mol. Biol. 228, 935-950.
16. Frank, G. (1989) New aspects in isocratic HPLC separation of phenylthiohydantoin amino acids through the application of ionic detergents, in Methods in protein sequence analysis (Wittmann-Liebold, B., ed.) Proceedings of the 7th International Conference, pp. 116-121, Springer-Verlag, Berlin.
17. Frank, G., Redweik, U., Rümbeli, M., Schoendon, G. & Blau, N. (1992) Cyanogen bromide cleavage of proteins on blots and subsequent separations of the fragments by polyacrylamide gel electrophoresis directly from those blots, in Methods in Protein Sequence Analysis (Kazutomo, I. & Sakiyama, F., eds) Proceedings of the 9th International Conference, pp. 79-85, Plenum Press, New-York.
18. Füglistaller, P., Rümbeli, R., Suter, F. & Zuber, H. (1984) Minor polypeptides from the phycobilisome of the cyanobacterium Mastigocladus laminosus. Isolation, characterization and amino acid sequences of a colourless 8. 9-kDa polypeptide and of a 16.2-kDa phycobiliprotein, Hoppe-Seyler's Z. Physiol. Chem. 365, 1085-1096.
19. Füglistaller, P., Suter, F. & Zuber, H. (1986) Linker polypeptides of the phycobilisome from the cyanobacterium Mastigocladus laminosus. I. Isolation and characterization of phycobiliprotein-linker-polypeptide complexes, Biol. Chem. Hoppe Seyler 367, 601-614.
20. C on the spectral properties of the phycobiliprotein subunits, Biol. Chem. Hoppe-Seyler 368, 353-367.
21. Gantt, E. (1988) Phycobilisomes: assesssment of core structure and thylakoid interaction, in Light-energy transduction in photosynthesis: higher plants and bacterial models (Stevens S. E. Jr & Bryant D. A., eds), pp. 91-101, American Society of Plant Physiologists, Rockville USA.
22. Gantt, E., Lipschultz, C. A., Grabowski, J. & Zimmerman, B. K. (1979) Phycobilisomes from blue-green and red algae. Isolation criteria and dissociation characteristics, Plant Physiol. (Bethesda) 63, 615-620.
23. Gingrich, J. C. Lundell, D. J. & Glazer, A. N. (1983) Core substructure in cyanobacterial phycobilisomes, J. Cell. Biochem 22, 1-14.
24. Glauser, M., Bryant, D. A., Frank, G., Wehrli, E., Rusconi, S. S., Sidler, W. & Zuber, H. (1992a) Phycobilisome structure in the cyanobacteria Mastigocladus laminosus and Anabaena sp. PCC 7120, Eur. J. Biochem. 205, 907-915.
25. Glauser, M., Sidler, W. A., Graham, K. W., Bryant, D. A., Frank, G., Wehrli, E. & Zuber, H. (1992b) Three C-phycoerythrin-associated linker polypeptides in the phycobilisome of green-light-grown Calothrix sp. PCC 7601 (cyanobacteria), FEBS Lett. 297, 19-23.
26. Glauser, M., Stirewalt, V. L., Bryant, D. A., Sidler, W. & Zuber, H. (1992c) Structure of the genes encoding the rod-core linker polypeptides of Mastigocladus laminosus phycobilisomes and functional aspects of the phycobiliprotein/linker-polypeptide interactions, Eur. J. Biochem. 205, 927-973.
27. Glauser, M., Sidler, W. & Zuber, H. (1993) Isolation, characterization and reconstitution of phycobiliprotein rod-core linker polypeptide complexes from the phycobilisome of Mastigocladus laminosus, Photochem. Photobiol. 57, 344-351.
28. Glazer, A. N. (1981) Photosynthetic accessory proteins with bilin prosthetic groups, in The biochemistry of plants (Hatch, M. D. & Boardman, N. K., eds) vol. 8, pp. 51-96, Academic Press, New York.
29. Glazer, A. N. (1984) Phycobilisome. A macromolecular complex optimized for light energy transfer, Biochim. Biophys. Acta 768, 29-51.
30. Glazer, A. N. (1987) Phycobilisomes: assembly and attachment, in The cyanobacteria (Fay, P. & Van Baalen, C., eds) pp. 69-88, Elsevier Biomedical, Amsterdam.
31. Glazer, A. N. (1989) Light guides, J. Biol. Chem. 264, 1-4.
32. Click, R. E. & Zilinskas, B. A. (1982) Role of the colourless polypeptides in phycobilisome reconstitution from separated phycobiliproteins, Plant Physiol. (Bethesda) 69, 991-997.
33. Gottschalk, L., Fischer, R., Lottspeich, F. & Scheer, H. (1991) Origin of the red shifted absorption in phycocyanin 632 from Mastigocladus laminosus, Photochem. Photobiol. 54, 283-288.
34. Grossman, A. R. (1990) Chromatic adaption and the events involved in phycobilisome biosynthesis, Plant, Cell and Environment 13, 651-666.
35. Houmard, J, Capuano, V., Coursin, T. & Tandeau de Marsac, N. (1988) Isolation and molecular characterization of the gene encoding allophycocyanin B, a terminal energy acceptor in cyanobacterial phycobilisomes, Mol. Microbiol. 2, 101-107.
36. Houmard, J., Capuano, V., Colombano, M. V., Coursin, T. & Tandeau de Marsac, N. (1990) Molecular characterization of the terminal energy acceptor of cyanobacterial phycobilisomes, Proc. Natl Acad. Sci. USA 87, 2152-2156.
37. Isono, T. & Katoh, T. (1982) Cylindrical phycobilisomes from a blue-green alga, Anabaena variabilis, Plant Cell Physiol. 23, 1347-1355.
38. Isono, T. & Katoh, T. (1983) Subparticles of Anabaena phycobilisomes. I. Reconstitution of allophycocyanin cores and entire phycobilisomes, Plant Cell Physiol. 24, 357-368.
39. Isono, T. & Katoh, T. (1987) Subparticles of Anabaena phycobilisomes. II. Molecular assembly of allophycocyanin cores in reference to anchor protein. Arch. Biochem. Biophys. 256, 317-324.
40. Laemmli, U. K. (1970) Cleavage of stuctural proteins during the assembly of the head of bacteriophage T4, Nature 227, 680-685.
41. max 650 nm), J. Biol. Chem. 256, 12600-12606.
42. Lundell, D. J. & Glazer, A. N. (1983a) Molecular architecture of a light-harvesting antenna. Strucure of the 18S core-rod subassembly of the Synechococcus 6301 phycobilisome, J. Biol. Chem. 258, 894-901.
43. Lundell, D. J. & Glazer, A. N. (1983b) Molecular architecture of a light-harvesting antenna. Core substructure in Synechococcus 6301 phycobilisomes: two new allophycocyanin and allophycocyanin B complexes, J. Biol. Chem. 258, 902-908.
44. Lundell, D. J. & Glazer, A. N. (1983c) Molecular architecture of a light-harvesting antenna. Quaternary interactions in the Synechococcus 6301 phycobilisome core as revealed by partial tryptic digestion and circular dichroism studies, J. Biol. Chem. 258, 8708-8713.
45. MacColl, R. & Guard-Friar, D. (1987) Phycobiliproteins (MacColl, R. & Guard-Friar, D., eds) pp. 1-211, CRC Press Inc., Boca Raton.
46. Mimuro, M., Lipschultz C. & Gantt, E. (1986) Energy flow in the phycobilisome of Nostoc sp. (MAC): two independent terminal pigments, Biochim. Biophys. Acta 852, 126-133.
47. Mörschel, E. & Rhiel, E. (1987) Phycobilisomes and thylakoids: the light-harvesting system of cyanobacteria and red algae, in Membranous structures (Harris J. R. & Horne, R. W., eds) pp. 210-254, Academic Press, London.
48. Reuter, W. & Wehrmeyer, W. (1988) Core substructure in Mastigocladus laminosus phycobilisomes I. Microheterogeneity in two of three allophycocyanin core complexes, Arch. Microbiol. 150, 534-540.
49. CM - contains the anchor polypeptide and no allophycocyanin B, Arch. Mircobiol. 153, 111-117.
50. 16.2 of the allophycocyanin core from the cyanobacterium Mastigocladus laminosus. Characterization and complete amino acid sequence, Biol. Chem. Hoppe-Seyler 368, 1-9.
51. Schirmer, T., Bode, W., Huber, R., Sidler, W. & Zuber, H. (1985) X-ray crystallographic structure of the light-harvesting biliprotein C-phycocyanin from the thermophilic cyanobacterium Mastigocladus laminosus and its resemblance to globin structures, J. Mol. Biol. 184, 257-277.
52. Schirmer, T., Huber, R., Schneider, M., Bode, W., Miller, M. & Hackert, M. L. (1986) Crystal structure analysis and refinement at 2.5 Å of hexameric C-phycocyanin from the cyanobacterium Agmenellum quadruplicatum. The molecular model and its implications for light-harvesting, J. Mol. Biol. 188, 651-676.
53. Schirmer, T., Bode, W. & Huber, R. (1987) Refined three-dimensional structures of two cyanobacterial C-phycocyanins at 2.1 and 2.5 Å resolution. A common principle of phycobilin-protein interaction, J. Mol. Biol. 196, 677-695.
54. + oxidoreductase in cyanobacteria. Cloning and sequence of the petH gene of Synechococcus sp PCC 7002 and studies on the gene product, Biochemistry 31, 3092-3102.
55. Sidler, W. (1994) Phycobilisome and phycobiliprotein structures, in The biology of cyanobacteria (Bryant, D. A., ed.), pp. 139-216, Kluwer Academic Publishers, Dordrecht.
56. Siegelman, H. W., Wieczorek, G. A. & Turner, B. C. (1965) Preparation of calcium phosphate for protein chromatography, Anal. Biochem. 13, 402-404.
57. Stanier, R. Y., Kunisawa, R., Mandel, M. & Cohen-Bazire, G. (1971) Purification and properties of unicellular blue-green algae (Order Chroococcales), Bacteriol. Rev. 35, 171-205.
58. Swanson, R. V., de Lorimier, R. & Glazer, A. N. (1992) Genes encoding the phicobilisome rod substructure are clustered on the Anabaena chromosome: characterization of the phycoerythrocyanin operon, J. Bacteriol. 174, 2640-2647.
59. Tandeau de Marsac, N. (1991) Chromatic adaptation by cyanobacteria, Cell Culture Somatic Cell Genet. Plants 7B, 419-446.
60. 2 terminus of the α and β subunits of allophycocyanins I, II and III, J. Biol. Chem. 255, 9380-9387.
61. Wehrmeyer, W. (1990) Phycobilisomes: structures and function, in Experimental phycology: cell walls and surfaces, reproduction, photosynthesis (Wissner, W., Robinson, D. G. & Star, R. C., eds) pp. 158-172, Springer Verlag, Berlin.
62. Williams, R. C., Gingrich, J. C. & Glazer, A. N. (1980) Cyanobacterial phycobilisomes: particles from Synechocystis 6701 and two pigment mutants, J. Cell Biol. 85, 558-566.
63. Yamanaka, G., Glazer, A. N. & Williams, R. C. (1980) Molecular architecture of a light-harvesting antenna. Comparison of wild type and mutant Synechococcus 6301 phycobilisomes, J. Biol. Chem. 255, 11004-11010.
64. Zhao, Z., Zhou, J. & Bryant, D. A. (1992) Energy transfer processes in phycobilisomes as deduced from analyses of mutants of Synechococcus sp. PCC 7002, in Research in photosynthesis (Murata N., ed.) vol I, pp. 25-32, Kluwer Academic Publishers, Dordrecht.
65. Zuber, H. (1985) Structure and function of the light-harvesting complexes and their polypeptides, Photochem. Photobiol. 42, 821-844.
66. Zuber, H. (1986) Structure of light-harvesting antenna complexes of photosinthetic bacteria and red algae, Trends Biochem. Sci. 11, 414-419.
67. Zuber, H. (1987) The structure of light-harvesting pigment-protein complexes, in The light reactions (Barber, J., ed) pp. 157-259, Elsevier Biomedical, Amsterdam.
68. Zuber. H., Brunnisholz, R. & Sidler, W. (1987) Structure and function of light-harvesting pigment-protein complexes, Photosynthesis 15, 233-271.