Abstract
The phycobilisomes and phycobiliproteins of Synechococcus sp. PCC 7002 wild-type strain PR6000 have been isolated and characterized. The hemidiscoidal phycobilisomes of strain PR6000 are composed of eleven different polypeptides: phycocyanin α and β subunits; allophycocyanin α and β subunits; α subunit of allophycocyanin B; the allophycocyanin β-subunit-like polypeptide of Mr 18 000; the linker phycobiliprotein of Mr 99 000; and non-chromophore-carrying linker polypeptides of Mr 33 000, 29 000, 9000, and 8000. Several of these polypeptides were purified to homogeneity and their amino acid compositions and amino-terminal amino acid sequences were determined. Analyses of the phycobiliproteins of Synechococcus sp. PCC 7002 were greatly facilitated by comparative studies performed with a mutant strain, PR6008, constructed to be devoid of the phycocyanin α and β subunits by recombinant DNA techniques and transformation of strain PR6000. The absence of phycocyanin did not greatly affect the allophycocyanin content of the mutant strain but caused the doubling time to increase 2–7-fold depending upon the light intensity at which the cells were grown. Although intact phycobilisome cores could not be isolated from this mutant, it is probable that functionally intact cores do exist in vivo.
Similar content being viewed by others
Abbreviations
- SDS-PAGE:
-
polyacrylamide gel electrophoresis in the presence of sodium dodecylsulfate
- 2D-PAGE:
-
two-dimensional gel electrophoresis in which the first dimension consisted of isoelectric focusing in the presence of 8.0 M urea in the pH range 4–6 and the second dimension consisted of electrophoresis in the presence of sodium dodecylsulfate. The nomenclature employed for the phycobiliprotein subunits and linker polypeptides is that defined by Glazer (1985)
References
AndersonLK, EiserlingFA (1986) Asymmetrical core structure in phycobilisomes of the cyanobacterium Synechocystis 6701. J Mol Biol 191: 441–451
AndersonLK, RaynerMC, EiserlingFA (1984) Ultra-violet mutagenesis of Synechocystis sp. 6701: mutations in chromatic adaptation and phycobilisome assembly. Arch Microbiol 138: 237–243
BelknapWR, HaselkornR (1987) Cloning and light regulation of expression of the phycocyanin operon of the cyanobacterium Anabaena. EMBO J 6: 871–884
BoussibaS, RichmondAE (1980) C-Phycocyanin as a storage protein in the blue-green alga Spirulina platensis. Arch Microbiol 125: 143–147
BruceD, BrimbleS, BryantDA (1989) State transitions in a phycobilisome-less mutant of the cyanobacterium Synechococcus sp. PCC 7002. Biochim Biophys Acta 974: 66–73
BryantDA (1987) The cyanobacterial photosynthetic apparatus: comparison to those of higher plants and photosynthetic bacteria. In: PlattT, LiWKW (eds) Photosynthetic picoplankton. Canadian Bulletin of Fisheries and Aquatic Sciences, vol 214. Dept. of Fisheries and Oceans Ottawa, Canada, pp 423–500
BryantDA (1988) Genetic analysis of phycobilisome biosynthesis, assembly, and function in the cyanobacterium Synechococcus sp. PCC 7002. In: StevensSEJr, BryantDA (eds) Light-energy transduction in photosynthesis: higher plant and bacterial models. American Soc Plant Physiologists, Rockville, MD, pp 62–90
BryantDA (1990) Phycobilisomes of Synechococcus sp. PCC 7002: progress towards a complete structural and functional analysis via molecular genetics. In: BogoradL, VasilIK (eds) Cell culture and somatic cell genetics of plants, vol 7: The molecular biology of plastids and mitochondria. Academic Press, New York (in press)
BryantDA, deLorimierR, GuglielmiG, StirewaltVL, CantrellA, StevensSEJr (1987) The cyanobacterial photosynthetic apparatus: a structural and functional analysis employing molecular genetics. In: BigginsJ (ed) Progress in photosynthesis research, vol IV. Martinus Nijhoff, Dordrecht, pp 749–755
BryantDA, GlazerAN, EiserlingFA (1976) Characterization and structural properties of the major biliproteins of Anabaena sp. Arch Microbiol 110: 61–75
BryantDA, GuglielmiG, Tandeau de MarsacN, CastesA-M, Cohen-BazireG (1979) The structure of cyanobacterial phycobilisomes: a model. Arch Microbiol 123: 113–127
BryantDA, Tandeau de MarsacN (1988) Isolation of genes encoding components of the photosynthetic apparatus. Methods Enzymol 167: 755–765
BuzbyJS, PorterRD, StevensSEJr (1983) Plasmid transformation in Agmenellum quadruplicatum PR-6: Construction of biphasic plasmids and characterization of their transformation properties. J Bacteriol 154: 1446–1450
BuzbyJS, PorterRD, StevensSEJr (1985) Expression of the Escherichia coli lacZ gene on a plasmid vector in a cyanobacterium. Science 230: 805–807
Cohen-BazireG, BeguinS, RimonS, GlazerAN, BrownDM (1977) Physico-chemical and immunological properties of allophycocyanins. Arch Microbiol 111: 225–238
Cohen-BazireG, BryantDA (1982) Phycobilisomes: composition and structure. In: CarnNG, WhittonBA (eds) The biology of the cyanobacteria. Blackwell Scientific, Oxford, pp 143–190
DagertM, EhrlichSD (1979) Prolonged incubation in calcium chloride improves the competence of E. coli cells. Gene 6: 23–28
deLorimierR, BryantDA, PorterRD, LiuW-Y, JayE, StevensSEJr (1984) Genes for the α and β subunits of phycocyanin. Proc Natl Acad Sci USA 81: 7946–7950
deLorimierR, GuglielmiG, BryantDA, StevensSEJr (1990a) Structure and mutation of a gene encoding a Mr 33000 phycocyanin-associated linker polypeptide. Arch Microbiol 153: 541–549
de Lorimier R, Bryant DA, Stevens SE Jr (1990 b) Genetic analysis of a 9 kDa phycocyanin-associated linker polypeptide. Biochim Biophys Acta (in press)
DukeCS, CezeauxA, AllenMM (1989) Changes in polypeptide composition of Synechocystis sp. strain 6308 phycobilisomes induced by nitrogen starvation. J Bacteriol 171: 1960–1966
ElmorjaniK, ThomasJ-C, SebbanP (1986) Phycobilisomes of wild type and pigment mutants of the cyanobacterium Synechocystis PCC 6803. Arch Microbiol 146: 186–191
FontanaA, DalzoppoD, GrandiC, ZamboninM (1981) Chemical cleavage of tryptophanyl and tyrosyl peptide bonds via oxidative halogenation mediated by o-iodosobenzoic acid. Biochemistry 20: 6997–7004
GanttE (1981) Phycobilisomes. Annu Rev Plant Physiol 32: 327–347
GanttE, CunninghamFXJr, LipschultzCA, MimuroM (1988) N-terminus conservation in the terminal pigment of phycobilisomes from a prokaryotic and eukaryotic alga. Plant Physiol 86: 996–998
GardnerEE, StevensSEJr, FoxJL (1980) Purification and characterization of the C-phycocyanin from Agmenellum quadruplicatum. Biochim Biophys Acta 624: 187–195
GingrichJC, LundellDJ, GlazerAN (1983) Core substructure in cyanobacterial phycobilisomes. J Cell Biochem 22: 1–14
GlazerAN (1974) Phycocyanins: structure and function. Photochem Photobiol Rev 1: 71–115
GlazerAN (1982) Phycobilisomes: Structure and dynamics. Annu Rev Microbiol 36: 173–198
GlazerAN (1984) Phycobilisome. A macromolecular complex optimized for light energy transfer. Biochim Biophys Acta 768: 29–51
GlazerAN (1985) Light harvesting by phycobilisomes. Annu Rev Biophys Biophys Chem 14: 47–77
GlazerAN (1987) Phycobilisomes: assembly and attachment. In: FayP, VanBaalenC (eds) The cyanobacteria. Elsevier Biomedical, Amsterdam, pp 69–94
GlazerAN (1988) Phycobiliproteins. Meth Enzymol 167: 291–303
GlazerAN, BryantDA (1975) Allophycocyanin B (559-1 671, 618 nm). A new cyanobacterial phycobiliprotein. Arch Microbiol 104: 15–22
GlazerAN, WilliamsRC, YamanakaG, SchachmanHK (1979) Characterization of cyanobacterial phycobilisomes in zwitterionic detergents. Proc Natl Acad Sci USA 76: 6162–6166
GrossmanAR, LemauxPG, ConleyPB, BrunsBU, AndersonLK (1988) Characterization of phycobiliprotein and linker polypeptide genes in Fremyella diplosiphon and their regulated expression during complementary chromatic adaptation. Photosyn Res 17: 23–56
KallaSR, LindLK, GustafssonP (1989) Genetic analysis of phycobilisome mutants in the cyanobacterium Synechococcus species PCC 6301. Mol Microbiol 3: 339–347
LaemmliUK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (Lond) 227: 680–685
LundellDJ, GlazerAN (1981) Allophycocyanin B. A common β subunit in Synechococcus allophycocyanin B (559-2 670 nm) and allophycocyanin (559-3 650 nm). J Biol Chem 256: 12600–12606
LundellDJ, GlazerAN (1983) Molecular architecture of a light-harvesting antenna. Structure of the 18 S core-rod subassembly of the Synechococcus 6301 phycobilisome. J Biol Chem 258: 894–901
MacCollR, Guard-FriarD (1987) Phycobiliproteins. CRC Press, Boca Raton
ManiatisT, FritschEF, SambrookJ (1982) Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor
MaxsonP, SauerK, ZhouJ, BryantDA, GlazerAN (1989) Spectroscopic studies of cyanobacterial phycobilisomes lacking core polypeptides. Biochim Biophys Acta 977: 40–51
O'FarrellPH (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250: 4007–4021
PilotTJ, FoxJL (1984) Cloning and sequencing of the genes encoding the α and β subunits of C-phycocyanin from the cyanobacterium Agmenellum quadruplicatum. Proc Natl Acad Sci USA 81: 6983–6987
PorterRD (1986) Transformation in cyanobacteria. CRC Crit Rev Microbiol 13: 111–132
RapsS, KyciaJH, LedbetterMC, SiegelmanHW (1985) Light intensity adaptation and phycobilisome composition of Microcystis aeruginosa. Plant Physiol 79: 983–987
RumbeliR, WirthM, SuterF, ZuberH, (1987) The phycobiliprotein 559-4 of the allophycocyanin core from the cyanobacterium Mastigocladus laminosus. Biol Chem Hoppe-Seyler 368: 1–9
SchirmerT, HuberR, SchneiderM, BodeW, MillerM, HackertML (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
SchirmerT, BodeW, HuberR (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
SchroederWA, SheltonJB, SheltonJR (1969) An examination of conditions for the cleavage of polypeptide chains with cyanogen bromide: application to catalase. Arch Biochem Biophys 130: 551–556
SiegelmanHW, WieczorekGA, TurnerBC (1965) Preparation of calcium phosphate for protein chromatography. Anal Biochem 13: 402–404
SouthernEM (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98: 503–517
StevensSEJr, PattersonCOP, MyersJ (1973) The production of hydrogen peroxide by blue-green algae: a survey. J Phycol 9: 427–430
SwankRT, MunkresKD (1971) Molecular weight analysis of oligopeptides by electrophoresis in polyacrylamide gel with sodium dodecyl sulfate. Anal Biochem 39: 462–477
Tandeau de MarsacN, Cohen-BazireG (1977) Molecular composition of cyanobacterial phycobilisomes. Proc Natl Acad Sci USA 74: 1635–1639
Tandeau de MarsacN, MazelD, DamervalT, GuglielmiG, CapuanoV, HoumardJ (1988) Photoregulation of gene expression in the filamentous cyanobacterium Calothrix sp. PCC 7601: light-harvesting complexes and cell differentiation. Photosyn Res 18: 99–132
WehrmeyerW (1983) Phycobiliproteins and phycobiliprotein organization in the photosynthetic apparatus of cyanobacteria, red algae, and cryptophytes. In: JensenU, FairbrothersDE (eds) Proteins and nucleic acids in plant systematics. Springer, Berlin Heidelberg New York, pp 143–167
YamanakaG, GlazerAN (1980) Dynamic aspects of phycobilisome structure. Phycobilisome turnover during nitrogen starvation in Synechococcus sp. Arch Microbiol 124: 39–47
YamanakaG, GlazerAN (1981) Dynamic aspects of phycobilisome structure: modulation of phycocyanin content of Synechococcus phycobilisomes. Arch Microbiol 130: 23–30
YamanakaG, GlazerAN, WilliamsRC (1978) Cyanobacterial phycobilisomes. Characterization of the phycobilisomes of Synechococcus sp. 6301. J Biol Chem 253: 8303–8310
ZilinskasBA, GreenwaldLS (1986) Phycobilisome structure and function. Photosyn Res 10: 7–35
ZuberH (1987) The structure of light-harvesting pigment-protein complexes. In: BarberJ (ed) The light reactions. Elsevier Biomedical, Amsterdam, pp 197–259
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Bryant, D.A., de Lorimier, R., Guglielmi, G. et al. 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 (1990). https://doi.org/10.1007/BF00245264
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00245264