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A multigene family in Calothrix sp. PCC 7601 encodes phycocyanin, the major component of the cyanobacterial light-harvesting antenna

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Summary

In cyanobacteria, light is harvested by phycobilisomes which are essentially made up of chromophoric proteins called phycobiliproteins. We have characterized two gene clusters (cpcB1, cpcA1 and cpcB3, cpcA3) each encoding the two subunits of phycocyanin (βPC and αPC, respectively), one of the major phycobiliproteins in Calothrix 7601. Downstream from the gene encoding the PCα subunit in cluster 1, an open reading frame was found, cpcE1. These genes are organized in two transcriptional units, namely: cpcB3 A3 and cpcB1 A1 E1. All these genes are transcribed whatever the chromatic light received during cell growth. Consequently, although only one type of “constitutive” PC has been biochemically characterized, we have demonstrated that there are two cpc operons “constitutively” transcribed in this strain. With the previously described red light “inducible” cpcB2 A2 operon, there are three copies of the PC encoding genes in Calothrix 7601. The significance of this newly described multigene family in cyanobacteria is discussed. We have also mapped the 5′ and 3′ termini of the major transcript from the cpc1 operon. Analysis of the 5′ untranslated region of this transcript has revealed alternative secondary structures which are proposed to play a role in the regulation of the expression of this operon.

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References

  • Aiba H, Adhya S, de Combrugghe B (1981) Evidence for two functional gal promoters in intact Escherichia coli cells. J Biol Chem 256:11905–11910

    Google Scholar 

  • Anderson LK, Rayner MC, Sweet RM, Eiserling FA (1983) Regulation of Nostoc sp. phycobilisome structure by light and temperature. J Bacteriol 155:1407–1416

    Google Scholar 

  • Belasco JG, Beatty JT, Adams CW, von Gabain A, Cohen SN (1985) Differential expression of photosynthesis genes in R. capsulata results from segmental differences in stability within the polycistronic rxcA transcript. Cell 40:171–181

    Google Scholar 

  • Belknap WR, Haselkorn R (1987) Cloning and light regulation of expression of the phycocyanin operon of the cyanobacterium Anabaena. EMBO J 6:871–884

    Google Scholar 

  • Brawerman G (1987) Determinants of messenger RNA stability. Cell 48:5–6

    Google Scholar 

  • Bryant DA, de Lorimier R, Guglielmi G, Stirewalt VL, Dubbs JM, Illman B, Gasparich G, Buzby J, Cantrell A, Murphy RC, Gingrich J, Porter RD, Steven SE Jr (1986) The cyanobacterial photosynthetic apparatus: a molecular genetic analysis. In: Youvan DC, Daldal F (eds) Microbial Energy Transduction: Genetics, Structure and Function of Membrane Proteins. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, p 39

    Google Scholar 

  • Casey J, Davidson N (1977) Rates of formation and thermal stabilities of RNA: DNA and DNA: DNA duplexes at high concentrations of formamide. Nucleic Acids Res 4:1539–1552

    Google Scholar 

  • Cech TR, Tanner NK, Tinoco I Jr, Weir BR, Zuker M, Perlman P (1983) Secondary structure of the Tetrahymena ribosomal RNA intervening sequence: Structural homology with fungal mitochondrial intervening sequences. Proc Natl Acad Sci USA 80:3903–3907

    Google Scholar 

  • Conley PB, Lemaux PG, Grossman AR (1985) Cyanobacterial light-harvesting complex subunits encoded in two red light-induced transcripts. Science 230:550–553

    Google Scholar 

  • Conley PB, Lemaux PG, Lomax TL, Grossman AR (1986) Genes encoding major light-harvesting polypeptides are clustered on the genome of the cyanobacterium Fremyella diplosiphon. Proc Natl Acad Sci USA 83:3924–3928

    Google Scholar 

  • Csiszàr K, Houmard J, Damerval T, Tandeau de Marsac N (1987) Transcriptional analysis of the canobacterial gvpABC operon in differentiated cells: occurrence of an antisense RNA complementary to three overlapping transcripts. Gene 60:29–38

    Google Scholar 

  • Curtis SE, Haselkorn R (1984) Isolation, sequence and expression of two members of the 32 Kd thylakoid membrane protein gene family from the cyanobacterium Anabaena 7120. Plant Mol Biol 3:249–258

    Google Scholar 

  • Damerval T, Houmard J, Guglielmi G, Csiszàr K, Tandeau de Marsac N (1987) A developmentally regulated gvpABC operon is involved in the formation of gas vesicles in the cyanobacterium Calothrix 7601. Gene 54:83–92

    Google Scholar 

  • De Lorimier R, Bryant DA, Porter RD, Liu WY, Jay E, Stevens SE, Jr (1984) Genes for the α and β subunits of phycocyanin. Proc Natl Acad Sci USA 81:7946–7950

    Google Scholar 

  • Donovan WP, Kushner SR (1986) Polynucleotide phosphorylase and ribonuclease II are required for cell viability and mRNA turnover in Escherichia coli K-12. Proc Natl Acad Sci USA 83:120–124

    Google Scholar 

  • Frank G, Sidler W, Widmer H, Zuber H (1978) The complete amino acid sequence of both subunits of C-phycocyanin from the cyanobacterium Mastigocladus laminosus. Hoppe Seyler's Z Physiol Chem 359:1491–1507

    Google Scholar 

  • Freidenreich P, Apell GS, Glazer AN (1978) Structural studies on phycobiliproteins. II. C-phycocyanin: Amino acid sequence of the β-subunit. Specific cleavage of the α-subunit. J Biol Chem 253:212–219

    Google Scholar 

  • Füglistaller P, Suter F, Zuber H (1986) Linker polypeptides of the phycobilisome from the cyanobacterium Mastigocladus laminosus. I. Amino-acid sequences and functions. Biol Chem Hoppe Seyler 367:615–626

    Google Scholar 

  • Glazer AN (1976) Phycocyanins: Structure and function. Photochem Photobiol Rev 1:71–115

    Google Scholar 

  • Glazer AN (1980) Structure and evolution of photosynthetic accessory pigment systems with special reference to phycobiliproteins. In: Sigman DS, Brazier MAB (eds) The Evolution of Protein Structure and Function. Academic Press, London, New York, p 221

    Google Scholar 

  • Glazer AN (1985) Light harvesting by phycobilisomes. Annu Rev Biophys Biophys Chem 14:47–77

    Google Scholar 

  • Glazer AN, Apell GS, Hixson CS, Bryant DA, Rimon S, Brown DM (1976) Biliproteins of cyanobacteria and rhodophyta. Homologous family of photosynthetic accessory pigments. Proc Natl Acad Sci USA 73:428–431

    Google Scholar 

  • Glick RE, Zilinskas BA (1982) Role of the colorless polypeptides in phycobilisome reconstitution. Plant Physiol 69:991–997

    Google Scholar 

  • Golden SS, Brusslan J, Haselkorn R (1986) Expression of a family of psbA genes encoding a photosystem II polypeptide in the cyanobacterium Anacystis nidulans R2. EMBO J 5:2789–2798

    Google Scholar 

  • Hayes PK, Walsby AE, Walker JE (1986) Complete amino acid sequence of cyanobacterial gas vesicle protein indicates 70-residue molecule that corresponds in size to the crystallographic unit cell. Biochem J 236:31–36

    Google Scholar 

  • Houmard J, Mazel D, Moguet C, Bryant DA, Tandeau de Marsac N (1986) Organization and nucleotide sequence of genes encoding core components of the phycobilisomes from Synechococcus 6301. Mol Gen Genet 205:404–410

    Google Scholar 

  • Klotz AV, Leary JA, Glazer AN (1986) Post-translational methylation of asparaginyl residues. J Biol Chem 261:15891–15894

    Google Scholar 

  • Lachance MA (1981) Genetic relatedness of heterocystous cyanobacteria by deoxyribonucleic acid-deoxyribonucleic acid reassociation. Int J Sytem Bacteriol 31:139–147

    Google Scholar 

  • Lipman DJ, Pearson WR (1985) Rapid and sensitive protein similarity searches. Science 227:1435–1441

    Google Scholar 

  • Lomax TL, Conley PB, Schilling J, Grossman AR (1987) Isolation and characterization of light-regulated phycobilisome linker polypeptide genes and their transcription as a polycistronic mRNA. J Bacteriol 169:2675–2684

    Google Scholar 

  • Maxam AM, Gilbert W (1980) Sequencing of end labeled DNA with base specific chemical cleavage. Methods Enzymol 65:499–560

    Google Scholar 

  • Mazel D, Guglielmi G, Houmard J, Sidler W, Bryant DA, Tandeau de Marsac N (1986) Green light induces transcription of the phycoerythrin operon in the cyanobacterium Calothrix 7601. Nucleic Acids Res 14:8279–8290

    Google Scholar 

  • Mulligan B, Schultes N, Chen L, Bogorad L (1984) Nucleotide sequence of a multiple-copy gene for the B protein of photosystem II of a cyanobacterium. Proc Natl Acad Sci USA 81:2693–2697

    Google Scholar 

  • Newbury SF, Smith NH, Robinson EC, Hiles ID, Higgins CF (1987) Stabilization of translationally active mRNA by prokaryotic REP sequences. Cell 48:297–310

    Google Scholar 

  • Pilot TJ, Fox JL (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

    Google Scholar 

  • Platt T (1986) Transcription termination and the regulation of gene expression. Annu Rev Biochem 55:339–372

    Google Scholar 

  • Robinson SJ, Haselkorn R (1985) Second copy of the gene for nitrogenase reductase in Anabaena. Abstracts of the Vth International Symposium on Photosynthetic Prokaryotes, Grindelwald, Switzerland, p 346

  • Salser W (1977) Globin mRNA sequences: Analysis of base pairing and evolutionary implications. Cold Spring Harbor Symp Quant Biol 77:985–1010

    Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467

    Google Scholar 

  • 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

    Google Scholar 

  • Schirmer T, Huber R, Schneider M, Bode W, Miller M, Hackert ML (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

    Google Scholar 

  • Tandeau de Marsac N (1983) Phycobilisomes and complementary chromatic adaptation in cyanobacteria. Bull Inst Pasteur 81:201–254

    Google Scholar 

  • Tandeau de Marsac N, Houmard J (1987) Advances in cyanobacterial molecular genetics. In: Fay P, Van Baalen C (eds) The Cyanobacteria. Elsevier Science Publishers B.V. (Biomedical Division), Holland, p 251–302

    Google Scholar 

  • Tandeau de Marsac N, Mazel D, Bryant DA, Houmard J (1985) Molecular cloning and nucleotide sequence of a developmentally regulated gene from the cyanobacterium Calothrix PCC 7601: A gas vesicle protein gene. Nucleic Acids Res 13:7223–7236

    Google Scholar 

  • Vogelstein B, Gillespie D (1979) Preparation and analytical purification of DNA from agarose. Proc Natl Acad Sci USA 76:615–619

    Google Scholar 

  • Williams VP, Glazer AN (1978) Structural studies on phycobiliproteins. I. Bilin-containing peptides of C-phycocyanin. J Biol Chem 253:202–211

    Google Scholar 

  • Wong HC, Chang S (1986) Identification of a positive retroregulator that stabilizes mRNAs in bacteria. Proc Natl Acad Sci USA 83:3233–3237

    Google Scholar 

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Communicated by R. Herrmann

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Mazel, D., Houmard, J. & de Marsac, N.T. A multigene family in Calothrix sp. PCC 7601 encodes phycocyanin, the major component of the cyanobacterial light-harvesting antenna. Mol Gen Genet 211, 296–304 (1988). https://doi.org/10.1007/BF00330607

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