Abstract
The genes encoding the Rieske iron-sulfur protein and cytochrome f from a unicellular, naturally transformable, photoheterotrophic cyanobacterium, Synechococcus sp. PCC 7002, formerly Agmenellum quadruplicatum, have been isolated and sequenced. The two genes were found to be on a single operon, petCA.
The Synechococcus sp. PCC 7002 iron-sulfur protein contains 181 amino acids, the conserved putative iron-binding domains CTHLGCV, residues 108–114, and CPCHGS, residues 128–133, no presequence and has a 73% sequence identity to the Nostoc PCC 7906 iron-sulfur protein. The 325 amino acid apocytochrome f sequence contains a 42 amino acid presequence, a CANCH heme binding domain, residues 20–24 from the presumed start of the mature protein, and a predicted hydrophobic membrane-spanning domain, residues 250–269. The mature cytochrome f sequence has a 71.5% sequence identity with Nostoc PCC 7906 cytochrome f and possesses a large (-14) negative charge and low calculated pI of 4.47 compared to higher plant chloroplast sequences. Nine separate domains showing differences in charged residues among cyanobacteria and plants have been identified and the possibility that these domains are involved in the ionic interactions with plastocyanin or cytochrome c-553 is discussed.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Adam Z and Malkin R (1989) On the interaction between cytochrome f and plastocyanin. Biochim Biophys Acta 975: 158–163
Alt J and Herrmann RG (1984) Nucleotide sequence of the gene for preapocytochrome f in the spinach plastid chromosome. Curr Genet 8: 551–557
Anderson GP, Draheim JE and Gross EL (1985) Plastocyanin conformation: The effect of the oxidation state on the pKa of nitrotyrosine-83. Biochim Biophys Acta 810: 123–131
Ausubel FM, Brent R, Kingston RE et al. (1989) Current Protocols in Molecular Biology, Greene Publ. and Wiley-Interscience, New York
Beckmann JD, Ljungdahl PO, Lopez JL and Trumpower BL (1987) Isolation and characterization of the nuclear gene encoding the Rieske iron-sulfur protein (RIP1) from Saccharomyces cerevisiae. J Biol Chem 262: 8901–8909
Beckmann JD, Ljungdahl PO and Trumpower BL (1989) Mutational analysis of the mitochondrial Rieske iron-sulfur protein of Saccharomyces cerevisiae. J Biol Chem 264: 3713–3722
Burks C, Fickett JW, Goad WB, Kanehisa M, Lewritter FI, Rindone WP, Swindell CD, Tung CS and Bilofsky HS (1985) The Genbank(R) nucleic acid sequence database. CABIOS 1: 225–233
Colman PM, Freeman HC, Guss JM, Murata M, Norris VA, Ramshaw JAM and Ventatappa MP (1978) X-ray crystal structure analysis of plastocyanin at 2.7 A resolution. Nature 272: 319–324
Cramer WA and Crofts AR (1983) Electron and proton transport. In: Photosynthesis: Energy Conservation by Plants and Animals, Vol 1, pp 387–467. Academic Press, New York
Cramer WA and Knaff DB (1990) Energy Transduction in Biological Membranes, pp 165–171. Springer-Verlag, New York
Crofts AR (1985) The mechanism of ubiquinol: cytochrome c oxido-reductases of mitochondria and Rb. sphaerodies. In: Martonosi A (ed) The Enzymes of Biological Membranes, pp 347–382. Plenum Press, New York
Davidson E and Daldal F (1987) Primary structure of the bc1 complex of Rhodopseudomonas capsulata. Nucleotide sequence of the pet operon encoding the Rieske, cytochrome b and cytochrome c1 apoproetins. J Mol Biol 195: 13–24
Davis DJ, Frame MK and Johansen DA (1988) Resonance Raman spectroscopy indicates a lysine as the sixth iron ligand in cytochrome f. Biochim Biophys Acta 936: 61–66
Devereux J, Haeberli P and Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucl Acids Res 12: 387–395
Dillela AG and Woo SLC (1985) Cosmid cloning of genomic DNA. FOCUS. 7 #2: 1–5.
Feinberg AP and Vogelstein B (1983) A technique for radiolabeling endonuclease fragments to high specific activity. Anal Biochem 132: 6–13
Gatti DL, Meinhardt SW, Ohnishi T and Tzagoloff A (1989) Structure and function of the mitochondrial bc1 complex: A mutational analysis of the yeast Rieske iron-sulfur protein. J Mol Biol 205: 421–435
George DG, Barker WC and Hunt LT (1986) The protein identification resource (PIR). Nucleic Acids Res 14: 11–15
Giovannoni SJ, Turner S, Olsen GJ, Barns S, Lane DJ and Pace NR (1988) Evolutionary relationships among cyanobacteria and green chloroplasts. J Bacteriol 170: 3584–3592
Gonzalez-Halphen D, Lindonfer HA and Capaldi RA (1988) Subunit arrangement in beef heart complex III. Biochem 27: 7021–7031
Guss JM and Freeman HC (1983) Structure of oxidized poplar plastocyanin at 1.6 A resolution. J Mol Biol 169: 521–563
Haley J and Bogorad L (1989) A 4-KDa maize chloroplast polypeptide associated with the cytochrome b 6 f complex: subunit 5 encoded by the chloroplast petE gene. Proc Natl Acad Sci 86: 1534–1538
Hanahan D (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166: 557–580
Hartl F-U, Pfanner N, Nicholson DW and Neuport W (1989) Mitochondrial protein import. Biochim Biophys Acta 988: 1–45
Ho KK and Krogmann DW (1980) Cytochrome f from spinach and cyanobacteria. J Biol Chem 255: 3855–3861
Ho KK and Krogmann DW (1984) Electron donors to P700 in cyanobacteria and algae an instance of unusual genetic variability. Biochim Biophys Acta 766: 310–316
Kallas T, Spiller S and Malkin R (1988a) Primary structure of contranscribed genes encoding the Rieske Fe-S and cytochrome f proteins of the cyanobacterium Nostoc PCC 7906. Proc Natl Acad Sci 85: 5794–5798
Kallas T, Spiller S and Malkin R (1988b) Charterization of two operons encoding the cytochrome b 6-f complex of the cyanobacterium Nostoc PCC 7906. J Biol Chem 263: 14334–14342
Ko K and Straus NA (1987) Sequence of the apocytochrome f gene encoded by the Vicia faba chloroplast genome. Nucl Acids Res 15: 2391
Kyte J and Doolittle RF (1982) A simple methods for displaying the hydropathic character of a protein. J Mol Biol 157: 105–132
Margoliash E and Bosshard HR (1983) Guided by electrostatics, a textbook protein comes of age. Trends Biochem Sci 8: 316–320
Merchant S and Bogorad L (1986) Regulation by Cu of the expression of plastocyanin and cytochrome c552 in Chlamydomonas reinhardtii. Mol Cell Biol 6: 462–469
Morand LZ, Frame MK, Colvert KK, Johnson DA, Krogmann DW and Davis DJ (1989) Plastocyanin cytochrome f interaction. Biochem 28: 8039–8047
Ohyama K, Fukuzawa H, Konchi T, Shirai H, Sano T, Sano S, Umesono K, Shiki Y, Takeuchi M, Chang Z, Aota S-I, Inokuchi H and Ozeki H (1986) Chloroplast gene organization deduced from complete sequence of liverworth Marchantia polymorpha chloroplast DNA. Nature 322: 572–574
Pallotta D, Bernier F, Hamelin M, Martel R and Lemieux G (1986) cDNA cloning of Physarum polycephalum stagespecific mRNA's. In: Dove DF, Dee J, Hatano S, Haugli FB and Wolfarth-Botterman K-E (eds) The Molecular Biology of Physarum polycephalum, pp 315–328. Plenum Press, New York and London
Pfefferkorn B and Meyer HE (1986) N-terminal amino acid sequence of the Rieske iron-sulfur protein from the cytochrome b 6/f complex of spinach thylakoids. FEBS Lett 26: 233–237
Rippka R, Deruelles J, Waterbury JB, Herdman M and Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111: 1–61
Rosenberg SM, Stahl MM, Kobayashi I and Stahl FW (1985) Improved in vitro packaging of coliphage lambda DNA: A one-strain system free from endogenous phage. Gene 38: 165–175
Sanger F, Nicklen S and Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci 74: 5463–5467
Schagger H, Borchart U, Machleidt W, Link TA and VonJagow G (1987) Isolation and amino acid sequence of the ‘Rieske’ iron-sulfur protein of beef heart ubiquinol: cytochrome c reductase. FEBS Lett 219: 161–168
Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinozaki K, Ohto C, Torazawa K, Meng BY, Sugita M, Deno H, Kamogoshira K, Yamada K, Kusuda J, Takaiwa F, Kato A, Tohdoh N et al. (1986) The complete nucleotide sequence of the tobacco chloroplast genome: Its gene organization and expression. EMBO J 5: 2043–2049
Stepuhn J, Rotter C, Hermans J, Jansen T, Salnikow J, Hauska G and Herrmann RG (1987) The complete amino acid sequence of the Rieske FeS precursor protein from spinach chloroplasts deduced from cDNA analysis. Mol Gen Genet 210: 171–177
Stevens SE, Patterson COP and Myers J (1973) The production of hydrogen peroxide in blue by blue-green algae: A survey. J Phycol 9: 427–430
Sykes AG (1985) Structure and electron transfer reactivity of the blue copper protein plastocyanin. Chem Soc Rev 140: 283–315
Szczepaniak A and Cramer WA (1989) On the topography and function of the chloroplast b 6-f complex. Zeit fur Naturfosch 44c: 123–131
Takabe T and Ishikawa H (1989) Kinetic studies on a cross-linked complex between plastocyanin and cytochrome f. Biochem J 105: 98–102
Tyagi AK and Herrmann RG (1986) Location and nucleotide sequence of the preapocytochrome f gene on the Oenothera hookeri plastid chromosome (Euoenothera plastome I). Curr Genet 10: 481–486
Widger WR and Cramer WA (1991) The cytochrome b 6/f complex. In: Bogarad L (eds) Cell Culture and Somatic Cell Genetics of Plants, Vol 7B, pp 149–176. Academic Press Inc, New York
Widger WR, Cramer WA, Herrmann RG and Trebst A (1984) Sequence homology and structural similarity between cytochrome b of mitochondrial complex III and the chloroplast b 6-f complex: Position of the cytochrome b hemes in the membrane. Proc Natl Acad Sci 81: 674–678
Wikstrom MKF and Saraste M (1984) The mitochondrial respiratory chain. In: Ernster L (ed) Bioenergetics, pp 49–94. Elsevier, Amsterdam
Willey DL and Gray JC (1988) Synthesis and assembly of the cytochrome b-f complex in higher plants. Photosynth Res 17: 125–144
Willey DL, Auffet AD and Gray JC (1984a) Structure and topology of chytochrome f in pea chloroplast membranes. Cell 36: 556–562
Willey DL, Howe CJ, Auffret AD, Bowman CM, Dyer TA and Gray JC (1984b) Location and nucleotide sequence of the gene for cytochrome f in wheat chloroplast DNA. Mol Gen Genet 194: 416–422
Wu N-H, Cote JC and Wu R (1986) Nucleotide sequence of the rice cytochrome f gene and the presence of sequence variation near this gene. Gene 50: 271–278
Yu L, Mei Q-C and Yu C-A (1984) Characterization of purified cytochrome b-c1 complex from Rhodopseudomonas sphaeroides R-26. J Biol Chem 259: 271–278
Author information
Authors and Affiliations
Additional information
The sequences reported in this paper have been deposited in the EMBL/Genbank data base (IntelliGenetics, Mountain View, CA, and Eur. Mol. Biol. Lab., Heidelberg) (accession no. M74514).
Rights and permissions
About this article
Cite this article
Widger, W.R. The cloning and sequencing of Synechococcus sp. PCC 7002 petCA operon: Implications for the cytochrome c-553 binding domain of cytochrome f . Photosynth Res 30, 71–84 (1991). https://doi.org/10.1007/BF00042005
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00042005