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The atp1 and atp2 operons of the cyanobacterium Synechocystis sp. PCC 6803

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Abstract

The two operons atp1 and atp2, encoding the subunits of the FOF1 ATP-synthase, have been cloned and sequenced from the cyanobacterium Synechocystis sp. PCC 6803. The organization of the different genes in the operons have been found to resemble that of the cyanobacteria Synechococcus sp. PCC 6301 and Anabaena sp. PCC 7120. The Synechocystis FOF1 ATP-synthase has nine subunits. A tenth open reading frame with unknown function was detected at the 5′ end of atp1, coding for a putative gene product similar to uncI in Escherichia coli.

A promoter structure was inferred for the Synechocystis atp operons and compared to other known promoters of cyanobacteria. Even though the operon structure of atp1 and atp2 in Synechocystis resembles the corresponding operons of Synechococcus, the amino acid sequences of individual gene products show marked differences. Genetic distances between cyanobacterial genes and genes for ATP-synthase subunits from other species have been calculated and compiled into evolutionary trees.

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References

  1. Mitchell, P: Coupling of phosphorylation to electron and hydrogen transfer by a chemiosmotic type of mechanism. Nature 191: 144–148 (1961).

    Google Scholar 

  2. Futai, M, Noumi, T, Maeda, M: ATP synthase (H+-ATPase): results by combined biochemical and molecular biological approaches. Annu Rev Biochem 58: 111–136 (1989).

    Google Scholar 

  3. Schneider, E, Altendorf, K: Bacterial adenosine 5′-triphosphate synthase (F1FO): purification and reconstitution of FO complexes and biochemical and functional characterization of their subunits. Microbiol Rev 51: 477–497 (1987).

    Google Scholar 

  4. Herrmann, RG, Westhoff, P, Alt, J, Tittgen, J, Nelson, N: Thylakoid membrane proteins and their genes. In: van, Vlooten-Doting, L, Groot, GSP, Halls, TC (eds), Molecular Form and Function of the Plant Genome, pp. 233–256. Plenum, New York (1985).

    Google Scholar 

  5. Henning, J, Herrmann, RG: Chloroplast ATP synthase of spinach contains nine nonidentical subunit species, six of which are encoded by plastid chromosomes in two operons in a phylogenetically conserved arrangement. Mol Gen Genet 203: 117–128 (1986).

    Google Scholar 

  6. Margulis, L: In Symbiosis in Cell Evolution, pp. 37–62. W.H. Freeman & Co., San Francisco (1987).

    Google Scholar 

  7. Lill, H, Nelson, N: Molecular evolution of proton-ATPases. In: Baltscheffsky, M (ed) Current Research in Photosynthesis Vol. III, pp. 128–136. Kluwer Academic Publishers, Dordrecht, Netherlands (1990).

    Google Scholar 

  8. Curtis, SE: Structure, organization and expression of cyanobacterial ATP synthase genes. Photosynth Res 18: 223–244 (1988).

    Google Scholar 

  9. Grigorieva, G, Shestakov, S: Transformation in the cyanobacterium Synechocystis 6803. FEMS Microbiol Lett 13: 367–370 (1982).

    Google Scholar 

  10. Kolowsky, KS, Williams, JGK, Szalay, AA: Length of foreign DNA in chimeric plasmids determines the efficiency of its integration into the chromosome of the cyanobacterium Synechococcus R2. Gene 27: 289–299 (1984).

    Google Scholar 

  11. Vermaas, WFJ, Williams, JGK, Rutherford, AW, Mathis, P, Arntzen, CJ: Genetically engineered mutant of the cyanobacterium Synechocystis lacks the photosystem II chlorophyll-binding protein. Proc Natl Acad Sci USA 83: 9474–9477 (1986).

    Google Scholar 

  12. Williams, JGK: Construction of specific mutations in photosystem II photosynthetic reaction center by genetic engineering methods in Synechocystis 6803. Meth Enzymol 167: 766–778 (1988).

    Google Scholar 

  13. Noumi T, Beltrán C, Nelson H, Nelson N: Mutational analysis of yeast vacuolar H+-ATPase. Proc Natl Acad Sci USA (in press) (1991).

  14. Cozens, AL, Walker, JE: The organization and sequence of the genes for ATP synthase subunits in the cyanobacterium Synechococcus 6301. Support for an endosymbiontic origin of chloroplasts. J Mol Biol 194: 359–383 (1987).

    Google Scholar 

  15. Shinozaki, K, Deno, H, Kato, A, Sugiura, M: Overlap and cotranscription of the genes for the β and ε subunits of tobacco chloroplast ATPase. Gene 24: 147–155 (1983).

    Google Scholar 

  16. Maniatis, T, Fritsch, EF, Sambrook, J: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor NY (1982).

    Google Scholar 

  17. Sanger, F, Nicklen, S, Coulson, AR: DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–546 (1977).

    Google Scholar 

  18. Henikoff, S: Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene 28: 351–359 (1984).

    Google Scholar 

  19. Devereux, J, Haeberli, P, Smithies, O: A comprehensive set of sequence analysis programs for the VAX. Nucl Acids Res 12: 387–395 (1984).

    Google Scholar 

  20. Felsenstein, J: PHYLIP 3.2. Manual. University of California Herbarium, Berkeley (1989).

    Google Scholar 

  21. Golden, SS, Cho, D-SC, Nalty, MS: Two functional psbD genes in the cyanobacterium Synechococcus strain PCC 7942. J Bact 171: 4707–4713 (1989).

    Google Scholar 

  22. McCarn, DF, Whitaker, RA, Alam, J, Vrba, JM, Curtis, SE: The genes encoding the α, γ, δ and four FO subunits of the ATP synthase constitute an operon in the cyanobacterium Anabaena strain PCC 7120. J Bact 170: 3448–3458 (1988).

    Google Scholar 

  23. Curtis, SE: Genes encoding the β and ε subunits of the proton translocating ATPase from Anabaena strain PCC 7120. J Bact 169: 80–86 (1987).

    Google Scholar 

  24. Reznikoff, WS, Siegele, DA, Cowing, DW, Gross, CA: The regulation of transcription initiation in bacteria. Ann Rev Genet 9: 355–388 (1985).

    Google Scholar 

  25. Shine, J, Dalgarno, L: 3′-terminal sequence of Escherichia coli 16S ribosomal RNA. Complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci USA 71: 1342–1346 (1974).

    Google Scholar 

  26. Brusilow, WSA, Klionsky, DJ, Simoni, RD: Differentiation polypeptide synthesis of the proton-translocating ATPase of Escherichia coli. J Bact 151: 1363–1371 (1982).

    Google Scholar 

  27. Werner, S, Schumann, J, Strotmann, HH: The primary structure of the γ-subunit of the ATPase from Synechocystis 6803. FEBS Lett 261: 204–208 (1990).

    Google Scholar 

  28. Sander C, Schneider R: Database of homology derived protein structures and the structural meaning of sequence alignment. In: Mewes HW (ed) Abstracts of the Workshop on Computer Applications in Biosciences, MPI Biochemie, Munich, Germany (1990).

  29. Engelbrecht, S, Deckers-Hebestreit, G, Altendorf, K, Junge, W: Cross-reconstitution of the FO-F1-ATP synthases of chloroplasts and Escherichia coli with special emphasis on subunit δ. Eur J Biochem 181: 485–491 (1989).

    Google Scholar 

  30. Schmidt, G, Rodgers, AJW, Howitt, SM, Munn, AL, Hudson, GS, Holten, TA, Whitfeld, PR, Bottomley, W, Gibson, F, Cox, GB: The chloroplast CFOI subunit can replace the b-subunit of the FOF1-ATPase in a mutant strain of Escherichia coli K12. Biochim Biophys Acta 1015: 195–199 (1990).

    Google Scholar 

  31. Morden, CW, Golden, SS: psbA genes indicate common ancestry of prochlorophytes and chloroplasts. Nature 337: 382–385 (1989), with correction in Nature 339: 400 (1989).

    Google Scholar 

  32. Gogarten, JP, Kibak, H, Dittrich, P, Taiz, L, Bowman, EJ, Bowman, BJ, Manolson, MF, Poole, RJ, Date, T, Oshima, T, Konishi, J, Denda, K, Yoshida, M: Evolution of the vacuolar hydrogen ion-ATPase: implications for the origin of eukaryotes. Proc Natl Acad Sci USA 86: 6661–6665 (1989).

    Google Scholar 

  33. Reichelt, BY, Delaney, SF: The nucleotide sequence of the large subunit of ribulose 1,5-bisphosphate carboxylase from a unicellular cyanobacterium, Synechococcus PCC 6301. DNA 2: 121–129 (1983).

    Google Scholar 

  34. Nierzwicki-Bauer, SA, Curtis, SE: Cotranscription of genes encoding the small and large subunits of ribulose 1,5-bisphosphate carboxylase in the cyanobacterium Anabaena 7120. Proc Natl Acad Sci USA 81: 5961–5965 (1984).

    Google Scholar 

  35. Mulligan, ME, Haselkorn, R: Nitrogen fixation (nif) genes of the cyanobacterium Anabaena species strain PCC 7120. J Biol Chem 264: 19200–19207 (1989).

    Google Scholar 

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

    Google Scholar 

  37. Zurawski, G, Bottomley, W, Whitfeld, PR: Structures of the genes for the β and ε subunits of spinach chloroplast ATPase indicate a dicistronic mRNA and an overlapping translation stop/start signal. Proc Natl Acad Sci USA 79: 6260–6264 (1982).

    Google Scholar 

  38. Saraste, M, Gay, NJ, Eberle, A, Runswick, MJ, Walker, JE: The atp operon: nucleotide sequence of the genes for the γ, β, and ε subunits of Escherichia coli ATP synthase. Nucl Acids Res 9: 5287–5296 (1981).

    Google Scholar 

  39. Ohta, S, Yohda, M, Ishizuka, M, Hirata, H, Hamamoto, T, Otawara-Hamamoto, Y, Matsuda, K, Kagawa, Y: Sequence and over-expression of subunits of adenosine triphosphate synthase in thermophilic bacterium PS3. Biochim Biophys Acta 933: 141–155 (1988).

    Google Scholar 

  40. Hawthorne, A, Brusilow, WSA: Sequence of the genes for the β and ε subunits of the ATP synthase of Bacillus megaterium QM B1551. Biophys Biochem Res Commun 151: 926–931 (1988).

    Google Scholar 

  41. Falk, G, Hampe, A, Walker, JE: Nucleotide sequence of the Rhodospirillum rubrum atp operon. Biochem J 228: 391–407 (1985).

    Google Scholar 

  42. Breen, GAM, Holmans, PL, Garnett, KE: Isolation and characterization of a complementary DNA for the nuclear-coded precursor of the β-subunit of the bovine mitochondrial F1-ATPase. Biochemistry 27: 3955–3961 (1988).

    Google Scholar 

  43. Hermans, J, Rother, C, Bichler, J, Stepphun, J, Herrmann, RG: Nucleotide sequence of cDNA clones encoding the complete precursor for subunit δ of thylakoid-located ATP synthase from spinach. Plant Mol Biol 10: 323–330 (1988).

    Google Scholar 

  44. Gay, NJ, Walker, JE: The atp operon: nucleotide sequence of the region encoding the α-subunit of Escherichia coli ATP-synthase. Nucl Acids Res 9: 3919–3926 (1981).

    Google Scholar 

  45. Brusilow, WSA, Scarpetta, MA, Hawthorne, CA, Clark, WP: Organization and sequence of the genes coding for the proton-translocating ATPase of Bacillus megaterium. J Biol Chem 264: 1528–1533 (1989).

    Google Scholar 

  46. Walker, JE, Gay, NJ, Powell, SJ, Kostina, M, Dyer, M: ATP synthase from bovine mitochondria: sequences of imported precursors of oligomycin sensitivity conferral protein, factor 6, and adenosinetriphosphatase inhibitor protein. Biochemistry 26: 8613–8619 (1987).

    Google Scholar 

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Lill, H., Nelson, N. The atp1 and atp2 operons of the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol Biol 17, 641–652 (1991). https://doi.org/10.1007/BF00037050

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