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. 1988 Aug;170(8):3448–3458. doi: 10.1128/jb.170.8.3448-3458.1988

Genes encoding the alpha, gamma, delta, and four F0 subunits of ATP synthase constitute an operon in the cyanobacterium Anabaena sp. strain PCC 7120.

D F McCarn 1, R A Whitaker 1, J Alam 1, J M Vrba 1, S E Curtis 1
PMCID: PMC211314  PMID: 2900236

Abstract

A cluster of genes encoding subunits of ATP synthase of Anabaena sp. strain PCC 7120 was cloned, and the nucleotide sequences of the genes were determined. This cluster, denoted atp1, consists of four F0 genes and three F1 genes encoding the subunits a (atpI), c (atpH), b' (atpG), b (atpF), delta (atpD), alpha (aptA), and gamma (atpC) in that order. Closely linked upstream of the ATP synthase subunit genes is an open reading frame denoted gene 1, which is equivalent to the uncI gene of Escherichia coli. The atp1 gene cluster is at least 10 kilobase pairs distant in the genome from apt2, a cluster of genes encoding the beta (atpB) and epsilon (atpE) subunits of the ATP synthase. This two-clustered ATP synthase gene arrangement is intermediate between those found in chloroplasts and E. coli. A unique feature of the Anabaena atp1 cluster is overlap between the coding regions for atpF and atpD. The atp1 cluster is transcribed as a single 7-kilobase polycistronic mRNA that initiates 140 base pairs upstream of gene 1. The deduced translation products for the Anabaena sp. strain PCC 7120 subunit genes are more similar to chloroplast ATP synthase subunits than to those of E. coli.

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Selected References

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  1. Alam J., Whitaker R. A., Krogmann D. W., Curtis S. E. Isolation and sequence of the gene for ferredoxin I from the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol. 1986 Dec;168(3):1265–1271. doi: 10.1128/jb.168.3.1265-1271.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Andreo C. S., Patrie W. J., McCarty R. E. Effect of ATPase activation and the delta subunit of coupling factor 1 on reconstitution of photophosphorylation. J Biol Chem. 1982 Sep 10;257(17):9968–9975. [PubMed] [Google Scholar]
  3. Belknap W. R., Haselkorn R. Cloning and light regulation of expression of the phycocyanin operon of the cyanobacterium Anabaena. EMBO J. 1987 Apr;6(4):871–884. doi: 10.1002/j.1460-2075.1987.tb04833.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bird C. R., Koller B., Auffret A. D., Huttly A. K., Howe C. J., Dyer T. A., Gray J. C. The wheat chloroplast gene for CF(0) subunit I of ATP synthase contains a large intron. EMBO J. 1985 Jun;4(6):1381–1388. doi: 10.1002/j.1460-2075.1985.tb03790.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Borbely G., Simoncsits A. 3'-Terminal conserved loops of 16S rRNAs from the cyanobacterium Synechococcus AN PCC 6301 and maize chloroplast differ only in two bases. Biochem Biophys Res Commun. 1981 Aug 14;101(3):846–852. doi: 10.1016/0006-291x(81)91827-1. [DOI] [PubMed] [Google Scholar]
  6. Brusilow W. S., Klionsky D. J., Simoni R. D. Differential polypeptide synthesis of the proton-translocating ATPase of Escherichia coli. J Bacteriol. 1982 Sep;151(3):1363–1371. doi: 10.1128/jb.151.3.1363-1371.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cozens A. L., Walker J. E., Phillips A. L., Huttly A. K., Gray J. C. A sixth subunit of ATP synthase, an F(0) component, is encoded in the pea chloroplast genome. EMBO J. 1986 Feb;5(2):217–222. doi: 10.1002/j.1460-2075.1986.tb04201.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cozens A. L., Walker J. E. The organization and sequence of the genes for ATP synthase subunits in the cyanobacterium Synechococcus 6301. Support for an endosymbiotic origin of chloroplasts. J Mol Biol. 1987 Apr 5;194(3):359–383. doi: 10.1016/0022-2836(87)90667-x. [DOI] [PubMed] [Google Scholar]
  9. Curtis S. E. Genes encoding the beta and epsilon subunits of the proton-translocating ATPase from Anabaena sp. strain PCC 7120. J Bacteriol. 1987 Jan;169(1):80–86. doi: 10.1128/jb.169.1.80-86.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Curtis S. E., Haselkorn R. Isolation and sequence of the gene for the large subunit of ribulose-1,5-bisphosphate carboxylase from the cyanobacterium Anabaena 7120. Proc Natl Acad Sci U S A. 1983 Apr;80(7):1835–1839. doi: 10.1073/pnas.80.7.1835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dunn S. D., Heppel L. A. Properties and functions of the subunits of the Escherichia coli coupling factor ATPase. Arch Biochem Biophys. 1981 Sep;210(2):421–436. doi: 10.1016/0003-9861(81)90206-x. [DOI] [PubMed] [Google Scholar]
  12. Foster D. L., Fillingame R. H. Stoichiometry of subunits in the H+-ATPase complex of Escherichia coli. J Biol Chem. 1982 Feb 25;257(4):2009–2015. [PubMed] [Google Scholar]
  13. Futai M., Kanazawa H. Structure and function of proton-translocating adenosine triphosphatase (F0F1): biochemical and molecular biological approaches. Microbiol Rev. 1983 Sep;47(3):285–312. doi: 10.1128/mr.47.3.285-312.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gay N. J., Walker J. E. The atp operon: nucleotide sequence of the promoter and the genes for the membrane proteins, and the delta subunit of Escherichia coli ATP-synthase. Nucleic Acids Res. 1981 Aug 25;9(16):3919–3926. doi: 10.1093/nar/9.16.3919. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gay N. J., Walker J. E. The atp operon: nucleotide sequence of the region encoding the alpha-subunit of Escherichia coli ATP-synthase. Nucleic Acids Res. 1981 May 11;9(9):2187–2194. doi: 10.1093/nar/9.9.2187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hatefi Y. The mitochondrial electron transport and oxidative phosphorylation system. Annu Rev Biochem. 1985;54:1015–1069. doi: 10.1146/annurev.bi.54.070185.005055. [DOI] [PubMed] [Google Scholar]
  17. Hicks D. B., Yocum C. F. Properties of the cyanobacterial coupling factor ATPase from Spirulina platensis. I. Electrophoretic characterization and reconstitution of photophosphorylation. Arch Biochem Biophys. 1986 Feb 15;245(1):220–229. doi: 10.1016/0003-9861(86)90208-0. [DOI] [PubMed] [Google Scholar]
  18. Hicks D. B., Yocum C. F. Properties of the cyanobacterial coupling factor ATPase from Spirulina platensis. II. Activity of the purified and membrane-bound enzymes. Arch Biochem Biophys. 1986 Feb 15;245(1):230–237. doi: 10.1016/0003-9861(86)90209-2. [DOI] [PubMed] [Google Scholar]
  19. Howe C. J., Auffret A. D., Doherty A., Bowman C. M., Dyer T. A., Gray J. C. Location and nucleotide sequence of the gene for the proton-translocating subunit of wheat chloroplast ATP synthase. Proc Natl Acad Sci U S A. 1982 Nov;79(22):6903–6907. doi: 10.1073/pnas.79.22.6903. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Krebbers E. T., Larrinua I. M., McIntosh L., Bogorad L. The maize chloroplast genes for the beta and epsilon subunits of the photosynthetic coupling factor CF1 are fused. Nucleic Acids Res. 1982 Aug 25;10(16):4985–5002. doi: 10.1093/nar/10.16.4985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lubberding H. J., Zimmer G., van Walraven H. S., Schrickx J., Kraayenhof R. Isolation, purification and characterization of the ATPase complex from the thermophilic cyanobacterium Synechococcus 6716. Eur J Biochem. 1983 Dec 1;137(1-2):95–99. doi: 10.1111/j.1432-1033.1983.tb07800.x. [DOI] [PubMed] [Google Scholar]
  22. McCarty R. E., Racker E. Partial resolution of the enzymes catalyzing photophosphorylation. 3. Activation of adenosine triphosphatase and 32P-labeled orthophosphate -adeno-sine triphosphate exchange in chloroplasts. J Biol Chem. 1968 Jan 10;243(1):129–137. [PubMed] [Google Scholar]
  23. Moroney J. V., Fullmer C. S., McCarty R. E. Characterization of the cysteinyl-containing peptides of the gamma subunit of coupling factor 1. J Biol Chem. 1984 Jun 10;259(11):7281–7285. [PubMed] [Google Scholar]
  24. Nierzwicki-Bauer S. A., Curtis S. E., Haselkorn R. Cotranscription of genes encoding the small and large subunits of ribulose-1,5-bisphosphate carboxylase in the cyanobacterium Anabaena 7120. Proc Natl Acad Sci U S A. 1984 Oct;81(19):5961–5965. doi: 10.1073/pnas.81.19.5961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Palmer J. D. Comparative organization of chloroplast genomes. Annu Rev Genet. 1985;19:325–354. doi: 10.1146/annurev.ge.19.120185.001545. [DOI] [PubMed] [Google Scholar]
  26. Pick U., Racker E. Purification and reconstitution of the N,N'-dicyclohexylcarbodiimide-sensitive ATPase complex from spinach chloroplasts. J Biol Chem. 1979 Apr 25;254(8):2793–2799. [PubMed] [Google Scholar]
  27. Reznikoff W. S., Siegele D. A., Cowing D. W., Gross C. A. The regulation of transcription initiation in bacteria. Annu Rev Genet. 1985;19:355–387. doi: 10.1146/annurev.ge.19.120185.002035. [DOI] [PubMed] [Google Scholar]
  28. Rice D., Mazur B. J., Haselkorn R. Isolation and physical mapping of nitrogen fixation genes from the cyanobacterium Anabaena 7120. J Biol Chem. 1982 Nov 10;257(21):13157–13163. [PubMed] [Google Scholar]
  29. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Saraste M., Gay N. J., Eberle A., Runswick M. J., Walker J. E. The atp operon: nucleotide sequence of the genes for the gamma, beta, and epsilon subunits of Escherichia coli ATP synthase. Nucleic Acids Res. 1981 Oct 24;9(20):5287–5296. doi: 10.1093/nar/9.20.5287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Shine J., Dalgarno L. The 3'-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1342–1346. doi: 10.1073/pnas.71.4.1342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Shinozaki K., Deno H., Wakasugi T., Sugiura M. Tobacco chloroplast gene coding for subunit I of proton-translocating ATPase: comparison with the wheat subunit I and E. coli subunit b. Curr Genet. 1986;10(5):421–423. doi: 10.1007/BF00418416. [DOI] [PubMed] [Google Scholar]
  33. Tinoco I., Jr, Borer P. N., Dengler B., Levin M. D., Uhlenbeck O. C., Crothers D. M., Bralla J. Improved estimation of secondary structure in ribonucleic acids. Nat New Biol. 1973 Nov 14;246(150):40–41. doi: 10.1038/newbio246040a0. [DOI] [PubMed] [Google Scholar]
  34. Zurawski G., Bottomley W., Whitfeld P. R. Structures of the genes for the beta and epsilon subunits of spinach chloroplast ATPase indicate a dicistronic mRNA and an overlapping translation stop/start signal. Proc Natl Acad Sci U S A. 1982 Oct;79(20):6260–6264. doi: 10.1073/pnas.79.20.6260. [DOI] [PMC free article] [PubMed] [Google Scholar]

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