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. 1997 Jun;179(11):3588–3593. doi: 10.1128/jb.179.11.3588-3593.1997

Isolation and characterization of multiple adenylate cyclase genes from the cyanobacterium Anabaena sp. strain PCC 7120.

M Katayama 1, M Ohmori 1
PMCID: PMC179152  PMID: 9171404

Abstract

Adenylate cyclase genes, designated cyaA, cyaB1, cyaB2, cyaC, and cyaD, were isolated from the filamentous cyanobacterium Anabaena sp. strain PCC 7120 by complementation of a strain of Escherichia coli defective for the presence of cya. These genes encoded polypeptides consisting of 735, 859, 860, 1,155, and 546 amino acid residues, respectively. Deduced amino acid sequences of the regions near the C-terminal ends of these cya genes were similar to those of catalytic domains of eukaryotic adenylate cyclases. The remaining part of each cya gene towards its N-terminal end showed a characteristic structure. CyaA had two putative membrane-spanning regions. Both CyaB1 and CyaB2 had regions that were very similar to the cyclic GMP (cGMP)-binding domain of cGMP-stimulated cGMP phosphodiesterase. CyaC consisted of four distinct domains forming sequentially from the N terminus: a response regulator-like domain, a histidine kinase-like domain, a response regulator-like domain, and the catalytic domain of adenylate cyclase. CyaD contained the forkhead-associated domain in its N-terminal region. Expression of these genes was examined by reverse transcription-PCR. The transcript of cyaC was shown to be predominant in this cyanobacterium. The cellular cyclic AMP level in the disruptant of the cyaC mutant was much lower than that in the wild type.

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Selected References

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  1. Aiba H., Kawamukai M., Ishihama A. Cloning and promoter analysis of the Escherichia coli adenylate cyclase gene. Nucleic Acids Res. 1983 Jun 11;11(11):3451–3465. doi: 10.1093/nar/11.11.3451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Alexandre S., Paindavoine P., Tebabi P., Pays A., Halleux S., Steinert M., Pays E. Differential expression of a family of putative adenylate/guanylate cyclase genes in Trypanosoma brucei. Mol Biochem Parasitol. 1990 Dec;43(2):279–288. doi: 10.1016/0166-6851(90)90152-c. [DOI] [PubMed] [Google Scholar]
  3. Archdeacon J., Talty J., Boesten B., Danchin A., O'Gara F. Cloning of the second adenylate cyclase gene (cya2) from Rhizobium meliloti F34: sequence similarity to eukaryotic cyclases. FEMS Microbiol Lett. 1995 May 1;128(2):177–184. doi: 10.1111/j.1574-6968.1995.tb07519.x. [DOI] [PubMed] [Google Scholar]
  4. Beuve A., Boesten B., Crasnier M., Danchin A., O'Gara F. Rhizobium meliloti adenylate cyclase is related to eucaryotic adenylate and guanylate cyclases. J Bacteriol. 1990 May;172(5):2614–2621. doi: 10.1128/jb.172.5.2614-2621.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Black T. A., Cai Y., Wolk C. P. Spatial expression and autoregulation of hetR, a gene involved in the control of heterocyst development in Anabaena. Mol Microbiol. 1993 Jul;9(1):77–84. doi: 10.1111/j.1365-2958.1993.tb01670.x. [DOI] [PubMed] [Google Scholar]
  6. Bolivar F., Rodriguez R. L., Greene P. J., Betlach M. C., Heyneker H. L., Boyer H. W., Crosa J. H., Falkow S. Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. Gene. 1977;2(2):95–113. [PubMed] [Google Scholar]
  7. Botsford J. L., Harman J. G. Cyclic AMP in prokaryotes. Microbiol Rev. 1992 Mar;56(1):100–122. doi: 10.1128/mr.56.1.100-122.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cai Y. P., Wolk C. P. Use of a conditionally lethal gene in Anabaena sp. strain PCC 7120 to select for double recombinants and to entrap insertion sequences. J Bacteriol. 1990 Jun;172(6):3138–3145. doi: 10.1128/jb.172.6.3138-3145.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  10. Claros M. G., von Heijne G. TopPred II: an improved software for membrane protein structure predictions. Comput Appl Biosci. 1994 Dec;10(6):685–686. doi: 10.1093/bioinformatics/10.6.685. [DOI] [PubMed] [Google Scholar]
  11. Cohen P. Protein phosphorylation and the control of glycogen metabolism in skeletal muscle. Philos Trans R Soc Lond B Biol Sci. 1983 Jul 5;302(1108):13–25. doi: 10.1098/rstb.1983.0034. [DOI] [PubMed] [Google Scholar]
  12. Colicelli J., Field J., Ballester R., Chester N., Young D., Wigler M. Mutational mapping of RAS-responsive domains of the Saccharomyces cerevisiae adenylyl cyclase. Mol Cell Biol. 1990 Jun;10(6):2539–2543. doi: 10.1128/mcb.10.6.2539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Danchin A. Phylogeny of adenylyl cyclases. Adv Second Messenger Phosphoprotein Res. 1993;27:109–162. [PubMed] [Google Scholar]
  14. Dorocicz I. R., Williams P. M., Redfield R. J. The Haemophilus influenzae adenylate cyclase gene: cloning, sequence, and essential role in competence. J Bacteriol. 1993 Nov;175(22):7142–7149. doi: 10.1128/jb.175.22.7142-7149.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Elhai J., Wolk C. P. Conjugal transfer of DNA to cyanobacteria. Methods Enzymol. 1988;167:747–754. doi: 10.1016/0076-6879(88)67086-8. [DOI] [PubMed] [Google Scholar]
  16. Gascuel O., Danchin A. Protein export in prokaryotes and eukaryotes: indications of a difference in the mechanism of exportation. J Mol Evol. 1986;24(1-2):130–142. doi: 10.1007/BF02099961. [DOI] [PubMed] [Google Scholar]
  17. Golden J. W., Wiest D. R. Genome rearrangement and nitrogen fixation in Anabaena blocked by inactivation of xisA gene. Science. 1988 Dec 9;242(4884):1421–1423. doi: 10.1126/science.3144039. [DOI] [PubMed] [Google Scholar]
  18. Henikoff S. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene. 1984 Jun;28(3):351–359. doi: 10.1016/0378-1119(84)90153-7. [DOI] [PubMed] [Google Scholar]
  19. Hood E. E., Armour S., Ownby J. D., Handa A. K., Bressan R. A. Effect of nitrogen starvation on the level of adenosine 3',5'-monophosphate in Anabaena variabilis. Biochim Biophys Acta. 1979 Dec 3;588(2):193–200. doi: 10.1016/0304-4165(79)90202-2. [DOI] [PubMed] [Google Scholar]
  20. Hrabak E. M., Willis D. K. The lemA gene required for pathogenicity of Pseudomonas syringae pv. syringae on bean is a member of a family of two-component regulators. J Bacteriol. 1992 May;174(9):3011–3020. doi: 10.1128/jb.174.9.3011-3020.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Jayaratne P., Keenleyside W. J., MacLachlan P. R., Dodgson C., Whitfield C. Characterization of rcsB and rcsC from Escherichia coli O9:K30:H12 and examination of the role of the rcs regulatory system in expression of group I capsular polysaccharides. J Bacteriol. 1993 Sep;175(17):5384–5394. doi: 10.1128/jb.175.17.5384-5394.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kataoka T., Broek D., Wigler M. DNA sequence and characterization of the S. cerevisiae gene encoding adenylate cyclase. Cell. 1985 Dec;43(2 Pt 1):493–505. doi: 10.1016/0092-8674(85)90179-5. [DOI] [PubMed] [Google Scholar]
  23. Katayama M., Wada Y., Ohmori M. Molecular cloning of the cyanobacterial adenylate cyclase gene from the filamentous cyanobacterium Anabaena cylindrica. J Bacteriol. 1995 Jul;177(13):3873–3878. doi: 10.1128/jb.177.13.3873-3878.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Khramtsov N. V., Feshchenko E. A., Suslova V. A., Shmukler B. E., Terpugov B. E., Rakitina T. V., Atabekova N. V., Lipkin V. M. The human rod photoreceptor cGMP phosphodiesterase beta-subunit. Structural studies of its cDNA and gene. FEBS Lett. 1993 Aug 2;327(3):275–278. doi: 10.1016/0014-5793(93)81003-i. [DOI] [PubMed] [Google Scholar]
  25. Krupinski J., Coussen F., Bakalyar H. A., Tang W. J., Feinstein P. G., Orth K., Slaughter C., Reed R. R., Gilman A. G. Adenylyl cyclase amino acid sequence: possible channel- or transporter-like structure. Science. 1989 Jun 30;244(4912):1558–1564. doi: 10.1126/science.2472670. [DOI] [PubMed] [Google Scholar]
  26. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  27. Lee T. Y., Makino K., Shinagawa H., Amemura M., Nakata A. Phosphate regulon in members of the family Enterobacteriaceae: comparison of the phoB-phoR operons of Escherichia coli, Shigella dysenteriae, and Klebsiella pneumoniae. J Bacteriol. 1989 Dec;171(12):6593–6599. doi: 10.1128/jb.171.12.6593-6599.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Makino K., Shinagawa H., Amemura M., Nakata A. Nucleotide sequence of the phoB gene, the positive regulatory gene for the phosphate regulon of Escherichia coli K-12. J Mol Biol. 1986 Jul 5;190(1):37–44. doi: 10.1016/0022-2836(86)90073-2. [DOI] [PubMed] [Google Scholar]
  29. McAllister-Lucas L. M., Sonnenburg W. K., Kadlecek A., Seger D., Trong H. L., Colbran J. L., Thomas M. K., Walsh K. A., Francis S. H., Corbin J. D. The structure of a bovine lung cGMP-binding, cGMP-specific phosphodiesterase deduced from a cDNA clone. J Biol Chem. 1993 Oct 25;268(30):22863–22873. [PubMed] [Google Scholar]
  30. Mock M., Crasnier M., Duflot E., Dumay V., Danchin A. Structural and functional relationships between Pasteurella multocida and enterobacterial adenylate cyclases. J Bacteriol. 1991 Oct;173(19):6265–6269. doi: 10.1128/jb.173.19.6265-6269.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Montminy M. R., Bilezikjian L. M. Binding of a nuclear protein to the cyclic-AMP response element of the somatostatin gene. Nature. 1987 Jul 9;328(6126):175–178. doi: 10.1038/328175a0. [DOI] [PubMed] [Google Scholar]
  32. Mutoh N., Simon M. I. Nucleotide sequence corresponding to five chemotaxis genes in Escherichia coli. J Bacteriol. 1986 Jan;165(1):161–166. doi: 10.1128/jb.165.1.161-166.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Pitt G. S., Milona N., Borleis J., Lin K. C., Reed R. R., Devreotes P. N. Structurally distinct and stage-specific adenylyl cyclase genes play different roles in Dictyostelium development. Cell. 1992 Apr 17;69(2):305–315. doi: 10.1016/0092-8674(92)90411-5. [DOI] [PubMed] [Google Scholar]
  34. Sanchez M. A., Zeoli D., Klamo E. M., Kavanaugh M. P., Landfear S. M. A family of putative receptor-adenylate cyclases from Leishmania donovani. J Biol Chem. 1995 Jul 21;270(29):17551–17558. doi: 10.1074/jbc.270.29.17551. [DOI] [PubMed] [Google Scholar]
  35. Schlüter C., Duchrow M., Wohlenberg C., Becker M. H., Key G., Flad H. D., Gerdes J. The cell proliferation-associated antigen of antibody Ki-67: a very large, ubiquitous nuclear protein with numerous repeated elements, representing a new kind of cell cycle-maintaining proteins. J Cell Biol. 1993 Nov;123(3):513–522. doi: 10.1083/jcb.123.3.513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Siegelbaum S. A., Camardo J. S., Kandel E. R. Serotonin and cyclic AMP close single K+ channels in Aplysia sensory neurones. Nature. 1982 Sep 30;299(5882):413–417. doi: 10.1038/299413a0. [DOI] [PubMed] [Google Scholar]
  37. Sonnenburg W. K., Mullaney P. J., Beavo J. A. Molecular cloning of a cyclic GMP-stimulated cyclic nucleotide phosphodiesterase cDNA. Identification and distribution of isozyme variants. J Biol Chem. 1991 Sep 15;266(26):17655–17661. [PubMed] [Google Scholar]
  38. Stock J. B., Ninfa A. J., Stock A. M. Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol Rev. 1989 Dec;53(4):450–490. doi: 10.1128/mr.53.4.450-490.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Stone J. M., Collinge M. A., Smith R. D., Horn M. A., Walker J. C. Interaction of a protein phosphatase with an Arabidopsis serine-threonine receptor kinase. Science. 1994 Nov 4;266(5186):793–795. doi: 10.1126/science.7973632. [DOI] [PubMed] [Google Scholar]
  40. Taussig R., Gilman A. G. Mammalian membrane-bound adenylyl cyclases. J Biol Chem. 1995 Jan 6;270(1):1–4. doi: 10.1074/jbc.270.1.1. [DOI] [PubMed] [Google Scholar]
  41. Wang J. Y., Clegg D. O., Koshland D. E., Jr Molecular cloning and amplification of the adenylate cyclase gene. Proc Natl Acad Sci U S A. 1981 Aug;78(8):4684–4688. doi: 10.1073/pnas.78.8.4684. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wang S. P., Sharma P. L., Schoenlein P. V., Ely B. A histidine protein kinase is involved in polar organelle development in Caulobacter crescentus. Proc Natl Acad Sci U S A. 1993 Jan 15;90(2):630–634. doi: 10.1073/pnas.90.2.630. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Wurtzel E. T., Chou M. Y., Inouye M. Osmoregulation of gene expression. I. DNA sequence of the ompR gene of the ompB operon of Escherichia coli and characterization of its gene product. J Biol Chem. 1982 Nov 25;257(22):13685–13691. [PubMed] [Google Scholar]
  44. Yashiro K., Sakamoto T., Ohmori M. Molecular characterization of an adenylate cyclase gene of the cyanobacterium Spirulina platensis. Plant Mol Biol. 1996 Apr;31(1):175–181. doi: 10.1007/BF00020618. [DOI] [PubMed] [Google Scholar]
  45. van Es S., Virdy K. J., Pitt G. S., Meima M., Sands T. W., Devreotes P. N., Cotter D. A., Schaap P. Adenylyl cyclase G, an osmosensor controlling germination of Dictyostelium spores. J Biol Chem. 1996 Sep 27;271(39):23623–23625. doi: 10.1074/jbc.271.39.23623. [DOI] [PubMed] [Google Scholar]

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