Molecular and General Genetics MGG

, Volume 226, Issue 1–2, pp 107–112 | Cite as

Deletion of the psbG1 gene of the cyanobacterium Synechocystis sp. PCC6803 leads to the activation of the cryptic psbG2 gene

  • Klaus Steinmüller
  • Ulrike Ellersiek
  • Lawrence Bogorad
Article

Summary

The genes psbG1 and psbG2 in the cyanobacterium Synechocystis sp. PCC6803 are homologous. The psbG1 gene is located on the chromosome and is part of the ndhC-psbGI -ORF157 operon, while psbG2 is located on a plasmid and is not flanked by equivalent ndhC or ORF157 genes. Mutants in which psbG1 is deleted grow well under autotrophic conditions, while their growth is impeded in mixotrophic medium. These results argue against a functional role for psbG1 in photosynthesis, i.e. photosystem II, and are more compatible with a function in respiration. The psbG2 gene is not transcribed in wild-type cells, but in psbGl mutants the insertion of DNA sequences in close proximity to the psbG2 reading frame has led to transcriptional activation of psbG2. Thus, psbG2 represents an example of a cryptic gene, similar to those found in other bacteria.

Key words

psbG Synechocystis 6803 Cryptic gene 

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References

  1. Beck E, Ludwig G, Auerswald EA, Reiss B, Schaller H (1982) Nucleotide sequence and exact localization of the neomycin phosphotransferase gene from transposon Tn5. Gene 19:327–336Google Scholar
  2. Bennoun P (1982) Evidence for a respiratory chain in the chloroplast. Proc Natl Acad Sci USA 79:4342–4356Google Scholar
  3. Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81:1991–1995Google Scholar
  4. Dzelzkalns VA, Bogorad L (1986) Stable transformation of the cyanobacterium Synechocystis sp. PCC6803 induced by UV irradiation. J Bacteriol 165:964–971Google Scholar
  5. Dzelzkalns VA, Bogorad L (1988) Molecular analysis of a mutant defective in photosynthetic oxygen evolution and isolation of a complementing clone by a novel screening procedure. EMBO J 7:333–338Google Scholar
  6. Feinberg AP, Vogelstein B (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132:6–13Google Scholar
  7. Gfeller RP, Gibbs M (1985) Fermentative metabolism of Chlamydomonas reinhardii. II. Role of plastoquinone. Plant Physiol 77:509–511Google Scholar
  8. Godde D (1982) Evidence for a membrane-bound NADH-plastoquinone-oxidoreductase in Chlamydomonas reinhardii CW-15. Arch Microbiol 131:197–202Google Scholar
  9. Godde D, Trebst A (1980) NADH as electron donor for the photosynthetic membrane of Chlamydomonas reinhardii. Arch Microbiol 127:245–252Google Scholar
  10. Hall BG, Yokoyama S, Calhoun DH (1983) Role of cryptic genes in microbial evolution. Mol Biol Evol 1:109–124Google Scholar
  11. Hirano M, Satoh K, Katoh S (1980) Plastoquinone as a common link between photosynthesis and respiration in a blue-green alga. Photosynth Res 1:149–162Google Scholar
  12. Hiratsuka J, Shimada H, Whittier R, Ishibashi T, Sakamoto M, Mori M, Kondo C, Honji Y, Sun CR, Meng BY, Li YQ, Kanno A, Nishizawa Y, Hirai A, Shinozaki K, Sugiura M (1989) The complete sequence of the rice (Oryza sativa) chloroplast genome: Intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals. Mol Gen Genet 217:185–194Google Scholar
  13. Jansson C, Debus RJ, Osiewacz HD, Gurevitz M, McIntosh L (1987) Construction of an obligate photoheterotrophic mutant of the cyanobacterium Synechocystis 6803. Plant Physiol 85:1021–1025Google Scholar
  14. Labarre J, Chauvat F, Thuriaux P (1989) Insertional mutagenesis by random cloning of antibiotic resistance genes into the genome of the cyanobacterium Synechocystis Strain PCC6803. J Bacteriol 171: 3449–3457Google Scholar
  15. Lockau W (1981) Evidence for a dual role of cytochrome c-553 and plastocyanin in photosynthesis and respiration of the cyanobacterium Anabaena variabilis. Arch Microbiol 128:336–340Google Scholar
  16. Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New YorkGoogle Scholar
  17. Mann N, Carr NG (1974) Control of macromolecular composition and cell division in the blue-green alga Anacystis nidulans. J Gen Microbiol 83:399–405Google Scholar
  18. Matsubayashi T, Wakasugi T, Shinozaki K, Yamaguchi-Shinozaki K, Zaita N, Hidaka T, Meng BY, Ohto C, Tanaka M, Kato A, Maruyama T, Sugiura M (1987) Six chloroplast genes (ndhA-F) homologous to human mitochondrial genes encoding components of the respiratory chain NADH dehydrogenase are actively expressed: Determination of the splice sites in ndhA and ndhB pre-mRNAs. Mol Gen Genet 210:385–393Google Scholar
  19. Matthijs HCP, Lubberding HJ (1988) Dark respiration in cyanobacteria. In: Rogers LJ, Gallon JR (eds) Biochemistry of the algae and cyanobacteria. Proc of the Phytochem Soc of Europe, vol 28. Oxford University Press, Oxford, pp 131–145Google Scholar
  20. Mayes SR, Cook KM, Barber J (1990) Nucleotide sequence of the second psbG gene in Synechocystis 6803. Possible implications for psbG function as a NAD(P)H dehydrogenase subunit gene. FEBS Lett 262:49–54Google Scholar
  21. McMaster GK, Carmichael GG (1977) Analysis of single- and double-stranded nucleic acid on polyacrylamide and agarose gels by using glyoxal and acridine orange. Proc Natl Acad Sci USA 74:2835–2838Google Scholar
  22. Nixon PJ, Gounaris K, Coomber SA, Hunter CN, Dyer TA, Barber J (1989) psbG is not a photosystem two gene but may be an ndh Gene. J Biol Chem 264:14129–14135Google Scholar
  23. Ohyama K, Kohchi T, Sano T, Yamada Y (1988) Newly identified groups of genes in chloroplasts. Trends Biochem Sci 13:19–22Google Scholar
  24. Peschek GA (1983) The cytochrome f-b electron transport complex. A common link between photosynthesis and respiration in the cyanobacterium Anacystis nidulans. Biochem J 210:269–272Google Scholar
  25. Peschek GA (1987) Respiratory electron transport. In: Fay P, Van Baalen C (eds) The Cyanobacteria. Elsevier, Amsterdam, pp 119–161Google Scholar
  26. Philbrick JB, Zilinskas BA (1987) Cloning, nucleotide sequence and mutational analysis of the gene encoding the Photosystem II manganese-stabilizing polypeptide of Synechocystis 6803. Mol Gen Genet 212:418–425Google Scholar
  27. Pritchard AE, Seilhamer JJ, Mahalingam R, Sable CL, Venuti SE, Cummings DJ (1990) Nucleotide sequence of the mitochondrial genome of Paramecium. Nucleic Acids Res 18:173–180Google Scholar
  28. Rao RN, Rogers SG (1979) Plasmid pKC7: A vector containing ten restriction endonuclease sites suitable for cloning DNA segments. Gene 7:79–82Google Scholar
  29. Reed KC, Mann DA (1985) Rapid transfer of DNA from agarose gels to nylon membranes. Nucleic Acids Res 13:7207–7221Google Scholar
  30. Reynolds AE, Feltow J, Wright A (1981) Insertion of DNA activates the cryptic bgl operon in E. coli K12. Nature 293:625–629Google Scholar
  31. Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467Google Scholar
  32. Scherer S, Almon H, Böger P (1988) Interaction of photosynthesis, respiration and nitrogen fixation in cyanobacteria. Photosynth Res 15:95–114Google Scholar
  33. Sherman L, Bricker T, Guikema J, Pakrasi H (1987) The protein composition of the photosynthetic complexes from the cyanobacterial thylakoid membrane. In: Fay P, van Baalen C (eds) The Cyanobacteria. Elsevier, Amsterdam, pp 1–33Google Scholar
  34. Steinmetz AA, Castroviejo M, Sayre RT, Bogorad L (1986) Protein PSII-G. An additional component of photosystem 11 identified through its plastid gene in maize. J Biol Chem 261:2485–7188Google Scholar
  35. Steinmüller K, Bogorad L (1990) Identification of a psbG-homolo-gous gene in Synechocystis sp. PCC6803. In: Baltscheffsky M (ed) Current Research in Photosynthesis, vol III. Kluwer Academic, Dordrecht, pp 12557–12560Google Scholar
  36. Steinmüller K, Ley AC, Steinmetz AA, Sayre RT, Bogorad L (1989) Characterization of the ndhC-psbG-ORF157/159 operon of maize plastid DNA and of the cyanobacterium Synechocystis sp. PCC6803. Mol Gen Genet 216:60–69Google Scholar

Copyright information

© Springer-Verlag 1991

Authors and Affiliations

  • Klaus Steinmüller
    • 1
  • Ulrike Ellersiek
    • 1
  • Lawrence Bogorad
    • 2
  1. 1.Institut für Entwicklungs- und Molekularbiologie der PflanzenHeinrich-Heine-Universität DüsseldorfDüsseldorfGermany
  2. 2.The Biological LaboratoriesHarvard UniversityCambridgeUSA

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