1887

Abstract

sp. strain PCC 7120 ( PCC 7120) is a filamentous, nitrogen-fixing cyanobacterium. Upon deprivation of combined nitrogen, about 5–10 % of the cells become heterocysts, i.e. cells devoted to N fixation. Heterocysts are intercalated among vegetative cells and distributed in a semi-regular pattern, and adjacent heterocysts are rarely observed. Previously, we showed that the cell cycle could play a regulatory function during heterocyst development, although the mechanism involved remains unknown. As a further step to understand this phenomenon, we identified the region for chromosomal DNA replication, located between and . The region of PCC 7120 was able to support the self-replication of a plasmid in the unicellular cyanobacterium sp. PCC 6803. Surprisingly, integration of the region into the chromosome of PCC 7120 through homologous recombination led to much slower cell growth in the absence of a combined-nitrogen source and to multiple contiguous proheterocysts after prolonged incubation. Real-time RT-PCR showed that expression of two heterocyst-related genes, and , was altered in these strains: expression remained high 48 h after induction, and increased to high levels after induction for 12 h. These results suggest that the balance between and DnaA could be important for heterocyst development.

Funding
This study was supported by the:
  • Natural Science Foundation of China (Award 30970088 and 30670046)
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2011-07-01
2024-04-26
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References

  1. Bauer C. C., Ramaswamy K. S., Endley S., Scappino L. A., Golden J. W., Haselkorn R. ( 1997). Suppression of heterocyst differentiation in Anabaena PCC 7120 by a cosmid carrying wild-type genes encoding enzymes for fatty acid synthesis. FEMS Microbiol Lett 151:23–30 [View Article][PubMed]
    [Google Scholar]
  2. Black T. A., Wolk C. P. ( 1994). Analysis of a Het mutation in Anabaena sp. strain PCC 7120 implicates a secondary metabolite in the regulation of heterocyst spacing. J Bacteriol 176:2282–2292[PubMed]
    [Google Scholar]
  3. Black T. A., Cai Y., Wolk C. P. ( 1993). Spatial expression and autoregulation of hetR, a gene involved in the control of heterocyst development in Anabaena . Mol Microbiol 9:77–84 [View Article][PubMed]
    [Google Scholar]
  4. Boye E., Løbner-Olesen A., Skarstad K. ( 2000). Limiting DNA replication to once and only once. EMBO Rep 1:479–483[PubMed] [CrossRef]
    [Google Scholar]
  5. Buikema W. J., Haselkorn R. ( 1991). Characterization of a gene controlling heterocyst differentiation in the cyanobacterium Anabaena 7120. Genes Dev 5:321–330 [View Article][PubMed]
    [Google Scholar]
  6. Buikema W. J., Haselkorn R. ( 2001). Expression of the Anabaena hetR gene from a copper-regulated promoter leads to heterocyst differentiation under repressing conditions. Proc Natl Acad Sci U S A 98:2729–2734 [View Article][PubMed]
    [Google Scholar]
  7. Cai Y. P., Wolk C. P. ( 1990). Use of a conditionally lethal gene in Anabaena sp. strain PCC 7120 to select for double recombinants and to entrap insertion sequences. J Bacteriol 172:3138–3145[PubMed]
    [Google Scholar]
  8. Callahan S. M., Buikema W. J. ( 2001). The role of HetN in maintenance of the heterocyst pattern in Anabaena sp. PCC 7120. Mol Microbiol 40:941–950 [View Article][PubMed]
    [Google Scholar]
  9. Dereeper A., Guignon V., Blanc G., Audic S., Buffet S., Chevenet F., Dufayard J. F., Guindon S., Lefort V. et al. ( 2008). Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:Web Server issueW465–W469 [View Article][PubMed]
    [Google Scholar]
  10. Elhai J., Wolk C. P. ( 1988). Conjugal transfer of DNA to cyanobacteria. Methods Enzymol 167:747–754 [View Article][PubMed]
    [Google Scholar]
  11. Gantar M., Elhai J., Jia J., Ow M. ( 1995). Predisposition towards heterocyst differentiation by individual cells of Anabaena . Program and Abstracts, Vth Cyanobacterial Molecular Biology Workshop25 Pacific Grove, CA: Asilomar Conference Center;
    [Google Scholar]
  12. Gao F., Zhang C. T. ( 2008). Origins of replication in Cyanothece 51142. Proc Natl Acad Sci U S A 105:E125 [View Article][PubMed]
    [Google Scholar]
  13. Golden J. W., Robinson S. J., Haselkorn R. ( 1985). Rearrangement of nitrogen fixation genes during heterocyst differentiation in the cyanobacterium Anabaena . Nature 314:419–423 [View Article][PubMed]
    [Google Scholar]
  14. Grigorieva G. A., Shestakov S. V. ( 1982). Transformation in the cyanobacterium Synechocystis sp. PCC 6803. FEMS Microbiol Lett 13:367–370 [View Article]
    [Google Scholar]
  15. Kuhn I., Peng L., Bedu S., Zhang C.-C. ( 2000). Developmental regulation of the cell division protein FtsZ in Anabaena sp. strain PCC 7120, a cyanobacterium capable of terminal differentiation. J Bacteriol 182:4640–4643 [View Article][PubMed]
    [Google Scholar]
  16. Livak K. J., Schmittgen T. D. ( 2001). Analysis of relative gene expression data using real-time quantitative PCR and the method. Methods 25:402–408 [View Article][PubMed]
    [Google Scholar]
  17. Mackiewicz P., Zakrzewska-Czerwinska J., Zawilak A., Dudek M. R., Cebrat S. ( 2004). Where does bacterial replication start? Rules for predicting the oriC region. Nucleic Acids Res 32:3781–3791 [View Article][PubMed]
    [Google Scholar]
  18. Marraccini P., Bulteau S., Cassier-Chauvat C., Mermet-Bouvier P., Chauvat F. ( 1993). A conjugative plasmid vector for promoter analysis in several cyanobacteria of the genera Synechococcus and Synechocystis . Plant Mol Biol 23:905–909 [View Article][PubMed]
    [Google Scholar]
  19. Meeks J. C., Elhai J. ( 2002). Regulation of cellular differentiation in filamentous cyanobacteria in free-living and plant-associated symbiotic growth states. Microbiol Mol Biol Rev 66:94–121 [View Article][PubMed]
    [Google Scholar]
  20. Messer W. ( 2002). The bacterial replication initiator DnaA. DnaA and oriC, the bacterial mode to initiate DNA replication. FEMS Microbiol Rev 26:355–374[PubMed]
    [Google Scholar]
  21. Messer W., Weigel C. ( 1997). DnaA initiator – also a transcription factor. Mol Microbiol 24:1–6 [View Article][PubMed]
    [Google Scholar]
  22. Mizushima T., Tomura A., Shinpuku T., Miki T., Sekimizu K. ( 1994). Loss of flagellation in dnaA mutants of Escherichia coli . J Bacteriol 176:5544–5546[PubMed]
    [Google Scholar]
  23. Prentki P., Krisch H. M. ( 1984). In vitro insertional mutagenesis with a selectable DNA fragment. Gene 29:303–313 [View Article][PubMed]
    [Google Scholar]
  24. Rocha E. P., Danchin A., Viari A. ( 1999). Universal replication biases in bacteria. Mol Microbiol 32:11–16 [View Article][PubMed]
    [Google Scholar]
  25. Sakr S., Jeanjean R., Zhang C.-C., Arcondeguy T. ( 2006a). Inhibition of cell division suppresses heterocyst development in Anabaena sp. strain PCC 7120. J Bacteriol 188:1396–1404 [View Article][PubMed]
    [Google Scholar]
  26. Sakr S., Thyssen M., Denis M., Zhang C.-C. ( 2006b). Relationship among several key cell cycle events in the developmental cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 188:5958–5965 [View Article][PubMed]
    [Google Scholar]
  27. Sambrook J., Fritsch E. F., Maniatis T. ( 1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  28. Schaper S., Messer W. ( 1995). Interaction of the initiator protein DnaA of Escherichia coli with its DNA target. J Biol Chem 270:17622–17626 [View Article][PubMed]
    [Google Scholar]
  29. Schmitt M. E., Brown T. A., Trumpower B. L. ( 1990). A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae . Nucleic Acids Res 18:3091–3092 [View Article][PubMed]
    [Google Scholar]
  30. Smulczyk-Krawczyszyn A., Jakimowicz D., Ruban-Osmialowska B., Zawilak-Pawlik A., Majka J., Chater K., Zakrzewska-Czerwinska J. ( 2006). Cluster of DnaA boxes involved in regulation of Streptomyces chromosome replication: from in silico to in vivo studies. J Bacteriol 188:6184–6194 [View Article][PubMed]
    [Google Scholar]
  31. Southern E. M. ( 1975). Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98:503–517 [View Article][PubMed]
    [Google Scholar]
  32. Theisen P. W., Grimwade J. E., Leonard A. C., Bogan J. A., Helmstetter C. E. ( 1993). Correlation of gene transcription with the time of initiation of chromosome replication in Escherichia coli . Mol Microbiol 10:575–584 [View Article][PubMed]
    [Google Scholar]
  33. Tong Y., Shi D. J., Ran L., Zhang P. P., Deng Y. G., Song D. H., Zhao X. G., Zhang Y. N. ( 2006). An improved method for the plasmid DNA isolation from cyanobacteria. Plant Physio Commu 42–2:281–284
    [Google Scholar]
  34. Veening J. W., Murray H., Errington J. ( 2009). A mechanism for cell cycle regulation of sporulation initiation in Bacillus subtilis . Genes Dev 23:1959–1970 [View Article][PubMed]
    [Google Scholar]
  35. Vioque A. ( 1997). The RNase P RNA from cyanobacteria: short tandemly repeated repetitive (STRR) sequences are present within the RNase P RNA gene in heterocyst-forming cyanobacteria. Nucleic Acids Res 25:3471–3477 [View Article][PubMed]
    [Google Scholar]
  36. Wolk C. P., Ernst A., Elhai J. ( 1994). Heterocyst metabolism and development. The Molecular Biology of Cyanobacteria769–823 Bryant D. A. Dordrecht: Kluwer Academic Publishers;
    [Google Scholar]
  37. Young-Robbins S. S., Risser D. D., Moran J. R., Haselkorn R., Callahan S. M. ( 2010). Transcriptional regulation of the heterocyst patterning gene patA from Anabaena sp. strain PCC 7120. J Bacteriol 192:4732–4740 [View Article][PubMed]
    [Google Scholar]
  38. Zhang C.-C. ( 1993). A gene encoding a protein related to eukaryotic protein kinases from the filamentous heterocystous cyanobacterium Anabaena PCC 7120. Proc Natl Acad Sci U S A 90:11840–11844 [View Article][PubMed]
    [Google Scholar]
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