1887

Abstract

sp. strain PCC 7120 is a filamentous cyanobacterium in which certain vegetative cells differentiate into heterocysts, which are specialized cells for nitrogen fixation. Heterocysts are unable to carry out photosynthesis and are supplied with carbohydrate required for nitrogen fixation from neighbouring vegetative cells. Thus, filament integrity is very important for diazotrophic growth of the heterocystous cyanobacteria. The gene (), encoding a putative Ser/Thr protein kinase, was upregulated in heterocysts after nitrogen deprivation. Its expression was developmentally regulated by the gene. Expression levels of genes involved in heterocyst maturation, such as , and , in the disruptant were similar to those of the wild-type strain. The disruptant was able to form heterocysts with nitrogenase activity, but most heterocysts were detached from filaments. Hence, the disruptant showed a growth defect in the medium without combined nitrogen. It is concluded that the gene is not involved in the development of heterocyst function but is involved in maintaining connections between heterocysts and vegetative cells.

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2012-06-01
2024-03-28
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References

  1. 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]
  2. 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]
  3. 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]
  4. Campbell E. L., Cohen M. F., Meeks J. C. ( 1997). A polyketide-synthase-like gene is involved in the synthesis of heterocyst glycolipids in Nostoc punctiforme strain ATCC 29133. Arch Microbiol 167:251–258 [View Article][PubMed]
    [Google Scholar]
  5. Cormack B. P., Valdivia R. H., Falkow S. ( 1996). FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173:1 Spec No33–38 [View Article][PubMed]
    [Google Scholar]
  6. Ehira S., Ohmori M. ( 2006a). NrrA, a nitrogen-responsive response regulator facilitates heterocyst development in the cyanobacterium Anabaena sp. strain PCC 7120. Mol Microbiol 59:1692–1703 [View Article][PubMed]
    [Google Scholar]
  7. Ehira S., Ohmori M. ( 2006b). NrrA directly regulates expression of hetR during heterocyst differentiation in the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 188:8520–8525 [View Article][PubMed]
    [Google Scholar]
  8. Ehira S., Ohmori M. ( 2011). NrrA, a nitrogen-regulated response regulator protein, controls glycogen catabolism in the nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120. J Biol Chem 286:38109–38114 [View Article][PubMed]
    [Google Scholar]
  9. Ehira S., Ohmori M., Sato N. ( 2003). Genome-wide expression analysis of the responses to nitrogen deprivation in the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120. DNA Res 10:97–113 [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. Espinosa J., Brunner T., Fiedler N., Forchhammer K., Muro-Pastor A. M., Maldener I. ( 2010). DevT (Alr4674), resembling a Ser/Thr protein phosphatase, is essential for heterocyst function in the cyanobacterium Anabaena sp. PCC 7120. Microbiology 156:3544–3555 [View Article][PubMed]
    [Google Scholar]
  12. Fan Q., Lechno-Yossef S., Ehira S., Kaneko T., Ohmori M., Sato N., Tabata S., Wolk C. P. ( 2006). Signal transduction genes required for heterocyst maturation in Anabaena sp. strain PCC 7120. J Bacteriol 188:6688–6693 [View Article][PubMed]
    [Google Scholar]
  13. Flores E., Herrero A. ( 2010). Compartmentalized function through cell differentiation in filamentous cyanobacteria. Nat Rev Microbiol 8:39–50 [View Article][PubMed]
    [Google Scholar]
  14. Flores E., Pernil R., Muro-Pastor A. M., Mariscal V., Maldener I., Lechno-Yossef S., Fan Q., Wolk C. P., Herrero A. ( 2007). Septum-localized protein required for filament integrity and diazotrophy in the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 189:3884–3890 [View Article][PubMed]
    [Google Scholar]
  15. Golden J. W., Wiest D. R. ( 1988). Genome rearrangement and nitrogen fixation in Anabaena blocked by inactivation of xisA gene. Science 242:1421–1423 [View Article][PubMed]
    [Google Scholar]
  16. Hanks S. K., Hunter T. ( 1995). Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J 9:576–596[PubMed]
    [Google Scholar]
  17. Herrero A., Muro-Pastor A. M., Valladares A., Flores E. ( 2004). Cellular differentiation and the NtcA transcription factor in filamentous cyanobacteria. FEMS Microbiol Rev 28:469–487 [View Article][PubMed]
    [Google Scholar]
  18. Higa K. C., Callahan S. M. ( 2010). Ectopic expression of hetP can partially bypass the need for hetR in heterocyst differentiation by Anabaena sp. strain PCC 7120. Mol Microbiol 77:562–574 [View Article][PubMed]
    [Google Scholar]
  19. Hirokawa T., Boon-Chieng S., Mitaku S. ( 1998). SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 14:378–379 [View Article][PubMed]
    [Google Scholar]
  20. Holland D., Wolk C. P. ( 1990). Identification and characterization of hetA, a gene that acts early in the process of morphological differentiation of heterocysts. J Bacteriol 172:3131–3137[PubMed]
    [Google Scholar]
  21. Huang X., Dong Y., Zhao J. ( 2004). HetR homodimer is a DNA-binding protein required for heterocyst differentiation, and the DNA-binding activity is inhibited by PatS. Proc Natl Acad Sci U S A 101:4848–4853 [View Article][PubMed]
    [Google Scholar]
  22. Jang J., Wang L., Jeanjean R., Zhang C. C. ( 2007). PrpJ, a PP2C-type protein phosphatase located on the plasma membrane, is involved in heterocyst maturation in the cyanobacterium Anabaena sp. PCC 7120. Mol Microbiol 64:347–358 [View Article][PubMed]
    [Google Scholar]
  23. Kamei A., Yuasa T., Geng X., Ikeuchi M. ( 2002). Biochemical examination of the potential eukaryotic-type protein kinase genes in the complete genome of the unicellular cyanobacterium Synechocystis sp. PCC 6803. DNA Res 9:71–78 [View Article][PubMed]
    [Google Scholar]
  24. Kumar K., Mella-Herrera R. A., Golden J. W. ( 2010). Cyanobacterial heterocysts. Cold Spring Harb Perspect Biol 2:a000315 [View Article][PubMed]
    [Google Scholar]
  25. Laurent S., Chen H., Bédu S., Ziarelli F., Peng L., Zhang C. C. ( 2005). Nonmetabolizable analogue of 2-oxoglutarate elicits heterocyst differentiation under repressive conditions in Anabaena sp. PCC 7120. Proc Natl Acad Sci U S A 102:9907–9912 [View Article][PubMed]
    [Google Scholar]
  26. Mariscal V., Herrero A., Nenninger A., Mullineaux C. W., Flores E. ( 2011). Functional dissection of the three-domain SepJ protein joining the cells in cyanobacterial trichomes. Mol Microbiol 79:1077–1088 [View Article][PubMed]
    [Google Scholar]
  27. Merino-Puerto V., Mariscal V., Mullineaux C. W., Herrero A., Flores E. ( 2010). Fra proteins influencing filament integrity, diazotrophy and localization of septal protein SepJ in the heterocyst-forming cyanobacterium Anabaena sp.. Mol Microbiol 75:1159–1170 [View Article][PubMed]
    [Google Scholar]
  28. Merino-Puerto V., Schwarz H., Maldener I., Mariscal V., Mullineaux C. W., Herrero A., Flores E. ( 2011). FraC/FraD-dependent intercellular molecular exchange in the filaments of a heterocyst-forming cyanobacterium, Anabaena sp.. Mol Microbiol 82:87–98 [View Article][PubMed]
    [Google Scholar]
  29. Muro-Pastor A. M., Olmedo-Verd E., Flores E. ( 2006). All4312, an NtcA-regulated two-component response regulator in Anabaena sp. strain PCC 7120. FEMS Microbiol Lett 256:171–177 [View Article][PubMed]
    [Google Scholar]
  30. Nakao M., Okamoto S., Kohara M., Fujishiro T., Fujisawa T., Sato S., Tabata S., Kaneko T., Nakamura Y. ( 2010). CyanoBase: the cyanobacteria genome database update 2010. Nucleic Acids Res 38:Database issueD379–D381 [View Article][PubMed]
    [Google Scholar]
  31. Nayar A. S., Yamaura H., Rajagopalan R., Risser D. D., Callahan S. M. ( 2007). FraG is necessary for filament integrity and heterocyst maturation in the cyanobacterium Anabaena sp. strain PCC 7120. Microbiology 153:601–607 [View Article][PubMed]
    [Google Scholar]
  32. Ohmori M., Ikeuchi M., Sato N., Wolk P., Kaneko T., Ogawa T., Kanehisa M., Goto S., Kawashima S. et al. ( 2001). Characterization of genes encoding multi-domain proteins in the genome of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120. DNA Res 8:271–284 [View Article][PubMed]
    [Google Scholar]
  33. Pinto F. L., Thapper A., Sontheim W., Lindblad P. ( 2009). Analysis of current and alternative phenol based RNA extraction methodologies for cyanobacteria. BMC Mol Biol 10:79 [View Article][PubMed]
    [Google Scholar]
  34. Saha S. K., Golden J. W. ( 2011). Overexpression of pknE blocks heterocyst development in Anabaena sp. strain PCC 7120. J Bacteriol 193:2619–2629 [View Article][PubMed]
    [Google Scholar]
  35. Shi L., Li J. H., Cheng Y., Wang L., Chen W. L., Zhang C. C. ( 2007). Two genes encoding protein kinases of the HstK family are involved in synthesis of the minor heterocyst-specific glycolipid in the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 189:5075–5081 [View Article][PubMed]
    [Google Scholar]
  36. Walsby A. E. ( 2007). Cyanobacterial heterocysts: terminal pores proposed as sites of gas exchange. Trends Microbiol 15:340–349 [View Article][PubMed]
    [Google Scholar]
  37. Wang L., Sun Y. P., Chen W. L., Li J. H., Zhang C. C. ( 2002). Genomic analysis of protein kinases, protein phosphatases and two-component regulatory systems of the cyanobacterium Anabaena sp. strain PCC 7120. FEMS Microbiol Lett 217:155–165 [View Article][PubMed]
    [Google Scholar]
  38. Wolk C. P., Ernst A., Elhai J. ( 1994). Heterocyst metabolism and development. The Molecular Biology of Cyanobacteria769–823 Bryant D. A. Dordrecht, The Netherlands: Kluwer Academic Publishers;
    [Google Scholar]
  39. Yoon H. S., Golden J. W. ( 1998). Heterocyst pattern formation controlled by a diffusible peptide. Science 282:935–938 [View Article][PubMed]
    [Google Scholar]
  40. Zhang C. C., Friry A., Peng L. ( 1998). Molecular and genetic analysis of two closely linked genes that encode, respectively, a protein phosphatase 1/2A/2B homolog and a protein kinase homolog in the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 180:2616–2622[PubMed]
    [Google Scholar]
  41. Zhang X., Zhao F., Guan X., Yang Y., Liang C., Qin S. ( 2007). Genome-wide survey of putative serine/threonine protein kinases in cyanobacteria. BMC Genomics 8:395 [View Article][PubMed]
    [Google Scholar]
  42. Zhao M. X., Jiang Y. L., He Y. X., Chen Y. F., Teng Y. B., Chen Y., Zhang C. C., Zhou C. Z. ( 2010). Structural basis for the allosteric control of the global transcription factor NtcA by the nitrogen starvation signal 2-oxoglutarate. Proc Natl Acad Sci U S A 107:12487–12492 [View Article][PubMed]
    [Google Scholar]
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