1887

Abstract

sp. strain PCC 7120 is a filamentous cyanobacterium that differentiates nitrogen-fixing heterocysts when fixed nitrogen becomes growth limiting in the medium. The gene (designated herein), located immediately upstream of the master regulator of differentiation , was identified in a genetic screen for mutants unable to grow diazotrophically. Filaments with a mutation in were unable to fix nitrogen or synthesize heterocyst-specific glycolipids, and they fragmented initially to approximately nine cells in length at 24 h after induction of heterocyst development and eventually became unicellular. The fragmentation phenotype could be duplicated in the presence of fixed nitrogen when differentiation of heterocysts was elicited by overexpression of , suggesting that a defect in differentiation, and not a lack of fixed nitrogen in the medium, was the more direct cause of fragmentation. An intact gene was necessary for differentiation of mature heterocysts, but was not required for proper pattern formation, as indicated by a normal pattern of expression of in a mutant. A transcriptional GFP reporter fusion indicated that the level of expression of was low in vegetative cells in both nitrogen-replete and nitrogen-free media, and was induced in heterocysts. appears to play a role in filament integrity and differentiation of proheterocysts into mature heterocysts.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2006/002535-0
2007-02-01
2024-12-10
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/2/601.html?itemId=/content/journal/micro/10.1099/mic.0.2006/002535-0&mimeType=html&fmt=ahah

References

  1. Bauer C. C., Buikema W. J., Black K., Haselkorn R. 1995; A short-filament mutant of Anabaena sp. strain PCC 7120 that fragments in nitrogen-deficient medium. J Bacteriol 177:1520–1526
    [Google Scholar]
  2. 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 [CrossRef]
    [Google Scholar]
  3. Borthakur P. B., Orozco C. C., Young-Robbins S. S., Haselkorn R., Callahan S. M. 2005; Inactivation of patS and hetN causes lethal levels of heterocyst differentiation in the filamentous cyanobacterium Anabaena sp. PCC 7120. Mol Microbiol 57:111–123 [CrossRef]
    [Google Scholar]
  4. Buikema W. J., Haselkorn R. 1991a; Isolation and complementation of nitrogen fixation mutants of the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 173:1879–1885
    [Google Scholar]
  5. Buikema W. J., Haselkorn R. 1991b; Characterization of a gene controlling heterocyst development in the cyanobacterium Anabaena 7120. Genes Dev 5:321–330 [CrossRef]
    [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 [CrossRef]
    [Google Scholar]
  7. 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 [CrossRef]
    [Google Scholar]
  8. Ernst A., Black T., Cai Y., Panoff J.-M., Tiwari D. N., Wolk C. P. 1992; Synthesis of nitrogenase in mutants of the cyanobacterium Anabaena sp. strain PCC 7120 affected in heterocyst development or metabolism. J Bacteriol 174:6025–6032
    [Google Scholar]
  9. Fan Q., Huang G., Lechno-Yossef S., Wolk C. P., Kaneko T., Tabata S. 2005; Clustered genes required for synthesis and deposition of envelope glycolipids in Anabaena sp. strain PCC 7120. Mol Microbiol 58:227–243 [CrossRef]
    [Google Scholar]
  10. Fellay R., Frey J., Krisch H. 1987; Interposon mutagenesis of soil and water bacteria: a family of DNA fragments designed for in vitro insertional mutagenesis of Gram-negative bacteria. Gene 52:147–154 [CrossRef]
    [Google Scholar]
  11. Golden J. W., Wiest D. R. 1988; Genome rearrangement and nitrogen fixation in Anabaena blocked by inactivation of xisA gene. Science 242:1421–1423 [CrossRef]
    [Google Scholar]
  12. 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 [CrossRef]
    [Google Scholar]
  13. Huang G., Fan Q., Lechno-Yossef S., Wojciuch E., Wolk C. P., Kaneko T., Tabata S. 2005; Clustered genes required for the synthesis of heterocyst envelope polysaccharide in Anabaena sp. strain PCC 7120. J Bacteriol 187:1114–1123 [CrossRef]
    [Google Scholar]
  14. Kaneko T., Nakamura Y., Wolk C. P., Kuritz T., Sasamoto S., Watanabe A., Iriguchi M., Ishikawa A., Kawashima K. other authors 2001; Complete genome sequence of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120. DNA Res 8:205–213 227–253
    [Google Scholar]
  15. Khudyakov I., Golden J. W. 2001; Identification and inactivation of three group 2 sigma factor genes in Anabaena sp. strain PCC 7120. J Bacteriol 183:6667–6675 [CrossRef]
    [Google Scholar]
  16. Leganés F., Blanco-Rivero A., Fernandez-Pinas F., Redondo M., Fernandez-Valiente E., Fan Q., Lechno-Yossef S., Wolk C. P. 2005; Wide variation in the cyanobacterial complement of presumptive penicillin-binding proteins. Arch Microbiol 184:234–248 [CrossRef]
    [Google Scholar]
  17. Marchler-Bauer A., Anderson J. B., DeWeese-Scott C., Fedorova N. D., Geer L. Y., He S., Hurwitz D. I., Jackson J. D., Jacobs A. R. other authors 2003; cdd: a curated Entrez database of conserved domain alignments. Nucleic Acids Res 31:383–387 [CrossRef]
    [Google Scholar]
  18. 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 [CrossRef]
    [Google Scholar]
  19. Murry M. A., Wolk C. P. 1989; Evidence that the barrier to the penetration of oxygen into heterocysts depends upon two layers of the cell envelope. Arch Microbiol 151:469–474 [CrossRef]
    [Google Scholar]
  20. Nichols B. W., Wood B. J. B. 1968; New glycolipid specific to nitrogen-fixing blue-green algae. Nature 217:767–768 [CrossRef]
    [Google Scholar]
  21. Orozco C. C., Risser D. D., Callahan S. M. 2006; Epistasis analysis of four genes from Anabaena sp. strain PCC 7120 suggests a connection between PatA and PatS in heterocyst pattern formation. J Bacteriol 188:1808–1816 [CrossRef]
    [Google Scholar]
  22. Thomas J., Meeks J. C., Wolk C. P., Shaffer P. W., Austin S. M., Chen W. S. 1977; Formation of glutamine from [13N]ammonia, [13N]dinitrogen, and [14C]glutamate by heterocysts isolated from Anabaena cylindrica . J Bacteriol 129:1545–1555
    [Google Scholar]
  23. Walsby A. E. 1985; The permeability of heterocysts to the gases nitrogen and oxygen. Proc R Soc Lond B Biol Sci 226:345–366
    [Google Scholar]
  24. Wei T.-F., Ramasubramanian R., Golden J. W. 1994; Anabaena sp. strain PCC 7120 ntcA gene required for growth on nitrate and heterocyst development. J Bacteriol 176:4473–4482
    [Google Scholar]
  25. Winkenbach F., Wolk C. P., Jost M. 1972; Lipids of membranes and of the cell envelope in heterocysts of a blue-green alga. Planta 107:69–80 [CrossRef]
    [Google Scholar]
  26. Wolk C. P. 2000; Heterocyst formation in Anabaena . In Prokaryotic Development pp 83–104 Edited by Brun Y. V., Shimkets L. J. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  27. Wolk C. P., Cai Y. P., Panoff J. M. 1991; Use of a transposon with luciferase as a reporter to identify environmentally responsive genes in a cyanobacterium. Proc Natl Acad Sci U S A 88:5355–5359 [CrossRef]
    [Google Scholar]
  28. Yoon H.-S., Golden J. W. 2001; PatS and products of nitrogen fixation control heterocyst pattern. J Bacteriol 183:2605–2613 [CrossRef]
    [Google Scholar]
  29. Zhang C.-C., Laurent S., Sakr S., Peng L., Bedu S. 2006; Heterocyst differentiation and pattern formation in cyanobacteria: a chorus of signals. Mol Microbiol 59:367–375 [CrossRef]
    [Google Scholar]
  30. Zhou R., Wei X., Jiang N., Li H., Dong Y., Hsi K.-L., Zhao J. 1998; Evidence that HetR is an unusual serine-type protease. Proc Natl Acad Sci U S A 95:4959–4963 [CrossRef]
    [Google Scholar]
/content/journal/micro/10.1099/mic.0.2006/002535-0
Loading
/content/journal/micro/10.1099/mic.0.2006/002535-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error