1887

Abstract

Three mutant strains (, , ) of the cyanobacterium unable to differentiate heterocysts were characterized and examined for their ability to form a symbiotic association with the bryophyte . Previously unknown characteristics of the . mutant include differentiation of chilling-resistant akinetes, while vegetative cells of the mutant randomly lysed, yielding short filaments, following ammonium deprivation. Strains with mutations in and infected with similar frequency to that of wild-type but did not support growth of the plant partner. These results confirm that the infection of by hormogonia leading to the establishment of an association is physiologically uncoupled from the development of a functional diazotrophic association. They also indicate that heterocyst regulatory elements downstream from HetR and HetF are required in both free-living and symbiotic heterocyst differentiation and nitrogenase expression. A strain with a mutation in the global nitrogen regulator did not infect despite its ability to differentiate hormogonia at a low frequency. When complemented with one or more copies of , the mutant strain infected at a similar frequency as the wild-type and supported growth of the plant partner in the absence of combined nitrogen. These results established a connection between the presence of a functional copy of and the magnitude of hormogonium differentiation, and the behaviour of the formed hormogonia.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-148-1-315
2002-01-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/micro/148/1/1480315a.html?itemId=/content/journal/micro/10.1099/00221287-148-1-315&mimeType=html&fmt=ahah

References

  1. Adams D. G., Duggan P. S. 1999; Heterocyst and akinete differentiation in cyanobacteria. New Phytol 144:3–33 [CrossRef]
    [Google Scholar]
  2. Altschul S. F., Madden T. L., Schaffer A. A., Zhang J., Zhang Z., Milller W., Lipman D. J. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402 [CrossRef]
    [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 [CrossRef]
    [Google Scholar]
  4. 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 USA 98:2729–2734 [CrossRef]
    [Google Scholar]
  5. 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
    [Google Scholar]
  6. Campbell E. L., Meeks J. C. 1989; Characteristics of hormogonia formation by symbiotic Nostoc spp. in response to the presence of Anthoceros punctatus or its extracellular products. Appl Environ Microbiol 55:125–131
    [Google Scholar]
  7. Campbell E. L., Meeks J. C. 1992; Evidence for plant-mediated regulation of nitrogenase expression in the Anthoceros–Nostoc symbiotic association. J Gen Microbiol 138:473–480 [CrossRef]
    [Google Scholar]
  8. Campbell E. L., Hagen K. D., Cohen M. F., Summers M. L., Meeks J. C. 1996; The devR gene product is characteristic of receivers of two-component regulatory systems and is essential for heterocyst development in the filamentous cyanobacterium Nostoc sp. strain ATCC 29133. J Bacteriol 178:2037–2043
    [Google Scholar]
  9. 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 [CrossRef]
    [Google Scholar]
  10. Campbell E. L., Brahamsha B., Meeks J. C. 1998; Mutation of an alternative sigma factor in the cyanobacterium Nostoc punctiforme results in increased infection of its symbiotic plant partner, Anthoceros punctatus. . J Bacteriol 180:4938–4941
    [Google Scholar]
  11. Castenholz R. W., Waterbury J. B. 1989; Oxygenic photosynthetic bacteria (section 19), group 1. Cyanobacteria. In Bergey’s Manual of Systematic Bacteriology pp 1710–1728 Edited by Staley J. T. Bryant M. P., Pfenning N., Holt J. G. Baltimore: Williams & Wilkins;
    [Google Scholar]
  12. Cohen M. F., Meeks J. C. 1997; A hormogonium regulating locus, hrmUA , of the cyanobacterium Nostoc punctiforme strain ATCC 29133 and its response to an extract of a symbiotic plant partner Anthoceros punctatus. . Mol Plant-Microbe Interact 10:280–289 [CrossRef]
    [Google Scholar]
  13. Cohen M. F., Wallis J. G., Campbell E. L., Meeks J. C. 1994; Transposon mutagenesis of Nostoc sp. strain ATCC 29133, a filamentous cyanobacterium with multiple cellular differentiation alternatives. Microbiology 140:3233–3240 [CrossRef]
    [Google Scholar]
  14. Denison R. F. 2000; Legume sanctions and the evolution of symbiotic cooperation by rhizobia. Am Nat 156:567–576 [CrossRef]
    [Google Scholar]
  15. Elhai J., Wolk C. P. 1990; Developmental regulation and spatial pattern of expression of the structural genes for nitrogenase in the cyanobacterium Anabaena. EMBO J 9:3379–3388
    [Google Scholar]
  16. Enderlin C. S., Meeks J. C. 1983; Pure culture and reconstitution of the Anthoceros–Nostoc symbiotic association. Planta 158:157–165 [CrossRef]
    [Google Scholar]
  17. 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]
  18. Fiedler G., Muro-Pastor A., Flores E., Maldener I. 2001; NtcA-dependent expression of the devBCA operon, encoding a heterocyst-specific ATP-binding cassette transporter in Anabaena spp. J Bacteriol 183:3795–3799 [CrossRef]
    [Google Scholar]
  19. Frı́as J. E., Flores E., Herrero A. 1994; Requirement of the regulatory protein NtcA for the expression of nitrogen assimilation and heterocyst development genes in the cyanobacterium Anabaena sp. PCC 7120. Mol Microbiol 14:823–832 [CrossRef]
    [Google Scholar]
  20. Herrero A., Muro-Pastor A. M., Flores E. 2001; Nitrogen control in cyanobacteria. J Bacteriol 183:411–425 [CrossRef]
    [Google Scholar]
  21. Joseph C. M., Meeks J. C. 1987; Regulation of expression of glutamine synthetase in a symbiotic Nostoc strain associated with Anthoceros punctatus. J Bacteriol 1692471–2475
    [Google Scholar]
  22. Knight C. D., Adams D. G. 1996; A method for studying chemotaxis in nitrogen fixing cyanobacterium–plant symbiosis. Physiol Mol Plant Pathol 49:73–77 [CrossRef]
    [Google Scholar]
  23. Leganés F., Fernández-Piñas F., Wolk C. P. 1994; Two mutations that block heterocyst differentiation have different effects on akinete differentiation in Nostoc ellipsosporum. . Mol Microbiol 12:679–684 [CrossRef]
    [Google Scholar]
  24. Liang J., Scappino L., Haselkorn R. 1992; The patA gene product, which contains a region similar to CheY of Escherichia coli , controls heterocyst pattern formation in the cyanobacterium Anabaena 7120. Proc Natl Acad Sci USA 89:5655–5659 [CrossRef]
    [Google Scholar]
  25. Meeks J. C. 1998; Symbiosis between nitrogen-fixing cyanobacteria and plants. BioScience 48:266–276 [CrossRef]
    [Google Scholar]
  26. Meeks J. C., Enderlin C. S., Joseph C. M., Chapman J. S., Lollar M. W. 1985; Fixation of [13N]N2 and transfer of fixed nitrogen in the Anthoceros–Nostoc symbiotic association. Planta 164:406–414 [CrossRef]
    [Google Scholar]
  27. Oke V., Long S. R. 1999; Bacteroid formation in the Rhizobium–legume symbiosis. Curr Opin Microbiol 2:641–646 [CrossRef]
    [Google Scholar]
  28. Rippka R., Herdman M. 1992 In Pasteur Culture Collection of Cyanobacteria in Axenic Culture pp 44–57 Paris: Institut Pasteur;
    [Google Scholar]
  29. Sambrook J., Maniatis T., Fritsch E. F. 1989 Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  30. Sauer J., Forchhammer K., Görl M. 1999; Nitrogen starvation in Synechococcus PCC 7942: involvement of glutamine synthetase and NtcA in phycobiliprotein degradation and survival. Arch Microbiol 172:247–255 [CrossRef]
    [Google Scholar]
  31. Schultze M., Kondorosi A. 1998; Regulation of symbiotic root nodule development. Annu Rev Genet 32:33–57 [CrossRef]
    [Google Scholar]
  32. Steinberg N. A., Meeks J. C. 1989; Photosynthetic CO2 fixation and ribulose bisphosphate carboxylase/oxygenase activity of Nostoc sp. strain UCD 7801 in symbiotic association with Anthoceros punctatus. J Bacteriol 171:6227–6233
    [Google Scholar]
  33. Steinberg N. A., Meeks J. C. 1991; Physiological sources of reductant for nitrogen fixation activity in Nostoc sp. strain UCD 7801 in symbiotic association with Anthoceros punctatus. J Bacteriol 173:7324–7329
    [Google Scholar]
  34. Summers M. L., Wallis J. G., Campbell E. L., Meeks J. C. 1995; Genetic evidence of a major role for glucose-6-phosphate dehydrogenase in nitrogen fixation and dark growth of the cyanobacterium Nostoc sp . strain ATCC 29133. J Bacteriol 177:6184–6194
    [Google Scholar]
  35. Tandeau de Marsac N. 1994; Differentiation of hormogonia and relationships with other biological processes. In The Molecular Biology of Cyanobacteria pp 825–842 Edited by Bryant D. A. Dordrecht: Kluwer;
    [Google Scholar]
  36. Thiel T., Lyons E. M., Erker J. C., Ernst A. 1995; A second nitrogenase in vegetative cells of a heterocyst-forming cyanobacterium. Proc Natl Acad Sci USA 92:9358–9362 [CrossRef]
    [Google Scholar]
  37. Vance C. P., Miller S. S., Driscoll B. T., Robinson D. L., Trepp G., Gantt J. S., Samas D. A. 1998; Nodule carbon metabolism: organic acids for N2 fixation. In Biological Nitrogen Fixation for the 21st Century pp 443–448 Edited by Elmerich C. Kondorosi A., Newton W. E. Dordrecht: Kluwer;
    [Google Scholar]
  38. Wei T. F., Ramasubramanian T. S., Pu F., Golden J. W. 1993; Anabaena sp. strain PCC 7120 bifA gene encoding a sequence-specific DNA-binding protein cloned by in vivo transcriptional interference selection. J Bacteriol 175:4025–4035
    [Google Scholar]
  39. Wei T. F., Ramasubramanian T. S., 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]
  40. 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]
  41. Wolk C. P., Ernst A., Elhai J. 1994; Heterocyst metabolism and development. In The Molecular Biology of Cyanobacteria pp 769–823 Edited by Bryant D. A. Dordrecht: Kluwer Academic Publishers;
    [Google Scholar]
  42. Wong F. C., Meeks J. C. 2001; The hetF gene product is essential to heterocyst differentiation and affects HetR function in the cyanobacterium Nostoc punctiforme. J Bacteriol 183:2654–2661 [CrossRef]
    [Google Scholar]
  43. Zhou R., Wei X., Jiang N., Li H., Dong Y., Hsi K. L., Zhao J. 1998; Evidence that HetR protein is an unusual serine-type protease. Proc Natl Acad Sci USA 95:4959–4963 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-148-1-315
Loading
/content/journal/micro/10.1099/00221287-148-1-315
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