Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1996 Apr;178(7):2037–2043. doi: 10.1128/jb.178.7.2037-2043.1996

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.

E L Campbell 1, K D Hagen 1, M F Cohen 1, M L Summers 1, J C Meeks 1
PMCID: PMC177902  PMID: 8606181

Abstract

Strain UCD 311 is a transposon-induced mutant of Nostoc sp. strain ATC C 29133 that is unable to fix nitrogen in air but does so under anoxic conditions and is able to establish a functional symbiotic association with the hornwort Anthoceros punctatus. These properties of strain UCD 311 are consistent with previous observations that protection against oxygen inactivation of nitrogenase is physiologically provided within A. punctatus tissue. Upon deprivation of combined nitrogen, strain UCD 311 clearly differentiates heterocysts and contains typical heterocyst-specific glycolipids; it also makes apparently normal akinetes upon phosphate starvation. Sequence analysis adjacent to the point of the transposon insertion revealed an open reading frame designated devR. Southern analysis established that similar sequences are present in other heterocyst-forming cyanobacteria. devR putatively encodes a protein of 135 amino acids with high similarity to the receiver domains of response regulator proteins characteristics of two-component regulatory systems. On the basis of its size and the absence of other functional domains, DevR is most similar to CheY and Spo0F. Reconstruction of the mutation with an interposon vector confirmed that the transposition event was responsible for the mutant phenotype. The presence of wild-type devR on a plasmid in strain UCD 311 restored the ability to fix nitrogen in air. While devR was not essential for differentiation of akinetes, its presence in trans in Nostoc sp. strain ATCC 29133 stimulated their formation to above normal levels in aging medium. On the basis of RNA analysis, devR is constitutively expressed with respect to the nitrogen source for growth. The devR gene product is essential to the development of mature heterocysts and may be involved in a sensory pathway that is not directly responsive to cellular nitrogen status.

Full Text

The Full Text of this article is available as a PDF (455.4 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adams D. G., Carr N. G. The developmental biology of heterocyst and akinete formation in cyanobacteria. Crit Rev Microbiol. 1981;9(1):45–100. doi: 10.3109/10408418109104486. [DOI] [PubMed] [Google Scholar]
  2. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  3. Brahamsha B., Haselkorn R. Identification of multiple RNA polymerase sigma factor homologs in the cyanobacterium Anabaena sp. strain PCC 7120: cloning, expression, and inactivation of the sigB and sigC genes. J Bacteriol. 1992 Nov;174(22):7273–7282. doi: 10.1128/jb.174.22.7273-7282.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Buikema W. J., Haselkorn R. Characterization of a gene controlling heterocyst differentiation in the cyanobacterium Anabaena 7120. Genes Dev. 1991 Feb;5(2):321–330. doi: 10.1101/gad.5.2.321. [DOI] [PubMed] [Google Scholar]
  5. Cai Y. P., Wolk C. P. Use of a conditionally lethal gene in Anabaena sp. strain PCC 7120 to select for double recombinants and to entrap insertion sequences. J Bacteriol. 1990 Jun;172(6):3138–3145. doi: 10.1128/jb.172.6.3138-3145.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Campbell E. L., Meeks J. C. Characteristics of Hormogonia Formation by Symbiotic Nostoc spp. in Response to the Presence of Anthoceros punctatus or Its Extracellular Products. Appl Environ Microbiol. 1989 Jan;55(1):125–131. doi: 10.1128/aem.55.1.125-131.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cohen M. F., Wallis J. G., Campbell E. L., Meeks J. C. Transposon mutagenesis of Nostoc sp. strain ATCC 29133, a filamentous cyanobacterium with multiple cellular differentiation alternatives. Microbiology. 1994 Dec;140(Pt 12):3233–3240. doi: 10.1099/13500872-140-12-3233. [DOI] [PubMed] [Google Scholar]
  8. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Elhai J., Wolk C. P. Developmental regulation and spatial pattern of expression of the structural genes for nitrogenase in the cyanobacterium Anabaena. EMBO J. 1990 Oct;9(10):3379–3388. doi: 10.1002/j.1460-2075.1990.tb07539.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ernst A., Black T., Cai Y., Panoff J. M., Tiwari D. N., Wolk C. P. Synthesis of nitrogenase in mutants of the cyanobacterium Anabaena sp. strain PCC 7120 affected in heterocyst development or metabolism. J Bacteriol. 1992 Oct;174(19):6025–6032. doi: 10.1128/jb.174.19.6025-6032.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Frías J. E., Flores E., Herrero A. 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. 1994 Nov;14(4):823–832. doi: 10.1111/j.1365-2958.1994.tb01318.x. [DOI] [PubMed] [Google Scholar]
  12. Grossman A. D. Integration of developmental signals and the initiation of sporulation in B. subtilis. Cell. 1991 Apr 5;65(1):5–8. doi: 10.1016/0092-8674(91)90353-z. [DOI] [PubMed] [Google Scholar]
  13. Ireton K., Rudner D. Z., Siranosian K. J., Grossman A. D. Integration of multiple developmental signals in Bacillus subtilis through the Spo0A transcription factor. Genes Dev. 1993 Feb;7(2):283–294. doi: 10.1101/gad.7.2.283. [DOI] [PubMed] [Google Scholar]
  14. Joseph C. M., Meeks J. C. Regulation of expression of glutamine synthetase in a symbiotic Nostoc strain associated with Anthoceros punctatus. J Bacteriol. 1987 Jun;169(6):2471–2475. doi: 10.1128/jb.169.6.2471-2475.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Leganés F., Fernández-Piñas F., Wolk C. P. Two mutations that block heterocyst differentiation have different effects on akinete differentiation in Nostoc ellipsosporum. Mol Microbiol. 1994 May;12(4):679–684. doi: 10.1111/j.1365-2958.1994.tb01055.x. [DOI] [PubMed] [Google Scholar]
  16. Liang J., Scappino L., Haselkorn R. 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 U S A. 1992 Jun 15;89(12):5655–5659. doi: 10.1073/pnas.89.12.5655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Maldener I., Fiedler G., Ernst A., Fernández-Piñas F., Wolk C. P. Characterization of devA, a gene required for the maturation of proheterocysts in the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol. 1994 Dec;176(24):7543–7549. doi: 10.1128/jb.176.24.7543-7549.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mann N. H. Protein phosphorylation in cyanobacteria. Microbiology. 1994 Dec;140(Pt 12):3207–3215. doi: 10.1099/13500872-140-12-3207. [DOI] [PubMed] [Google Scholar]
  19. Nagaya M., Aiba H., Mizuno T. The sphR product, a two-component system response regulator protein, regulates phosphate assimilation in Synechococcus sp. strain PCC 7942 by binding to two sites upstream from the phoA promoter. J Bacteriol. 1994 Apr;176(8):2210–2215. doi: 10.1128/jb.176.8.2210-2215.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Parkinson J. S., Kofoid E. C. Communication modules in bacterial signaling proteins. Annu Rev Genet. 1992;26:71–112. doi: 10.1146/annurev.ge.26.120192.000443. [DOI] [PubMed] [Google Scholar]
  21. Parkinson J. S., Parker S. R., Talbert P. B., Houts S. E. Interactions between chemotaxis genes and flagellar genes in Escherichia coli. J Bacteriol. 1983 Jul;155(1):265–274. doi: 10.1128/jb.155.1.265-274.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Steinberg N. A., Meeks J. C. Physiological sources of reductant for nitrogen fixation activity in Nostoc sp. strain UCD 7801 in symbiotic association with Anthoceros punctatus. J Bacteriol. 1991 Nov;173(22):7324–7329. doi: 10.1128/jb.173.22.7324-7329.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Summers M. L., Wallis J. G., Campbell E. L., Meeks J. C. 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. 1995 Nov;177(21):6184–6194. doi: 10.1128/jb.177.21.6184-6194.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Thiel T., Lyons E. M., Erker J. C., Ernst A. A second nitrogenase in vegetative cells of a heterocyst-forming cyanobacterium. Proc Natl Acad Sci U S A. 1995 Sep 26;92(20):9358–9362. doi: 10.1073/pnas.92.20.9358. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Wei T. F., Ramasubramanian T. S., Golden J. W. Anabaena sp. strain PCC 7120 ntcA gene required for growth on nitrate and heterocyst development. J Bacteriol. 1994 Aug;176(15):4473–4482. doi: 10.1128/jb.176.15.4473-4482.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Wilcox M., Mitchison G. J., Smith R. J. Pattern formation in the blue-green alga, Anabaena. I. Basic mechanisms. J Cell Sci. 1973 May;12(3):707–723. doi: 10.1242/jcs.12.3.707. [DOI] [PubMed] [Google Scholar]
  27. Wolk C. P., Cai Y., Panoff J. M. Use of a transposon with luciferase as a reporter to identify environmentally responsive genes in a cyanobacterium. Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5355–5359. doi: 10.1073/pnas.88.12.5355. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES