Skip to main content
Log in

Organization of the nif genes in cyanobacteria in symbiotic association with Azolla and Anthoceros

  • Original Papers
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

The sizes of endonuclease digestion fragments of DNA from cyanobacteria in symbiotic association with Azolla caroliniana or Anthoceros punctatus, or in free-living culture, were compared by Southern hybridization using cloned nitrogenase (nif) genes from Anabaena sp. PCC 7120 as probes. The restriction fragment pattern produced by cyanobacteria isolated from A. caroliniana by culture through symbiotic association with Anthoceros differed from that of the major symbiotic cyanobacterium freshly separated from A. caroliniana. The results indicate that minor cyanobacterial symbionts occur in association with Azolla and that the dominant symbiont was not cultured in the free-living state. Both the absence of hybridization to an xisA gene probe and the mapping of restriction fragments indicated a contiguous nifHDK organization in all cells of the symbiont in association with Azolla. On the other hand, in the cultured isolate from Azolla and in Nostoc sp. 7801, the nifD and nifK genes are nominally separated by an interval of unknown length, compatible with the interruption of the nifHDK operon by a DNA element as observed in Anabaena sp. PCC 7120. In the above cultured strains, restriction fragments consistent with a contiguous nifHDK operon were also present at varying hybridization intensities, especially in Nostoc sp. 7801 grown in association with Anthoceros, presumably due to gene rearrangement in a fraction of the cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

bp:

base pairs

kb:

kilobase pairs

kd:

kilodaltons

References

  • Enderlin CS, Meeks JC (1983) Pure culture and reconstitution of the Anthoceros-Nostoc symbiotic association. Planta 158:157–165

    Google Scholar 

  • Franche C, Cohen-Bazire G (1985) The structural nif genes of four symbiotic Anabaena azollae show a highly conserved physical arrangement. Plant Sci 39:125–131

    Google Scholar 

  • Franche C, Cohen-Bazire G (1987) Evolutionary divergence in the nifK,D,H gene region among nine symbiotic Anabaena azollae and between Anabaena azollae and some free-living heterocystous cyanobacteria. Symbiosis 3:159–178

    Google Scholar 

  • Gates JE, Fisher RW, Goggin TW, Azrolan NI (1980) Antigenic differences between Anabaena azollae fresh from the Azolla fern leaf cavity and free-living cyanobacteria. Arch Microbiol 128:126–129

    Google Scholar 

  • Golden JW, Robinson SJ, Haselkorn R (1985) Rearrangement of nitrogen fixation genes during heterocyst differentiation in the cyanobacterium Anabaena. Nature 314:419–423

    Google Scholar 

  • Habte M (1986) Azolla filiculoides nitrogenase activity decrease induced by inoculation with Chlamycomonas sp. Appl Environ Microbiol 52:1123–1127

    Google Scholar 

  • Haselkorn R (1986) Organization of the genes for nitrogen fixation in photosynthetic bacteria and cyanobacteria. Annu Rev Microbiol 40:525–547

    Google Scholar 

  • Herrero A, Wolk CP (1986) Genetic mapping of the chromosome of the cyanobacterium, Anabaena variabilis. J Biol Chem 261:7748–7754

    Google Scholar 

  • Hill DJ (1975) The pattern of development of Anabaena in the Azolla-Anabaena symbiosis. Planta 122:179–184

    Google Scholar 

  • Joseph CM, Meeks JC (1987) Regulation of expression of glutamine synthetase in a symbiotic Nostoc strain associated with Anthoceros punctatus. J Bacteriol 169:2471–2475

    Google Scholar 

  • Kallas T, Coursin T, Rippka R (1985) Different organization of nif genes in nonheterocystous and heterocystous cyanobacteria. Plant Mol Biol 5:321–329

    Google Scholar 

  • Kaplan D, Peters GA (1981) The Azolla-Anabaena azollae relationship. X. 15N2 fixation and transport in main stem axes. New Phytol 89:337–346

    Google Scholar 

  • Ladha JK, Watanabe I (1982) Antigenic similarity among Anabaena azollae separated from different species of Azolla. Biochem Biophys Res Commun 109:675–682

    Google Scholar 

  • Lammers PJ, Golden JW, Haselkorn R (1986) Identification and sequence of a gene required for a developmentally regulated DNA excision in Anabaena. Cell 44:905–911

    Google Scholar 

  • Maniatis Y, Fritsch EF, Sambrook J (1982) Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York

    Google Scholar 

  • Meeks JC, Enderlin CS, Joseph CM, Chapman JS, Lollar MWL (1985a) Fixation of [13N]N2 and transfer of fixed nitrogen in the Anthoceros-Nostoc symbiotic association. Planta 164:406–414

    Google Scholar 

  • Meeks JC, Steinberg N, Joseph CM Enderlin CS, Jorgensen PA, Peters GA (1985b) Assimilation of exogenous and dinitrogenderived 13NH +4 by Anabaena azollae separated from Azolla caroliniana Willd. Arch Microbiol 142:229–233

    Google Scholar 

  • Moore AW (1969) Azolla: biology and agronomic significance. Bot Rev 35:17–34

    Google Scholar 

  • Newton JW, Herman AI (1979) Isolation of cyanobacteria from the aquatic fern, Azolla. Arch Microbiol 120:161–165

    Google Scholar 

  • Nierzwicki-Bauer SA, Haselkorn R (1986) Differences in mRNA levels in Anabaena living freely or in symbiotic association with Azolla. EMBO J 5:29–35

    Google Scholar 

  • Peters GA, Calvert HE (1983) The Azolla-Anabaena symbiosis. In: Goff LJ (ed) Algal symbiosis. University Press Cambridge, pp 109–145

    Google Scholar 

  • Peters GA, Mayne BC (1974) The Azolla-Anabaena relationship. I. Initial characterization of the association. Plant Physiol 53: 813–819

    Google Scholar 

  • Peters GA, Ray TB, Mayne BC, Toia RE Jr (1980) Azolla-Anabaena association: morphological and physiological studies. In: Newton WE, Orme-Johnson WH (eds) Nitrogen fixation, vol II. University Park Press, Baltimore, pp 293–309

    Google Scholar 

  • Rice D, Mazur BJ, Haselkorn R (1982) Isolation and physical mapping of nitrogen fixation genes from the cyanobacterium Anabaena 7120. J Biol Chem 257:13157–13163

    Google Scholar 

  • Tel-Or E, Sandovsky T (1982) The response of the nitrogen-fixing cyanobacterium Anabaena azollae to combined nitrogen compounds and sugar. Isr J Bot 31:329–336

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Meeks, J.C., Joseph, C.M. & Haselkorn, R. Organization of the nif genes in cyanobacteria in symbiotic association with Azolla and Anthoceros . Arch. Microbiol. 150, 61–71 (1988). https://doi.org/10.1007/BF00409719

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00409719

Key words

Navigation