Abstract
Among nitrogen-fixing microorganisms, nitrogen-fixing cyanobacteria are unique in their ability to carry out oxygen-evolving photosynthesis and oxygen-labile nitrogen fixation within the same organisms1–3. These seemingly incompatible reactions take place in heterocystous cyanobacteria by the spatial separation of the site of nitrogen fixation (heterocysts) from the site of photosynthesis (vegetative cells)4,5. Several hypotheses have been proposed to explain these mechanisms in non-heterocystous cyanobacteria3,6–11. Using batch cultures of Gloeothece (Gloeocapsa) spp., Gallon and collaborators demonstrated the mechanism of temporal separation of photosynthesis and nitrogen fixation into the light and dark periods of growth, respectively9. However, the mechanisms by which these two incompatible reactions can occur under continuous light conditions still remained ambiguous. Using novel strains of aerobic nitrogen-fixing, unicellular marine cyanobacteria, Synechococcus spp., grown under synchronized conditions, we report here that nitrogen fixation and photosynthesis occur at different phases in the cell division cycle. Our data, obtained under both diurnal light/dark cycle and continuous illumination, indicate that the temporal separation of the two phases during the cell division cycle is the mechanism by which these unicells can grow photoautotrophically under nitrogen-fixing conditions.
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References
Stanier, R. Y. & Cohen-Bazire, G. A. Rev. Microbiol. 31, 225–274 (1977).
Stewart, W. D. P. A. Rev. Microbiol. 34, 497–536 (1980).
Gallon, J. R. Trends biochem. Sci. 6, 19–23 (1981).
Haselkorn, R. A. Rev. Plant Physiol. 29, 319–344 (1978).
Fay, P. in Recent Advances in Biological Nitrogen Fixation (ed. Subba Rao, N. S.) 121–165 (Arnold, London, 1980).
Fay, P., Kumar, H. D. & Fogg, G. E. J. gen. Microbiol. 35, 351–360 (1964).
Gallon, J. R., LaRue, T. A. & Kurz, W. G. W. Can. J. Microbiol. 20, 1633–1637 (1974).
Weare, N. M. & Benemann, J. R. J. Bact. 119, 258–265 (1974).
Mullineaux, P. M., Gallon, J. R. & Chaplin, A. E. FEMS Microbiol. Lett. 10, 245–247 (1981).
Kallas, T. et al. in Photosynthetic Prokaryotes: Cell Differentiation and Function (eds Papageorgiou, G. C. & Packer, L.) 281–302 (Elsevier, New York, 1983).
Stal, L. J. & Krumbein, W. E. Archs Microbiol. 143, 67–71 (1985).
Mitsui, A. in Proc. 5th Int. Ocean Dev. Conf. 1(B1), 29–52 (Seino, Tokyo, 1978).
Mitsui, A. et al. Ann. N. Y. Acad. Sci. 413, 514–530 (1983).
Mitsui, A. et al. in Biotechnology and Bioprocess Engineering (ed. Ghose, T. K.) 119–155 (United India, New Delhi, 1985).
Gallon, J. R. & Hamadi, A. F. J. gen. Microbiol. 130, 495–503 (1984).
Sandmann, G. & Malkin, R. Archs biochem. Biophys. 234, 105–111 (1984).
Smith, A. J. in The Biology of Cyanobacteria (eds Carr, N. G. & Whitton, B. A.) 47–85 (University of California Press, Berkeley, 1982).
Mitsui, A., Takahasi, A., Ikemoto, H., Cao, S. & Arai, T. 5th Int. Symp. Photosynth. Prokaryotes, Abstr. 63 (Grindelwald, Switzerland, 1985).
Mullineaux, P. M., Chaplin, A. E. & Gallon, J. R. J. gen Microbiol. 120, 227–232 (1980).
Kumazawa, S. & Mitsui, A. Int. J. Hydrogen Energy 6, 339–348 (1981).
Ernst, A. & Böger, P. J. gen. Microbiol. 131, 3147–3153 (1985).
Chaplin, A. E. & Gallon, J. R. 5th Int. Symp. Photosynth. Prokaryotes Abstr. 253 (Grindelwald, Switzerland, 1985).
Stal, L. J. & Krumbein, W. E. Archs Microbiol. 143, 72–76 (1985).
León, C., Kumazawa, S. & Mitsui, A. Curr. Microbiol. 13, 149–153 (1986).
Kumazawa, S. & Mitsui, A. Appl. environ. Microbiol. 50, 287–291 (1985).
Dubois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. A. & Smith, F. Analyt. Chem. 28, 350–356 (1956).
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Mitsui, A., Kumazawa, S., Takahashi, A. et al. Strategy by which nitrogen-fixing unicellular cyanobacteria grow photoautotrophically. Nature 323, 720–722 (1986). https://doi.org/10.1038/323720a0
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DOI: https://doi.org/10.1038/323720a0
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