Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-09T07:22:05.210Z Has data issue: false hasContentIssue false

Solar-powered N2 fixation in ferns: the Azolla-Anabaena symbioses

Published online by Cambridge University Press:  05 December 2011

G. A. Peters
Affiliation:
Charles F. Kettering Research Laboratory, Yellow Springs, Ohio 45387, U.S.A.
D. Kaplan
Affiliation:
Charles F. Kettering Research Laboratory, Yellow Springs, Ohio 45387, U.S.A.
H. E. Calvert
Affiliation:
Charles F. Kettering Research Laboratory, Yellow Springs, Ohio 45387, U.S.A.
Get access

Synopsis

The heterosporous aquatic ferns in the genus Azolla contain a heterocystous cyanobacterium, Anabaena azollae, as a symbiont. The Anabaena occupies cavities formed in the aerial dorsal leaf lobes of the ferns and can provide the symbiotic associations with their total N requirement via the fixation of atmospheric nitrogen. The photosynthetic pigments of the fern and cyanobacterium are complementary. Photosynthesis is of course the source of energy for growth and the ultimate source of the ATP and reductant required for N2 fixation in the light or dark. However, nitrogen fixation is maximal in the light and the phycobili-proteins of the Anabaena are as effective as its chlorophyll in driving this photosystem I-linked process.

The partners exhibit a coordinated pattern of development with the Azolla exerting a control over the Anabaena, affecting both its metabolism and differentiation. Anabaena filaments associated with the fern apices lack heterocysts. As cavities are formed and occupied by the Anabaena, it differentiates a high proportion of heterocysts and exhibits nitrogenase activity. In mature cavities, the Anabaena receives fixed carbon from the Azolla and releases fixed N2 as ammonium. The ammonium is assimilated and/or transported by the Azolla toward its stem apices. Special epidermal cavity trichomes, which are intimately associated with the Anabaena at all stages in the ontogeny of the association, may facilitate metabolite exchange between the fern and cyanobacterium.

Type
Research Article
Copyright
Copyright © Royal Society of Edinburgh 1985

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ashton, P. J. 1974. The effect of some environmental factors on the growth of Azolla filiculoides Lam. In The Orange River, Progress Report, ed. V. Zinderren Bakker, E. M. Sr, pp. 123138. Bloemfontein, Orange Free State: Institute for Environmental Sciences.Google Scholar
Ashton, P. J. Walmsley, R. D. 1976. The aquatic fern Azolla and its Anabaena symbiont. Endeavour 19, 3943.Google Scholar
Calvert, H. E., Perkins, S. K. and Peters, G. A. 1983. Sporocarp structure in the heterosporous water fern Azolla mexicana Presl. Scanning Electron Microscopy 3, 14991510.Google Scholar
Calvert, H. E. and Peters, G. A. 1981. The Azolla-Anabaena relationship. IX. Morphological analysis of leaf cavity hair population. New Phytol. 89, 327335.CrossRefGoogle Scholar
Campbell, D. H. 1893. On the development of Azolla filiculoides Lam. Ann. Bot. 7, 155187.Google Scholar
Dao, T. T. and Tran, T. Q. 1979. Use of Azolla in rice production in Vietnam. In Nitrogen and Rice, pp. 395405. Los Banos, Laguna, Philippines: International Rice Research Institute.Google Scholar
Eady, F. 1974. The aquatic weed problem. I. Identification. N.Z. Jl Agric. 128, 4045.Google Scholar
Haselkorn, R., Mazur, B., Orr, J., Rice, D., Wood, N. and Rippka, R. 1980. Heterocyst differentiation and nitrogen fixation in cyanobacteria (blue-green algae). In Nitrogen Fixation, ed. Newton, W. E. and Orme-Johnson, W. H., Vol. 1, pp. 259278. Baltimore: University Park Press.Google Scholar
Hill, D. J. 1975. The pattern of development of Anabaena in the Azolla-Anabaena symbiosis. Planta 222, 179184.Google Scholar
Hill, D. J. 1977. The role of Anabaena in the Azolla-Anabaena symbiosis. New Phytol. 78, 611616.CrossRefGoogle Scholar
Kaplan, D., Calvert, H. E. and Peters, G. A. 1982. Phycobiliprotein in the Azolla endophyte as a function of leaf age and cell type. Pl. Physiol. 69, S156.Google Scholar
Kaplan, D. and Peters, G. A. 1981. The Azolla-Anabaena relationship. X. 15N2 fixation and transport in main stem axes. New Phytol. 89, 337346.Google Scholar
Konar, R. N. and Kapoor, R. K. 1974. Embryology of Azolla pinnata. Phytomorphology 24, 228261.Google Scholar
Ladha, J. K. and Watanabe, I. 1982. Antigenic similarity among Anabaena azollae separted from different species of Azolla. Biochem. Biophys. Res. Commun. 109, 675682.CrossRefGoogle Scholar
Liu, C. C. 1979. Use of Azolla in rice production in China. In Nitrogen and Rice, pp. 375394. Los Banos, Laguna, Philippines: International Rice Research Institute.Google Scholar
Lumpkin, T. A. and Plucknett, D. L. 1980. Azolla: Botany, physiology and use as a green manure. Econ. Bot. 34, 111153.Google Scholar
Moore, A. W. 1969. Azolla: Biology and agronomic significance. Bot. Rev. 35, 1734.Google Scholar
Orr, J. and Haselkorn, R. 1982. Regulation of glutamine synthetase activity and synthesis in free-living and symbiotic Anabaena spp. J. Bact. 152, 626635.CrossRefGoogle ScholarPubMed
Peters, G. A. 1975. The Azolla-Anabaena azollae relationship. III. Studies on metabolic capabilities and a further characterization of the symbiont. Arch. Microbiol. 103, 113122.Google Scholar
Peters, G. A. 1976. Studies on the Azolla-Anabaena symbiosis. In Proceedings of the 1st International Symposium on Nitrogen Fixation, ed. Newton, W. E. and Nyman, C. J., pp. 592610. Pullman, Washington: Washington State University Press.Google Scholar
Peters, G. A. 1977. The Azolla-Anabaena azollae symbiosis. In Genetic Engineering for Nitrogen Fixation, ed. Hollaender, A. et al. , pp. 231258. New York: Plenum.Google Scholar
Peters, G. A. Calvert, H. E. 1983. The Azolla-Anabaena symbiosis. In Algal Symbioses: A Continuum of Interaction Strategies, ed. Goff, L., pp. 109145. New York: Cambridge University Press.Google Scholar
Peters, G. A. Calvert, H. E. Kaplan, D., Ito, O. and Toia, R. E. Jr 1982. The Azolla-Anabaena symbiosis: Morphology, physiology and use. Israel J. Bot. 31, 305323.Google Scholar
Peters, G. A. Evans, W. R. Toia, R. E. Jr 1976. Azolla-Anabaena relationship. IV. Photosynthetically driven, nitrogenase-catalyzed H2 production. Pl. Physiol., Lancaster 58, 119126.CrossRefGoogle Scholar
Peters, G. A. Ito, O., Tyagi, V. V. S. and Kaplan, D. 1981. Physiological studies on N2-fixing Azolla. In Genetic Engineering of Symbiotic Nitrogen Fixation and Conservation of Fixed Nitrogen, ed. Lyons, J. M. et al. , pp. 343362. New York: Plenum.Google Scholar
Peters, G. A. Kaplan, D. 1981. Soluble carbohydrate pool in the Azolla-Anabaena symbiosis. Pl. Physiol., Lancaster 67, S37.Google Scholar
Peters, G. A. Mayne, B. C. 1974a. The Azolla, Anabaena azollae relationship. I. Initial characterization of the association. Pl. Physiol., Lancaster 53, 813819.Google Scholar
Peters, G. A. Mayne, B. C. 1974b. The Azolla, Anabaena azollae relationship. II. Localization of nitrogenase activity as assayed by acetylene reduction. Pl. Physiol., Lancaster 53, 820824.Google Scholar
Peters, G. A. Mayne, B. C. Ray, T. B. and Toia, R. E. Jr 1979. Physiology and biochemistry of the Azolla-Anabaena symbiosis. In Nitrogen and Rice, pp. 325344. Los Banos, Laguna, Philippines: International Rice Research Institute.Google Scholar
Peters, G. A. Toia, R. E. Jr, Evans, W. R., Crist, D. K., Mayne, B. C. and Poole, R. E. 1980a. Characterization and comparisons of five N2-fixing Azolla-Anabaena associations. I. Optimization of growth conditions for biomass increase and N content in a controlled environment. Pl. Cell Envir. 3, 261269.Google Scholar
Peters, G. A. Ray, T. B., Mayne, B. C. and Toia, R. E. Jr 1980b. Azolla-Anabaena association: Morphological and physiological studies. In Nitrogen Fixation, ed. Newton, W. E. and Orme-Johnson, W. H., Vol. 2, pp. 293309. Baltimore: University Park Press.Google Scholar
Peters, G. A. Toia, R. E. Jr and Lough, S. M. 1977. Azolla-Anabaena azollae relationship. V. 15N2 fixation, acetylene reduction and H2 production. Pl. Physiol., Lancaster 59, 10211025.Google Scholar
Peters, G. A. Toia, R. E. Jr Raveed, D. and Levine, N. J. 1978. The Azolla-Anabaena azollae relationship. VI. Morphological aspects of the association. New Phytol. 80, 583593.CrossRefGoogle Scholar
Ray, T. B., Mayne, B. C., Toia, R. E. Jr and Peters, G. A. 1979. Azolla-Anabaena relationship. VIII. Photosynthetic characterization of the association and individual partners. Pl. Physiol., Lancaster 64, 791795.CrossRefGoogle ScholarPubMed
Ray, T. B., Peters, G. A., Toia, R. E. Jr and Mayne, B. C. 1978. Azolla-Anabaena relationship. VII. Distribution of ammonia-assimilating enzymes, protein, and chlorophyll between host and symbiont. Pl. Physiol., Lancaster 62, 463467.CrossRefGoogle ScholarPubMed
Shi, D. J., Li, J. G., Zhong, Z. P., Wang, F. Z., Zhu, L. P. and Peters, G. A. 1981. Sudies on nitrogen fixation and photosynthesis in Azolla imbricata (Roxb.) and Azolla filiculoides Lam. Acta Bot. Sinica 23, 306315 (In Chinese).Google Scholar
Svenson, H. K. 1944. The new world species of Azolla. Am. Fern J. 34, 6984.CrossRefGoogle Scholar
Tyagi, V. V. S., Mayne, B. C. and Peters, G. A. 1980. Purification and initial characterization of phycobiliproteins from the endophytic cyanobacterium of Azolla. Arch. Microbiol. 128, 4144.Google Scholar
Tyagi, V. V. S., Ray, T. B., Mayne, B. C. and Peters, G. A. 1981. The Azolla-Anabaena relationship. XI. Phycobiliproteins in the action spectrum for nitrogenase-catalyzed acetylene reduction. Pl. Physiol., Lancaster 68, 14791484.Google Scholar