Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-20T03:52:12.220Z Has data issue: false hasContentIssue false
  • English
  • Français

Evolution of nitrogen-fixing symbioses

Published online by Cambridge University Press:  05 December 2011

J. I. Sprent  and
J. A. Raven
J. I. Sprent
Affiliation:
Department of Biological Sciences, University of Dundee, Dundee DD1 4HN
J. A. Raven
Affiliation:
Department of Biological Sciences, University of Dundee, Dundee DD1 4HN
Get access

Synopsis

Because of both the energy costs and the slowness of the reactions of the nitrogenase complex compared with those involving some form of combined nitrogen (oxidised or reduced), we argue that the evolution of nitrogen-fixing organisms required an environment which was very limited in combined nitrogen. This is thought to have occurred after phototrophy evolved, but before water was used as a hydrogen donor (and therefore oxygen was present in the atmosphere). After oxygenic photosynthesis evolved, the need for a high level of biological nitrogen-fixation remained, since abiotic inputs were insufficient to keep pace with the rapidly evolving biomass (flora and fauna). Symbiotic fixation probably first evolved in the form of casual associations between cyanobacteria and most other groups of plants. By inhabiting the sporophytic generation of evolving land plants (cycads in particular), protection against nitrogenase-inactivating oxygen and a more desiccating environment was achieved simultaneously.

We envisage nodulated plants arising by the transfer of nif genes into tumour-forming bacteria. In the case of legumes, these would be ancestors of extant agrobacteria, which gain entry into their hosts via wounds. Co-evolution of symbionts from nitrogen-fixing tumours has taken several routes, leading to extant nodules differing in mode of infection, structure and physiology. Evolution towards optimisation of oxygen usage is continuing.

Nitrogen-fixing symbiosis in animal systems is only advantageous in specialised ecological niches in which wood is the sole dietary intake. In the case of shipworms, the symbiosis has many of the advanced features associated with nitrogen fixing root nodules.

Type
Research Article
Information
Proceedings of the Royal Society of Edinburgh, Section B: Biological Sciences , Volume 85 , Issue 3-4: Symbiosis and Plant Nutrition , 1985 , pp. 215 - 237
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

Abelson, P. 1966. Chemical events on the primitive earth. Proc. Natn. Acad. Sci. U.S.A. 55, 1365–1372.CrossRefGoogle ScholarPubMed
Antoniw, L. D. 1976. Effect of irradiance on the growth and nitrogen fixing activity of Phaseolus vulgaris L. Ph.D. Thesis, University of Dundee.Google Scholar
Ashendorf, D. 1980. Are sulfur isotope ratios sufficient to determine the antiquity of sulfate reduction? Origins of Life 10, 325–333.CrossRefGoogle ScholarPubMed
Bada, J. C. and Miller, S. L. 1967. Ammonium ion concentration in the primitive ocean. Science, N. Y. 159, 423–425.CrossRefGoogle Scholar
Baker, D. and Miller, N. G. 1980. Ultrastructural evidence for the existence of actinorhizal symbioscs in the late pleistocene. Can. J. Bot. 58, 1612–1620.CrossRefGoogle Scholar
Bhuveneswari, T. V., Bhagwat, A. A. and Bauer, W. D. 1981. Transient susceptibility of root cells in four common legumes to nodulation by rhizobia. Pl. Physiol. 68, 1144 1149.CrossRefGoogle Scholar
Bond, G. 1983. Taxonomy and distribution of non-legume nitrogen fixing systems. In Biological Nitrogen Fixation in Forest Ecosystems: Foundations and Applications, ed. Gordon, J. C. and Wheeler, C. T., pp. 55–87. The Hague: Martinus Nihoff/Junk.CrossRefGoogle Scholar
Broda, E. 1978. The Evolution of Bioenergelic Processes (revised reprint of first edition). Oxford: Pergamon Press.Google Scholar
Broda, E. and Peschek, G. A. 1979. Did respiration or photosynthesis come first? J. Theorel. Biol. 81, 201 212.CrossRefGoogle ScholarPubMed
Broda, E. and Peschek, G. A. 1980. Evolutionary considerations of the thermodynamics of nitrogen fixation. Biosyslems 13, 47 56.CrossRefGoogle ScholarPubMed
Broda, E. and Peschek, G. A. 1983. Nitrogen fixation as evidence for the reducing nature of the early biosphere. Biosyslems 16, 1–8.CrossRefGoogle ScholarPubMed
Burgess, P. K. 1984. Structure and reactivity of nitrogenase- an overview. In Advances in Nitrogen Fixation Research, ed. Veeger, C. and Newton, W. E., pp. 103 114. The Hague: Martinus Nijhoff/Junk.CrossRefGoogle Scholar
Burgraaf, A. J. P., van der Linden, J. and Tak, T. 1983. Studies on the localization of infectible cells on Alnus glutinosa. Pl. Soil 74, 175–188.CrossRefGoogle Scholar
Callaham, D. and Torrey, J. G. 1981. The structural basis for infection of root hairs of Trifolium repens by Rhizobium. Can. J. Bot. 59, 1647–1664.CrossRefGoogle Scholar
Canuto, V. M., Levine, J. S., Augustsson, T. R. and Imhoff, C. L. 1982. U.V. radiation from the sun and oxygen and ozone levels in the prebiological atmosphere. Nature, Lond. 296, 816 820.CrossRefGoogle Scholar
Chandler, M. R. 1978. Some observations on infection of Arachis hypogea L. by Rhizobium. J. Exp. Bot. 29, 749–755.CrossRefGoogle Scholar
Chandler, M. R., Date, R. A. and Roughley, R. J. 1982. Infection and root nodule development in Styiosanthes species by Rhizobium. J. Exp. Bot. 33, 47–57.CrossRefGoogle Scholar
Corby, H. D. L., Polhill, R. M. and Sprent, J. I. 1983. Taxonomy. In Nitrogen Fixation, Vol. 3 Legumes, ed. Broughton, W. J., pp. 1–35. Oxford: University Press.Google Scholar
Cowling, E. B. and Merrill, W. 1966. Nitrogen in wood and its role in wood deterioration. Can. J. Bot. 44, 1539–1554.CrossRefGoogle Scholar
Croft, W. N. and George, E. A. 1959. Blue-green algae from the Middle Devonian of Rhynie, Aberdeenshire. Bull. Br. Mus. (Nat. Hist.) Geol. 3, 341–353.Google Scholar
De Bruijn, F. J., Sundaresan, V., Szeto, W. W., Ow, D. W. and Ausubel, F. M. 1984. Regulation of the nitrogen fixing (nif) genes of Klebsiella pneumoniae and Rhizobium meliloti: role of nitrogen regulation (ntr) genes. In Advances in Nitrogen Fixation Research, ed. Veeger, C. and Newton, W. E., pp. 627–633. The Hague: Martinus Nijhoff/Junk.CrossRefGoogle Scholar
De Cleene, M. and De Ley, J. 1976. The host range of crown gall. Bot. Rev. 42, 389–466.CrossRefGoogle Scholar
De Cleene, M. and De Ley, J. 1981. The host range of infectious hairy root. Bot. Rev. 47, 147–194.CrossRefGoogle Scholar
Delwiche, C. C. 1977. Energy relations in the global nitrogen cycle. Ambio 6, 106–111.Google Scholar
Dixon, R. O. D. 1969. Rhizobia (with particular reference to relationships with host plants). A. Rev. Microbiol. 23, 137–158.CrossRefGoogle ScholarPubMed
Dudman, W. F. 1984. The polysaccharides and oligosaccharides of Rhizobium and their role in the infection process. In Recent Advances in Nitrogen Fixation Research, ed. Veeger, C. and Newton, W. E., pp. 397–404. The Hague: Martinus Nijhoff/Junk.CrossRefGoogle Scholar
Egeraat, A. W. S. M. van 1975. The possible role of homoserine in the development of Rhizobium leguminosarum in the rhizosphere of pea seedlings. Pl. Soil 42, 381–383.CrossRefGoogle Scholar
Faria, S. M. de, Franco, A. A., Jesus, R. M. de, Menandro, M. de, S., Baitello, J. B., Mucco, E. S. F., Dobereiner, J. and Sprent, J. I. 1984. New nodulating legume trees for South East Brazil. New Phytol. 98, 317–328.CrossRefGoogle Scholar
Fekete, F. A., Spence, J. T. and Emery, T. 1983. Siderophores produced by nitrogen-fixing Azotobacter vinelandii OP in iron-limited continuous culture. Appl. Env. Microbiol. 46, 1297–1300.CrossRefGoogle ScholarPubMed
Fyson, A. and Sprent, J. I. 1980. A light and scanning electron microscope study of stem nodules in Vicia faba. J. Exp. Bot. 31, 1001–1006.CrossRefGoogle Scholar
Gebhardt, C., Turner, G. L., Gibson, A. H., Dreyfus, B. L. and Bergersen, F. J. 1984. Nitrogen fixing growth in continuous culture of a strain of Rhizobium sp. isolated from stem nodules in Sesbania roslrala. J. Gen. Microbiol. 130, 843–848.Google Scholar
Goldman, S. J., Lammers, P. J., Berman, M. S. and Sandersloehr, J. 1983. Siderophore-mediated iron uptake in different strains of Anabaena sp. J. Bad. 156, 1144–1150.Google ScholarPubMed
Gresshoff, P. M., Skotnicki, M. L. and Rolfe, B. G. 1979. Crown gall teratoma formation is plasmid and plant controlled. J. Bad. 137, 1020–1021.Google ScholarPubMed
Grove, T. S., O'Connell, A. M. and Malajczuk, N. 1980. Effects of fire on the growth, nutrient content and rate of nitrogen fixation of the cycad Macrozamia riedlii. Aust. J. Bot. 28, 271–281.CrossRefGoogle Scholar
Guerrero, M. G., Vega, J. M. and Losada, M. 1981. The assimilatory nitrate-reducing system and its regulation. A. Rev. Pl. Physiol. 32, 169–204.CrossRefGoogle Scholar
Gutschick, V. P. 1981. Energetics of microbial fixation of dinitrogen. Adv. Biochem. Eng. 21, 109–167.Google Scholar
Hahn, J. and Crutzen, P. J. 1982. The role of fixed nitrogen in atmospheric photochemistry. Phil. Trans. Roy. Soc. Lond. 296, 521–541.Google Scholar
Hallbauer, D. K., Jahns, H. M. and Beltman, H. A. 1977. Morphological and anatomical observations on some precambrian plants from the Wittwatersrand, South Africa. Geol. Rundsch. 66, 477–491.CrossRefGoogle Scholar
Hallbom, L. 1984. Sarcosine: a possible regulatory compound in the Peltigera praetexta-Nostic symbiosis. FEMS Microbiol. Lett. 22, 119–121.CrossRefGoogle Scholar
Hanus, F. J., Maier, R. J. and Evans, H. J. 1979. Autotrophic growth of H2-uptake-positive strains of Rhizobium japonicum in an atmosphere supplied with hydrogen gas. Proc. Natn. Acad. Sci. U.S.A. 76, 1788–1792.CrossRefGoogle Scholar
Harland, W. B., Holland, C. H., House, M. R., Hughes, N. F., Reynolds, A. B., Rudwick, M. J. S., Satterthwaite, G. E., Tarlo, L. S. H. and Willey, E. C. 1967. The Fossil Record: A Symposium with Documentation. London: Geological Society of London.Google Scholar
Hart, M. H. 1979. Was the pre-biotic atmosphere of the earth heavily reducing? Origins of Life 9, 261–266.CrossRefGoogle ScholarPubMed
Hellebust, J. A. 1974. Extracellular products. In Algal Physiology and Biochemistry, ed. Stewart, W. D. P., pp. 828–863. Oxford: Blackwell Scientific Publications.Google Scholar
Holt, J. G. and Krieg, N. R. (eds) 1984. Bergey's Manual of Systematic Bacteriology, (9th edn) Vol.1. London: Williams and Wilkins.Google Scholar
Hopmans, P., Chalk, P. M. and Douglas, L. A. 1983. Symbiotic N2, fixation by legumes growing in pots II. Uptake of 15N labelled NO3, C2H2 reduction and H2 evolution by Trifolium subterraneum L., Medicago truncatula Gaertn. and Acacia dealbata Link. Pl. Soil 74, 333–342.CrossRefGoogle Scholar
Jordan, C. D. 1984. The Rhizobiaceae. In Bergey's Manual of Systematic Bacteriology (9th edn), ed. Holt, J. G. and Krieg, N. R., Vol. 1, pp. 234–243. London: Williams and Wilkins.Google Scholar
Lancelle, S. A. and Torrey, J.G. 1984. Early development of Rhizobium-induced root nodule of Parasponia ribida. Infection and early nodulation. Protoplasma 123, 26–37.CrossRefGoogle Scholar
Law, R. and Lewis, D. H. 1983. Biotic environments and the maintenance of sex—some evidence from mutualistic symbioses. Biol. J. Linn. Soc. 20, 249–276.CrossRefGoogle Scholar
Ludwig, R.A. 1980. Regulation of Rhizobium nitrogen fixation by the unadenylated glutamine synthetase I system. Proc. Natn. Acad. Sci. U.S.A. 77, 5817–5821.CrossRefGoogle Scholar
Ludwig, R. A. 1984. Rhizobium free-living nitrogen fixation occurs in specialised non growing cells. Proc. Natn. Acad. Sci. U.S.A. 81, 1566–1569.CrossRefGoogle Scholar
Mague, T. H., Weare, N. H. and Holm-Hansen, O. 1974. Nitrogen fixation in the North Pacific Ocean. Mar. Biol. 24, 109–119.CrossRefGoogle Scholar
Meyen, S. V. 1984. Basic features of Gymnosperm systematics and phylogeny evidenced by the fossil record. Bot. Rev. 50, 1–111.CrossRefGoogle Scholar
Miller, S. L. and Orgel, L. E. 1974. The Origins of life on the Earth. Engelwood Cliffs, New Jersey: Prentice-Hall.Google Scholar
Moore, R. C. (ed.) 1969. Treatise on Invertebrate Palaeontology, Part N, Vol.2, Mollusca 6, Bivalva. Kansas: Geological Society of America and University of Kansas.Google Scholar
Muller, J. 1981. Fossil pollen records of extant angiosperms. Bot. Rev. 47, 1–142.CrossRefGoogle Scholar
Murry, M. A., Home, A. J. and Benemann, J. R. 1984. Physiological studies of oxygen protection mechanisms in the heterocysts of Anabaena cylindrica. Appl. Env. Microbiol. 47, 449–454.CrossRefGoogle ScholarPubMed
Neilands, J. B. 1982. Microbial envelope proteins related to iron. A. Rev. Microbiol. 36, 285–309.CrossRefGoogle ScholarPubMed
Newcomb, W. 1981. Nodule morphogenesis and differentiation. Int. Rev. Cytol. suppl. 13, 247–298.Google Scholar
Oghoghorie, C. and Pate, J. S. 1972. Exploration of the nitrogen transport system of a nodulated legume using 15N. Planta 104, 35–49.CrossRefGoogle ScholarPubMed
Pflug, H. D. 1984. Early geological record and the origin of life. Naturwissenschaften 71, 63–68.CrossRefGoogle Scholar
Polhill, R. M. and Raven, P. H. (eds) 1981. Advances in Legume Systematics, Part 1. Kew: Royal Botanic Gardens.Google Scholar
Polhill, R. M., Raven, P. H. and Stirton, C. H. 1981. In Advances in Legume Systematics, ed. Polhill, R. M. and Raven, P. H., pp. 1–26. Kew: Royal Botanic Gardens.Google Scholar
Postgate, J. R. 1974. Evolution within nitrogen fixing systems. Symp. Soc. Gen. Microbiol. 24, 265–292.Google Scholar
Postgate, J. R. 1982. The Fundamentals of Nitrogen Fixation. Cambridge: University Press.Google Scholar
Prestwich, G. D. and Bentley, B. L. 1981. Nitrogen fixation by intact colonies of the termite Nasutitermes cornigea. Oecologia 49, 249–251.CrossRefGoogle Scholar
Raven, J. A. 1976. Division of labour between chloroplasts and cytoplasm. In The Intact Chloroplast, ed. Barber, J., pp. 403–443. Amsterdam: Elsevier.Google Scholar
Raven, J. A. 1977. The evolution of vascular land plants in relation to supracellular transport processes. Adv. Bot. Res. 5, 153–219.CrossRefGoogle Scholar
Raven, J. A. 1984a. The role of membranes in pH regulation: implications for energetics and water use efficiency of higher plant growth with nitrate as nitrogen source. In Annual Proceedings of the Phytochemical Society of Europe 24, ed. Baudet, A., pp. 89–98. Oxford: University Press.Google Scholar
Raven, J. A. 1984b. Energetics and Transport in Aquatic Plants. New York: A. R. Liss.Google Scholar
Raven, J. A. and Smith, F. A. 1981. H+ transport in the evolution of photosynthesis. Biosystems 14, 95–111.CrossRefGoogle ScholarPubMed
Schidlowski, M. 1982. Content and isotopic composition of reduced carbon in sediments. In Mineral Deposits and the Evolution of the Biosphere, ed. Holland, H. D. and Schidlowski, M., pp. 103–122. Berlin: Springer.CrossRefGoogle Scholar
Schoeninger, M. J. and DeNiro, M. J. 1984. Nitrogen and carbon isotopic composition of bone collagen from marine and terrestrial animals. Geochim. Cosmochim. Ada 48, 625–639.CrossRefGoogle Scholar
Sethi, R. S. and Reporter, M. 1981. Calcium localization patterns in clover root hair cells associated with infection processes: studies with aureomycin. Protoplasma 105, 321–325.CrossRefGoogle Scholar
Sheehy, J. E., Minchin, F. R. and Witty, J. F. 1983. Biological control of the resistance to oxygen flux in nodules. Ann. Bot. 52, 565–571.CrossRefGoogle Scholar
Silvester, W. B. 1976. Endophyte adaptation in Gunnera-Nostoc symbiosis. In Symbiotic Nitrogen Fixation in Plants, ed. Nutman, P. S., pp. 521–538. Cambridge: University Press.Google Scholar
Silvester, W. B. 1977. Dinitrogen fixation by plant associations excluding legumes. In A Treatise on Dinitrogen Fixation Section IV Agronomy and Ecology, ed. Hardy, R. W. F. and Gibson, A. H., pp. 141–190. New York: Wiley Interscience.Google Scholar
Sprent, J. I. 1979. The Biology of Nitrogen Fixing Organisms. Maidenhead: McGraw Hill.Google Scholar
Sprent, J. I. 1980. Root nodule anatomy, type of export product and evolutionary origin in some Leguminosae. Pl. Cell Env. 3, 35–43.CrossRefGoogle Scholar
Sprent, J. I. 1984a. Nitrogen Fixation. In Advanced Plant Physiology, ed. Wilkins, M. B., pp. 249–276. London: Pitman.Google Scholar
Sprent, J. I. 1984b. Effects of drought and salinity on heterotrophic nitrogen fixing bacteria and on infection of legumes by rhizobia. In Advances in Nitrogen Fixation Research, ed. Veeger, C. and Newton, W. E., pp. 295–302. The Hague: Martinus Nijhoff/Junk.CrossRefGoogle Scholar
Sprent, J. I. and Thomas, R. J. 1984. Nitrogen nutrition of seedling grain legumes: some taxonomic and physiological constraints. Pl. Cell Environ. 7, 637–645.CrossRefGoogle Scholar
Stewart, W. D. P. 1980. Systems involving blue-green algae (Cyanobacteria). In Methods for evaluating Biological Nitrogen Fixation, ed. Bergerson, F. J., pp. 583–635. London: John Wiley.Google Scholar
Stewart, W. D. P. and Rodgers, G. A. 1977. The Cyanophyte-hepatic symbiosis II Nitrogen fixation and the interchange of nitrogen and carbon. New Phytol. 78, 459–471.CrossRefGoogle Scholar
Stouthamer, A. H. 1984. Energy generation and hydrogen metabolism in Rhizobium. In Advances in Nitrogen Fixation Research, ed. Veeger, C. and Newton, W. E., pp. 189–197. The Hague: Martinus Nijhoff/Junk.CrossRefGoogle Scholar
Sutherland, J. M. and Sprent, J. I. 1984. Calcium oxalate crystals and crystal cells in determinate root nodules of legumes. Planta 161, 193–200.CrossRefGoogle ScholarPubMed
Sutton, W. D. and Peterson, A. D. 1980. Effects of plant host on detergent sensitivity and viability of Rhizobium bacteroids. Planta 148, 287–292.CrossRefGoogle ScholarPubMed
Tel-Or, E. and Stewart, W. D. P. 1977. Photosynthetic components and activities of nitrogen-fixing isolated heterocysts of Anabaena cylindrica. Proc. Roy. Soc. Lond. 198B, 61–86.Google Scholar
Tjepkema, J. D. 1984. Oxygen, hemoglobins, and energy usage in actinorrhizal nodules. In Advances in Nitrogen Fixation Research, ed. Veeger, C. and Newton, W. E., pp. 467–473. The Hague: Martinus Nijhoff/Junk.CrossRefGoogle Scholar
Trinick, M. J. 1982. Biology. In Nitrogen Fixation, Vol.2 Rhizobium, ed. Broughton, W. J., pp. 76–146. Oxford: University Press.Google Scholar
Trudinger, P. A. and Williams, N. 1982. Stratified sulfide deposition in modern and ancient environments. In Mineral Deposits and the Evolution of the Biosphere, ed. Holland, M. D. and Schidlowski, M., pp. 177–198. Berlin: Springer.CrossRefGoogle Scholar
Tsien, H. C., Dreyfus, B. L. and Schmidt, E. L. 1983. Initial stages in the morphogenesis of nitrogen-fixing stem nodules of Sesbania rostrata. J. Bad. 156, 888–897.Google ScholarPubMed
Virginia, R. A. and Delwiche, C. C. 1982. Natural 15N abundance of presumes N2-fixing and non-N2-fixing plants from selected ecosystems. Oecologia 54, 317–325.CrossRefGoogle Scholar
Waterbury, J. B., Calloway, C. D. and Turner, R. D. 1983. A cellulolytic nitrogen-fixing bacterium form the gland of Deshayes in shipworms (Bivalvia: teredinidae). Science, N.Y. 221, 1401–1403.CrossRefGoogle Scholar
Williams, L. E., DeJong, T. M. and Phillips, D. A. 1981. Carbon and nitrogen limitations on soybean seedling development. Pl Physiol. 68, 1206–1209.CrossRefGoogle ScholarPubMed
Wilson, P. W. and Umbreit, W. W. 1937. Fixation and transfer of nitrogen in the soybean. Zentbl. Bakl. Parasitkde Abt. 2 96, 402–411.Google Scholar
Witty, J. F., Minchin, F. R., Sheehy, J. E. and Minguez, M. I. 1984. Acetylene-induced changes in the oxygen diffusion resistance and nitrogenase activity of legume root nodules. Ann. Bot. 53, 13–20.CrossRefGoogle Scholar
Wong, C. H., Pankhurst, C. E., Kondorosa, A. and Broughton, W. J. 1983. Morphology of root nodules and nodule-like structures formed by Rhizobium and Agrobacterium strains containing a Rhizobium meliloti megaplasmid. J. Cell Biol. 97, 787–794.CrossRefGoogle ScholarPubMed
Yun, Z. 1984. A Gunflint type of microfossil assemblage from early Proterozoic stromatolite cherts in China. Nature, Lond. 309, 547–549.CrossRefGoogle Scholar