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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
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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

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