Physiological Adaptations in Nitrogen-fixing Nostoc–Plant Symbiotic Associations

Abstract

Abstract Nostoc species establish nitrogen-fixing symbiotic associations with representa- tives of the four main lineages of terrestrial plants: bryophyte hornworts and liverworts, the pteridophyte fern Azolla, gymnosperm cycads, and the angiosperm genus Gunnera. However, the plant partners represent only narrowly selected groups within these lin- eages. The plant partner benefits by the acquisition of fixed nitrogen, but the benefits to the Nostoc partner are unclear. Thus, the associations are considered a commensal form of symbiosis. A working hypothesis of this chapter is that these associations evolved as the lineage of the plant partner emerged. Inherent in this hypothesis is that the plant partners may have evolved different regulatory signals and targets in control of the Nos- toc partner. The physiological interactions between the two partners can be modeled as a two-step process. First is the establishment of an association and involves the differenti- ation and behavior of motile hormogonium filaments, the infective units. Hormogonium formation is essential, but not singularly sufficient for establishment of an association. Second is the development of a functional nitrogen-fixing association involving the dif- ferentiation and behavior of heterocysts, the functional units. Heterocysts are the cellular sites of nitrogen fixation, protecting nitrogenase from inactivation by oxygen. The sym- biotic growth state of Nostoc spp. is characterized by a reduced rate of growth, depressed carbon dioxide and ammonium assimilation, transition to a heterotrophic metabolic182 J.C. Meeks mode, an elevated heterocyst frequency, and an enhanced rate of nitrogen fixation. In all but one association (cycads), dinitrogen-derived ammonium is made available to the plant partner. Physiological measurements indicate that different reactions of Nostoc pho- tosynthetic carbon dioxide and ammonium assimilation are modulated by the various plant partners. These results appear to support the working hypothesis and indicate that different mechanisms may be operational, allowing for manipulation of