Adaptations of symbiotic nitrogen fixation minimize its contribution to ecosystem nitrogen cycles

Abstract

Plant symbiosis with dinitrogen-fixing bacteria is a plant trait that affects plant fitness directly. Indirectly, symbiotic N-fixation influences the ecosystem nitrogen cycle. However, little is known about the ecology of symbiotic nitrogen fixation and specifically its feedback with the addition and recycling of soil nitrogen. Our studies examined how the conditions that influence plant performance also influence its regulation of symbiotic nitrogen fixation at the level of individual plants, and how these two, in turn, determine whether new nitrogen enters the soil, or other components of the ecosystem. Our findings indicate that a diversity of nitrogen fixation strategies have been adopted by ephemeral herbaceous legumes, while perennial drought-adapted legumes, which have to survive through a dry rainless summer, always downregulated their investment in fixation when provided with external nitrogen source (facultative strategy).  We found that stress conditions (such as plant-plant competition) also invoked strong downregulation of nitrogen fixation in response to nitrogen availability in the soil. Downregulation of symbiotic nitrogen fixation was stronger in juveniles compared to mature individuals, and in woody perennials compared to herbaceous annuals. These results highlight that regulation of N-fixation is influenced both by plant N-demand and by a tradeoff between N-fixation and other carbon-demanding processes. At the level of the ecosystem nitrogen cycle we found that, contrary to expectations, there is no added nitrogen in the surrounding of our studied N-fixing shrubs. Instead, we show that fixed nitrogen is allocated to different tissues within the plant and is lost and decomposed indirectly, primarily via grazing and fruit predation. We conclude that regulation of nitrogen fixation and nitrogen conservation, are key adaptations influencing the fitness and persistence of nitrogen-fixing plants in the community, with broader consequences on existing perceptions on how N-fixation influences the ecosystem nitrogen cycle.