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Diversity of nitrogen fixation strategies in Mediterranean legumes

Abstract

Symbiotic N2 fixation (SNF) brings nitrogen into ecosystems, fuelling much of the world's agriculture1 and sustaining carbon storage2,3. However, it can also cause nitrogen saturation, exacerbating eutrophication and greenhouse warming47. The balance of these effects depends on the degree to which N2-fixing plants adjust how much N2 they fix based on their needs (their SNF ‘strategies’)5,6. Genetic, biochemical and physiological details of SNF are well known for certain economically important species8,9, but the diversity of N2-fixing plants10 and bacteria11 is enormous, and little is known about most N2-fixing symbioses in natural ecosystems12. Here, we show that co-occurring, closely related herbs exhibit diverse SNF strategies. In response to a nitrogen supply gradient, four species fixed less N2 than they needed (over-regulation), two fixed what they needed (facultative) and two did not downregulate SNF (obligate). No species downregulated but fixed more N2 than it needed (under-regulation or incomplete downregulation), but some species under-regulated or incompletely downregulated structural allocation to SNF. In fact, most species maintained nodules (the root structures that house symbionts) when they did not fix N2, suggesting decoupling of SNF activity and structure. Simulations showed that over-regulation of SNF activity is more adaptive than under-regulation or incomplete downregulation, and that different strategies have wildly different effects on ecosystem-level nitrogen cycling.

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Figure 1: Experimental set-up to detect symbiotic N2 fixation (SNF) strategies.
Figure 2: N2 fixation responses to nitrogen addition for Medicago polymorpha and Trifolium willdenovii.
Figure 3: Simulated community and ecosystem consequences of five N2 fixation strategies.

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Acknowledgements

J. Rosene-Mirvis, J. Eastling, A. Martinez, A. Marquez, M. Rosenfield, D. Hardwick and S. Buchholz helped with greenhouse work, and G. Maltais-Landry, K. Epps and N. Lincoln helped with growing medium analysis. S. Perakis, S. Batterman and P. Vitousek commented on the manuscript. P. Vitousek also provided advice and support throughout the project. Funding for the project came from the Carbon Mitigation Initiative, with funding from BP and Ford, as well as Stanford University, Columbia University and Chapman University.

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D.N.L.M., A.A.W. and J.L.F. designed the study, performed experiments and gathered data. D.N.L.M. developed and ran models, analysed data and was primary writer. A.A.W. and J.L.F. contributed to writing.

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Correspondence to Duncan N. L. Menge.

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Menge, D., Wolf, A. & Funk, J. Diversity of nitrogen fixation strategies in Mediterranean legumes. Nature Plants 1, 15064 (2015). https://doi.org/10.1038/nplants.2015.64

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