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Molybdenum limitation of asymbiotic nitrogen fixation in tropical forest soils

Abstract

Nitrogen fixation, the biological conversion of di-nitrogen to plant-available ammonium, is the primary natural input of nitrogen to ecosystems1, and influences plant growth and carbon exchange at local to global scales2,3,4,5,6. The role of this process in tropical forests is of particular concern, as these ecosystems harbour abundant nitrogen-fixing organisms1,4 and represent one third of terrestrial primary production4,7,8. Here we show that the micronutrient molybdenum, a cofactor in the nitrogen-fixing enzyme nitrogenase, limits nitrogen fixation by free-living heterotrophic bacteria in soils of lowland Panamanian forests. We measured the fixation response to long-term nutrient manipulations in intact forests, and to short-term manipulations in soil microcosms. Nitrogen fixation increased sharply in treatments of molybdenum alone, in micronutrient treatments that included molybdenum by design and in treatments with commercial phosphorus fertilizer, in which molybdenum was a ‘hidden’ contaminant. Fixation did not respond to additions of phosphorus that were not contaminated by molybdenum. Our findings show that molybdenum alone can limit asymbiotic nitrogen fixation in tropical forests and raise new questions about the role of molybdenum and phosphorus in the tropical nitrogen cycle. We suggest that molybdenum limitation may be common in highly weathered acidic soils, and may constrain the ability of some forests to acquire new nitrogen in response to CO2 fertilization9.

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Figure 1: Nitrogenase acetylene reduction activity (ARA) in response to long-term nutrient fertilization and direct additions of molybdenum and phosphorus.
Figure 2: Relative nitrogenase acetylene reduction activity (ARA) in soil samples as a function of soil Mo enrichment, across all nutrient manipulations.

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Acknowledgements

We thank D. Menge, D. Sigman and F. Morel for helpful comments, and M. Ketterer for Mo analyses. L. Stanley, A. Strong, L. Bennett, B. Kennedy and H. Waters assisted in the field and laboratory. This work was supported by an NSF-GRF, EPA STAR and STRI-PDF to A.R.B., grants from the A.W. Mellon Foundation and the NSF to L.O.H., a grant from the NSF (DEB-0614116) to L.O.H, A.M.L.K. and A.R.B, a grant from the NSF-funded Center for Environmental BioInorganic Chemistry (CHE-0221978) to A.M.L.K. and J.P.B., and the Smithsonian Scholarly Studies programme and the A. W. Mellon Foundation to S.J.W.

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Correspondence to Lars O. Hedin.

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Barron, A., Wurzburger, N., Bellenger, J. et al. Molybdenum limitation of asymbiotic nitrogen fixation in tropical forest soils. Nature Geosci 2, 42–45 (2009). https://doi.org/10.1038/ngeo366

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