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Stoichiometric control of organic carbon–nitrate relationships from soils to the sea

Abstract

The production of artificial fertilizers, fossil fuel use and leguminous agriculture worldwide has increased the amount of reactive nitrogen in the natural environment by an order of magnitude since the Industrial Revolution1. This reorganization of the nitrogen cycle has led to an increase in food production2, but increasingly causes a number of environmental problems1,3. One such problem is the accumulation of nitrate in both freshwater and coastal marine ecosystems. Here we establish that ecosystem nitrate accrual exhibits consistent and negative nonlinear correlations with organic carbon availability along a hydrologic continuum from soils, through freshwater systems and coastal margins, to the open ocean. The trend also prevails in ecosystems subject to substantial human alteration. Across this diversity of environments, we find evidence that resource stoichiometry (organic carbon:nitrate) strongly influences nitrate accumulation by regulating a suite of microbial processes that couple dissolved organic carbon and nitrate cycling. With the help of a meta-analysis we show that heterotrophic microbes maintain low nitrate concentrations when organic carbon:nitrate ratios match the stoichiometric demands of microbial anabolism. When resource ratios drop below the minimum carbon:nitrogen ratio of microbial biomass4, however, the onset of carbon limitation appears to drive rapid nitrate accrual, which may then be further enhanced by nitrification. At low organic carbon:nitrate ratios, denitrification appears to constrain the extent of nitrate accretion, once organic carbon and nitrate availability approach the 1:1 stoichiometry5 of this catabolic process. Collectively, these microbial processes express themselves on local to global scales by restricting the threshold ratios underlying nitrate accrual to a constrained stoichiometric window. Our findings indicate that ecological stoichiometry can help explain the fate of nitrate across disparate environments and in the face of human disturbance.

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Figure 1: NO3- concentration as a function of DOC or POC concentration among Earth’s major ecosystems.
Figure 2: Resource stoichiometry controls on microbial NO3- processing.

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Acknowledgements

We thank N. Fierer, D. McKnight, J. Neff, W. Wieder and P. Vitousek for their contributions to the ideas and text reflected here, and R. Cory and R. Jaffe for unpublished data. We also thank all the organizations, institutions, collaborative projects and scientists that provided unpublished data via online repositories, without which this analysis would be impossible. We are particularly grateful for the contributions made by scientists affiliated with the US LTER network and the JGOFS/BCO-DMO; see a detailed list of data sets, associated Principal Investigators and access information in the Supplementary Information Notes.

Author Contributions P.G.T. conceived the project, gathered the requisite data, and performed statistical analyses. P.G.T and A.R.T. developed the conceptual model, interpreted the empirical findings, and wrote the manuscript.

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Correspondence to Philip G. Taylor.

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This file contains Supplementary Figures S1-S6 with legends, a Supplementary Discussion, Supplementary Tables S1-S6 and Supplementary References and Data Lists. (PDF 3104 kb)

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Taylor, P., Townsend, A. Stoichiometric control of organic carbon–nitrate relationships from soils to the sea. Nature 464, 1178–1181 (2010). https://doi.org/10.1038/nature08985

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