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Arable soil nitrogen dynamics reflect organic inputs via the extended composite phenotype

Nature Food volume 4, pages 51–60 (2023)Cite this article

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Abstract

Achieving food security requires resilient agricultural systems with improved nutrient-use efficiency, optimized water and nutrient storage in soils, and reduced gaseous emissions. Success relies on understanding coupled nitrogen and carbon metabolism in soils, their associated influences on soil structure and the processes controlling nitrogen transformations at scales relevant to microbial activity. Here we show that the influence of organic matter on arable soil nitrogen transformations can be decoded by integrating metagenomic data with soil structural parameters. Our approach provides a mechanistic explanation of why organic matter is effective in reducing nitrous oxide losses while supporting system resilience. The relationship between organic carbon, soil-connected porosity and flow rates at scales relevant to microbes suggests that important increases in nutrient-use efficiency could be achieved at lower organic carbon stocks than currently envisaged.

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Fig. 1: SOC and soil Ntot stock dynamics in Broadbalk soils.
Fig. 2: Contrasting long-term soil management results in quantitatively different process-form states.
Fig. 3: Nitrogen metabolism-associated gene assemblages in triplicate pseudo-replicate soil metagenomes from FYM-amended, inorganically fertilized (144NPK, 192NK and PK) arable soils of the Broadbalk Winter Wheat Experiment and unmanaged (woodland and grassland) soils, determined from shotgun metagenomics.
Fig. 4: Kernel density estimation of the distribution of N2O emissions from FYM-amended (n = 25) and inorganically fertilized (240NPK, n = 30; 144NPK, n = 24; 192NK, n = 25; and PK, n = 23) soils of the Broadbalk Winter Wheat Experiment measured between April and November 2019.
Fig. 5: Long term non-equilibrium nitrogen use efficiency of FYM-amended and inorganically fertilized soils.

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Data availability

Data relating to the Broadbalk and Highfield long-term experiments can be accessed via the electronic Rothamsted Archive (http://www.era.rothamsted.ac.uk/experiment/rbk1 and http://www.era.rothamsted.ac.uk/experiment/rrn1, respectively). Historical data relating to nitrogen inputs (as ammonium nitrate fertilizer or FYM, within seed grain and atmospheric deposition), off-takes (as harvested grain and straw) and soil nitrogen stocks are available at https://doi.org/10.23637/rbk1-yldS10115-01. All soil images are available upon reasonable request from the corresponding author. Sequence data associated with this research have been deposited in the European Nucleotide Archive with the accession number PRJEB43407. X-ray computed tomography was performed at the Hounsfield Facility of the University of Nottingham where the resulting images are stored. Due to the large number and size of the files, original greyscale and converted binary images are available upon reasonable request from Sacha Mooney, University of Nottingham (sacha.mooney@nottingham.ac.uk). Source data are provided with this paper.

Code availability

C++code for lattice Boltzmann simulation of the dissolution and diffusion of oxygen in 3D soil structures under different soil water contents is available at https://doi.org/10.6084/m9.figshare.21493704.

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Acknowledgements

This research was supported by UK Research and Innovation’s (UKRI) Biotechnology and Biological Science Research Council (BBSRC)-funded Soil to Nutrition strategic programme (BBS/E/C/000I0310 for A.L.N., X.Z., D.H., I.M.C. and J.W.C., and BBS/E/C/000I0320 for T.T. and L.M.C.). The Broadbalk Wheat Experiment is part of the Rothamsted Long-term Experiments National Capability supported by BBSRC (BBS/E/C/000J0300 for M.L.G.) and the Lawes Agricultural Trust. H.A.B. was supported by funding from the Soils Training and Research Studentships programme provided by UKRI’s BBSRC and Natural Environment Research Council. L.-J.G. and R.K. were supported by the Hartree National Centre for Digital Innovation, a collaboration between UKRI’s Science and Technology Facilities Council and IBM Research Europe.

Author information

Author notes

  1. Harry A. Barrat

    Present address: The Carbon Trust, London, UK

  2. Aurélie Bacq-Lebreuil

    Present address: Genesis, Lisors, France

Authors and Affiliations

  1. Net Zero and Resilient Farming, Rothamsted Research, North Wyke, UK

    Andrew L. Neal, Harry A. Barrat, Taro Takahashi & Laura M. Cárdenas

  2. School of Biosciences, The University of Nottingham, Sutton Bonington, UK

    Aurélie Bacq-Lebreuil, Karl Ritz & Sacha J. Mooney

  3. Department of Environmental Sciences, Wageningen University, Wageningen, The Netherlands

    Yuwei Qin

  4. Sustainable Soils and Crops, Rothamsted Research, Harpenden, UK

    Xiaoxian Zhang & Ian M. Clark

  5. Bristol Veterinary School, University of Bristol, Langford, UK

    Taro Takahashi

  6. Programa de Producción y Sustentabilidad Ambiental, Instituto Nacional de Investigación Agropecuaria (INIA), Estación Experimental INIA La Estanzuela, Colonia, Uruguay

    Valentina Rubio

  7. School of Integrative Plant Science, Cornell University, Ithaca, NY, USA

    Valentina Rubio

  8. Intelligent Data Ecosystems, Rothamsted Research, Harpenden, UK

    David Hughes & Margaret L. Glendining

  9. IBM Research Europe - Daresbury, The Hartree Centre, Warrington, UK

    Laura-Jayne Gardiner & Ritesh Krishna

  10. Adam Smith Business School, University of Glasgow, Glasgow, UK

    John W. Crawford

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Contributions

A.L.N., conceptualization, methodology, software, formal analysis, writing—original draft, writing—review and editing, visualization, funding acquisition; H.A.B., formal analysis, investigation; A.B.-L., formal analysis, investigation; Y.Q., investigation; X.Z., conceptualization, investigation, software, writing—review and editing; T.T., conceptualization, methodology, formal analysis, investigation; V.R., formal analysis, investigation; D.H., software, data curation; I.M.C., software, investigation, data curation; L.M.C., resources, writing—review and editing, supervision; L.-J.G., software, formal analysis, data curation; R.K., software, formal analysis, data curation; M.L.G., data curation, writing—review and editing; K.R., conceptualization, writing—review and editing, supervision; S.J.M., conceptualization, writing—review and editing, resources, supervision; J.W.C., conceptualization, writing—review and editing, funding acquisition.

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Correspondence to Andrew L. Neal.

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Nature Food thanks Shuli Niu and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Methods and Results, and Figs. 1–3.

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Source data

Source Data Fig. 1

Statistical source data for soil organic carbon and total nitrogen stocks between 1881 and 2015 for soils of the Broadbalk Winter Wheat Experiment and unmanaged grassland. This is also the source data for Supplementary Fig. 1.

Source Data Fig. 2

Statistical source data for: (A) soil organic carbon and total nitrogen stocks between 1843 and 2015 for soils of the Broadbalk Winter Wheat Experiment and unmanaged grassland; (B) observed connected porosity, simulated hydraulic conductivity and soil organic carbon (SOC) stocks of soils of the Broadbalk Winter Wheat Experiment and unmanaged grassland; (C) simulated proportion of anoxic pore space at different soil matric potentials based on lattice Boltzmann simulation of the pore network behaviour observed in soils of the Broadbalk Winter Wheat Experiment and unmanaged grassland.

Source Data Fig. 4

Raw statistical source data for soil nitrous oxide emissions from soils of the Broadbalk Winter Wheat Experiment collected using in situ static chambers between 11 April and 7 October 2019. This is also the source data for Supplementary Fig. 2.

Source Data Fig. 5

Statistical source data for nitrogen inputs to soil and off-takes in wheat grain and straw and total annual rainfall for soils of the Broadbalk Winter Wheat Experiment from 1966 to 2015. This is also the source data for Supplementary Fig 3.

Source Data Table 2

Statistical source data for measured soil total porosity and connected porosity derived from X-ray computed tomography, and simulated permeability, relative diffusion coefficient and hydraulic conductivity for soils of the Broadbalk Winter Wheat Experiment and unmanaged grassland.

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Neal, A.L., Barrat, H.A., Bacq-Lebreuil, A. et al. Arable soil nitrogen dynamics reflect organic inputs via the extended composite phenotype. Nat Food 4, 51–60 (2023). https://doi.org/10.1038/s43016-022-00671-z

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