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Recently identified microbial guild mediates soil N2O sink capacity

Abstract

Nitrous oxide (N2O) is the predominant ozone-depleting substance and contributes approximately 6% to overall global warming1,2. Terrestrial ecosystems account for nearly 70% of total global N2O atmospheric loading, of which at least 45% can be attributed to microbial cycling of nitrogen in agriculture3. The reduction of N2O to nitrogen gas by microorganisms is critical for mitigating its emissions from terrestrial ecosystems, yet the determinants of a soil’s capacity to act as a source or sink for N2O remain uncertain4. Here, we demonstrate that the soil N2O sink capacity is mostly explained by the abundance and phylogenetic diversity of a newly described N2O-reducing microbial group5,6, which mediate the influence of edaphic factors. Analyses of interactions and niche preference similarities suggest niche differentiation or even competitive interactions between organisms with the two types of N2O reductase. We further identified several recurring communities comprised of co-occurring N2O-reducing bacterial genotypes that were significant indicators of the soil N2O sink capacity across different European soils.

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Figure 1: Range of potential soil N2O sink capacity.
Figure 2: Phylogenetic placement of nosZ pyrosequencing reads within a reference phylogeny.
Figure 3: Structural equation model showing the relative influence of soil abiotic and denitrifier community factors on the soil N2O sink capacity.
Figure 4: Network analysis of nosZ sequence groups identifying N2O-reducing communities associated with soils acting as potential N2O sinks.

References

  1. Ravishankara, A. R., Daniel, J. S. & Portmann, R. W. Nitrous oxide (N2O): The dominant ozone-depleting substance emitted in the 21st century. Science 326, 123–125 (2009).

    Article  CAS  Google Scholar 

  2. Montzka, S. A., Dlugokencky, E. J. & Butler, J. H. Non-CO2 greenhouse gases and climate change. Nature 476, 43–50 (2011).

    Article  CAS  Google Scholar 

  3. Syakila, A. & Kroeze, C. The global nitrous oxide budget revisited. Greenhouse Gas Meas. Manage. 1, 17–26 (2011).

    Article  CAS  Google Scholar 

  4. Butterbach-Bahl, K., Baggs, E. M., Dannenmann, M., Kiese, R. & Zechmeister-Boltenstern, S. Nitrous oxide emissions from soils: How well do we understand the processes and their controls? Phil. Trans. R. Soc. B. 368, 20130122 (2013).

    Article  Google Scholar 

  5. Jones, C. M., Graf, D. R. H., Bru, D., Philippot, L. & Hallin, S. The unaccounted yet abundant nitrous oxide-reducing microbial community: A potential nitrous oxide sink. ISME J. 7, 417–426 (2013).

    Article  CAS  Google Scholar 

  6. Sanford, R. A. et al. Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils. Proc. Natl Acad. Sci. USA 109, 19709–19714 (2012).

    Article  CAS  Google Scholar 

  7. Hofmann, D. J. et al. The role of carbon dioxide in climate forcing from 1979 to 2004: Introduction of the annual greenhouse gas index. Tellus B 58, 614–619 (2006).

    Article  Google Scholar 

  8. Chapuis-Lardy, L., Wrage, N., Metay, A., Chotte, J. & Bernoux, M. Soils, a sink for N2O? A review. Glob. Change Biol. 13, 1–17 (2007).

    Article  Google Scholar 

  9. Richardson, D., Felgate, H., Watmough, N., Thomson, A. & Baggs, E. Mitigating release of the potent greenhouse gas N2O from the nitrogen cycle—could enzymic regulation hold the key? Trends Biotechnol. 27, 388–397 (2009).

    Article  CAS  Google Scholar 

  10. Spiro, S. Nitrous oxide production and consumption: Regulation of gene expression by gas-sensitive transcription factors. Phil. Trans. R. Soc. B 367, 1213–1225 (2012).

    Article  CAS  Google Scholar 

  11. Jones, C. M., Stres, B., Rosenquist, M. & Hallin, S. Phylogenetic analysis of nitrite, nitric oxide, and nitrous oxide respiratory enzymes reveal a complex evolutionary history for denitrification. Mol. Biol. Evol. 25, 1955–1966 (2008).

    Article  CAS  Google Scholar 

  12. Zumft, W. & Kroneck, P. Respiratory transformation of nitrous oxide (N2O) to dinitrogen by Bacteria and Archaea. Adv. Microb. Physiol. 52, 107–227 (2007).

    Article  CAS  Google Scholar 

  13. Philippot, L., Andert, J., Jones, C. M., Bru, D. & Hallin, S. Importance of denitrifiers lacking the genes encoding the nitrous oxide reductase for N2O emissions from soil. Glob. Change Biol. 17, 1497–1504 (2011).

    Article  Google Scholar 

  14. Wood, D. et al. The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294, 2317–2323 (2001).

    Article  CAS  Google Scholar 

  15. Petersen, D. G. et al. Abundance of microbial genes associated with nitrogen cycling as indices of biogeochemical process rates across a vegetation gradient in Alaska. Environ. Microbiol. 14, 993–1008 (2012).

    Article  CAS  Google Scholar 

  16. Jones, C. M. & Hallin, S. Ecological and evolutionary factors underlying global and local assembly of denitrifier communities. ISME J. 4, 633–641 (2010).

    Article  Google Scholar 

  17. Enwall, K., Throbäck, I. N., Stenberg, M., Söderström, M. & Hallin, S. Soil resources influence spatial patterns of denitrifying communities at scales compatible with land management. Appl. Environ. Microbiol. 76, 2243–2250 (2010).

    Article  CAS  Google Scholar 

  18. Philippot, L. et al. Mapping field-scale spatial patterns of size and activity of the denitrifier community. Environ. Microbiol. 11, 1518–1526 (2009).

    Article  Google Scholar 

  19. Braker, G., Dorsch, P. & Bakken, L. R. Genetic characterization of denitrifier communities with contrasting intrinsic functional traits. FEMS Microbiol. Ecol. 79, 542–554 (2012).

    Article  CAS  Google Scholar 

  20. Philippot, L. et al. Loss in microbial diversity affects nitrogen cycling in soil. ISME J. 7, 1609–1619 (2013).

    Article  CAS  Google Scholar 

  21. Cuhel, J. & Simek, M. Proximal and distal control by pH of denitrification rate in a pasture soil. Agr. Ecosyst. Environ. 141, 230–233 (2011).

    Article  CAS  Google Scholar 

  22. Baggs, E. M., Smales, C. L. & Bateman, E. J. Changing pH shifts the microbial source as well as the magnitude of N2O emission from soil. Biol. Fert. Soils 46, 793–805 (2010).

    Article  CAS  Google Scholar 

  23. Firestone, M. K., Firestone, R. B. & Tiedje, J. M. Nitrous oxide from soil denitrification: Factors controlling its biological production. Science 208, 749–751 (1980).

    Article  CAS  Google Scholar 

  24. Penton, C. R. et al. Functional genes to assess nitrogen cycling and aromatic hydrocarbon degradation: Primers and processing matter. Front. Microbiol. 4, 279 (2013).

    Article  Google Scholar 

  25. Matsen, F. A., Kodner, R. B. & Armbrust, E. V. pplacer: Linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree. BMC Bioinformatics 11, 538 (2010).

    Article  Google Scholar 

  26. Faith, D. P. Conservation evaluation and phylogenetic diversity. Biol. Conserv. 61, 1–10 (1992).

    Article  Google Scholar 

  27. Rosseel, Y. lavaan: An R package for structural equation modeling. J. Stat. Softw. 48, 1–36 (2012).

    Article  Google Scholar 

  28. Grace, J. B. & Bollen, K. A. Representing general theoretical concepts in structural equation models: The role of composite variables. Environ. Ecol. Stat. 15, 191–213 (2007).

    Article  Google Scholar 

  29. Stone, E. A. & Ayroles, J. F. Modulated modularity clustering as an exploratory tool for functional genomic inference. PLoS Genet. 5, e1000479 (2009).

    Article  Google Scholar 

  30. Strobl, C., Boulesteix, A. L., Kneib, T. & Augustin, T. Conditional variable importance for random forests. BMC Bioinformatics 9, 307 (2008).

    Article  Google Scholar 

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Acknowledgements

We thank all of our collaborators who contributed to the soil sampling. This research was supported by the European Commission within the EcoFINDERS project (FP7-264465), the French Embassy in Dublin, the Conseil Régional de Bourgogne, Teagasc and The Swedish Research Council Formas (2009-741).

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Contributions

C.M.J., A.S., S.H. and L.P. designed the study, analysed the data and compiled the manuscript with the help of B.G. and P.L. Soil samples were collected by D.B., F.P.B., C.M.J., A.S. and L.P. with support from the EcoFINDERS project. Microcosm set-up and gas analysis was performed by M-C.B., D.B., F.P.B. and C.M.J., and soil DNA extractions, real-time PCR and 454 sequencing was performed by A.S., M-C.B. and D.B.

Corresponding authors

Correspondence to Christopher M. Jones, Ayme Spor or Sara Hallin.

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The authors declare no competing financial interests.

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Jones, C., Spor, A., Brennan, F. et al. Recently identified microbial guild mediates soil N2O sink capacity. Nature Clim Change 4, 801–805 (2014). https://doi.org/10.1038/nclimate2301

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