Ammonia oxidation and nitrate reduction marker genes are key indicators of nitrogen losses in temperate forest catchments
Language English Country England, Great Britain Media print-electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
- MeSH
- Ammonia MeSH
- Archaea genetics MeSH
- Denitrification MeSH
- Nitrates * MeSH
- Nitrogen analysis MeSH
- Nitrites MeSH
- Forests MeSH
- Microbiota * genetics MeSH
- Nitrification MeSH
- Oxidation-Reduction MeSH
- Soil MeSH
- Soil Microbiology MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Ammonia MeSH
- Nitrates * MeSH
- Nitrogen MeSH
- Nitrites MeSH
- Soil MeSH
Chronic nitrogen inputs can alleviate N limitation and potentially impose N losses in forests, indicated by soil enrichment in 15 N over 14 N. However, the complexity of the nitrogen cycle hinders accurate quantification of N fluxes. Simultaneously, soil ecologists are striving to find meaningful indicators to characterise the "openness" of the nitrogen cycle. We integrate soil δ15 N with constrained ecosystem N losses and the functional gene potential of the soil microbiome in 14 temperate forest catchments. We show that N losses are associated with soil δ15 N and that δ15 N scales with the abundance of soil bacteria. The abundance of the archaeal amoA gene, representing the first step in nitrification (ammonia oxidation to nitrite), followed by the abundance of narG and napA genes, associated with the first step in denitrification (nitrate reduction to nitrite), explains most of the variability in soil δ15 N. These genes are more informative than the denitrification genes nirS and nirK, which are directly linked to N2 O production. Nitrite formation thus appears to be the critical step associated with N losses. Furthermore, we show that the genetic potential for ammonia oxidation and nitrate reduction is representative of forest soil 15 N enrichment and thus indicative of ecosystem N losses.
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Adair, K., Blazewicz, S.J., Hungate, B.A., Hart, S.C., Dijkstra, P. & Schwartz, E. (2013) A positive relationship between the abundance of ammonia oxidizing archaea and natural abundance δ15N of ecosystems. Soil Biology and Biochemistry, 65, 313-315.
Barnard, R., Leadley, P.W. & Hungate, B.A. (2005) Global change, nitrification, and denitrification: a review. Global Biogeochemical Cycles, 19, GB1007. https://doi.org/10.1029/2004GB002282
Blaško, R., Bach, L.H., Yarwood, S.A., Trumbore, S.E., Högberg, P. & Högberg, M.N. (2015) Shifts in soil microbial community structure, nitrogen cycling and the concomitant declining N availability in ageing primary boreal forest ecosystems. Soil Biology & Biochemistry, 91, 200-211.
Braker, G., Fesefeldt, A. & Witzel, K.-P. (1998) Development of PCR primer systems for amplification of nitrite reductase genes nirK and nirS to detect denitrifying bacteria in environmental samples. Applied and Environmental Microbiology, 64, 3769-3775.
Denk, T.R.A., Mohn, J., Decock, C., Lewicka-Szczebak, D., Harris, E., Butterbach-Bahl, K. et al. (2017) The nitrogen cycle: a review of isotope effects and isotope modeling approaches. Soil Biology and Biochemistry, 105, 121-137.
Fang, Y., Koba, K., Makabe, A., Takahashi, C., Zhu, W., Hayashi, T. et al. (2015) Microbial denitrification dominates nitrate losses from forest ecosystems. Proceedings of the National Academy of Sciences, 112, 1470-1474.
Groffman, P.M., Altabet, M.A., Bohlke, J.K., Butterbach-Bahl, K., David, M.B., Firestone, M.K. et al. (2006) Methods for measuring denitrification: diverse approaches to a difficult problem. Ecological Applications, 16, 2091-2122.
Harter, J., Krause, H.-M., Schuettler, S., Ruser, R., Fromme, M., Scholten, T. et al. (2014) Linking N2O emissions from biochar-amended soil to the structure and function of the N-cycling microbial community. The ISME Journal, 8, 660-674.
Hobbie, E.A. & Ouimette, A.P. (2009) Controls of nitrogen isotope patterns in soil profiles. Biogeochemistry, 95, 355-371.
Houlton, B.Z., Sigman, D.M. & Hedin, L.O. (2006) Isotopic evidence for large gaseous nitrogen losses from tropical rainforests. Proceedings of the National Academy of Sciences of the United States of America, 103, 8745-8750.
Lashof, D.A. & Ahuja, D.R. (1990) Relative contributions of greenhouse gas emissions to global warming. Nature, 344, 529-531.
Lehtovirta-Morley, L.E. (2018) Ammonia oxidation: ecology, physiology, biochemistry and why they must all come together. FEMS Microbiology Letters, 365, fny058. https://doi.org/10.1093/femsle/fny058
Liang, Y., Wu, C., Wei, X., Liu, Y., Chen, X., Qin, H. et al. (2021) Characterization of nirS- and nirK-containing communities and potential denitrification activity in paddy soil from eastern China. Agriculture, Ecosystems & Environment, 319, 107561.
Lindahl, B.D., Ihrmark, K., Boberg, J., Trumbore, S.E., Hogberg, P., Stenlid, J. et al. (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytologist, 173, 611-620.
Oulehle, F., Goodale, C.L., Evans, C.D., Chuman, T., Hruška, J., Krám, P. et al. (2021) Dissolved and gaseous nitrogen losses in forests controlled by soil nutrient stoichiometry. Environmental Research Letters, 16, 064025.
Prosser, J.I. & Nicol, G.W. (2012) Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends in Microbiology, 20, 523-531.
Sabo, R.D., Scanga, S.E., Lawrence, G.B., Nelson, D.M., Eshleman, K.N., Zabala, G.A. et al. (2016) Watershed-scale changes in terrestrial nitrogen cycling during a period of decreased atmospheric nitrate and sulfur deposition. Atmospheric Environment, 146, 271-279.
Stempfhuber, B., Engel, M., Fischer, D., Neskovic-Prit, G., Wubet, T., Schöning, I. et al. (2015) pH as a driver for ammonia-oxidizing archaea in forest soils. Microbial Ecology, 69, 879-883.
Tahovská, K., Choma, M., Kaštovská, E., Oulehle, F., Bárta, J., Šantrůčková, H. et al. (2020) Positive response of soil microbes to long-term nitrogen input in spruce forest: results from Gårdsjön whole-catchment N-addition experiment. Soil Biology and Biochemistry, 143, 107732.
Taylor, P.G. & Townsend, A.R. (2010) Stoichiometric control of organic carbon-nitrate relationships from soils to the sea. Nature, 464, 1178-1181.
Templer, P.H., Arthur, M.A., Lovett, G.M. & Weathers, K.C. (2007) Plant and soil natural abundance δ15N: indicators of relative rates of nitrogen cycling in temperate forest ecosystems. Oecologia, 153, 399-406.
Tzanakakis, V.A., Taylor, A.E., Bakken, L.R., Bottomley, P.J., Myrold, D.D. & Dörsch, P. (2019) Relative activity of ammonia oxidizing archaea and bacteria determine nitrification-dependent N2O emissions in Oregon forest soils. Soil Biology and Biochemistry, 139, 107612.
Yang, R., Yuan, L.-j., Wang, R., Wang, G. & Zhu, M. (2022) Role of nitrite reductase in N2O production under aerobic conditions: an index for predicting the intensity of N2O production. Biochemical Engineering Journal, 177, 108242.
