Abstract
Purpose
The abundance of nitrogen (N)-cycling genes is frequently used to indicate N cycling and predict N2O emissions. However, it remains difficult to clearly define how soil N-cycling genes in different ecosystems respond to anthropogenic N additions.
Methods
We applied a meta-analysis approach to examine data about N-cycling genes (nifH, ammonia-oxidizing archaea (AOA), ammonia-oxidizing bacteria (AOB), nirK, nirS, and nosZ) in different ecosystems from 119 peer-reviewed articles.
Results
In the ecosystems examined, the patterns of change in the abundances of the target genes, apart from AOA, varied considerably. This variation reflects the distinctive soil characteristics of ecosystems that develop when different forms of N are applied at different rates and over different durations. The nifH abundance decreased significantly, by 32.79%, in forests but did not change in grasslands and croplands. The AOB abundance increased in all three ecosystems, by 193.06% in grasslands, 73.26% in forests, and 151.86% in croplands, respectively. The denitrification gene abundances, namely the nirK, nirS, and nosZ, in croplands also increased significantly, by 60.74%, 47.42%, and 69.54%, respectively.
Conclusion
In general, climate factors and long-term applications of organic N at high rates had significant effects on the gene abundances in different ecosystems, through their influence on soil properties. An enhanced understanding of how N additions influence the abundance of other N-cycling functional genes can help us improve our ability to model the populations and activities of microbial functional communities and predict N fluxes.
Similar content being viewed by others
Data availability
All the data presented in this manuscript are available in the supporting information.
References
Abdalla M, Hastings A, Cheng K, Yue Q, Chadwick D, Espenberg M, Truu J, Rees RM, Smith P (2019) A critical review of the impacts of cover crops on nitrogen leaching, net greenhouse gas balance and crop productivity. Glob Change Biol 25:2530–2543. https://doi.org/10.1111/gcb.14644
Acosta-Martínez V, Mikha MM, Vigil MF (2007) Microbial communities and enzyme activities in soils under alternative crop rotations compared to wheat-fallow for the Central Great Plains. Appl Soil Ecol 37:41–52. https://doi.org/10.1016/j.apsoil.2007.03.009
Aronson E, Allison S (2012) Meta-analysis of environmental impacts on nitrous oxide release in response to N amendment. Frontiers in Microbiology 3. https://doi.org/10.3389/fmicb.2012.00272
Assémien FL, Pommier T, Gonnety JT, Gervaix J, Le Roux X (2017) Adaptation of soil nitrifiers to very low nitrogen level jeopardizes the efficiency of chemical fertilization in west african moist savannas. Sci Rep 7:10275. https://doi.org/10.1038/s41598-017-10185-5
Bai E, Li W, Li S, Sun J, Peng B, Dai W, Jiang P, Han S (2014) Pulse increase of soil N2O emission in response to N addition in a temperate forest on Mt Changbai. Northeast China Plos One 9:e102765. https://doi.org/10.1371/journal.pone.0102765
Bonan GB (2008) Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science 320:1444. https://doi.org/10.1126/science.1155121
Bowman WD, Cleveland CC, Halada Ĺ, Hreško J, Baron JS (2008) Negative impact of nitrogen deposition on soil buffering capacity. Nat Geosci 1:767–770. https://doi.org/10.1038/ngeo339
Calcagno V, de Mazancourt C (2010) glmulti: An R package for easy automated model selection with (generalized) linear models. Journal Of Statistical Software 34. https://doi.org/10.18637/jss.v034.i12.
Canfield DE, Glazer AN, Falkowski PG (2010) The evolution and future of earth’s nitrogen cycle. Science 330:192–196. https://doi.org/10.1126/science.1186120
Cannavo P, Richaume A, Lafolie F (2004) Fate of nitrogen and carbon in the vadose zone: in situ and laboratory measurements of seasonal variations in aerobic respiratory and denitrifying activities. Soil Biol Biochem 36:463–478. https://doi.org/10.1016/j.soilbio.2003.10.023
Cantarel AAM, Bloor JMG, Pommier T, Guillaumaud N, Moirot C, Soussana J-F, Poly F (2012) Four years of experimental climate change modifies the microbial drivers of N2O fluxes in an upland grassland ecosystem. Glob Change Biol 18:2520–2531. https://doi.org/10.1111/j.1365-2486.2012.02692.x
Cao Y, He Z, Zhu T, Zhao F (2021) Organic-C quality as a key driver of microbial nitrogen immobilization in soil: A meta-analysis. Geoderma 383. https://doi.org/10.1016/j.geoderma.2020.114784
Carey CJ, Dove NC, Beman JM, Hart SC, Aronson EL (2016) Meta-analysis reveals ammonia-oxidizing bacteria respond more strongly to nitrogen addition than ammonia-oxidizing archaea. Soil Biol Biochem 99:158–166. https://doi.org/10.1016/j.soilbio.2016.05.014
Cavicchioli R, Ripple WJ, Timmis KN, Azam F, Bakken LR, Baylis M, Behrenfeld MJ, Boetius A, Boyd PW, Classen AT, Crowther TW, Danovaro R, Foreman CM, Huisman J, Hutchins DA, Jansson JK, Karl DM, Koskella B, Mark Welch DB, Martiny JBH, Moran MA, Orphan VJ, Reay DS, Remais JV, Rich VI, Singh BK, Stein LY, Stewart FJ, Sullivan MB, van Oppen MJH, Weaver SC, Webb EA, Webster NS (2019) Scientists’ warning to humanity: microorganisms and climate change. Nat Rev Microbiol 17:569–586. https://doi.org/10.1038/s41579-019-0222-5
Chen Y, Feng J, Yuan X, Zhu B (2020) Effects of warming on carbon and nitrogen cycling in alpine grassland ecosystems on the Tibetan Plateau: A meta-analysis. Geoderma 370:114363. https://doi.org/10.1016/j.geoderma.2020.114363
Deng L, Huang C, Kim D-G, Shangguan Z, Wang K, Song X, Peng C (2020) Soil GHG fluxes are altered by N deposition: New data indicate lower N stimulation of the N2O flux and greater stimulation of the calculated C pools. Glob Change Biol 26:2613–2629. https://doi.org/10.1111/gcb.14970
Di HJ, Cameron KC, Shen JP, Winefield CS, O’Callaghan M, Bowatte S, He JZ (2009) Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat Geosci 2:621–624. https://doi.org/10.1038/ngeo613
Dodor DE, Ali Tabatabai M (2005) Glycosidases in soils as affected by cropping systems. J Plant Nutr Soil Sci 168:749–758. https://doi.org/10.1002/jpln.200521761
Dynarski K, Houlton B (2017) Nutrient limitation of terrestrial free-living nitrogen fixation. New Phytologist 217. https://doi.org/10.1111/nph.14905
Feng J, Zhu B (2019) A global meta-analysis of soil respiration and its components in response to phosphorus addition. Soil Biol Biochem 135:38–47. https://doi.org/10.1016/j.soilbio.2019.04.008
Fernández-Martínez M, Vicca S, Janssens IA, Sardans J, Luyssaert S, Campioli M, Chapin Iii FS, Ciais P, Malhi Y, Obersteiner M, Papale D, Piao SL, Reichstein M, Rodà F, Peñuelas J (2014) Nutrient availability as the key regulator of global forest carbon balance. Nat Clim Chang 4:471–476. https://doi.org/10.1038/nclimate2177
Friedland AJ, Miller EK (1999) Major-element cycling in a high-elevation adirondack forest: patterns and changes, 1986–1996. Ecol Appl 9:958–967. https://doi.org/10.1890/1051-0761(1999)009[0958:MECIAH]2.0.CO;2
Gaby JC, Buckley DH (2012) A comprehensive evaluation of PCR primers to amplify the nifH gene of nitrogenase. PLoS ONE 7:e42149. https://doi.org/10.1371/journal.pone.0042149
Geisseler D, Scow KM (2014) Long-term effects of mineral fertilizers on soil microorganisms - A review. Soil Biol Biochem 75:54–63. https://doi.org/10.1016/j.soilbio.2014.03.023
Zhu Y, Wang X, Yang X, Xu H, Jia Y (2014) Key microbial processes in nitrous oxide emissions of agricultural soil and mitigation strategies. Environmental Science 35: 9. https://doi.org/10.13227/j.hjkx.2014.02.008.
Hedges, Larry V, Gurevitch, Jessica (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80: 1150-1156. https://doi.org/10.1890/0012-9658(1999)080[1150:TMAORR]2.0.CO;2.
Hallin S, Jones CM, Schloter M, Philippot L (2009) Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. ISME J 3:597–605. https://doi.org/10.1038/ismej.2008.128
Henry S, Bru D, Stres B, Hallet S, Philippot L (2006) Quantitative detection of the nosZ gene, encoding nitrous oxide reductase, and comparison of the abundances of 16S rRNA, narG, nirK, and nosZ genes in soils. Appl Environ Microbiol 72:5181–5189. https://doi.org/10.1128/AEM.00231-06
Homyak PM, Allison SD, Huxman TE, Goulden ML, Treseder KK (2017) Effects of drought manipulation on soil nitrogen cycling: A meta-analysis. J Geophys Res Biogeosci 122:3260–3272. https://doi.org/10.1002/2017JG004146
Hovenden MJ, Leuzinger S, Newton PCD, Fletcher A, Fatichi S, Lüscher A, Reich PB, Andresen LC, Beier C, Blumenthal DM, Chiariello NR, Dukes JS, Kellner J, Hofmockel K, Niklaus PA, Song J, Wan S, Classen AT, Langley JA (2019) Globally consistent influences of seasonal precipitation limit grassland biomass response to elevated CO2. Nature Plants 5:167–173. https://doi.org/10.1038/s41477-018-0356-x
Hu R, Wang X, Xu J, Zhang Y, Pan Y, Su X (2020) The mechanism of soil nitrogen transformation under different biocrusts to warming and reduced precipitation: From microbial functional genes to enzyme activity. Sci Total Environ 722:137849. https://doi.org/10.1016/j.scitotenv.2020.137849
Hu H, He J (2018) Manipulating the soil microbiome for improved nitrogen management. Microbiology Australia 39. https://doi.org/10.1071/MA18007
Kallenbach C, Grandy S (2011) Controls over soil microbial biomass responses to carbon amendments in agricultural systems: A meta-analysis. Agr Ecosyst Environ 144:241–252. https://doi.org/10.1016/j.agee.2011.08.020
Klarenberg IJ, Keuschnig C, Russi Colmenares AJ, Warshan D, Jungblut AD, Jónsdóttir IS, Vilhelmsson O (2021) Long-term warming effects on the microbiome and nifH gene abundance of a common moss species in sub-Arctic tundra. New Phytologist. https://doi.org/10.1111/nph.17837
Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu Rev Microbiol 55:485–529. https://doi.org/10.1146/annurev.micro.55.1.485
Kramer SB, Reganold JP, Glover JD, Bohannan BJM, Mooney HA (2006) Reduced nitrate leaching and enhanced denitrifier activity and efficiency in organically fertilized soils. Proc Natl Acad Sci 103:4522. https://doi.org/10.1073/pnas.0600359103
Kuperman RG, Edwards CA (1997) Effects of acidic deposition on soil invertebrates and microorganisms. In: W G.W., N H.N., B A. (eds) Reviews of Environmental Contamination & Toxicology. Springer, New York.
Kuypers MMM, Marchant HK, Kartal B (2018) The microbial nitrogen-cycling network. Nat Rev Microbiol 16:263–276. https://doi.org/10.1038/nrmicro.2018.9
Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120. https://doi.org/10.1128/AEM.00335-09
Levy-Booth DJ, Prescott CE, Grayston SJ (2014) Microbial functional genes involved in nitrogen fixation, nitrification and denitrification in forest ecosystems. Soil Biol Biochem 75:11–25. https://doi.org/10.1016/j.soilbio.2014.03.021
Li Z, Zeng Z, Tian D, Wang J, Fu Z, Zhang F, Zhang R, Chen W, Luo Y, Niu S (2020) Global patterns and controlling factors of soil nitrification rate. Glob Change Biol 26:4147–4157. https://doi.org/10.1111/gcb.15119
Liu L, Greaver TL (2010) A global perspective on belowground carbon dynamics under nitrogen enrichment. Ecol Lett 13:819–828. https://doi.org/10.1111/j.1461-0248.2010.01482.x
Makowski D (2019) N2O increasing faster than expected. Nat Clim Chang 9:909–910. https://doi.org/10.1038/s41558-019-0642-2
Marinho V, Higgins J, Logan S, Sheiham A (2003) Topical fluoride (toothpastes, mouthrinses, gels, varnishes) for preventing dental caries in children and adolescents. Cochrane database of systematic reviews (Online) 4: CD002782. https://doi.org/10.1002/14651858.CD002782.
Morales SE, Cosart T, Holben WE (2010) Bacterial gene abundances as indicators of greenhouse gas emission in soils. ISME J 4:799–808. https://doi.org/10.1038/ismej.2010.8
Morley N, Baggs EM (2010) Carbon and oxygen controls on N2O and N2 production during nitrate reduction. Soil Biol Biochem 42:1864–1871. https://doi.org/10.1016/j.soilbio.2010.07.008
Nelson MB, Martiny AC, Martiny JBH (2016) Global biogeography of microbial nitrogen-cycling traits in soil. Proc Natl Acad Sci 113:8033. https://doi.org/10.1073/pnas.1601070113
Ouyang Y, Norton JM, Stark JM (2017) Ammonium availability and temperature control contributions of ammonia oxidizing bacteria and archaea to nitrification in an agricultural soil. Soil Biol Biochem 113:161–172. https://doi.org/10.1016/j.soilbio.2017.06.010
Ouyang Y, Evans SE, Friesen ML, Tiemann LK (2018) Effect of nitrogen fertilization on the abundance of nitrogen cycling genes in agricultural soils: A meta-analysis of field studies. Soil Biol Biochem 127:71–78. https://doi.org/10.1016/j.soilbio.2018.08.024
Phillips RP, Fahey TJ (2007) Fertilization effects on fineroot biomass, rhizosphere microbes and respiratory fluxes in hardwood forest soils. New Phytol 176:655–664. https://doi.org/10.1111/j.1469-8137.2007.02204.x
Prosser J, Nicol G (2012) Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol 20:523–531. https://doi.org/10.1016/j.tim.2012.08.001
Rao L, Parker D, Bytnerowicz A, Allen E (2009) Nitrogen mineralization across an atmospheric nitrogen deposition gradient in Southern California deserts. J Arid Environ 73:920–930. https://doi.org/10.1016/j.jaridenv.2009.04.007
Rosenberg M, Adams D, Gurevitch J (2000) MetaWin: Statistical software for meta-analysis. Version 2.0. Sinauer Associates.
Schmidt M, Torn M, Abiven S, Dittmar T, Guggenberger G, Janssens I, Kleber M, Kögel-Knabner I, Lehmann J, Manning D, Nannipieri P, Rasse D, Weiner S, Trumbore S (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56. https://doi.org/10.1038/nature10386
Smith RG, Gross KL, Robertson GP (2008) Effects of crop diversity on agroecosystem function: crop yield response. Ecosystems 11:355–366. https://doi.org/10.1007/s10021-008-9124-5
Song H, Che Z, Cao W, Huang T, Wang J, Dong Z (2016) Changing roles of ammonia-oxidizing bacteria and archaea in a continuously acidifying soil caused by over-fertilization with nitrogen. Environ Sci Pollut Res 23:11964–11974. https://doi.org/10.1007/s11356-016-6396-8
Srikanthasamy T, Leloup J, N’Dri AB, Barot S, Gervaix J, Koné AW, Koffi KF, Le Roux X, Raynaud X, Lata J-C (2018) Contrasting effects of grasses and trees on microbial N-cycling in an African humid savanna. Soil Biol Biochem 117:153–163. https://doi.org/10.1016/j.soilbio.2017.11.016
Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM Carbon and other biogeochemical cycles. In Climate change 2013: the physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, United Kingdom and New York, NY, USA.
Sulman BN, Phillips RP, Oishi AC, Shevliakova E, Pacala SW (2014) Microbe-driven turnover offsets mineral-mediated storage of soil carbon under elevated CO2. Nat Clim Chang 4:1099–1102. https://doi.org/10.1038/nclimate2436
Sun R, Wang F, Hu C, Liu B (2021) Metagenomics reveals taxon-specific responses of the nitrogen-cycling microbial community to long-term nitrogen fertilization. Soil Biol Biochem 156:108214. https://doi.org/10.1016/j.soilbio.2021.108214
Tang L, Zhong L, Xue K, Wang S, Xu Z, Lin Q, Luo C, Rui Y, Li X, Li M, Liu W-t, Yang Y, Zhou J, Wang Y (2019) Warming counteracts grazing effects on the functional structure of the soil microbial community in a Tibetan grassland. Soil Biol Biochem 134:113–121. https://doi.org/10.1016/j.soilbio.2019.02.018
Terrer C, Vicca S, Hungate BA, Phillips RP, Prentice IC (2016) Mycorrhizal association as a primary control of the CO2 fertilization effect. Science 353:72. https://doi.org/10.1126/science.aaf4610
Tiedje J (1988) Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In: Z A.J.B. (ed) Biology of Anaerobic Microorganisms. John Wiley & Sons, New York, USA.
Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418:671–677. https://doi.org/10.1038/nature01014
Van Breemen N, Mulder J, Driscoll CT (1983) Acidification and alkalization of soils. Plant Soil 75:283–308. https://doi.org/10.1007/BF02369968
Verma P, Sagar R (2020) Effect of nitrogen (N) deposition on soil-N processes: a holistic approach. Sci Rep 10:10470. https://doi.org/10.1038/s41598-020-67368-w
Viechtbauer W (2010) Conducting meta-analyses in R with the metafor package. J Stat Softw 36. https://doi.org/10.18637/jss.v036.i03.
Wang Q, Zhang L-M, Shen J-P, Du S, Han L-L, He J-Z (2016) Nitrogen fertiliser-induced changes in N2O emissions are attributed more to ammonia-oxidising bacteria rather than archaea as revealed using 1-octyne and acetylene inhibitors in two arable soils. Biol Fertil Soils 52:1163–1171. https://doi.org/10.1007/s00374-016-1151-3
Yang F, Zhang Z, Barberán A, Yang Y, Hu S, Guo H (2021) Nitrogen-induced acidification plays a vital role driving ecosystem functions: Insights from a 6-year nitrogen enrichment experiment in a Tibetan alpine meadow. Soil Biol Biochem 153:108107. https://doi.org/10.1016/j.soilbio.2020.108107
Zak DR, Holmes WE, White DC, Peacock AD, Tilman D (2003) Plant diversity, soil microbial communities, and ecosystem function: Are there any links? Ecology 84:2042–2050. https://doi.org/10.1890/02-0433
Zhang Q, Zhou J, Li X, Zheng Y, Xie L, Yang Z, Liu X, Xu C, Lin H, Yuan X, Liu C, Zhu B, Chen Y, Yang Y (2022) Contrasting effects of warming and N deposition on soil microbial functional genes in a subtropical forest. Geoderma 408:115588. https://doi.org/10.1016/j.geoderma.2021.115588
Zhang Y, Zhang F, Abalos D, Luo Y, Hui D, Hungate BA, García-Palacios P, Kuzyakov Y, Olesen JE, Jørgensen U, Chen J (2021) Stimulation of ammonia oxidizer and denitrifier abundances by nitrogen loading: Poor predictability for increased soil N2O emission. Global Change Biology n/a. https://doi.org/10.1111/gcb.16042
Zhao J, Ni T, Li J, Lu Q, Fang Z, Huang Q, Zhang R, Li R, Shen B, Shen Q (2016) Effects of organic–inorganic compound fertilizer with reduced chemical fertilizer application on crop yields, soil biological activity and bacterial community structure in a rice–wheat cropping system. Appl Soil Ecol 99:1–12. https://doi.org/10.1016/j.apsoil.2015.11.006
Zhao Z, He J, Quan Z, Wu C, Sheng R, Zhang L, Geisen S (2020) Fertilization changes soil microbiome functioning, especially phagotrophic protists. Soil Biol Biochem 148:107863. https://doi.org/10.1016/j.soilbio.2020.107863
Acknowledgements
We would like to thank the reviewers and editor for proofreading and providing helpful suggestions on the manuscript. Sincere appreciation to the scientists whose research studies were included in this meta-analysis. This study was supported by the Second Tibetan Plateau Scientific Expedition and Research Program (STEP) [Grant No. 2019QZKK0608] and the National Natural Science Foundation of China [Grant No. 31770519].
Author information
Authors and Affiliations
Contributions
All the authors contributed to the study conception and design. Yinghui Liu and Jingyi Dong conceived the ideas and designed the methodology; Jingyi Dong, Jiaqi Zhang, and Haichao Jing collected the data; Jingyi Dong and Jiaqi Zhang analysed the data, and Jingyi Dong wrote the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
There is no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Responsible Editor: Luca Bragazza.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Dong, J., Zhang, J., Liu, Y. et al. How climate and soil properties affect the abundances of nitrogen-cycling genes in nitrogen-treated ecosystems: a meta-analysis. Plant Soil 477, 389–404 (2022). https://doi.org/10.1007/s11104-022-05420-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-022-05420-6