Abstract
Atmospheric nitrogen (N) deposition resulting from human activities has significantly increased reactive N levels in terrestrial ecosystems, which is acknowledged as a primary driver of global change. The response and mechanism of soil organic nitrogen (SON) in N deposition are unclear, despite its critical role as a source and constituent of N. This study aims to investigate SON components and the involvement of soil microorganisms in response to N deposition. It also aims to predict changes in soil N dynamics by accumulating data. N deposition was simulated for 3 years (0, 30, 60, and 90 kg N ha−1 year−1). We examined SON components, the abundance of N-cycle functional genes (NFGs), soil enzyme activities, and N transformation through field surveys and indoor cultivation in a Pinus massoniana plantation with classified Luvisols soil. Acid-hydrolyzable N levels increase with N addition, particularly in mineralizable components, namely acid-hydrolyzable amino acid N and ammonia N. This increase correlated with total N and microbial biomass, leading to a positive impact on N hydrolase activities. Additionally, it results a higher relative abundance of NFGs, which serve as indicators of net N transformation. Net N mineralization increased significantly by a factor of 2.97–4.30 times with N addition compared with the control. Simulated N deposition resulted in an increase in mineralizable SON and NFGs, resulting in higher N availability. However, N addition raises concerns regarding potential organic matter losses and phosphorus limitation. Therefore, long-term monitoring is essential for areas with high N deposition.
Similar content being viewed by others
Data Availability
All data generated or analyzed during this study are included in this published article (and its supplementary information files).
References
Alef K, Nannipieri P (1995) Methods in applied soil microbiology and biochemistry. In: Alef K, Nannipieri P (eds) Enzyme activities. Academic Press, London, pp 311–373
Allison SD, Vitousek PM (2005) Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Boil Biochem 37:937–944. https://doi.org/10.1016/j.soilbio.2004.09.014
Antonio CH, Jesús GL, Eulogio JB (2018) Distinct effect of nitrogen fertilisation and soil depth on nitrous oxide emissions and nitrifiers and denitrifiers abundance. Biol Fertil Soils 54:829–840. https://doi.org/10.1007/s00374-018-1310-9
Barro F, Fontes AG, Maldonado JM (1991) Organic nitrogen content and nitrate and nitrite reductase activities in Tritordeum and wheat grown under nitrate or ammonium. Plant Soil 135:251–256. https://doi.org/10.1007/BF00010913
Bremner JM (1965) Organic forms of nitrogen. In: Black CA (ed) Methods of soil analysis. American Society of Agronomy, Madison, pp 1238–1255
Cao RR, Chen LC, Hou XC, Lu XT, Li HM (2021) Nitrogen addition reduced carbon mineralization of aggregates in forest soils but enhanced in paddy soils in South China. Ecol Processes 10:45. https://doi.org/10.1186/s13717-021-00319-z
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
Chen H, Li DJ, Zhao J, Xiao KC, Wang KL (2018) Effects of nitrogen addition on activities of soil nitrogen acquisition enzymes: a meta-analysis. Agr Ecosyst Environ 252:126–131. https://doi.org/10.1016/j.agee.2017.09.032
Chen HJ, Huang XF, Shi WM, Kronzucker HJ, Hou LH, Yang HY, Song QN, Liu J, Shi JM, Yang QP, Zou N (2021) Coordination of nitrogen uptake and assimilation favours the growth and competitiveness of moso bamboo over native tree species in high-NH4+ environments. J Plant Physiol 266:153508. https://doi.org/10.1016/j.jplph.2021.153508
Dong ZX, Zhu B, Jiang Y, Tang JL, Liu WL, Hu L (2018) Seasonal N2O emissions respond differently to environmental and microbial factors after fertilization in wheat-maize agroecosystem. Nutr Cycl Agroecosys 112:215–229. https://doi.org/10.1007/s10705-018-9940-8
Elrys AS, Ali A, Zhang HM, Cheng Y, Zhang JB, Cai ZC, Müller C, Chang SX (2021) Patterns and drivers of global gross nitrogen mineralization in soils. Global Change Biol 27:5950–5962. https://doi.org/10.1111/gcb.15851
Fowler D, Coyle M, Skiba U, Sutton MA, Cape JN, Reis S, Sheppard LJ, Jenkins A, Grizzetti B, Galloway JN, Vitousek P, Leach A, Bouwman AF, Butterbach-Bahl K, Dentener F, Stevenson D, Amann M, Voss M (2013) The global nitrogen cycle in the twenty-first century. Philos T R Soc B 368:20130164. https://doi.org/10.1098/rstb.2013.0164
Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai ZC, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892. https://doi.org/10.1126/science.1136674
Galloway JN, Winiwarter W, Leip A, Leach AM, Bleeker A, Erisman JW (2014) Nitrogen footprints: past, present and future. Environ Res Lett 9:115003. https://doi.org/10.1088/1748-9326/9/11/115003
Govindarajulu M, Pfeffer PE, Jin HR, Abubaker J, Douds DD, Allen JW, Bücking H, Lammers PJ, Shachar-Hill Y (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819–823. https://doi.org/10.1038/nature03610
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
He JZ, Shen JP, Zhang LM, Zhu YG, Zheng YM, Xu MG, Di H (2007) Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long- term fertilization practices. Environ Microbiol 9:2364–2374. https://doi.org/10.1111/j.1462-2920.2007.01358.x
He JZ, Hu HW, Zhang LM (2012) Current insights into the autotrophic thaumarchaeal ammonia oxidation in acidic soils. Soil Boil Biochem 55:146–154. https://doi.org/10.1016/j.soilbio.2012.06.006
Huang HP, Hu XJ, Tian JP, Jiang XN, Luo HB, Huang D (2021) Rapid detection of the reducing sugar and amino acid nitrogen contents of Daqu based on hyperspectral imaging. J Food Compos Anal 101:103970. https://doi.org/10.1016/j.jfca.2021.103970
Imran M, Sun XC, Hussain S, Ali U, Rana MS, Rasul F, Saleem MH, Moussa MG, Bhantana P, Afzal J, Elyamine AM, Hu CX (2019) Molybdenum-induced effects on nitrogen metabolism enzymes and elemental profile of winter wheat (Triticum aestivum L.) under different nitrogen sources. Int J Mol Sci 20:3009. https://doi.org/10.3390/ijms20123009
Jiao YP, Qi P, Wang XJ, Wu J, Yao YM, Cai LQ, Zhang RZ (2020) Effects of different nitrogen application rates on soil organic nitrogen components and enzyme activities in farmland. Sci Agr Sin 53:2423–2434. https://doi.org/10.3864/j.issn.0578-1752.2020.12.010
Kandeler E, Gerber H (1988) Short-term assay of soil urease activity using, colorimetric determination of ammonium. Biol Fertil Soil 6:68–72. https://doi.org/10.1007/BF00257924
Kandeler E, Brune T, Enowashu E, Dörr N, Guggenberger G, Lamersdorf N, Philippot L (2009) Response of total and nitrate-dissimilating bacteria to reduced N deposition in a spruce forest soil profile. Fems Microbiol Ecol 67:444–454. https://doi.org/10.1111/j.1574-6941.2008.00632.x
Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809. https://doi.org/10.1038/nature04983
Levy-Booth DJ, Winder RS (2010) Quantification of nitrogen reductase and nitrite reductase genes in soil of thinned and clear-cut douglas-fir stands by using real-time PCR. Appl Environ Microbiol 76:7116–7125. https://doi.org/10.1128/AEM.02188-09
Li SQ, Li SX, Shao MA, Guo DY (2004) Effects of long-term application of fertilizers on soil organic nitrogen components and microbial biomass nitrogen in semiarid farmland ecological system. Sci Agr Sin 37:859–864. https://doi.org/10.3321/j.issn:0578-1752.2004.06.013
Li H, Yang S, Xu ZW, Yan QY, Li XB, Nostrand JD, He ZL, Yao F, Han XG, Zhou JZ, Deng Y, Jiang Y (2017) Responses of soil microbial functional genes to global changes are indirectly influenced by aboveground plant biomass variation. Soil Boil Biochem 104:18–29. https://doi.org/10.1016/j.soilbio.2016.10.009
Li JJ, Wang GL, Yan BS, Liu GB (2020) The responses of soil nitrogen transformation to nitrogen addition are mainly related to the changes in functional gene relative abundance in artificial Pinus tabulaeformis forests. Sci Total Environ 723:137679. https://doi.org/10.1016/j.scitotenv.2020.137679
Liu LL, 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
Liu F, Qian GS, Zhao X, Hu XM (2022) Mechanism insights into the nitrogen removal of bio-augmented AAO: specifically focusing on the nitrogen metabolic pathways and microbial taxa-functional genes associations. J Water Process Eng 50:103245. https://doi.org/10.1016/j.jwpe.2022.103245
Lu X, Mao Q, Wang Z, Mori T, Mo J, Su F, Pang Z (2021) Long-term nitrogen addition decreases soil carbon mineralization in an N-rich primary tropical forest. Forests 12:734. https://doi.org/10.3390/f12060734
Luo G, Friman V, Chen H, Liu MQ, Wang M, Guo SW, Ling N, Shen QR (2018) Long-term fertilization regimes drive the abundance and composition of N-cycling-related prokaryotic groups via soil particle-size differentiation. Soil Boil Biochem 116:213–223. https://doi.org/10.1016/j.soilbio.2017.10.015
Ma LJ, Huo QY, Tian QY, Xu YX, Hao HB, Min W, Hou ZA (2023) Continuous application of biochar increases N-15 fertilizer translocation into soil organic nitrogen and crop uptake in drip-irrigated cotton field. J Soil Sediment 23:1204–1216. https://doi.org/10.1007/s11368-022-03416-4
Mergel A, Kloos K, Bothe H (2001) Seasonal fluctuations in the population of denitrifying and N2-fixing bacteria in an acid soil of a Norway spruce forest. Plant Soil 230:145–160. https://doi.org/10.1023/A:1004826116981
Nannipieri P, Eldor P (2009) The chemical and functional characterization of soil n and its biotic components. Soil Boil Biochem 41:2357–2369. https://doi.org/10.1016/j.soilbio.2009.07.013
Nave LE, Vance ED, Swanston CW, Curtis PS (2009) Impacts of elevated N inputs on north temperate forest soil C storage, C/N, and net N-mineralization. Geoderma 153:231–240. https://doi.org/10.1016/j.geoderma.2009.08.012
Ni YY, Jian ZJ, Zeng LX, Liu JF, Lei L, Zhu JH, Xu J, Xiao WF (2022) Climate, soil nutrients, and stand characteristics jointly determine large-scale patterns of biomass growth rates and allocation in Pinus massoniana plantations. Forest Ecol Manag 504:119839. https://doi.org/10.1016/j.foreco.2021.119839
Ouyang Y, Norton JM, Stark JM, Reeve JR, Habteselassie MY (2016) Ammonia-oxidizing bacteria are more responsive than archaea to nitrogen source in an agricultural soil. Soil Boil Biochem 96:4–15. https://doi.org/10.1016/j.soilbio.2016.01.012
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 Boil Biochem 127:71–78. https://doi.org/10.1016/j.soilbio.2018.08.024
Peñuelas J, Poulter B, Sardans J, Ciais P, van der Velde M, Bopp L, Boucher O, Godderis Y, Hinsinger P, Llusia J, Nardin E, Vicca S, Obersteiner M, Janssens IA (2013) Human-induced nitrogen–phosphorus imbalances alter natural and managed ecosystems across the globe. Nat Commun 4:2934. https://doi.org/10.1038/ncomms3934
Petersen DG, Blazewicz SJ, Firestone M, Herman DJ, Turetsky M, Waldrop M (2012) 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. https://doi.org/10.1111/j.1462-2920.2011.02679.x
Qin HL, Xing XY, Tang YF, Hou HJ, Yang J, Shen R, Zhang WZ, Liu Y, Wei WX (2019) Linking soil N2O emissions with soil microbial community abundance and structure related to nitrogen cycle in two acid forest soils. Plant Soil 435:95–109. https://doi.org/10.1007/s11104-018-3863-7
Qin WF, Zhao XC, Yang F, Chen JH, Mo QS, Cui S, Chen C, He SJ, Li Z (2023) Impact of fertilization and grazing on soil N and enzyme activities in a karst pasture ecosystem. Geoderma 437:116578. https://doi.org/10.1016/10.1016/j.geoderma.2023.116578
Rasche F, Knapp D, Kaiser C, Koranda M, Kitzler B, Zechmeister-Boltenstern S, Sessitsch A (2011) Seasonality and resource availability control bacterial and archaeal communities in soils of a temperate beech forest. ISME J 5:389–402. https://doi.org/10.1038/ismej.2010.138
Recous S, Machet JM, Mary B (1992) The partitioning of fertilizer-N between soil and crop: comparison of ammonium and nitrate applications. Plant Soil 144:101–111. https://doi.org/10.1007/BF00018850
Rice CW, Tiedje JM (1989) Regulation of nitrate assimilation by ammonium in soils and in isolated soil microorganisms. Soil Biol Bioche 21:597–602. https://doi.org/10.1016/0038-0717(89)90135-1
Rösch C, Mergel A, Bothe H (2002) Biodiversity of denitrifying and dinitrogen-fixing bacteria in an acid forest soil. AEM 68:3818–3829. https://doi.org/10.1128/AEM.68.8.3818-3829.2002
Shen LD, Liu X, Wu HS, Tian MH, Ran P, Liu JQ, Yang YL, Yang WT, Wang HY (2020) Effect of different fertilization regimes on the vertical distribution of anaerobic ammonium oxidation in paddy soils. Eur J Soil Biol 99:103206. https://doi.org/10.1016/j.ejsobi.2020.103206
Sinsabaugh RL, Hill BH, Shah JJF (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795–798. https://doi.org/10.1038/nature08632
Song YY, Song CC, Li YC, Hou CC, Yang GS, Zhu XY (2013) Short-term effects of nitrogen addition and vegetation removal on soil chemical and biological properties in a freshwater marsh in Sanjiang Plain, Northeast China. CATENA 104:265–271. https://doi.org/10.1016/j.catena.2012.12.008
Stevens CJ, Dise NB, Mountford JO, Gowing DJ (2004) Impact of nitrogen deposition on the species richness of grasslands. Science 303:1876–1879. https://doi.org/10.1126/science.1094678
Szukics U, Hackl E, Zechmeister-Boltenstern S, Sessitsch A (2012) Rapid and dissimilar response of ammonia oxidizing archaea and bacteria to nitrogen and water amendment in two temperate forest soils. Microbiol Res 167:103–109. https://doi.org/10.1016/j.micres.2011.04.002
Tian XF, Hu HW, Ding Q, Song MH, Xu XL, Zheng Y, Guo LD (2014) Influence of nitrogen fertilization on soil ammonia oxidizer and denitrifier abundance, microbial biomass, and enzyme activities in an alpine meadow. Biol Fertil Soils 50:703–713. https://doi.org/10.1007/s00374-013-0889-0
Tian JH, Wei K, Condron LM, Chen ZH, Xu ZW, Feng J, Chen LJ (2017) Effects of elevated nitrogen and precipitation on soil organic nitrogen fractions and nitrogen-mineralizing enzymes in semi-arid steppe and abandoned cropland. Plant Soil 417:217–229. https://doi.org/10.1007/s11104-017-3253-6
Tu LH, Chen G, Peng Y, Hu HL, Hu TX, Zhang J, Li XW, Liu L, Tang Y (2014) Soil biochemical responses to nitrogen addition in a bamboo forest. PLoS ONE 16:e102315. https://doi.org/10.1371/journal.pone.0102315
Vallino JJ, Hopkinson CS, Hobbie JE (1996) Modeling bacterial utilization of dissolved organic matter: optimization replaces Monod growth kinetics. Limnol Oceanogr 41:1591–1609. https://doi.org/10.4319/lo.1996.41.8.1591
Wang JS, Stewart JR, Khan SA, Dawson JO (2010) Elevated amino sugar nitrogen concentrations in soils: a potential method for assessing n fertility enhancement by actinorhizal plants. Symbiosis 50:71–76. https://doi.org/10.1007/s13199-009-0038-6
Wang CH, Butterbach-Bahl K, Han Y, Wang QB, Zhang LH, Han XG, Xing XR (2011) The effects of biomass removal and N additions on microbial N transformations and biomass at different vegetation types in an old-field ecosystem in northern China. Plant Soil 340:397–411. https://doi.org/10.1007/s11104-010-0611-z
Wang XL, Han C, Zhang JB, Huang QR, Deng H, Deng YC, Zhong WH (2015) Long-term fertilization effects on active ammonia oxidizers in an acidic upland soil in China. Soil Boil Biochem 84:28–37. https://doi.org/10.1016/j.soilbio.2015.02.013
Wang D, Chen WF, Han XR, Liu SY, Cao DY, Cheng XY, Wang QY, Zhan ZY, He WY (2023) The six-year biochar retention interacted with fertilizer addition alters the soil organic nitrogen supply capacity in bulk and rhizosphere soil. J Environ Manage 338:117757. https://doi.org/10.1016/j.jenvman.2023.117757
Weng BS, Xie XY, Yang JJ, Liu JC, Lu HL, Yan CL (2013) Research on the nitrogen cycle in rhizosphere of Kandelia obovata under ammonium and nitrate addition. Mar Pollut Bull 76:227–240. https://doi.org/10.1016/j.marpolbul.2013.08.034
Wu HQ, Du SY, Gao N, Zhang YL, Zou HT, Zhang YL, Yu N (2017) Effects of water and nitrogen regulation on soil organic nitrogen fractions, total nitrogen and mineral nitrogen in greenhouse soil. J Soil Water C 31: 212–219. https://doi.org/10.13870/j.cnki.stbcxb.2017.06.034
Wu HQ, Zhang YL, Zhang YL, Zou HT, Yu N (2018) Soil organic nitrogen fractions: a review. Chin J Soil Sci 49: 1240–1246. https://doi.org/10.19336/j.cnki.trtb.2018.05.35
Xu YC, Shen QR, Ran W (2003) Content and distribution of forms of organic N in soil and particle size fractions after long-term fertilization. Chemosphere 50:739–745. https://doi.org/10.1016/S0045-6535(02)00214-X
Yao GJ, Ren JQ, Zhou F, Liu YD, Li W (2021) Micro-nano aeration is a promising alternative for achieving high-rate partial nitrification. Sci Total Environ 795:148899. https://doi.org/10.1016/j.scitotenv.2021.148899
Zhang LM, Hu HW, Shen JP, He JZ (2012) Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME J 6:1032–1045. https://doi.org/10.1038/ismej.2011.168
Zhang YG, Liu X, Cong J, Lu H, Sheng YY, Wang XL, Li DQ, Liu XD, Yin HQ, Zhou JZ, Deng Y (2017) The microbially mediated soil organic carbon loss under degenerative succession in an alpine meadow. Mol Ecol 26:3676–3686. https://doi.org/10.1111/mec.14148
Zhang JF, Li J, Fan YX, Mo QF, Li YW, Li YX, Li ZA, Wang FM (2020) Effect of nitrogen and phosphorus addition on litter decomposition and nutrients release in a tropical forest. Plant Soi 454:139–153. https://doi.org/10.1007/s11104-020-04643-9
Zhang XM, Johnston ER, Wang YS, Yu Q, Tian DS, Wang ZP, Zhang YQ, Gong DZ, Luo C, Liu W, Yang JJ, Han XG (2019) Distinct drivers of core and accessory components of soil microbial community functional diversity under environmental changes. Msystems 4:e00374–19. https://doi.org/10.1128/mSystems.00374-19
Zhao Y, Wang YQ, Sun SN, Liu WT, Zhu L, Yan XB (2022) Different forms and proportions of exogenous nitrogen promote the growth of alfalfa by increasing soil enzyme activity. Plants 11:1057. https://doi.org/10.3390/plants11081057
Zheng DN, Wang XS, Xie SD, Duan L, Chen DS (2014) Simulation of atmospheric nitrogen deposition in China in 2010. China Environ Sci 34: 1089–1097. https://www.cnki.com.cn/Article/CJFDTOTAL-ZGHJ201405001.htm
Zhou Z, Wang C, Jin Y (2017) Stoichiometric responses of soil microflora to nutrient additions for two temperate forest soils. Biol Fertil Soils 53:397–406. https://doi.org/10.1007/s00374-017-1188-y
Acknowledgements
We would like to thank ZYEdit (https://www.zhiyunwenxian.cn/) for English language editing.
Funding
This study was supported by the National Non-profit Institute Research Grant of the Chinese Academy of Forestry (CAFYBB2022XD002) and the Fundamental Research Fund of the Chinese Academy of Forestry (No.CAFYBB2021ZE003).
Author information
Authors and Affiliations
Contributions
CT and CR envisioned and wrote the manuscript. SY, WL, SP, ZM, and LJ did the experimental work, which was supervised by XW. All authors contributed to the article and approved the submitted version.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Chen, T., Cheng, R., Xiao, W. et al. Nitrogen Addition Enhances Soil Nitrogen Mineralization Through an Increase in Mineralizable Organic Nitrogen and the Abundance of Functional Genes. J Soil Sci Plant Nutr 24, 975–987 (2024). https://doi.org/10.1007/s42729-023-01600-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42729-023-01600-0