Abstract
Purpose
The overall nitrogen (N) cycling potential integrating multiple processes has not been examined, and the relative contributions of biotic and abiotic factors remain elusive. In this study, we proposed the N cycling index (NCI), based on the potential of biological N fixation, N mineralization, nitrification, and denitrification, as a comprehensive indicator to characterize the overall soil N cycling potential in alpine meadow.
Materials and methods
The potential of individual N process sampled from the alpine meadow of Qinghai-Tibetan Plateau was quantified using incubation experiments in the laboratory. Four individual N process potentials (biological N fixation, N mineralization, nitrification, and denitrification) were quantified and used to construct the NCI. The relative contributions of biotic (e.g., N-related microbial gene abundances, microbial community) and abiotic (e.g., geo-climate, soil, and plant properties) drivers shaping NCI were investigated using variation partitioning analysis and partial mantel test. The mechanism of the key factors controlling the overall soil N cycling potential in alpine meadow was revealed using structural equation modeling (SEM).
Results and discussion
The soil NCI varied sensitively with the potential of individual N process, and it showed the highest and positive correlations with the denitrification potential in alpine meadows. Soil properties, N-related microbial gene abundances, α-diversity of bacterial and fungal communities, and fungal β-diversity showed significant and positive relationships with soil NCI. Soil total phosphorous (TP) showed the greatest influence on NCI among all the environmental factors. Soil TP remarkably mediated NCI directly and indirectly by affecting N-related gene abundances.
Conclusions
The NCI could be used to indicate overall soil N cycling potentials and soil TP played a critical role in mediating soil N cycling in alpine meadow. Together, these findings provided novel insights into the important prediction of TP in the overall soil N cycling potential in alpine ecosystem.
Similar content being viewed by others
Data availability
The data that support the findings of this study are available from the corresponding author, [Xiangzhen Li], upon reasonable request.
References
Archer E (2016) rfPermute: estimate permutation p-values for random forest importance metrics. R package (Zenodo) 2
Benner JW, Vitousek PM (2011) Cyanolichens: a link between the phosphorus and nitrogen cycles in a Hawaiian montane forest. J Trop Ecol 28:73–81
Bouyoucos GJ (1962) Hydrometer method improved for making particle size analyses of soils. Agron J 54:464–465
Chen H, Gurmesa GA, Zhang W, Zhu X, Zheng M, Mao Q, Zhang T, Mo J, Kitajima K (2015) Nitrogen saturation in humid tropical forests after 6 years of nitrogen and phosphorus addition: hypothesis testing. Funct Ecol 30:305–313
Cookson WR, Osman M, Marschner P, Abaye DA, Clark I, Murphy DV, Stockdale EA, Watson CA (2007) Controls on soil nitrogen cycling and microbial community composition across land use and incubation temperature. Soil Biol Biochem 39:744–756
Cui Y, Zhang Y, Duan C, Wang X, Zhang X, Ju W, Chen H, Yue S, Wang Y, Li S, Fang L (2020) Ecoenzymatic stoichiometry reveals microbial phosphorus limitation decreases the nitrogen cycling potential of soils in semi-arid agricultural ecosystems. Soil till Res 197:104463
DeForest JL, Otuya RK (2020) Soil nitrification increases with elevated phosphorus or soil pH in an acidic mixed mesophytic deciduous forest. Soil Biol Biochem 142:107716
Delgado-Baquerizo M, Maestre FT, Gallardo A, Bowker MA, Wallenstein MD, Quero JL, Ochoa V, Gozalo B, Garcia-Gomez M, Soliveres S, Garcia-Palacios P, Berdugo M, Valencia E, Escolar C, Arredondo T, Barraza-Zepeda C, Bran D, Carreira JA, Chaieb M, Conceicao AA, Derak M, Eldridge DJ, Escudero A, Espinosa CI, Gaitan J, Gatica MG, Gomez-Gonzalez S, Guzman E, Gutierrez JR, Florentino A, Hepper E, Hernandez RM, Huber-Sannwald E, Jankju M, Liu J, Mau RL, Miriti M, Monerris J, Naseri K, Noumi Z, Polo V, Prina A, Pucheta E, Ramirez E, Ramirez-Collantes DA, Romao R, Tighe M, Torres D, Torres-Diaz C, Ungar ED, Val J, Wamiti W, Wang D, Zaady E (2013) Decoupling of soil nutrient cycles as a function of aridity in global drylands. Nature 502:672–676
Deveautour C, Rojas-Pinzon PA, Veloso M, Rambaud J, Duff AM, Wall D, Carolan R, Philippot L, Richards KG, O’Flaherty V, Brennan F (2022) Biotic and abiotic predictors of potential N2O emissions from denitrification in Irish grasslands soils: A national-scale field study. Soil Biol Biochem 168:108637
Duan H, Xue X, Wang T, Kang W, Liao J, Liu S (2021) Spatial and temporal differences in alpine meadow, alpine steppe and all vegetation of the Qinghai-Tibetan Plateau and their responses to climate change. Remote Sens 13:669
Dynarski KA, Houlton BZ (2018) Nutrient limitation of terrestrial free-living nitrogen fixation. New Phytol 217:1050–1061
Elrys AS, Ali A, Zhang H, Cheng Y, Zhang J, Cai ZC, Muller C, Chang SX (2021a) Patterns and drivers of global gross nitrogen mineralization in soils. Glob Chang Biol 27:5950–5962
Elrys AS, Wang J, Metwally MAS, Cheng Y, Zhang JB, Cai ZC, Chang SX, Muller C (2021b) Global gross nitrification rates are dominantly driven by soil carbon-to-nitrogen stoichiometry and total nitrogen. Glob Chang Biol 27:6512–6524
Fick SE, Hijmans RJ (2017) WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int J Climatol 37:4302–4315
Gamfeldt L, Roger F (2017) Revisiting the biodiversity-ecosystem multifunctionality relationship. Nat Ecol Evol 1:168
Hardy RF, Holsten RD, Jackson EK, Burns RC (1968) The acetylene-ethylene assay for N2 fixation: laboratory and field evaluation. Plant Physiol 43:1185–1207
Harrell F, Dupont C (2018) Hmisc: harrell miscellaneous. R package version 4.1–1
Hector A, Bagchi R (2007) Biodiversity and ecosystem multifunctionality. Nature 448:188–190
Hu W, Ran J, Dong L, Du Q, Ji M, Yao S, Sun Y, Gong C, Hou Q, Gong H, Chen R, Lu J, Xie S, Wang Z, Huang H, Li X, Xiong J, Xia R, Wei M, Zhao D, Zhang Y, Li J, Yang H, Wang X, Deng Y, Sun Y, Li H, Zhang L, Chu Q, Li X, Aqeel M, Manan A, Akram MA, Liu X, Li R, Li F, Hou C, Liu J, He JS, An L, Bardgett RD, Schmid B, Deng J (2021) Aridity-driven shift in biodiversity-soil multifunctionality relationships. Nat Commun 12:5350
Kopáček J, Hejzlar J (1995) Semi-micro determination of total phosphorus in soils, sediments, and organic materials: a simplified perchloric acid digestion procedure. Commun Soil Sci Plan 26:1935–1946
Kou Y, Li C, Li J, Tu B, Wang Y, Li X (2019) Climate and soil parameters are more important than denitrifier abundances in controlling potential denitrification rates in Chinese grassland soils. Sci Total Environ 669:62–69
Kou Y, Li J, Wang Y, Li C, Tu B, Yao M, Li X (2017) Scale-dependent key drivers controlling methane oxidation potential in Chinese grassland soils. Soil Biol Biochem 111:104–114
Kuypers MMM, Marchant HK, Kartal B (2018) The microbial nitrogen-cycling network. Nat Rev Microbiol 16:263–276
Li J, Yang C, Liu X, Ji H, Shao X (2020a) Soil aggregate size influences the impact of inorganic nitrogen deposition on soil nitrification in an alpine meadow of the Qinghai-Tibet Plateau. PeerJ 8:e8230
Li Y, Zhou H, Chen W, Wu Y, Qiao L, Yan Z, Liu G, Xue S (2021) Long-term warming does not affect soil ecoenzyme activity and original microbial nutrient limitation on the Qinghai—Tibet Plateau. Soil Ecol Lett 4:383–398
Li Z, Tian D, Wang B, Wang J, Wang S, Chen HYH, Xu X, Wang C, He N, Niu S (2019) Microbes drive global soil nitrogen mineralization and availability. Glob Chang Biol 25:1078–1088
Li Z, Zeng Z, Tian D, Wang J, Fu Z, Zhang F, Zhang R, Chen W, Luo Y, Niu S (2020b) Global patterns and controlling factors of soil nitrification rate. Glob Chang Biol 26:4147–4157
Liu C, Cui Y, Li X, Yao M (2021) microeco: an R package for data mining in microbial community ecology. Fems Microbiol Ecol 97:fiaa255
Liu S, Liu W, Shi X, Li S, Hu T, Song L, Wu C (2018a) Dry-hot stress significantly reduced the nitrogenase activity of epiphytic cyanolichen. Sci Total Environ 619–620:630–637
Liu S, Zamanian K, Schleuss P-M, Zarebanadkouki M, Kuzyakov Y (2018b) Degradation of Tibetan grasslands: consequences for carbon and nutrient cycles. Agric Ecosyst Environ 252:93–104
Liu Y, He N, Wen X, Yu G, Gao Y, Jia Y (2016) Patterns and regulating mechanisms of soil nitrogen mineralization and temperature sensitivity in Chinese terrestrial ecosystems. Agric Ecosyst Environ 215:40–46
Lu X, Yan Y, Fan J, Wang X (2012) Gross nitrification and denitrification in alpine grassland ecosystems on the Tibetan Plateau. Arct Antarct Alp Res 44:188–196
Maestre FT, Quero JL, Gotelli NJ, Escudero A, Ochoa V, Delgado-Baquerizo M, García-Gómez M, Bowker MA, Soliveres S, Escolar C, García-Palacios P, Berdugo M, Valencia E, Gozalo B, Gallardo A, Aguilera L, Arredondo T, Blones J, Boeken B, Bran D, Conceição AA, Cabrera O, Chaieb M, Derak M, Eldridge DJ, Espinosa CI, Florentino A, Gaitán J, Gatica MG, Ghiloufi W, Gómez-González S, Gutiérrez JR, Hernández RM, Huang X, Huber-Sannwald E, Jankju M, Miriti M, Monerris J, Mau RL, Morici E, Naseri K, Ospina A, Polo V, Prina A, Pucheta E, Ramírez-Collantes DA, Romão R, Tighe M, Torres-Díaz C, Val J, Veiga JP, Wang D, Zaady E (2012) Plant species richness and ecosystem multifunctionality in global drylands. Science 335:214–218
Manning P, van der Plas F, Soliveres S, Allan E, Maestre FT, Mace G, Whittingham MJ, Fischer M (2018) Redefining Ecosystem Multifunctionality Nat Ecol Evol 2:427–436
Martinez AI, Labib SM (2023) Demystifying normalized difference vegetation index (NDVI) for greenness exposure assessments and policy interventions in urban greening. Environ Res 220:115155
Maxwell TL, Canarini A, Bogdanovic I, Bockle T, Martin V, Noll L, Prommer J, Seneca J, Simon E, Piepho HP, Herndl M, Potsch EM, Kaiser C, Richter A, Bahn M, Wanek W (2021) Contrasting drivers of belowground nitrogen cycling in a montane grassland exposed to a multifactorial global change experiment with elevated CO2, warming, and drought. Glob Chang Biol 28:2425–2441
Mehnaz KR, Dijkstra FA (2016) Denitrification and associated N2O emissions are limited by phosphorus availability in a grassland soil. Geoderma 284:34–41
Nelson DW, Sommers LE (1996) Total carbon, organic carbon, and organic matter. In: Swift RS, Sparks DL (eds) Methods of Soil Analysis: Part 3-Chemical Methods. SSSA, ASA, Madison, 961–1010
Norton JM, Stark JM (2011) Regulation and measurement of nitrification in terrestrial systems. Method Enzymol 486:343–368
Oksanen FJ, Blanchet G, Friendly M, Kindt R, others (2017) vegan: community ecology package. R package version 2.4–4
Pan B, Xia L, Lam SK, Wang E, Zhang Y, Mosier A, Chen D (2022) A global synthesis of soil denitrification: driving factors and mitigation strategies. Agric Ecosyst Environ 327:107850
R-Core-Development-Team (2010) R: A language and environment for statistical computing. Computing 14:12–21
Reed SC, Seastedt TR, Mann CM, Suding KN, Townsend AR, Cherwin KL (2007) Phosphorus fertilization stimulates nitrogen fixation and increases inorganic nitrogen concentrations in a restored prairie. Appl Soil Ecol 36:238–242
Risch AC, Zimmermann S, Ochoa-Hueso R, Schutz M, Frey B, Firn JL, Fay PA, Hagedorn F, Borer ET, Seabloom EW, Harpole WS, Knops JMH, McCulley RL, Broadbent AAD, Stevens CJ, Silveira ML, Adler PB, Baez S, Biederman LA, Blair JM, Brown CS, Caldeira MC, Collins SL, Daleo P, di Virgilio A, Ebeling A, Eisenhauer N, Esch E, Eskelinen A, Hagenah N, Hautier Y, Kirkman KP, MacDougall AS, Moore JL, Power SA, Prober SM, Roscher C, Sankaran M, Siebert J, Speziale KL, Tognetti PM, Virtanen R, Yahdjian L, Moser B (2019) Soil net nitrogen mineralisation across global grasslands. Nat Commun 10:4981
Rosseel Y (2012) lavaan: An R package for structural equation modeling. J Stat Softw 48:1–36
Rütting T, Schleusner P, Hink L, Prosser JI (2021) The contribution of ammonia-oxidizing archaea and bacteria to gross nitrification under different substrate availability. Soil Biol Biochem 160:108353
Tang Y, Yu G, Zhang X, Wang Q, Tian J, Niu S, Tian D, Ge J (2019) Different strategies for regulating free-living N2 fixation in nutrient-amended subtropical and temperate forest soils. Appl Soil Ecol 136:21–29
Taylor AE, Zeglin LH, Dooley S, Myrold DD, Bottomley PJ (2010) Evidence for different contributions of archaea and bacteria to the ammonia-oxidizing potential of diverse Oregon soils. Appl Environ Microbiol 76:7691–7698
Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB, Grimm NB, Howarth RW, Marino R, Martinelli L, Rastetter EB, Sprent JI (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57:1–45
Wang C, Wang G, Wu P, Rafique R, Zi H, Li X, Luo Y (2017a) Effects of ant mounds on the plant and soil microbial community in an alpine meadow of Qinghai-Tibet Plateau. Land Degrad Dev 28(5):1538–1548
Wang C, Wang X, Liu D, Wu H, Lü X, Fang Y, Cheng W, Luo W, Jiang P, Shi J, Yin H, Zhou J, Han X, Bai E (2014) Aridity threshold in controlling ecosystem nitrogen cycling in arid and semi-arid grasslands. Nat Commun 5:4799
Wang R, Bicharanloo B, Hou E, Jiang Y, Dijkstra FA (2022) Phosphorus supply increases nitrogen transformation rates and retention in soil: a global meta‐analysis. Earths Future 10:e2021EF002479
Wang S, Duan J, Xu G, Wang Y, Zhang Z, Rui Y, Luo C, Xu B, Zhu X, Chang X (2012) Effects of warming and grazing on soil N availability, species composition, and ANPP in an alpine meadow. Ecology 93:2365–2376
Wang Y, Li C, Kou Y, Wang J, Tu B, Li H, Li X, Wang C, Yao M (2017b) Soil pH is a major driver of soil diazotrophic community assembly in Qinghai-Tibet alpine meadows. Soil Biol Biochem 115:547–555
Wang Y, Li C, Shen Z, Rui J, Jin D, Li J, Li X (2019) Community assemblage of free-living diazotrophs along the elevational gradient of Mount Gongga. Soil Ecol Lett 1:136–146
Wei T, Simko V (2021) corrplot: visualization of a correlation matrix. R package version 0.92
Wu C, Wei X, Hu Z, Liu Y, Hu Y, Qin H, Chen X, Wu J, Ge T, Zhran M, Su Y (2021) Diazotrophic community variation underlies differences in nitrogen fixation potential in paddy soils across a climatic gradient in china. Microb Ecol 81:425–436
Xiao J, Dong S, Shen H, Li S, Wessell K, Liu S, Li W, Zhi Y, Mu Z, Li H (2022) N addition overwhelmed the effects of P addition on the soil C, N, and P cycling genes in alpine meadow of the Qinghai-Tibetan Plateau. Front Plant Sci 13:860590
Xu L, Zhang B, Wang E, Zhu B, Yao M, Li C, Li X (2021a) Soil total organic carbon/total nitrogen ratio as a key driver deterministically shapes diazotrophic community assemblages during the succession of biological soil crusts. Soil Ecol Lett 3:328–341
Xu L, Zhu B, Li C, Zhou Z, Yao M, Zhou X, Wang J, Zhang B, Li X (2021b) Increasing relative abundance of non-cyanobacterial photosynthetic organisms drives ecosystem multifunctionality during the succession of biological soil crusts. Geoderma 395:115052
Zhang K, Li M, Yan Z, Li M, Kang E, Yan L, Zhang X, Li Y, Wang J, Yang A, Niu Y, Kang X (2022a) Changes in precipitation regime lead to acceleration of the N cycle and dramatic N2O emission. Sci Total Environ 808:152140
Zhang L, Wang X, Wang J, Liao L, Lei S, Liu G, Zhang C (2022b) Alpine meadow degradation depresses soil nitrogen fixation by regulating plant functional groups and diazotrophic community composition. Plant Soil 473:319–335
Zhang S, Chen D, Sun D, Wang X, Smith JL, Du G (2011) Impacts of altitude and position on the rates of soil nitrogen mineralization and nitrification in alpine meadows on the eastern Qinghai-Tibetan Plateau, China. Biol Fert Soils 48:393–400
Zhang X, Jia X, Wu H, Li J, Yan L, Wang J, Li Y, Kang X (2020a) Depression of soil nitrogen fixation by drying soil in a degraded alpine peatland. Sci Total Environ 747:141084
Zhang X, Zhu B, Yu F, Cheng W (2021) Plant inputs mediate the linkage between soil carbon and net nitrogen mineralization. Sci Total Environ 790:148208
Zhang Y, Hu T, Wang H, Jin H, Liu Q, Chen Z, Xie Z (2022c) Nitrogen content and C/N ratio in straw are the key to affect biological nitrogen fixation in a paddy field. Plant Soil 481:535–546
Zhang Y, Zhang N, Yin J, Zhao Y, Yang F, Jiang Z, Tao J, Yan X, Qiu Y, Guo H, Hu S (2020b) Simulated warming enhances the responses of microbial N transformations to reactive N input in a Tibetan alpine meadow. Environ Int 141:105795
Zheng M, Zhou Z, Zhao P, Luo Y, Ye Q, Zhang K, Song L, Mo J (2020) Effects of human disturbance activities and environmental change factors on terrestrial nitrogen fixation. Glob Chang Biol 26:6203–6217
Zhong L, Wang S, Xu X, Yanfen R, Yichao Z (2018) Fungi regulate the response of the N2O production process to warming and grazing in a Tibetan grassland. Biogeosciences 15:4447–4457
Zhou H, Ma A, Zhou X, Chen X, Zhang J, Gen P, Liu G, Wang S, Zhuang G (2022) Soil phosphorus accumulation in mountainous alpine grassland contributes to positive climate change feedback via nitrifier and denitrifier community. Sci Total Environ 804:150032
Acknowledgements
We thank Jingwei Liu, Jun Mao, Zhenzhen Shao, for their assistances in field samplings and some laboratory work.
Funding
This work was supported by the National Natural Science Foundation of China (32071548, U20A2008), Second Tibetan Plateau Scientific Expedition and Research (STEP) Program (2019QZKK0302), and China Biodiversity Observation Networks (Sino BON).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Responsible editor: Jizheng He
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
Jing, Y., Lan, N., Lei, L. et al. Total phosphorus mediates soil nitrogen cycling in alpine meadows. J Soils Sediments 23, 3445–3457 (2023). https://doi.org/10.1007/s11368-023-03561-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11368-023-03561-4