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Total phosphorus mediates soil nitrogen cycling in alpine meadows

  • Soils, Sec 5 • Soil and Landscape Ecology • Research Article
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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.

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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

    Article  Google Scholar 

  • Bouyoucos GJ (1962) Hydrometer method improved for making particle size analyses of soils. Agron J 54:464–465

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Dynarski KA, Houlton BZ (2018) Nutrient limitation of terrestrial free-living nitrogen fixation. New Phytol 217:1050–1061

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Fick SE, Hijmans RJ (2017) WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int J Climatol 37:4302–4315

    Article  Google Scholar 

  • Gamfeldt L, Roger F (2017) Revisiting the biodiversity-ecosystem multifunctionality relationship. Nat Ecol Evol 1:168

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Kuypers MMM, Marchant HK, Kartal B (2018) The microbial nitrogen-cycling network. Nat Rev Microbiol 16:263–276

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Mehnaz KR, Dijkstra FA (2016) Denitrification and associated N2O emissions are limited by phosphorus availability in a grassland soil. Geoderma 284:34–41

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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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).

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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

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