Effects of nitrogen addition on plant–soil–microbe stoichiometry characteristics of different functional group species in Bothriochloa ischemum community

Highlights

• Both plants and microbes were strictly homeostatic.

• Companion species were more susceptible to P limitation than dominant species.

• Added N aggravated stoichiometric niche overlap among species.

• Compositae had a greater effect on soil microbes than Gramineae in the rhizosphere.

• Effects of N addition on species were different across functional groups.

Abstract

Nitrogen (N) deposition, the source of N input into terrestrial ecosystems, is exhibiting an increasingly serious impact on the biogeochemical cycle and functional stability of ecosystems. Grasslands are an important component of terrestrial ecosystems and play a key role in maintaining terrestrial ecosystem balance. Therefore, it is critical to understand the effects of nitrogen addition on grassland ecosystems. We conducted gradient N addition experiments (0, 3, 6, and 9 g N m⁻² y⁻¹) for three years in grassland communities with similar site conditions. We utilized four typical herbaceous plants, including the dominant species Bothriochloa ischemum (B. ischemum) and companion species Stipa bungeana (S. bungeana), Artemisia gmelinii (A. gmelinii), and Cleistogenes squarrosa (C. squarrosa), to explore how different plant–soil–microbe systems respond to N addition. Stoichiometric homeostasis analysis demonstrated that both plants and microbes were strictly homeostatic. However, the companion species were found to be more susceptible to P dominant species. Furthermore, aggravated overlap in stoichiometric niches between plant species were observed at the N6 and N9 levels. Vector analysis indicated that the vector angle was >45° regardless of plant species and N levels, suggesting that there was a strong P limitation in the rhizosphere microbial community. Variation partitioning analysis revealed that the Composite roots exhibited a greater effect (explaining 34.7% of the variation) on the rhizosphere microbes than on the Gramineae, indicating that there may be more intense nutrient competition in its rhizosphere. In general, the effects of N addition on species were different across functional groups, with a significant positive effect on the Gramineae (B. ischemum, S. bungeana, and C. squarrosa) and a significant negative effect on the Compositae (A. gmelinii), which should be fully considered in the future ecological management and restoration.

Graphical abstract

Keywords

N addition / Ecological stoichiometry / Stoichiometric homeostasis / Nutrient limitation / Stoichiometric niche / Plant–soil–m icrobe system

References

[1] Allison, S.D., Weintraub, M.N., Gartner, T.B., Waldrop, M.P., 2011. Evolutionary-Economic Principles as Regulators of Soil Enzyme Production and Ecosystem Function, In: Shukla, G., Varma, A. (Eds.), Soil Enzymology. Springer-Verlag Berlin, Berlin, pp. 229–243.

[2] Ashton, I.W., Miller, A.E., Bowman, W.D., Suding, K.N., 2010. Niche complementarity due to plasticity in resource use: plant partitioning of chemical N forms. Ecology 91, 3252–3260

[3] Atkinson, C.L., van Ee, B.C., Pfeiffer, J.M., 2020. Evolutionary history drives aspects of stoichiometric niche variation and functional effects within a guild. Ecology 101, e03100

[4] Bergstrom, A.K., Jansson, M., 2006. Atmospheric nitrogen deposition has caused nitrogen enrichment and eutrophication of lakes in the northern hemisphere. Global Change Biology 12, 635–643

[5] Bloom, A.J., Chapin, F.S. III, Mooney, H.A., 1985. Resource limitation in plants–An economic analogy. Annual Review of Ecology and Systematics 16, 363–392

[6] Bremner, J., Mulvaney, C., 1982. Nitrogen Total. Methods of Soil Analysis. Part 2. Chemical and Microbiological Properties. Soil Sci. Soc. Am. Inc Publisher, Madison, Wisconsin, USA.

[7] Brookes, P.C., Landman, A., Pruden, G., Jenkinson, D.S., 1985. Chloroform fumigation and the release of soil nitrogen: A rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biology & Biochemistry 17, 837–842

[8] Cadotte, M.W., 2017. Functional traits explain ecosystem function through opposing mechanisms. Ecology Letters 20, 989–996

[9] Cardinale, B.J., Srivastava, D.S., Duffy, J.E., Wright, J.P., Downing, A.L., Sankaran, M., Jouseau, C., 2006. Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443, 989–992

[10] Carnicer, J., Sardans, J., Stefanescu, C., Ubach, A., Bartrons, M., Asensio, D., Penuelas, J., 2015. Global biodiversity, stoichiometry and ecosystem function responses to human-induced C-N-P imbalances. Journal of Plant Physiology 172, 82–91

[11] Caruso, G., Monticelli, L., Azzaro, F., Azzaro, M., Decembrini, F., La Ferla, R., Leonardi, M., Zaccone, R., 2005. Dynamics of extracellular enzymatic activities in a shallow Mediterranean ecosystem (Tindari ponds, Sicily). Marine and Freshwater Research 56, 173–188

[12] Chen, W., Zhou, H., Wu, Y., Wang, J., Zhao, Z., Li, Y., Qiao, L., Chen, K., Liu, G., Xue, S., 2020. Direct and indirect influences of long-term fertilization on microbial carbon and nitrogen cycles in an alpine grassland. Soil Biology & Biochemistry 149, 107922

[13] Chen, W.Q., Zhang, Y.J., Mai, X.H., Shen, Y., 2016a. Multiple mechanisms contributed to the reduced stability of Inner Mongolia grassland ecosystem following nitrogen enrichment. Plant and Soil 409, 283–296

[14] Chen, Z.Q., Chen, Z.B., Yan, X.Y., Bai, L.Y., 2016b. Stoichiometric mechanisms of Dicranopteris dichotoma growth and resistance to nutrient limitation in the Zhuxi watershed in the red soil hilly region of China. Plant and Soil 398, 367–379

[15] Chesson, P., 2000. Mechanisms of maintenance of species diversity. Annual Review of Ecology and Systematics 31, 343–366

[16] Cleland, E.E., Chiariello, N.R., Loarie, S.R., Mooney, H.A., Field, C.B., 2006. Diverse responses of phenology to global changes in a grassland ecosystem. Proceedings of the National Academy of Sciences of the United States of America 103, 13740–13744

[17] Cui, Y.X., Fang, L.C., Deng, L., Guo, X.B., Han, F., Ju, W.L., Wang, X., Chen, H.S., Tan, W.F., Zhang, X.C., 2019. Patterns of soil microbial nutrient limitations and their roles in the variation of soil organic carbon across a precipitation gradient in an arid and semi-arid region. Science of the Total Environment 658, 1440–1451

[18] Cui, Y.X., Fang, L.C., Guo, X.B., Wang, X., Zhang, Y.J., Li, P.F., Zhang, X.C., 2018. Ecoenzymatic stoichiometry and microbial nutrient limitation in rhizosphere soil in the arid area of the northern Loess Plateau, China. Soil Biology & Biochemistry 116, 11–21

[19] Cui, Y.X., Zhang, Y.L., Duan, C.J., Wang, X., Zhang, X.C., Ju, W.L., Chen, H.S., Yue, S.C., Wang, Y.Q., Li, S.Q., Fang, L.C., 2020. Ecoenzymatic stoichiometry reveals microbial phosphorus limitation decreases the nitrogen cycling potential of soils in semi-arid agricultural ecosystems. Soil & Tillage Research 197, 10

[20] DeForest, J.L., Zak, D.R., Pregitzer, K.S., Burton, A.J., 2004. Atmospheric nitrate deposition, microbial community composition, and enzyme activity in northern hardwood forests. Soil Science Society of America Journal 68, 132–138

[21] Elser, J.J., Fagan, W.F., Denno, R.F., Dobberfuhl, D.R., Folarin, A., Huberty, A., Interlandi, S., Kilham, S.S., McCauley, E., Schulz, K.L., Siemann, E.H., Sterner, R.W., 2000. Nutritional constraints in terrestrial and freshwater food webs. Nature 408, 578–580

[22] Elser, J.J., Fagan, W.F., Kerkhoff, A.J., Swenson, N.G., Enquist, B.J., 2010. Biological stoichiometry of plant production: metabolism, scaling and ecological response to global change. New Phytologist 186, 593–608

[23] Enrique, A.G., Bruno, C., Christopher, A., Virgile, C., Steven, C., 2008. Effects of nitrogen availability on microbial activities, densities and functional diversities involved in the degradation of a Mediterranean evergreen oak litter (Quercus ilex L.). Soil Biology & Biochemistry 40, 1654–1661

[24] Fang, Y.T., Yoh, M., Koba, K., Zhu, W.X., Takebayashi, Y., Xiao, Y.H., Lei, C.Y., Mo, J.M., Zhang, W., Lu, X.K., 2011. Nitrogen deposition and forest nitrogen cycling along an urban-rural transect in southern China. Global Change Biology 17, 872–885

[25] Fu, B.J., Liu, Y., Lu, Y.H., He, C.S., Zeng, Y., Wu, B.F., 2011. Assessing the soil erosion control service of ecosystems change in the Loess Plateau of China. Ecological Complexity 8, 284–293

[26] Garcia, C., Roldan, A., Hernandez, T., 2005. Ability of different plant species to promote microbiological processes in semiarid soil. Geoderma 124, 193–202

[27] German, D.P., Weintraub, M.N., Grandy, A.S., Lauber, C.L., Rinkes, Z.L., Allison, S.D., 2011. Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biology & Biochemistry 43, 1387–1397

[28] Gonzalez, A.L., Dezerald, O., Marquet, P.A., Romero, G.Q., Srivastava, D.S., 2017. The Multidimensional Stoichiometric Niche. Frontiers in Ecology and Evolution 5, 17

[29] Gusewell, S., 2004. N: P ratios in terrestrial plants: variation and functional significance. New Phytologist 164, 243–266

[30] Han, W.X., Fang, J.Y., Guo, D.L., Zhang, Y., 2005. Leaf nitrogen and phosphorus stoichiometry across 753 terrestrial plant species in China. New Phytologist 168, 377–385

[31] Han, Y.H., Dong, S.K., Zhao, Z.Z., Sha, W., Li, S., Shen, H., Xiao, J.N., Zhang, J., Wu, X.Y., Jiang, X.M., Zhao, J.B., Liu, S.L., Dong, Q.M., Zhou, H.K., Jane, C.Y., 2019. Response of soil nutrients and stoichiometry to elevated nitrogen deposition in alpine grassland on the Qinghai-Tibetan Plateau. Geoderma 343, 263–268

[32] Hill, B.H., Elonen, C.M., Jicha, T.M., Kolka, R.K., Lehto, L.L.P., Sebestyen, S.D., Seifert-Monson, L.R., 2014. Ecoenzymatic stoichiometry and microbial processing of organic matter in northern bogs and fens reveals a common P-limitation between peatland types. Biogeochemistry 120, 203–224

[33] Jeyasingh, P.D., Weider, L.J., Sterner, R.W., 2009. Genetically-based trade-offs in response to stoichiometric food quality influence competition in a keystone aquatic herbivore. Ecology Letters 12, 1229–1237

[34] Jian, S.Y., Li, J.W., Chen, J., Wang, G.S., Mayes, M.A., Dzantor, K.E., Hui, D.F., Luo, Y.Q., 2016. Soil extracellular enzyme activities, soil carbon and nitrogen storage under nitrogen fertilization: A meta-analysis. Soil Biology & Biochemistry 101, 32–43

[35] Jones, D.L., Willett, V.B., 2006. Experimental evaluation of methods to quantify dissolved organic nitrogen (DON) and dissolved organic carbon (DOC) in soil. Soil Biology & Biochemistry 38, 991–999

[36] Kuzyakov, Y., Xu, X.L., 2013. Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytologist 198, 656–669

[37] LeBauer, D.S., Treseder, K.K., 2008. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89, 371–379

[38] Lefcheck, J.S., Byrnes, J.E.K., Isbell, F., Gamfeldt, L., Griffin, J.N., Eisenhauer, N., Hensel, M.J.S., Hector, A., Cardinale, B.J., Duffy, J.E., 2015. Biodiversity enhances ecosystem multifunctionality across trophic levels and habitats. Nature Communications 6, 6936

[39] Li, W., Wen, S.J., Hu, W.X., Du, G.Z., 2011. Root-shoot competition interactions cause diversity loss after fertilization: a field experiment in an alpine meadow on the Tibetan Plateau. Journal of Plant Ecology 4, 138–146

[40] Makino, W., Cotner, J.B., Sterner, R.W., Elser, J.J., 2003. Are bacteria more like plants or animals? Growth rate and resource dependence of bacterial C: N: P stoichiometry. Functional Ecology 17, 121–130

[41] Mao, W., Felton, A.J., Zhang, T., 2017. Linking changes to intraspecific trait diversity to community functional diversity and biomass in response to snow and nitrogen addition within an Inner Mongolian Grassland. Frontiers in Plant Science 8, 10

[42] Marklein, A.R., Houlton, B.Z., 2012. Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytologist 193, 696–704

[43] McKane, R.B., Johnson, L.C., Shaver, G.R., Nadelhoffer, K.J., Rastetter, E.B., Fry, B., Giblin, A.E., Kielland, K., Kwiatkowski, B.L., Laundre, J.A., Murray, G., 2002. Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 415, 68–71

[44] Moorhead, D.L., Sinsabaugh, R.L., Hill, B.H., Weintraub, M.N., 2016. Vector analysis of ecoenzyme activities reveal constraints on coupled C, N and P dynamics. Soil Biology & Biochemistry 93, 1–7

[45] Moreau, D., Bardgett, R.D., Finlay, R.D., Jones, D.L., Philippot, L., 2019. A plant perspective on nitrogen cycling in the rhizosphere. Functional Ecology 33, 540–552

[46] Niu, K.C., Choler, P., Zhao, B.B., Du, G.Z., 2009. The allometry of reproductive biomass in response to land use in Tibetan alpine grasslands. Functional Ecology 23, 274–283

[47] Obeso, J.R., 2002. The costs of reproduction in plants. New Phytologist 155, 321–348

[48] Olsen, S., Sommers, L., Page, A., 1982. Methods of Soil Analysis. Part 2. Chemical and Microbiological Properties of Phosphorus. ASA Monograph 9, 403–430.

[49] Peng, S.B., Buresh, R.J., Huang, J.L., Yang, J.C., Zou, Y.B., Zhong, X.H., Wang, G.H., Zhang, F.S., 2006. Strategies for overcoming low agronomic nitrogen use efficiency in irrigated rice systems in China. Field Crops Research 96, 37–47

[50] Peng, X.Q., Wang, W., 2016. Stoichiometry of soil extracellular enzyme activity along a climatic transect in temperate grasslands of northern China. Soil Biology & Biochemistry 98, 74–84

[51] Persson, J., Fink, P., Goto, A., Hood, J.M., Jonas, J., Kato, S., 2010. To be or not to be what you eat: regulation of stoichiometric homeostasis among autotrophs and heterotrophs. Oikos 119, 741–751

[52] Ru, J.Y., Zhou, Y.Q., Hui, D.F., Zheng, M.M., Wan, S.Q., 2018. Shifts of growing-season precipitation peaks decrease soil respiration in a semiarid grassland. Global Change Biology 24, 1001–1011

[53] Saiya-Cork, K.R., Sinsabaugh, R.L., Zak, D.R., 2002. The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biology & Biochemistry 34, 1309–1315

[54] Sinsabaugh, R.L., Moorhead, D.L., 1994. Resource allocation to extracellular enzyme production: A model for nitrogen and phosphorus control of litter decomposition. Soil Biology & Biochemistry 26, 1305–1311

[55] Song, L., Ba, X.M., Liu, X.J., Zhang, F.S., 2012. Impact of nitrogen addition on plant community in a semi-arid temperate steppe in China. Journal of Arid Land 4, 3–10

[56] Sterner, R.W., Elser, J.J., 2002. Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press.

[57] Tapia-Torres, Y., Elser, J.J., Souza, V., Garcia-Oliva, F., 2015. Ecoenzymatic stoichiometry at the extremes: How microbes cope in an ultra-oligotrophic desert soil. Soil Biology & Biochemistry 87, 34–42

[58] Vance, E.D., Brookes, P.C., Jenkinson, D.S., 1987. An extraction method for measuring soil microbial biomass C. Soil Biology & Biochemistry 19, 703–707

[59] Wang, C.T., Long, R.J., Wang, Q.L., Liu, W., Jing, Z.C., Zhang, L., 2010. Fertilization and litter effects on the functional group biomass, species diversity of plants, microbial biomass, and enzyme activity of two alpine meadow communities. Plant and Soil 331, 377–389

[60] Wang, G., Xue, S., Liu, F., Liu, G., 2017. Nitrogen addition increases the production and turnover of the lower-order roots but not of the higher-order roots of Bothriochloa ischaemum. Plant and Soil 415, 423–434

[61] Wang, H.Y., Wang, Z.W., Ding, R., Hou, S.L., Yang, G.J., Lu, X.T., Han, X.G., 2018. The impacts of nitrogen deposition on community N:P stoichiometry do not depend on phosphorus availability in a temperate meadow steppe. Environmental Pollution 242, 82–89

[62] Wardle, D.A., Bardgett, R.D., Klironomos, J.N., Setala, H., van der Putten, W.H., Wall, D.H., 2004. Ecological linkages between aboveground and belowground biota. Science 304, 1629–1633

[63] Wei, C.Z., Yu, Q., Bai, E., Lu, X.T., Li, Q., Xia, J.Y., Kardol, P., Liang, W.J., Wang, Z.W., Han, X.G., 2013. Nitrogen deposition weakens plant-microbe interactions in grassland ecosystems. Global Change Biology 19, 3688–3697

[64] Wu, G.L., Zhang, Z.N., Wang, D., Shi, Z.H., Zhu, Y.J., 2014. Interactions of soil water content heterogeneity and species diversity patterns in semi-arid steppes on the Loess Plateau of China. Journal of Hydrology (Amsterdam) 519, 1362–1367

[65] Xu, X., Ouyang, H., Richter, A., Wanek, W., Cao, G., Kuzyakov, Y., 2011. Spatio-temporal variations determine plant-microbe competition for inorganic nitrogen in an alpine meadow. Journal of Ecology 99, 563–571

[66] Yu, Q., Chen, Q.S., Elser, J.J., He, N.P., Wu, H.H., Zhang, G.M., Wu, J.G., Bai, Y.F., Han, X.G., 2010. Linking stoichiometric homoeostasis with ecosystem structure, functioning and stability. Ecology Letters 13, 1390–1399

[67] Yu, Q.A., Elser, J.J., He, N.P., Wu, H.H., Chen, Q.S., Zhang, G.M., Han, X.G., 2011. Stoichiometric homeostasis of vascular plants in the Inner Mongolia grassland. Oecologia 166, 1–10

[68] Zhang, J., Ai, Z., Liang, C., Wang, G., Liu, G., Xue, S., 2019. How microbes cope with short-term N addition in a Pinus tabuliformis forest-ecological stoichiometry. Geoderma 337, 630–640

Acknowledgments

This work was financially supported by Shaanxi Science Fund for Distinguished Young Scholars (2021JC-50), the National Natural Science Foundation of China (41771557), and Fundamental Research Funds for the Central Universities (2452021165). We would like to thank Editage (www.editage.cn) for English language editing.

Conflicts of interest

All the authors declare no conflicts of interest.

RIGHTS & PERMISSIONS

2021 Higher Education Press