Responses of plant diversity and soil microorganism diversity to nitrogen addition in the desert steppe, China

doi:10.1007/s40333-024-0008-0

Journal of Arid Land

2024, Vol. 16

Issue (3): 447-459 DOI: 10.1007/s40333-024-0008-0

Research article

Responses of plant diversity and soil microorganism diversity to nitrogen addition in the desert steppe, China

YE He¹^,², HONG Mei¹^,²^,^*(

), XU Xuehui¹^,², LIANG Zhiwei¹^,², JIANG Na¹^,², TU Nare¹^,², WU Zhendan¹^,²

¹College of Grassland, Resources and Environment, Inner Mongolia Agricultural University, Inner Mongolia Key Laboratory of Soil Quality and Nutrient Resources, Hohhot 010018, China
²Key Laboratory of Agricultural Ecological Security and Green Development at University of Inner Mongolia, Hohhot 010018, China

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Abstract

Nitrogen (N) deposition is a significant aspect of global change and poses a threat to terrestrial biodiversity. The impact of plant-soil microbe relationships to N deposition has recently attracted considerable attention. Soil microorganisms have been proven to provide nutrients for specific plant growth, especially in nutrient-poor desert steppe ecosystems. However, the effects of N deposition on plant-soil microbial community interactions in such ecosystems remain poorly understood. To investigate these effects, we conducted a 6-year N-addition field experiment in a Stipa breviflora Griseb. desert steppe in Inner Mongolia Autonomous Region, China. Four N treatment levels (N0, N30, N50, and N100, corresponding to 0, 30, 50, and 100 kg N/(hm²•a), respectively) were applied to simulate atmospheric N deposition. The results showed that N deposition did not significantly affect the aboveground biomass of desert steppe plants. N deposition did not significantly reduce the alfa-diversity of plant and microbial communities in the desert steppe, and low and mediate N additions (N30 and N50) had a promoting effect on them. The variation pattern of plant Shannon index was consistent with that of the soil bacterial Chao1 index. N deposition significantly affected the beta-diversity of plants and soil bacteria, but did not significantly affect fungal communities. In conclusion, N deposition led to co-evolution between desert steppe plants and soil bacterial communities, while fungal communities exhibited strong stability and did not undergo significant changes. These findings help clarify atmospheric N deposition effects on the ecological health and function of the desert steppe.

Key words： soil microorganisms plant-microbial community interaction plant diversity nitrogen deposition desert steppe

Received: 21 November 2023 Published: 31 March 2024

Corresponding Authors: *HONG Mei (E-mail: nmczhm1970@126.com)

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	YE He
	HONG Mei
	XU Xuehui
	LIANG Zhiwei
	JIANG Na
	TU Nare
	WU Zhendan

Cite this article:

YE He, HONG Mei, XU Xuehui, LIANG Zhiwei, JIANG Na, TU Nare, WU Zhendan. Responses of plant diversity and soil microorganism diversity to nitrogen addition in the desert steppe, China. Journal of Arid Land, 2024, 16(3): 447-459.

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http://jal.xjegi.com/10.1007/s40333-024-0008-0 OR http://jal.xjegi.com/Y2024/V16/I3/447

Table 1 Effects of nitrogen (N) treatments on plant biomass

Fig. 1 Biomass of plant functional group compositions (a), non-metric multidimensional scaling (NMDS) plot illustrating distances between plant community compositions (b), and plant Shannon index (c) under different N treatments. In Figure 1a, R value is the ANOSIM (analysis of similarities) statistic R, and P value is the significance from permutation; in Figure 1b, different lowercase letters within the same treatment indicate significant differences among different plant functional groups at P<0.05 level; in Figure 1c, different lowercase letters indicate significant differences among different N treatments at P<0.05 level. N0, control; N30, 30 kg N/(hm²•a); N50, 50 kg N/(hm²•a); N100, 100 kg N/(hm²•a). Bars are standard errors. The abbreviations are the same in the following figures.

Table 2 Effects of N treatments on soil physical-chemical characteristics

Fig. 2 Relative abundance of dominant bacterial phyla (a), fungal phyla (b), and non-metric multidimensional scaling (NMDS) plot illustrating distances between microbial community composition for bacteria (c) and fungi (d) under different N treatments

Fig. 3 Shannon index and Chao1 richness for soil bacterial community (a and b) and fungal community (c and d) under different N treatments. Different lowercase letters indicate significant differences among different N treatments at P<0.05 level. Bars are standard errors.

Fig. 4 Redundancy analysis (RDA) of environmental factor with bacteria (a) and fungi (b). AGB, aboveground biomass; TN, total nitrogen; SOC, soil organic carbon; C/N, soil organic carbon/total nitrogen.

Table S1 Correlation between environmental factors and dominant bacterial phyla

Table S2 Correlation between environmental factors and dominant fungal phyla

Table S3 Correlation between soil properties and plant community


[1]	Angerer J, Han G, Fujisaki I, et al. 2008. Climate change and ecosystems of Asia with emphasis on Inner Mongolia and Mongolia. Rangelands, 30(3): 46-51.

[2]	Bai Y, Wu J, Clark C M, et al. 2010. Tradeoffs and thresholds in the effects of nitrogen addition on biodiversity and ecosystem functioning: Evidence from inner Mongolia Grasslands. Global Change Biology, 16(1): 358-372. doi: 10.1111/gcb.2010.16.issue-1

[3]	Banerjee S, Schlaeppi K, van der Heijden M G A. 2018. Keystone taxa as drivers of microbiome structure and functioning. Nature Reviews Microbiology, 16: 567-576. doi: 10.1038/s41579-018-0024-1 pmid: 29789680

[4]	Bardgett R D, Mawdsley J L, Edwards S, et al. 1999. Plant species and nitrogen effects on soil biological properties of temperate upland grasslands. Functional Ecology, 13(5): 650-660. doi: 10.1046/j.1365-2435.1999.00362.x

[5]	Berg G, Smalla K. 2009. Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiology Ecology, 68(1): 1-13. doi: 10.1111/j.1574-6941.2009.00654.x pmid: 19243436

[6]	Bever J D. 2003. Soil community feedback and the coexistence of competitors: Conceptual frameworks and empirical tests. New Phytologist, 157(3): 465-473. doi: 10.1046/j.1469-8137.2003.00714.x pmid: 33873396

[7]	Bobbink R, Hicks K, Galloway J, et al. 2010. Global assessment of nitrogen deposition effects on terrestrial plant diversity: A synthesis. Ecological Applications, 20(1): 30-59. pmid: 20349829

[8]	Borer E T, Seabloom E W, Gruner D S, et al. 2014. Herbivores and nutrients control grassland plant diversity via light limitation. Nature, 508: 517-520. doi: 10.1038/nature13144

[9]	Chen S, Zhou Y, Chen Y, et al. 2018. Fastp: An ultra-fast all-in-one FASTQ preprocessor. Bioinformatics, 34(17): i884-i890. doi: 10.1093/bioinformatics/bty560

[10]	Chen W, Zhou H, Wu Y, et al. 2021. Plant-mediated effects of long-term warming on soil microorganisms on the Qinghai-Tibet Plateau. Catena, 204: 105391, doi: 10.1016/j.catena.2021.105391.

[11]	Chen Y, Li J, Ju W, et al. 2017. Quantitative assessments of water-use efficiency in Temperate Eurasian Steppe along an aridity gradient. PloS ONE, 12(7): e0179875, doi: 10.1371/journal.pone.0179875

[12]	Contosta A R, Frey S D, Cooper A B. 2015. Soil microbial communities vary as much over time as with chronic warming and nitrogen additions. Soil Biology and Biochemistry, 88: 19-24. doi: 10.1016/j.soilbio.2015.04.013

[13]	Dai Z, Su W, Chen H, et al. 2018. Long-term nitrogen fertilization decreases bacterial diversity and favors the growth of Actinobacteria and Proteobacteria in agro‐ecosystems across the globe. Global Change Biology, 24(8): 3452-3461. doi: 10.1111/gcb.2018.24.issue-8

[14]	de Vries F T, Griffiths R I, Bailey M, et al. 2018. Soil bacterial networks are less stable under drought than fungal networks. Nature Communications, 9: 3033, doi: 10.1038/s41467-018-05516-7. pmid: 30072764

[15]	Delgado-Baquerizo M, Maestre F T, Gallardo A, et al. 2013. Decoupling of soil nutrient cycles as a function of aridity in global drylands. Nature, 502: 672-676. doi: 10.1038/nature12670

[16]	Delgado-Baquerizo M, Reich P B, Trivedi C, et al. 2020. Multiple elements of soil biodiversity drive ecosystem functions across biomes. Nature Ecology & Evolution, 4: 210-220.

[17]	Dunn R M, Mikola J, Bol R, et al. 2006. Influence of microbial activity on plant-microbial competition for organic and inorganic nitrogen. Plant and Soil, 289: 321-334. doi: 10.1007/s11104-006-9142-z

[18]	Edgar R C. 2013. UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10: 996-998. doi: 10.1038/nmeth.2604 pmid: 23955772

[19]	Erisman J W, Galloway J N, Seitzinger S, et al. 2013. Consequences of human modification of the global nitrogen cycle. Philosophical Transactions of the Royal Society B: Biological Sciences, 368(1621): 0116, doi: 10.1098/rstb.2013.0116

[20]	Fan K, Delgado-Baquerizo M, Zhu Y, et al. 2020. Crop production correlates with soil multitrophic communities at the large spatial scale. Soil Biology and Biochemistry, 151: 108047, doi: 10.1016/j.soilbio.2020.108047.

[21]	Fan M, Li J, Tang Z, et al. 2020. Soil bacterial community succession during desertification in a desert steppe ecosystem. Land Degradation & Development, 31(13): 1662-1674. doi: 10.1002/ldr.v31.13

[22]	Gadgil M, Solbrig O T. 1972. The concept of r- and K-selection: Evidence from wild flowers and some theoretical considerations. The American Naturalist, 106(947): 14-31. doi: 10.1086/282748

[23]	Harpole W S, Ngai J T, Cleland E E, et al. 2011. Nutrient co-limitation of primary producer communities. Ecology Letters, 14(9): 852-862. doi: 10.1111/j.1461-0248.2011.01651.x pmid: 21749598

[24]	Harrington R A, Fownes J H, Vitousek P M. 2001. Production and resource use efficiencies in N- and P-limited tropical forests: A comparison of responses to long-term fertilization. Ecosystems, 4: 646-657. doi: 10.1007/s10021-001-0034-z

[25]	Hautier Y, Niklaus P A, Hector A. 2009. Competition for light causes plant biodiversity loss after eutrophication. Science, 324(5927): 636-638. doi: 10.1126/science.1169640 pmid: 19407202

[26]	Hautier Y, Seabloom E W, Borer E T, et al. 2014. Eutrophication weakens stabilizing effects of diversity in natural grasslands. Nature, 508: 521-525. doi: 10.1038/nature13014

[27]	Hortal S, Lozano Y M, Bastida F, et al. 2017. Plant-plant competition outcomes are modulated by plant effects on the soil bacterial community. Scientific Reports, 7: 17756, doi: 10.1038/s41598-017-18103-5. pmid: 29259319

[28]	Hu S, Chapin F S, Firestone M K, et al. 2001. Nitrogen limitation of microbial decomposition in a grassland under elevated CO₂. Nature, 409: 188-191. doi: 10.1038/35051576

[29]	Huang J, Xu Y, Yu H, et al. 2021. Soil prokaryotic community shows no response to 2 years of simulated nitrogen deposition in an arid ecosystem in northwestern China. Environmental Microbiology, 23(2): 1222-1237. doi: 10.1111/emi.v23.2

[30]	Kardol P, Cornips N J, van Kempen M M L. et al. 2007. Microbe-mediated plant-soil feedback causes historical contingency effects in plant community assembly. Ecological Monographs, 77(2): 147-162. doi: 10.1890/06-0502

[31]	Keymer D P, Lankau R A. 2017. Disruption of plant-soil-microbial relationships influences plant growth. Journal of Ecology, 105(3): 816-827. doi: 10.1111/jec.2017.105.issue-3

[32]	Lau J A, Lennon J T. 2011. Evolutionary ecology of plant-microbe interactions: Soil microbial structure alters selection on plant traits. New Phytologist, 192(1): 215-224. doi: 10.1111/j.1469-8137.2011.03790.x pmid: 21658184

[33]	Li H, Xu Z, Yan Q, et al. 2018. Soil microbial beta-diversity is linked with compositional variation in aboveground plant biomass in a semi-arid grassland. Plant and Soil, 423: 465-480. doi: 10.1007/s11104-017-3524-2

[34]	Liu X, Zhang Y, Han W, et al. 2013. Enhanced nitrogen deposition over China. Nature, 494: 459-462. doi: 10.1038/nature11917

[35]	Ma Q, Liu X, Li Y, et al. 2020. Nitrogen deposition magnifies the sensitivity of desert steppe plant communities to large changes in precipitation. Journal of Ecology, 108(2): 598-610. doi: 10.1111/jec.v108.2

[36]	Magoc T, Salzberg S L. 2011. FLASH: Fast length adjustment of short reads to improve genome assemblies. Bioinformatics, 27(21): 2957-2963. doi: 10.1093/bioinformatics/btr507 pmid: 21903629

[37]	McHugh T A, Morrissey E M, Mueller R C, et al. 2017. Bacterial, fungal, and plant communities exhibit no biomass or compositional response to two years of simulated nitrogen deposition in a semiarid grassland. Environmental Microbiology, 19(4): 1600-1611. doi: 10.1111/1462-2920.13678 pmid: 28120480

[38]	Panke-Buisse K, Poole A C, Goodrich J K, et al. 2015. Selection on soil microbiomes reveals reproducible impacts on plant function. The ISME Journal, 9: 980-989. doi: 10.1038/ismej.2014.196

[39]	Payne R J, Dise N B, Field C D, et al. 2017. Nitrogen deposition and plant biodiversity: past, present, and future. Frontiers in Ecology and the Environment, 15(8): 431-436. doi: 10.1002/fee.2017.15.issue-8

[40]	Peng Y, Chen H Y H, Yang Y. 2020. Global pattern and drivers of nitrogen saturation threshold of grassland productivity. Functional Ecology, 34(9): 1979-1990. doi: 10.1111/fec.v34.9

[41]	Ramirez K S, Craine J M, Fierer N. 2012. Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes. Global Change Biology, 18(6): 1918-1927. doi: 10.1111/gcb.2012.18.issue-6

[42]	Reynolds H L, Packer A, Bever J D. et al. 2003. Grassroots ecology: Plant-microbe-soil interactions as drivers of plant community structure and dynamics. Ecology, 84(9): 2281-2291. doi: 10.1890/02-0298

[43]	Schlatter D C, Bakker M G, Bradeen J M, et al. 2015. Plant community richness and microbial interactions structure bacterial communities in soil. Ecology, 96(1): 134-142. pmid: 26236898

[44]	Sha M, Xu J, Zheng Z, et al. 2021. Enhanced atmospheric nitrogen deposition triggered little change in soil microbial diversity and structure in a desert ecosystem. Global Ecology and Conservation, 31: e01879, doi: 10.1016/j.gecco.2021.e01879.

[45]	Shao Y, Liu T, Eisenhauer N, et al. 2018. Plants mitigate detrimental nitrogen deposition effects on soil biodiversity. Soil Biology and Biochemistry, 127: 178-186. doi: 10.1016/j.soilbio.2018.09.022

[46]	Stackebrandt E, Goebel B M. 1994. Taxonomic note: A place for DNA-DNA reassociation and 16s rRNA sequence analysis in the present species definition in bacteriology. International Journal of Systematic and Evolutionary Microbiology, 44: 846-849. doi: 10.1099/00207713-44-4-846

[47]	Stevens C J, Dise N B, Mountford J O, et al. 2004. Impact of nitrogen deposition on the species richness of grasslands. Science, 303(5665): 1876-1879. pmid: 15031507

[48]	Su J, Li X R, Li X J, et al. 2013. Effects of additional N on herbaceous species of desertified steppe in arid regions of China: A four-year field study. Ecological Research, 28: 21-28. doi: 10.1007/s11284-012-0994-9

[49]	Tang Z, Deng L, An H, et al. 2017. The effect of nitrogen addition on community structure and productivity in grasslands: A meta-analysis. Ecological Engineering, 99: 31-38. doi: 10.1016/j.ecoleng.2016.11.039

[50]	Treseder K K. 2008. Nitrogen additions and microbial biomass: A meta-analysis of ecosystem studies. Ecology Letters, 11: 1111-1120. doi: 10.1111/j.1461-0248.2008.01230.x pmid: 18673384

[51]	van der Putten W H. 2017. Belowground drivers of plant diversity. Science, 355(6321): 134-135. doi: 10.1126/science.aal4549 pmid: 28082548

[52]	Wang Q, Garrity G M, Tiedje J M, et al. 2007. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73(16): 5261-5267. doi: 10.1128/AEM.00062-07

[53]	Wang X, Feng J, Ao G, et al. 2023. Globally nitrogen addition alters soil microbial community structure, but has minor effects on soil microbial diversity and richness. Soil Biology and Biochemistry, 179: 108982, doi: 10.1016/j.soilbio.2023.108982.

[54]	Wang Z, Na R, Koziol L, et al. 2020. Response of bacterial communities and plant-mediated soil processes to nitrogen deposition and precipitation in a desert steppe. Plant and Soil, 448: 277-297. doi: 10.1007/s11104-020-04424-4

[55]	Wu Q, Ren H, Bisseling T, et al. 2021. Long-term warming and nitrogen addition have contrasting effects on ecosystem carbon exchange in a desert steppe. Environmental Science & Technology, 55: 7256-7265. doi: 10.1021/acs.est.0c06526

[56]	Yang X, Huang Z, Dong M, et al. 2019. Responses of community structure and diversity to nitrogen deposition and rainfall addition in contrasting steppes are ecosystem-dependent and dwarfed by year-to-year community dynamics. Annals of Botany, 124(3): 461-469. doi: 10.1093/aob/mcz098 pmid: 31161191

[57]	Yu G, Jia Y, He N, et al. 2019. Stabilization of atmospheric nitrogen deposition in China over the past decade. Nature Geoscience, 12: 424-429. doi: 10.1038/s41561-019-0352-4

[58]	Zha T G. 1997. Soil Physiochemical Analysis. Beijing: China Forestry Publishing House. (in Chinese)

[59]	Zhang T, Chen H Y H, Ruan H. 2018. Global negative effects of nitrogen deposition on soil microbes. The ISME Journal, 12: 1817-1825. doi: 10.1038/s41396-018-0096-y

[60]	Zilber-Rosenberg I, Rosenberg E. 2008. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiology Reviews, 32(5): 723-735. doi: 10.1111/j.1574-6976.2008.00123.x pmid: 18549407

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