Skip to main content

Advertisement

Log in

Interactive effects of nitrogen fertilizer and altered precipitation on fungal communities in arid grasslands of northern China

  • Soils, Sec 2 • Global Change, Environ Risk Assess, Sustainable Land Use • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

Fungi play an essential role in regulating the functioning of terrestrial ecosystems and are sensitive to climate change factors. Climate change incidents, such as N deposition and altered precipitation, create abiotic stress regarding the water use efficiency of soil and nutrient limitation impacting the activity of soil fungi. This study aimed to examine the combined effects of N fertilization and altered precipitation on soil fungal diversity and composition in the desert steppe.

Materials and methods

In the present study, we carried out a field experiment to assess the soil fungal diversity and composition of the desert steppe in response to N fertilizer (0 or 35 kg N ha−1 year−1) and precipitation changes (control, − 50% precipitation, or + 50% precipitation) in the desert steppe. The study was initiated in 2012, and plant and soil samples were collected after 5 years (August, 2017) of field treatments. High-throughput sequencing was applied to estimate the fungal diversity and composition.

Results and discussion

The soil fungal communities were dominated by Ascomycota (87.85% ± 1.26%), which primarily drove the fungal community composition. Decreased precipitation promoted strong shifts in fungal community composition under both N fertilizer levels. Increased precipitation significantly reduced Shannon-Wiener indices by 9.96%. The increasing relative abundances of fungal functional groups (lichenized saprotroph, animaland plant pathogens) resulted in a marked shift in fungal community composition from decreased precipitation to increased precipitation, which is attributed to the important role of the Ascomycota phylum in fungal communities. Structural equation modeling (SEM) indicated that C4 biomass was the predominant factor determining the Shannon-Wiener index for these fungi. Direct altered precipitation, indirect soil pH, and C4 biomass together controlled soil fungal community composition, with altered precipitation as the main driver.

Conclusions

The interactive effects of N fertilizer and altered precipitation on grassland plant density, biomass, and soil properties may play an essential role in determining fungal diversity and community composition. Precipitation is a primary limiting factor that influences fungal community composition. Effects of N fertilizer on soil fungal community composition are highly dependent on changes in precipitation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402

    CAS  Google Scholar 

  • Augé RM (2001) Water relations, drought and vesicular–arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42

    Google Scholar 

  • Bai YF, Wu JG, Xing Q, Pan QM, Huang JH, Yang DL, Han XG (2008) Primary production and rain use efficiency across a precipitation gradient on the Mongolia plateau. Ecology 89:2140–2153

    Google Scholar 

  • Bardgett RD, Bowman WD, Kaufmann R, Schmidt SK (2005) A temporal approach to linking aboveground and belowground ecology. Trends Ecol Evol 20:634–641

    Google Scholar 

  • Bunn RA, Ramsey PW, Lekberg Y (2015) Do native and invasive plants differ in their interactions with arbuscular mycorrhizal fungi? A meta-analysis. Aust J Ecol 103:1547–1566

    CAS  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336

    CAS  Google Scholar 

  • Cassman NA, Leite MFA, Pan Y, de Hollander M, van Veen JA, Kuramae EE (2016) Plant and soil fungal but not soil bacterial communities are linked in long-term fertilized grassland. Sci Rep 6:23680. https://doi.org/10.1038/srep23680

    Article  CAS  Google Scholar 

  • Chapin FS, Walker LR, Fastie CL, Sharman LC (1994) Mechanisms of primary succession following deglaciation at glacier bay, Alaska. Ecol Monogr 64:149–175

    Google Scholar 

  • Chen C, Chen HYH, Chen X, Huang Z (2019) Meta-analysis shows positive effects of plant diversity on microbial biomass and respiration. Nat Commun 10:1332. https://doi.org/10.1038/s41467-019-09258-y

    Article  CAS  Google Scholar 

  • Chen H, Jiang W (2014) Application of high-throughput sequencing in understanding human oral microbiome related with health and disease. Front Microbiol 5:6

    Google Scholar 

  • Chen YL, Xu TL, Veresoglou SD, Hu HW, Hao ZP, Hu YJ, Liu L, Deng Y, Rillig MC, Chen BD (2017a) Plant diversity represents the prevalent determinant of soil fungal community structure across temperate grasslands in northern China. Soil Biol Biochem 110:12–21

    CAS  Google Scholar 

  • Chen YL, Xu ZW, Xu TL, Veresoglou SD, Yang GW, Chen BD (2017b) Nitrogen deposition and precipitation induced phylogenetic clustering of arbuscular mycorrhizal fungal communities. Soil Biol Biochem 115:233–242

    CAS  Google Scholar 

  • Chen WQ, Xu Y, Chen J, Yuan X, Zhou L, Tan T, Zhang Y, Hu T (2018) Consistent responses of surface- and subsurface soil fungal diversity to N enrichment are mediated differently by acidification and plant community in a semi-arid grassland. Soil Biol Biochem 127:110–119

    CAS  Google Scholar 

  • Clemmensen KE, Finlay RD, Dahlberg A, Stenlid J, Wardle DA, Lindahl BD (2015) Carbon sequestration is related to mycorrhizal fungal community shifts during long-term succession in boreal forests. New Phytol 205:1525–1536

    CAS  Google Scholar 

  • Cline LC, Hobbie SE, Madritch MD, Buyaski C, Tilman D, Cavender-Bares JM (2018) Resource availability underlies the plant-fungal diversity relationship in a grassland ecosystem. Ecology 99(1):204–216

    Google Scholar 

  • Contosta AR, Frey SD, Cooper AB (2015) Soil microbial communities vary as much over time as with chronic warming and nitrogen additions. Soil Biol Biochem 88:19–24

    CAS  Google Scholar 

  • Craine JM, Reich PB, Tilman DG, Ellsworth D, Fargione J, Knops J, Naeem S (2003) The role of plant species in biomass production and response to elevated CO2 and N. Ecol Lett 6:623–625

    Google Scholar 

  • DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72(7):5069–5072

    CAS  Google Scholar 

  • Dostálek T, Pánková H, Münzbergová Z, Rydlová J (2013) The effect of AMF suppression on plant species composition in a nutrient-poor dry grassland. PLoS One 8(11):e80535

    Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461

    CAS  Google Scholar 

  • Eisenhauer N, Cesarz S, Koller R, Worm K, Reich PB (2012) Global change belowground: impacts of elevated CO2, nitrogen, and summer drought on soil food webs and biodiversity. Glob Chang Biol 18:435–447

    Google Scholar 

  • Fierer N, Lauber CL, Ramirez KS, Zaneveld J, Bradford MA, Knight R (2012) Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J l6:1007–1017

    Google Scholar 

  • Fornara DA, Tilman D (2008) Plant functional composition influences rates of soil carbon and nitrogen accumulation. Aust J Ecol 96:314–322

    CAS  Google Scholar 

  • Fornara DA, Tilman D, Hobbie SE (2009) Linkages between plant functional composition, fine root processes and potential soil N mineralization rates. Aust J Ecol 97:48–56

    CAS  Google Scholar 

  • Gill SR, Pop M, DeBoy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, Gordon JI, Relman DA, Fraser-Liggett CM, Nelson KE (2006) Metagenomic analysis of the human distal gut microbiome. Science 312(5778):1355–1359

    CAS  Google Scholar 

  • Hawkes CV, Kivlin SN, Rocca JD, Huguet V, Thomsen MA, Suttle KB (2011) Fungal community responses to precipitation. Glob Chang Biol 17:1637–1645

    Google Scholar 

  • Hooper DU, Vitousek PM (1997) The effects of plant composition and diversity on ecosystem processes. Science 277:1302–1305

    CAS  Google Scholar 

  • Jia M, Liu C, Li Y, Xu S, Han G, Huang J, Jin B, Zou Y, Zhang G (2017) Response of fungal composition and diversity to simulated nitrogen deposition and manipulation of precipitation in soils of an Inner Mongolia desert steppe of northern China. Can J Soil Sci 97(4):613–625

    CAS  Google Scholar 

  • Jumpponen A, Jones KL (2014) Tallgrass prairie soil fungal communities are resilient to climate change. Fungal Ecol 10:44–57

    Google Scholar 

  • Leff JW, Jones SE, Prober SM, Barberán A, Borer ET, Firn JL, Harpole WS, Hobbie SE, Hofmockel KS, Knops JMH, McCulley RL, La Pierre K, Risch AC, Seabloom EW, Schütz M, Steenbock C, Stevens CJ, Fierer N (2015) Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proc Natl Acad Sci U S A 112:10967–10972

    CAS  Google Scholar 

  • Li GL, Kim SJ, Han SH, Chang HN, Du D, Son Y (2018) Precipitation affects soil microbial and extracellular enzymatic responses to warming. Soil Biol Biochem 120:212–221

    CAS  Google Scholar 

  • Lin G, McCormack ML, Guo D (2015) Arbuscular mycorrhizal fungal effects on plant competition and community structure. J Ecol 103:1224–1232

    CAS  Google Scholar 

  • Lozupone CA, Hamady M, Kelley ST, Knight R (2007) Quantitative and qualitative beta diversity measures lead to different insights into factors that structure microbial communities. Appl Environ Microbiol 73(5):1576–1585

    CAS  Google Scholar 

  • Ma H, Bai G, Sun Y, Kostenko O, Zhu X, Lin S, Ruan W, Zhao N, Bezemer TM (2016) Opposing effects of nitrogen and water addition on soil bacterial and fungal communities in the Inner Mongolia Steppe: a field experiment. Appl Soil Ecol 108:128–135

    Google Scholar 

  • Magoc T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21):2957–2963

    CAS  Google Scholar 

  • Manzoni S, Schimel JP, Porporato A (2012) Responses of soil microbial communities to water stress: results from a meta-analysis. Ecology 93:930–938

    Google Scholar 

  • McHugh TA, Morrissey EM, Mueller RC, Gallego-Graves LV, Kuske CR, Reed SC (2017) Bacterial, fungal, and plant communities exhibit no response to two years of simulated nitrogen deposition in a semiarid grassland. Environ Microbiol 19(4):1600–1611

    CAS  Google Scholar 

  • Mueller RC, Belnap J, Kuske CR (2015) Soil bacterial and fungal community responses to nitrogen addition across soil depth and microhabitat in an arid shrubland. Front Microbiol 6:891

    Google Scholar 

  • Nelson D, Sommers LE (1980) Total nitrogen analysis for soil and plant tissues. J Assoc Off Anal Chem 63:770–778

    CAS  Google Scholar 

  • Nelson D, Sommers LE (1982) Total carbon, organic carbon and organic matter. In: Page AL (ed) Methods of Soil Analysis. Part 2: Chemical and Microbiological Properties, Madison

    Google Scholar 

  • Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20(1):241–248

    Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Wagner H (2013) Vegan: community ecology package. R package version 2.0-10. http://CRAN.Rproject.org/package=vegan

  • Rashid MI, Mujawar LH, Shahzad T, Almeelbi T, Ismail IMI, Oves M (2016) Bacteria and fungi can contribute to nutrients bioavailability and aggregate formation in degraded soils. Microbiol Res 183:26–41

    CAS  Google Scholar 

  • Sage RF, Pearcy RW (1987) The nitrogen use efficiency of C3 and C4 plants. Plant Physiol 84:954–958

    CAS  Google Scholar 

  • Schmidt PA, Schmitt I, Otte J, Bandow C, Römbke J, Bálint M, Rolshausen G (2018) Season-long experimental drought alters fungal community composition but not diversity in a grassland soil. Microb Ecol 75:468–478

    Google Scholar 

  • Skopp J, Jawson MD, Doran JW (1990) Steady-state aerobic microbial activity as a function of soil water content. Soil Sci Soc Am J 54:1619–1625

    Google Scholar 

  • Spehn EM, Josh J, Schmid B, Diemer M, Korner C (2000) Above-ground resource use increases with plant species richness in experimental grassland ecosystems. Funct Ecol 14:326–337

    Google Scholar 

  • Sterkenburg E, Bahr A, Durling MB, Clemmensen KE, Lindal B (2015) Changes in fungal communities along a boreal forest soil fertility gradient. New Phytol 207:1145–1158

    Google Scholar 

  • Stursova M, Crenshaw CL, Sinsabaugh RL (2006) Microbial responses to long-term N deposition in a semiarid grassland. Microb Ecol 51:90–98

    Google Scholar 

  • Su YG, Huang G, Lin YJ, Zhang YM (2016) No synergistic effects of water and nitrogen addition on soil microbial communities and soil respiration in a temperate desert. Catena 142:126–133

    CAS  Google Scholar 

  • Tedersoo L, Bahram M, Cajthaml T, Polme S, Hiiesalu I, Anslan S, Harend H, Buegger F, Pritsch K, Koricheva J (2016) Tree diversity and species identity effects on soil fungi, protists and animals are context dependent. ISME J 10:346–362

    CAS  Google Scholar 

  • Team RC (2016) R: a language and environment for statistical computing. R Development Core Team, Vienna

    Google Scholar 

  • Tian Q, Liu N, Bai W, Li L, Chen J, Reich PB, Yu Q, Guo D, Smith MD, Knapp AP, Cheng WX, Lu P, Gao Y, Yang A, Wang T, Li X, Wang ZW, Ma Y, Han X, Zhang W (2016) A novel soil manganese mechanism drives plant species loss with increased nitrogen deposition in a temperate steppe. Ecology 97(1):65–74

    Google Scholar 

  • Voriskova J, Baldrian P (2013) Fungal community on decomposing leaf litter undergoes rapid successional changes. ISME J 7:477–486

    CAS  Google Scholar 

  • Yang H, Wu M, Liu W, Zhang Z, Zhang N, Wang S (2011) Community structure and composition in response to climate change in a temperate steppe. Glob Chang Biol 17:452–465

    Google Scholar 

  • Wang Z, Li Y, Hao X, Zhao M, Han G (2015) Responses of plant community coverage to simulated warming and nitrogen addition in a desert steppe in Northern China. Ecol Res 30:605–614

    CAS  Google Scholar 

  • Zhang H, Wang L, Liu H, Zhao J, Li G, Wang H, Lai X, Li J, Xiu W, Yang D (2018a) Nitrogen deposition combined with elevated precipitation is conducive to maintaining the stability of the soil fungal diversity on the Stipa baicalensis steppe. Soil Biol Biochem 117:135–138

    CAS  Google Scholar 

  • Zhang T, Chen HYH, Ruan H (2018b) Global negative effects of nitrogen deposition on soil microbes. ISME J 12:1817–1825

    CAS  Google Scholar 

  • Zhang K, Shi Y, Jing X, He J-S, Sun R, Yang Y, Shade A, Chu H (2016a) Effects of short-term warming and altered precipitation on soil microbial communities in Alpine Grassland of the Tibetan Plateau. Front Microbiol 7:1032

    Google Scholar 

  • Zhang L, Xu M, Liu Y, Zhang F, Hodge A, Feng G (2016b) Carbon and phosphorus exchange may enable cooperation between an arbuscular mycorrhizal fungus and a phosphate-solubilizing bacterium. New Phytol 210:1022–1032

    CAS  Google Scholar 

  • Zhang NL, Wan SQ, Guo JX, Han GD, Gutknecht J, Schmid B, Yu L, Liu WX, Bi J, Wang Z, Ma KP (2015) Precipitation modifies the effects of warming and nitrogen addition on soil microbial communities in northern Chinese grasslands. Soil Biol Biochem 89:12–23

    CAS  Google Scholar 

  • Zhou J, Jiang X, Zhou B, Zhao B, Ma M, Guan D, Li J, Chen S, Cao F, Shen D, Qin J (2016) Thirty four years of nitrogen fertilization decreases fungal diversity and alters fungal community composition in black soil in northeast China. Soil Biol Biochem 95:135–143

    CAS  Google Scholar 

Download references

Acknowledgments

The study was carried out at Sunite Right Banner Desert Experiment and Research Station, Institute of Grassland Research, Chinese Academy of Agricultural Sciences, The authors thank Xiangjun Yun, Shixian Sun and Lei Ji for helping set up the experiment and the soil respiration field measurements.

Funding

This study was financially supported by the National Natural Science Foundation of China (Grant nos. 41601269 and 31770542), the Natural Science Foundation of Inner Mongolia, China (2019MS03001), the National Natural Science Foundation of China and USA (Grant nos. 31761123001-1), and Central Public-Interest Scientific Institution Basal Research Fund (Grant nos. 1610332018006, 1610332015020 and 1610332016006).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhen Wang.

Additional information

Responsible editor: Terrence H. Bell

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, H., Ta, N., Jin, K. et al. Interactive effects of nitrogen fertilizer and altered precipitation on fungal communities in arid grasslands of northern China. J Soils Sediments 20, 1344–1356 (2020). https://doi.org/10.1007/s11368-019-02512-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-019-02512-2

Keywords

Navigation