Abstract
Background and aims
Grazing pressure can degrade environmental quality and disrupt ecosystem structure and functions, while its potential effect on the soil microbiome is unclear.
Method
We evaluated the effects of grazing intensity (CK: no grazing, LG: light grazing, MG: moderate grazing, HG: heavy grazing, and OG: overgrazing) on soil microbial diversity and community composition in a desert steppe.
Results
Different microbial communities were found under different grazing intensities, resulting from differences in soil moisture, nutrients and plant species. Alpha-diversity in the bacterial community was strongly correlated with soil organic content (SOC) and soil water content, while the alpha-diversity of the fungi depended on the SOC and pH of the soil. Grazing treatments LG, HG and OG caused strong shifts in bacterial and fungal community composition. Heavy grazing (HG and OG) significantly increased the relative abundances of Chloroflexi, Gemmatimonadetes, and Firmicutes bacteria, while light grazing (LG) significantly decreased the relative abundance of Actinobacteria. Grazing intensities HG and OG increased the relative abundances of certain fungi (e.g., Ascomycota). Co-occurrence network analysis indicated that bacterial communities had a more complex network than fungal communities. A multivariate regression tree demonstrated that the bacterial community responded to grazing via changes in the biomass of perennial plant species and SOC, whereas the SOC and pH value altered the fungal community composition.
Conclusions
Our findings indicate that different grazing intensities can initiate different changes in the soil microbiome; sustainable grazing intensity over decades facilitates the recovery of primary productivity and ecosystem functions in a desert steppe.
Similar content being viewed by others
References
Augustine DJ, Derner JD, Milchunas D, Blumenthal D, Porensky LM (2017) Grazing moderates increases in C3 grass abundance over seven decades across a soil texture gradient in shortgrass steppe. J. Veg. Sci. 28:562–572
Averill C, Turner BL, Finzi AC (2014) Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505:543–545
Bai YF, Wu JG, Clark CM, Pan QM, Zhang LX, Chen SP, Wang QB, Han XG (2012) Grazing alters ecosystem functioning and C:N:P stoichiometry of grasslands along a regional precipitation gradient. Journal of Applied Ecology 49: 1204-1215.
Banerjee S, Walder F, Büchi L, Meyer M, Held AY, Gattinger A, Keller T, Charles R, van der Heijden MGA (2019) Agricultural intensification reduces microbial network complexity and the abundance of keystone taxa in roots. The ISME Journal 13:1722–1736
Bardgett RD, van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature 515:505–511
Bellemain E, Carlsen T, Brochmann C, Coissac E, Taberlet P, Kauserud H (2010) ITS as an environmental DNA barcode for fungi: an in silico approach reveals potential PCR biases. BMC Microbiol. 10:189. https://doi.org/10.1186/1471-2180-10-189
Bergmann GT, Bates TB, Eilers KG, Lauber CL, Gregory Caporaso J, Walters WA, Knight R, Fierer N (2011) The under-recognized dominance of Verrucomicrobia in soil bacterial communities. Soil Biol. Biochem. 43:1450–1455
Berry D, Widder S (2014) Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Front. Microbiol. 5:219
Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R et al (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat. Methods 10:57–59. https://doi.org/10.1038/nmeth.2276
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7:335–336
Chen Y, Xu T, Veresoglou SD, Hu H, Hao Z, Hu Y, Liu L, Deng Y, Rillig MC, Chen B (2017) Plant diversity represents the prevalent determinant of soil fungal community structure across temperate grasslands in northern China. Soil Biol. Biochem. 110:12–21
Crowther TW et al (2019) The global soil community and its influence on biogeochemistry. Science (80) 365:eaav0550
De’ Ath G (2002) Multivariate regression trees: a new technique for modeling species environment relationships. Ecology 83:1105–1117
Deforest JL (2009) The influence of time, storage temperature, and substrate age on potential soil enzyme activity in acidic forest soils using MUB-linked substrates and l -DOPA. Soil Biol. Biochem. 41(6):1180–1186
Dong WY, Liu EK, Yan CR, Tian J, Zhang HH, Zhang YQ (2017) Impact of no tillage vs. conventional tillage on the soil bacterial community structure in a winter wheat cropping succession in northern China. Eu J Soil Biol 80:35–42
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10(10):996–998. https://doi.org/10.1038/nmeth.2604
Egelkraut D, Kardol P, De Long JR, Olofsson J (2017) The role of plant-soil feedbacks in stabilizing a reindeer-induced vegetation shift in subarctic tundra. Functional Ecology 32:1–13
Eldridge DJ, Delgado-Baquerizo M, Travers SK, Val J, Oliver I, Hamonts K et al (2017) Competition drives the response of soil microbial diversity to increased grazing by vertebrate herbivores. Ecology 98:1922–1931
Fan L, Jin H, Zhang C, Zheng J, Zhang J, Han G (2021) Grazing intensity induced alternations of soil microbial community composition in aggregates drive soil organic carbon turnover in a desert steppe. Agriculture, Ecosystems and Environment 313:107387. https://doi.org/10.1016/j.agee.2021.107387
Ferrari B et al (2016) Geological connectivity drives microbial community structure and connectivity in polar, terrestrial ecosystems. Environmental Microbiology 18:1834–1849
German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD (2011) Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol. Biochem. 43:1387–1397
Goodfellow M, Williams ST (1983) Ecology of actinomycetes. Annu Rev Microbiol 37:189–216
Han GD, Biligetu GAD (2004) Comparison study on selective intake behavior of sheep at different stocking rates in Stipa breviflora desert steppe. Pratacultural Science 21:95–98 [In Chinese]
Hille Ris Lambers R, Rietkerk M, van den Bosch F, Prins HHT, de Kroon H (2001) Vegetation pattern formation in semi-arid grazing systems. Ecology 82:50–61
Hu Z, Li S, Guo Q, Niu S, He N, Li L et al (2016) A synthesis of the effect of grazing exclusion on carbon dynamics in grasslands in China. Glob. Change Biol. 22:1385–1393
Huhe CX, Hou F, Wu Y, Cheng Y (2017) Bacterial and Fungal Community Structures in Loess Plateau Grasslands with Different Grazing Intensities. Front. Microbiol. 8:606. https://doi.org/10.3389/fmicb.2017.00606
Kettler TA, Doran JW, Gilbert TL (2001) Simplified Method for Soil Particle-Size Determination to Accompany Soil-Quality Analyses. Soil Sci. Soc. Am. J. 65:849–852
Kivlin SN, Treseder KK (2014) Soil extracellular enzyme activities correspond with abiotic factors more than fungal community composition. Biogeochemistry 117(1):23–37
Kohler F, Hamelin J, Gillet F, Gobat JM, Buttler A (2005) Soil microbial community changes in wooded mountain pastures due to simulated effects of cattle grazing. Plant Soil 278:327–340
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. USA 112(35):10967–10972
Li SG, Harazono Y, Oikawa T, Zhao HL, He ZY, Chang XL (2000) Grassland desertification by grazing and the resulting micrometeorological changes in Inner Mongolia. Agric. Meteorol. 102(2–3):125–137
Li W, Huang HZ, Zhang Z, Wu GL (2011) Effects of grazing on the soil properties and C and N storage in relation to biomass allocation in an alpine meadow. J. Soil Sci. Plant Nutr. 11:27–39
Li Y, Li T, Zhao DQ, Wang ZT, Liao YC (2021) Different tillage practices change assembly, composition, and co-occurrence patterns of wheat rhizosphere diazotrophs. Sci Total Environ 766:1–11
Liu S, Wawrik B, Liu Z (2017) Different Bacterial Communities Involved in Peptide Decomposition between Normoxic and Hypoxic Coastal Waters. Front. Microbiol. 8:353. https://doi.org/10.3389/fmicb.2017.00353
Lü XT, Freschet GT, Kazakou E, Wang ZW, Zhou LS, Han XG (2015) Contrasting responses in leaf nutrient-use strategies of two dominant grass species along a 30-yr temperate steppe grazing exclusion chronosequence. Plant Soil 387:69–79
Lü XT, Reed S, Yu Q, He N, Wang Z, Han XG (2013) Convergent responses of nitrogen and phosphorus resorption to nitrogen inputs in a semiarid grassland. Glob. Change Biol. 19:2775–2784
Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics. 27(21):2957–2963. https://doi.org/10.1093/bioinformatics/btr507
Martensson LM, Olsson PA (2012) Reductions in microbial biomass along disturbance gradients in a semi-natural grassland. Applied Soil Ecology 62:8–13
McNaughton SJ (1979) Grazing as an optimization process: grass ungulate relationships in the Serengeti. American Naturalist 113:691–703
Morgan JA, Pataki DE, Körner C, Clark H, Del Grosso SJ, Grünzweig JM, Knapp AK, Mosier AR, Newton PCD, Niklaus PA, Nippert JB, Nowak RS, Parton WJ, Polley HW, Shaw MR (2004) Water relations in grassland and desert ecosystems exposed to elevated atmospheric CO2. Oecologia 140(1):11–25
Mueller P, Granse D, Nolte S, Do HT, Weingartner M, Hoth S et al (2017) Topdown control of carbon sequestration: grazing affects microbial structure and function in salt marsh soils. Ecol. Appl. 27:1435–1450
Munoz-Martin MA, Becerra-Absalon I, Perona E, Fernandez-Valbuena L, Garcia Pichel F, Mateo P (2019) Cyanobacterial biocrust diversity in Mediterranean ecosystems along a latitudinal and climatic gradient. New Phytologist 221:123–141
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
Panayiotou E, Dimou M, Monokrousos N (2017) The effects of grazing intensity on soil processes in a Mediterranean protected area. Environ Monit Assess 189:441. https://doi.org/10.1007/s10661-017-6161-6
Reshef DN, Reshef YA, Finucane HK, Grossman SR, McVean G, Turnbaugh PJ et al (2011) Detecting novel associations in large data sets. Science 334:1518–1524
Rossignol N, Bonis A, Bouzillé JB (2006) Consequence of grazing pattern and vegetation structure on the spatial variations of net N mineralization in a wet grassland. Applied Soil Ecology 31:62–70
Rousk J, Bååth E (2011) Growth of saprotrophic fungi and bacteria in soil. FEMS Microbiology Ecology 78:17–30
Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol. Biochem. 34:1309–1315
Santos-Medellín C, Edwards J, Liechty Z, Nguyen B, Sundaresan V (2017) Drought stress results in a compartment-specific restructuring of the rice root-associated microbiomes. mBio 8:e00764–e00717. https://doi.org/10.1128/mBio.00764-17
Schönbach P, Wan H, Gierus M, Bai Y, Müller K, Lin L, Susenbeth A, Taube F (2011) Grassland responses to grazing: effects of grazing intensity and management system in an Inner Mongolian steppe ecosystem. Plant Soil 340:103–115
Sengupta A, Dick WA (2015) Bacterial community diversity in soil under two tillage practices as determined by pyrosequencing. Microb Ecol 70:853–859
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D et al (2003) Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks. Genome Res. 13:2498–2504
Siciliano SD et al (2014) Soil fertility is associated with fungal and bacterial richness, whereas pH is associated with community composition in polar soil microbial communities. Soil Biol. Biochem. 78:10–20
Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB, Hobbie SE, Holland K, Keeler BL, Powers JS, Stursova M, Takacs-Vesbach C, Waldrop MP, Wallenstein MD et al (2008) Stoichiometry of soil enzyme activity at global scale. Ecol. Lett. 11(11):1252–1264
Stackebrandt E, Goebel BM (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 Bacteriology 44(4):846–849
Sterkenburg E, Bahr A, Durling MB, Clemmensen KE, Lindal B (2015) Changes in fungal communities along a boreal forest soil fertility gradient. New Phytologist 207:1145e1158
Su YZ, Li YL, Cui HY, Zhao WZ (2005) Influences of continuous grazing and livestock exclusion on soil properties in a degraded sandy grassland, Inner Mongolia, northern China. Catena 59:267–278
Treweek G, Di HJ, Cameron KC, Podolyan A (2016) Simulated animal trampling of a free-draining stony soil stimulated denitrifier growth and increased nitrous oxide emissions. Soil Use and Management 32:455–464
Wang L, Gan Y, Wiesmeier M, Zhao G, Zhang R, Han G et al (2018) Grazing exclusion—an effective approach for naturally restoring degraded grasslands in Northern China. Land. Degrad. Dev. 29:4439–4456
Wang Z, Hou X, Schellenberg MP, Qin Y, Yun X, Wei Z et al (2014) Different responses of plant species to deferment of sheep grazing in a desert steppe of Inner Mongolia. China. Rangeland J. 36:583–592
Wang Z, Ji L, Hou X, Schellenberg MP (2016) Soil respiration in semiarid temperate grasslands under various land management. PLoS One 11:e0147987
Wang Z, Li X, Ji B, Struik PC, Jin K, Tang S (2021) Coupling Between the Responses of Plants, Soil, and Microorganisms Following Grazing Exclusion in an Overgrazed Grassland. Front. Plant Sci. 12:640789. https://doi.org/10.3389/fpls.2021.640789
Xu M, Xia H, Wu J, Yang G, Zhang X, Peng H, Yu X, Li L, Xiao H, Qi H (2016) Shifts in the relative abundance of bacteria after wine-lees-derived biochar intervention in multi metal-contaminated paddy soil. Science of the Total Environment 599-600:1297–1307
Xun W, Yan R, Ren Y, Jin D, Xiong W, Zhang G, Cui Z, Xin X (2018) Grazing-induced microbiome alterations drive soil organic carbon turnover and productivity in meadow steppe. Microbiome 6:170. https://doi.org/10.1186/s40168-018-0544-y
Yang JE, Jacobsen JS (1990) Soil inorganic phosphorus fractions and their uptake relationships in calcareous soils. Soil Sci Soc Am J 54:1666–1669
Yang Y, Wu L, Lin Q, Yuan M, Xu D, Yu H et al (2013) Responses of the functional structure of soil microbial community to livestock grazing in the Tibetan alpine grassland. Glob. Change Biol. 19:637–648
Zhang H, Fu G (2021) Responses of plant, soil bacterial and fungal communities to grazing vary with pasture seasons and grassland types, northern Tibet. Land Degrad Dev. 32:1821–1832
Zhang R, Wang Z, Han G, Schellenberg MP, Wu Q, Gu C (2018) Grazing induced changes in plant diversity is a critical factor controlling grassland productivity in the Desert Steppe, Northern China. Agriculture, Ecosystem and Environment 265:73–83
Zhang R, Wang Z, Niu S, Tian D, Wu Q, Gao X, Schellenberg MP, Han G (2021) Diversity of plant and soil microbes mediates the response of ecosystem multifunctionality to grazing disturbance. Science of the Total Environment 776:145730. https://doi.org/10.1016/j.scitotenv.2021.145730
Zhang T, Li FY, Shi C, Li Y, Tang S, Baoyin T (2020) Enhancement of nutrient resorption efficiency increases plant production and helps maintain soil nutrients under summer grazing in a semi-arid steppe. Agriculture, Ecosystems and Environment 292:106840. https://doi.org/10.1016/j.agee.2020.106840
Zheng W, Zhao Z, Gong Q, Zhai B, Li Z (2018) Responses of fungal–bacterial community and network to organic inputs vary among different spatial habitats in soil. Soil Biology and Biochemistry 125:54–63
Zhou C, Ma Z, Zhu L, Xiao X, Xie Y, Zhu J, Wang J (2016) Rhizobacterial strain Bacillus megaterium BOFC15 induces cellular polyamine changes that improve plant growth and drought resistance. Int. J. Mol. Sci. 17:976. https://doi.org/10.3390/ijms17060976
Acknowledgements
We thank Jianjun Chen for help with setting up the experiment and collecting the soil samples. This work was supported by the National Natural Science Foundation of China (42077054 and 32071681) and the Central Public-Interest Scientific Institution Basal Research Fund (1610332020019, 1610332020005). This work was also supported by the Natural Science Foundation of Inner Mongolia, China (2019MS03003), the Applied Technology Research and Development Fund of Inner Mongolia (2021GG0088, 2020GG0113), and the Science and Technology Development Center Project (KJZXYZ202001).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethics approval and consent to participate
This article does not contain any studies with human participants. The sheep used for the grazing experiments were exposed to different levels of forage availability, but otherwise their well-being was not affected in any way. Ethical approval was not necessary for our study.
Conflict of interests
The authors declare that they have no competing interests.
Additional information
Responsible Editor: Manuel Delgado-Baquerizo.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Rights and permissions
About this article
Cite this article
Wang, Z., Jiang, S., Struik, P.C. et al. Plant and soil responses to grazing intensity drive changes in the soil microbiome in a desert steppe. Plant Soil 491, 219–237 (2023). https://doi.org/10.1007/s11104-022-05409-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-022-05409-1