Abstract
Aims
Nitrogen (N) fertilizer is applied to the soil to increase the nutrient level and plant productivity, but the effects of N addition on the soil microbial community diversity and functions are unclear. This study aimed to determine how changes in soil N influence soil microbial community diversity and potential functions.
Methods
We evaluated plant characteristics, soil chemical properties, microbial composition, and potential functions (N-fixation and functional fungal guild) after 3 years of urea fertilization at four different levels (0, 25, 50, and 100 kg N ha−1 year−1) in a semiarid grassland in China. Compositions of bacterial and fungal communities were determined by high-throughput sequencing, and their potential functions were predicted by comparing their data with those in the Tax4Fun and FUNGuild databases, respectively.
Results
Compared with the grassland without N input (N0), N fertilization significantly reduced soil bacterial diversity, possibly by reducing plant diversity. Fungal diversity increased with N fertilization and peaked in the N50 treatment, while the aboveground biomass showed a parallel increase and peak. A lower abundance of nif genes was found in the N100 than in the N0 treatment because the enhanced NO3− and NH4+ content alleviated the dependence of plants on biological N-fixation and reduced the N-fixation potential. N fertilization increased the relative abundance of saprotrophs (wood, plant, and dung saprotrophs) and pathogens (plant and animal pathogens). However, this promotion could be weakened when the excessive N fertilization was applied due to the lower abundance in the N100 than in the N50 treatment, and these changes could be attributed to the variation in aboveground biomass and soil organic C. Changes in the abundance of arbuscular mycorrhizal fungi were related to their host plants, exhibiting a transient increase in the N25 compared to the N0 treatment and then sharply decreasing.
Conclusions
Our results show that N-induced environmental changes have considerable influence on the composition and potential functions of soil bacterial and fungal communities, which are likely to be dependent on interactions between plants and soil.
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Data availability
Data available from Figshare: https://figshare.com/s/d1aa64da5f20b6cc1afa
References
Allison SD, Lu Y, Weihe C, Goulden ML, Martiny AC, Treseder KK, Martiny JB (2013) Microbial abundance and composition influence litter decomposition response to environmental change. Ecology 94:714–725
Ampt EA, van Ruijven J, Raaijmakers JM, Termorshuizen AJ, Mommer L (2019) Linking ecology and plant pathology to unravel the importance of soil-borne fungal pathogens in species-rich grasslands. Eur J Plant Pathol 154:141–156
Asshauer KP, Wemheuer B, Daniel R, Meinicke P (2015) Tax4Fun: predicting functional profiles from metagenomic 16S rRNA data. Bioinformatics 31:2882–2884
Baccini A, Walker W, Carvalho L, Farina M, Sulla-Menashe D, Houghton RA (2017) Tropical forests are a net carbon source based on aboveground measurements of gain and loss. Science 358:230–233
Becker J, Eisenhauer N, Scheu S, Jousset A (2012) Increasing antagonistic interactions cause bacterial communities to collapse at high diversity. Ecol Lett 15:468–474
Bobbink R, Hicks K, Galloway J, Spranger T, Alkemade R, Ashmore M, Bustamante M, Cinderby S, Davidson E, Dentener F, Emmett B, Erisman JW, Fenn M, Gilliam F, Nordin A, Pardo L, De Vries W (2010) Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecology Applications l 20:30–59
Cairney JW, Meharg AA (2002) Interactions between ectomycorrhizal fungi and soil saprotrophs: implications for decomposition of organic matter in soils and degradation of organic pollutants in the rhizosphere. Can J Bot 80:803–809
Che RX, Qin JL, Tahmasbian I, Wang F, Zhou ST, Xu ZH, Cui XY (2018) Litter amendment rather than phosphorus can dramatically change inorganic nitrogen pools in a degraded grassland soil by affecting nitrogen-cycling microbes. Soil Biol Biochem 120:145–152
Crits-Christoph A, Diamond S, Butterfield CN, Thomas BC, Banfield J (2018) Novel soil bacteria possess diverse genes for secondary metabolite biosynthesis. J Ecol 104:899–910
Cui YX, Bing HJ, Fang LC, Jiang M, Shen GT, Yu JL, Wang X, Zhu H, Wu YH, Zhang XC (2021) Extracellular enzyme stoichiometry reveals the carbon and phosphorus limitations of microbial metabolisms in the rhizosphere and bulk soils in alpine ecosystems. Plant and Soil 458(2):7–20
Dai Z, Su W, Chen H, Barberan A, Zhao H, Yu M, Yu L, Brookes PC, Schadt CW, Chang SX, Xu J (2018) Long-term nitrogen fertilization decreases bacterial diversity and favors the growth of Actinobacteria and Proteobacteria in agro-ecosystems across the globe. Glob Change Biol 24:3452–3461
DeMalach N, Zaady E, Weiner J, Kadmon R (2016) Size asymmetry of resource competition and the structure of plant communities. J Ecol 104(4):899–910
Dos Santos PC, Fang Z, Mason SW, Setubal JC, Dixon R (2012) Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes. BMC Genomics 13:162
Egerton-Warburton LM, Johnson NC, Allen EB (2007) Mycorrhizal community dynamics following nitrogen fertilization: a cross-site test in five grasslands. Ecol Monogr 77(4):527–544
Eldridge DJ, Delgado-Baquerizo M, Travers SK, Val J, Oliver I (2017) Do grazing intensity and herbivore type affect soil health? Insights from a semi-arid productivity gradient. J Appl Ecol 54:976–985
Fauvart M, Michiels J (2008) Rhizobial secreted proteins as determinants of host specificity in the rhizobium-legume symbiosis. Femsmicrobiol Lett 285(1):1–9
Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364
Fudal I, Balesdent MH, Rouxel T (2018) Effector biology in fungal pathogens of nonmodel crop plants. Trends Plant Sci 23:753–755
Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP, Asner GP, Cleveland CC, Green P, Holland EAJB (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226
Herridge DF, Peoples MB, Boddey RM (2008) Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil 331:1–18
Jones EBG, Sakayaroj J, Suetrong S, Somrithipol S, Pang KL (2009) Classification of marine Ascomycota, anamorphic taxa and Basidiomycota. Fungal Divers 35:1–187
Kiers ET, Rousseau RA, West SA, Denison RF (2003) Host sanctions and the legume-rhizobium mutualism. Nature 425(6953):78–81
Lange M, Eisenhauer N, Sierra CA, Bessler H, Engels C, Griffiths RI, Mellado-Vazquez PG, Malik AA, Roy J, Scheu S, Steinbeiss S, Thomson BC, Trumbore SE, Gleixner G (2015) Plant diversity increases soil microbial activity and soil carbon storage. Nat Commun 6:6707
Lennon JT, Jones SE (2011) Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev Microbiol 9:119–130
Lentendu G, Wubet T, Chatzinotas A, Wilhelm C, Buscot F, Schlegel M (2014) Effects of long-term differential fertilization on eukaryotic microbial communities in an arable soil: a multiple barcoding approach. Mol Ecol 23:3341–3355
Li SF, Huang XB, Lang XD, Shen JY, Xu FD, Su JR (2020) Cumulative effects of multiple biodiversity attributes and abiotic factors on ecosystem multifunctionality in the Jinsha River valley of southwestern China. For Ecol Manage 472:118281
Li YY, Pan FX, Yao HY (2019) Response of symbiotic and asymbiotic nitrogen-fixing microorganisms to nitrogen fertilizer application. J Soils Sediments 19:1948–1958
Liang JL, Liu J, Jia P, Yang TT, Zeng QW, Zhang SC, Liao B, Shu WS, Li JT (2020) Novel phosphate-solubilizing bacteria enhance soil phosphorus cycling following ecological restoration of land degraded by mining. ISME J 14:1–14
Liu JS, Zhang X, Wang H, Hui XL, Wang ZH, Qiu WH (2018) Long-term nitrogen fertilization impacts soil fungal and bacterial community structures in a dryland soil of Loess Plateau in China. Journal of Soil & Sediments 18:1632–1640
Ma A, Zhuang X, Wu J, Cui M, Lv D, Liu C, Zhuang G (2013) Ascomycota members dominate fungal communities during straw residue decomposition in arable soil. PLoS One 8(6):e66146
Maroti G, Kondorosi E (2014) Nitrogen-fixing Rhizobium-legume symbiosis: are polyploidy and host peptide-governed symbiont differentiation general principles of endosymbiosis? Front Microbiol 5:326
Nakaji T, Fukami M, Dokiya Y, Izuta T (2001) Effects of high nitrogen load on growth, photosynthesis and nutrient status of Cryptomeria japonica and Pinus densiflora seedlings. Trees 15:453–461
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 20:241–248
Perez-Fernandez MA, Lamont BB (2016) Competition and facilitation between Australian and Spanish legumes in seven Australian soils. Plant Spec Biol 31(4):256–271
Redecker D, Raab P (2006) Phylogeny of the Glomeromycota (arbuscular mycorrhizal fungi): recent developments and new gene markers. Mycologia 98:885–895
Reed SC, Cleveland CC, Townsend AR (2011) Functional ecology of free-living nitrogen fixation: a contemporary perspective. Soil Biol Biochem 42:489–512
Rillig MC, Mardatin NF, Leifheit EF, Antunes PM (2010) Mycelium of arbuscular mycorrhizal fungi increases soil water repellency and is sufficient to maintain water-stable soil aggregates. Soil Biol Biochem 42:1189–1191
Rousk J, Baath E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351
Ruijven J V, Ampt E, Francioli D, Mommer L (2020) Do soil-borne fungal pathogens mediate plant diversity-productivity relationships? Evidence and future opportunities. J Ecol 108
Schöps R, Goldmann K, Korell L, Bruelheide H, Wubet T, Buscot F (2020) Resident and phytometer plants host comparable rhizosphere fungal communities in managed grassland ecosystems. Sci Rep 10:919
Shen W, Ni Y, Gao N, Bian B, Zheng S, Lin X, Chu H (2016) Bacterial community composition is shaped by soil secondary salinization and acidification brought on by high nitrogen fertilization rates. Appl Soil Ecol 108:76–83
Sikes BA, Powell JR, Rillig MC (2010) Deciphering the relative contributions of multiple functions within plant-microbe symbioses. Ecology 91:1591–1597
Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt K, Tignor M, Miller H (2007) Climate Change 2007: The Physical Science Basis. Contribution of working group I to the fourth 16 assessment report of the intergovernmental panel on climate change 18: 95–123
Smith SE, Jakobsen I, Grønlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156:1050–1057
Sun LJ, QI YC, Dong YS, HE YT, Peng Q, Liu XC, Jia JQ, Guo SF, Cao CC, (2015) Interactions of water and nitrogen addition on soil microbial community composition and functional diversity depending on the inter-annual precipitation in a Chinese steppe. J Integr Agric 14:788–799
Sun H, Terhonen E, Koskinen K, Paulin L, Kasanen R, Asiegbu FO (2014) Bacterial diversity and community structure along different peat soils in boreal forest. Appl Soil Ecol 74:37–45
Treseder KK, Allen EB, Egerton-Warburton LM, Hart MM, Klironomos JN, Maherali H, Tedersoo L (2018) Arbuscular mycorrhizal fungi as mediators of ecosystem responses to nitrogen deposition: a trait-based predictive framework. J Ecol 106:480–489
Wang J, Liu G, Zhang C, Wang G (2020) Effect of long-term destocking on soil fungal functional groups and interactions with plants. Plant Soil 448:495–508
Wang J, Rhodes G, Huang Q, Shen Q (2018) Plant growth stages and fertilization regimes drive soil fungal community compositions in a wheat-rice rotation system. Biol Fertil Soils 54:731–742
Weber CF, Rytas V, Kuske CR (2013) Changes in fungal community composition in response to elevated atmospheric CO2 and nitrogen fertilization varies with soil horizon. Front Microbiol 4:78
Xiao D, Tan YJ, Liu X, Yang R, Zhang W, He XY, Xu ZH, Wang KL (2020) Responses of soil diazotrophs to legume species and density in a karst grassland, southwest China. Agriculture Ecosystems and Environment 288.
Xiao D, Liu X, Yang R, Tan Y, Zhang W, He X, Xu Z, Wang K, 2020. Nitrogen fertilizer and Amorpha fruticosa leguminous shrub diversely affect the diazotroph communities in an artificial forage grassland. Science of The Total Environment 711.
Xiong J, Peng F, Sun H, Zhang H, Xue X, Chu H (2014) Divergent responses of soil fungi functional groups to short-term warming. Microb Ecol 68:890–890
Yang H, Li Y, Wu M, Zhang Z, Li L, Wan S (2011) Plant community responses to nitrogen addition and increased precipitation: the importance of water availability and species traits. Glob Change Biol 17:2936–2944
Yang Y, Dou YX, An SS, Zhu ZL (2018) Abiotic and biotic factors modulate plant biomass and root/shoot (R/S) ratios in grassland on the Loess Plateau, China. Sci Total Environ 636:621–631
Zang H, Blagodatskaya E, Wang J, Xu X, Kuzyakov Y (2017) Nitrogen fertilization increases rhizodeposit incorporation into microbial biomass and reduces soil organic matter losses. Biol Fertil Soils 53:419–429
Zeng DH, Li LJ, Fahey TJ, Yu ZY, Fan ZP, Chen FS (2010) Effects of nitrogen addition on vegetation and ecosystem carbon in a semi-arid grassland. Biogeochemistry 98:185–193
Zeng J, Liu XJ, Song L, Lin XG, Zhang HY, Shen CC, Chu HY (2016) Nitrogen fertilization directly affects soil bacterial diversity and indirectly affects bacterial community composition. Soil Biol Biochem 92:41–49
Zhang C, Song ZL, Zhuang D, Wang J, Xue S, Liu GB (2019) Urea fertilization decreases soil bacterial diversity, but improves microbial biomass, respiration, and N-cycling potential in a semiarid grassland. Biol Fertil Soils 55:229–242
Zhang C, Wang J, Liu GB, Song ZL, Fang LC (2019) Impact of soil leachate on microbial biomass and diversity affected by plant diversity. Plant Soil 439:505–523
Zhang C, Xue S, Liu GB, Wang GL (2016) Soil bacterial community dynamics reflect changes in plant community and soil properties during the secondary succession of abandoned farmland in the Loess Plateau. Soil Biol Biochem 97:40–49
Zheng MH, Zhang W, Luo YQ, Mori TK, Mao QQ, Wang SH, Huang J, Lu XK, Mo JM (2017) Different responses of asymbiotic nitrogen fixation to nitrogen addition between disturbed and rehabilitated subtropical forests. Sci Total Environ 601:1505–1512
Zheng Z, Ma PF, Li J, Ren LF, Bai WM, Tian QY, Sun W, Zhang WH (2018) Arbuscular mycorrhizal fungal communities associated with two dominant species differ in their responses to long-term nitrogen addition in temperate grasslands. Funct Ecol 32:1575–1588
Zhou J, Guan DW, Zhou BK, Zhao BS, Ma MC, Qin J, Jiang X, Chen SF, Cao FM, Shen DL, Li J (2015) Influence of 34-years of fertilization on bacterial communities in an intensively cultivated black soil in northeast China. Soil Biol Biochem 90:42–51
Zhou J, Jiang X, Zhou BK, Zhao BS, Ma MC, Guan DW, Li J, Chen SF, Cao FM, Shen DL, 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
Zinati GM (2005) Compost in the 20th century: a tool to control plant diseases in nursery and vegetable crops. HortTechnology 15:61–66
Zhu SS, Vivanco JM, Manter DK (2016) Nitrogen fertilizer rate affects root exudation, the rhizosphere microbiome and nitrogen-use-efficiency of maize. Appl Soil Ecol 107:324–333
Funding
This work was financially supported by the “Light of the West” Cross Team Key Laboratory Cooperative Research Project of Chinese Academy of Science; Natural Science Basic Research Program of Shaanxi Province (2019KJXX-081; 2021JM-605); the National Natural Sciences Foundation of China (41771554, 51609237, 41807521); and the National Key Research and Development Program of China (2016YFC0501707).
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Liao, L., Wang, X., Wang, J. et al. Nitrogen fertilization increases fungal diversity and abundance of saprotrophs while reducing nitrogen fixation potential in a semiarid grassland. Plant Soil 465, 515–532 (2021). https://doi.org/10.1007/s11104-021-05012-w
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DOI: https://doi.org/10.1007/s11104-021-05012-w