Abstract
Background and aims
Soil microorganisms play key roles in soil nutrient turnover and plant community composition; however, the soil microbial community composition and species diversity are often influenced by nutrient enrichment which may affect how soil microbes influence nutrient cycles and the plant community structure. The resistance of soil fungal and bacterial communities to nitrogen (N) and phosphorus (P) additions and whether the responses of the soil microbes and the plant community are simultaneous in a N-limited temperate meadow ecosystem are still unclear.
Methods
We carried out a 7-year experiment with N and P additions in a temperate meadow. The community structures of soil bacteria and fungi were examined based on high-throughput sequencing targeting the 16S rRNA and ITS genes, respectively.
Results
Nitrogen addition did not influence the community composition or species richness of bacteria, but it did alter the soil fungal community composition and increased fungal operational taxonomic unit (OTU) richness. Phosphorus addition significantly altered the soil fungal and bacterial community compositions, decreased the richness of bacterial OTUs, and increased the OTU richness of fungi. Proteobacteria (38.5%) and Acidobacteria (22.3%) were the most dominant bacteria. Ascomycota were the dominant fungi (42.6%) across all samples. The enrichment of available P in the soil due to P addition reduced the bacterial β-diversity, while the β-diversity of soil fungi was mainly influenced by the concentrations of soil N and P, as well as soil moisture.
Conclusions
The sensitivity of soil fungi and bacteria to P addition was stronger than that of N addition, and the response of the soil microbes to N and P additions was more sensitive than that of the plant community. Our results highlight the unequal sensitivity of the soil fungal and bacterial community composition and structure to N and P additions, thereby causing changes in above and belowground community composition and structures in the studied temperate meadow ecosystem.
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References
Ahn H, James RT (2001) Variability, uncertainty, and sensitivity of phosphorus deposition load estimates in South Florida. Water Air Soil Poll 126:37–51. https://doi.org/10.1023/A:1005235118716
Bai Y, Wu J, Clark CM, Naeem S, Pan Q, Huang J, Zhang L, Han X (2010) Tradeoffs and thresholds in the effects of nitrogen addition on biodiversity and ecosystem functioning: evidence from inner Mongolia grasslands. Glob Chang Biol 16:358–372. https://doi.org/10.1111/j.1365-2486.2009.01950.x
Bender SF, Plantenga F, Neftel A, Jocher M, Oberholzer HR, Kohl L, Giles M, Daniell TJ, van der Heijden MGA (2014) Symbiotic relationships between soil fungi and plants reduce N2O emissions from soil. ISME J 8:1336–1345. https://doi.org/10.1038/ismej.2013.224
Bender SF, Conen F, van der Heijden MGA (2015) Mycorrhizal effects on nutrient cycling, nutrient leaching and N2O production in experimental grassland. Soil Biol Biochem 80:283–292. https://doi.org/10.1016/j.soilbio.2014.10.016
Bennett JA, Maherali H, Reinhart KO, Lekberg Y, Hart MM, Klironomos J (2017) Plant-soil feedbacks and mycorrhizal type influence temperate forest population dynamics. Science 355:181–184. https://doi.org/10.1126/science.aai8212
Campbell BJ, Polson SW, Hanson TE, Mack MC, Schuur EA (2010) The effect of nutrient deposition on bacterial communities in Arctic tundra soil. Environ Microbiol 12:1842–1854. https://doi.org/10.1111/j.1462-2920.2010.02189.x
Ceulemans T, Stevens CJ, Duchateau L, Jacquemyn H, Gowing DJG, Merckx R, Wallace H, van Rooijen N, Goethem T, Bobbink R, Dorland E, Gaudnik C, Alard D, Corcket E, Muller S, Dise NB, Dupré C, Diekmann M, Honnay O (2014) Soil phosphorus constrains biodiversity across European grasslands. Glob Chang Biol 20:3814–3822. https://doi.org/10.1111/gcb.12650
Cline LC, Zak DR (2015) Soil microbial communities are shaped by plant-driven changes in resource availability during secondary succession. Ecology 96:3374–3385. https://doi.org/10.1890/15-0184.1
Cui N, Shi L, Guo J, Zhang T (2021) Arbuscular mycorrhizal fungi alleviate elevated temperature and nitrogen deposition- induced warming potential by reducing soil N2O emissions in a temperate meadow. Ecol Indic 131:108193. https://doi.org/10.1016/j.ecolind.2021.108193
Delgado-Baquerizo M, Maestre FT, Reich PB, Jeffries TC, Gaitan JJ, Encinar D, Berdugo M, Campbell CD, Singh BK (2016) Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat Commun 7. https://doi.org/10.1038/ncomms10541
Eo J, Park KC (2016) Long-term effects of imbalanced fertilization on the composition and diversity of soil bacterial community. Agri Eco Environ 231:176–182. https://doi.org/10.1016/j.agee.2016.06.039
Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. P Natl Acad Sci USA 103:626–631. https://doi.org/10.1073/pnas.0507535103
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 6:1007–1017. https://doi.org/10.1038/ismej.2011.159
Freedman Z, Eisenlord SD, Zak DR, Xue K, He ZL, Zhou JZ (2013) Towards a molecular understanding of N cycling in northern hardwood forests under future rates of N deposition. Soil Biol Biochem 66:130–138. https://doi.org/10.1016/j.soilbio.2013.07.010
Freedman ZB, Romanowicz KJ, Upchurch RA, Zak DR (2015) Differential responses of total and active soil microbial communities to long-term experimental N deposition. Soil Biol Biochem 90:275–282. https://doi.org/10.1016/j.soilbio.2015.08.014
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x
Gong S, Guo R, Zhang T, Guo J (2015) Warming and nitrogen addition increase litter decomposition in a temperate meadow ecosystem. PLoS One 10:e0116013. https://doi.org/10.1371/journal.pone.0116013
Guo QX, Yan LJ, Korpelainen H, Niinemets U, Li CY (2019) Plant-plant interactions and N fertilization shape soil bacterial and fungal communities. Soil Biol Biochem 128:127–138. https://doi.org/10.1016/j.soilbio.2018.10.018
Harrison S (2020) Plant community diversity will decline more than increase under climatic warming. Philos T Roy Soc B 375(1794):20190106
He D, Xiang XJ, He JS, Wang C, Cao GM, Adams J, Chu HY (2016) Composition of the soil fungal community is more sensitive to phosphorus than nitrogen addition in the alpine meadow on the Qinghai-Tibetan plateau. Biol Fert Soil 52:1059–1072. https://doi.org/10.1007/s00374-016-1142-4
Huang J, Hu B, Qi K, Chen W, Pang X, Bao W, Tian G (2016) Effects of phosphorus addition on soil microbial biomass and community composition in a subalpine spruce plantation. Eur J Soil Biol 72:35–41. https://doi.org/10.1016/j.ejsobi.2015.12.007
Jiang FY, Zhang L, Zhou JC, George TS, Feng G (2021) Arbuscular mycorrhizal fungi enhance mineralisation of organic phosphorus by carrying bacteria along their extraradical hyphae. New Phytol 230:304–315. https://doi.org/10.1111/nph.17081
Kang F, Yang B, Wujisiguleng, Yang X, Wang L, Guo JX, Sun W, Zhang Q, Zhang T (2020) Arbuscular mycorrhizal fungi alleviate the negative effect of nitrogen deposition on ecosystem functions in meadow grassland. Land Degrad Dev 31:748–759. https://doi.org/10.1002/ldr.3491
Lee SH, Ka JO, Cho JC (2008) Members of the phylum Acidobacteria are dominant and metabolically active in rhizosphere soil. FEMS Microbiol Lett 285:263–269. https://doi.org/10.1111/j.1574-6968.2008.01232.x
Leff JW, Jones SE, Prober SM, Barberan A, Borer ET, Firn JL, Harpole WS, Hobbie SE, Hofmockel KS, Knops JMH, McCulley RL, La Pierre K, Risch AC, Seabloom EW, Schutz M, Steenbock C, Stevens CJ, Fierer N (2015) Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. P Natl Acad Sci USA 112:10967–10972. https://doi.org/10.1073/pnas.1508382112
Li J, Li ZA, Wang FM, Zou B, Chen Y, Zhao J, Mo QF, Li YW, Li XB, Xia HP (2015) Effects of nitrogen and phosphorus addition on soil microbial community in a secondary tropical forest of China. Biol Fert Soil 51:207–215. https://doi.org/10.1007/s00374-014-0964-1
Li PD, Jeewon R, Aruna B, Li HY, Lin FC, Wang HK (2019) Metabarcoding reveals differences in fungal communities between unflooded versus tidal flat soil in coastal saline ecosystem. Sci Total Environ 690:911–922. https://doi.org/10.1016/j.scitotenv.2019.06.473
Li J, Li C, Kou Y, Yao M, He Z, Li X (2020) Distinct mechanisms shape soil bacterial and fungal co-occurrence networks in a mountain ecosystem. FEMS Microbiol Ecol 96(4):fiaa030. https://doi.org/10.1093/femsec/fiaa030
Li J, Sang C, Yang J, Qu L, Xia Z, Sun H, Jiang P, Wang X, He H, Wang C (2021) Stoichiometric imbalance and microbial community regulate microbial elements use efficiencies under nitrogen addition. Soil Biol Biochem 156. https://doi.org/10.1016/j.soilbio.2021.108207
Limpens J, Berendse F, Klees H (2004) How phosphorus availability affects the impact of nitrogen deposition on sphagnum and vascular plants in bogs. Ecosystems 7:793–804. https://doi.org/10.1007/s10021-004-0274-9
Ling N, Chen D, Guo H, Wei J, Bai Y, Shen Q, Hu S (2017) Differential responses of soil bacterial communities to long-term N and P inputs in a semi-arid steppe. Geoderma 292:25–33. https://doi.org/10.1016/j.geoderma.2017.01.013
Liu L, Gundersen P, Zhang T, Mo J (2012) Effects of phosphorus addition on soil microbial biomass and community composition in three forest types in tropical China. Soil Biol Biochem 44:31–38. https://doi.org/10.1016/j.soilbio.2011.08.017
Liu M, Liu J, Chen X, Jiang C, Wu M, Li Z (2018) Shifts in bacterial and fungal diversity in a paddy soil faced with phosphorus surplus. Biol Fert Soil 54:259–267. https://doi.org/10.1007/s00374-017-1258-1
Mei LL, Yang X, Zhang SQ, Zhang T, Guo JX (2019) Arbuscular mycorrhizal fungi alleviate phosphorus limitation by reducing plant N:P ratios under warming and nitrogen addition in a temperate meadow ecosystem. Sci Total Environ 686:1129–1139. https://doi.org/10.1016/j.scitotenv.2019.06.035
Mori H, Maruyama F, Kato H, Toyoda A, Dozono A, Ohtsubo Y, Nagata Y, Fujiyama A, Tsuda M, Kurokawa K (2014) Design and experimental application of a novel non-degenerate universal primer set that amplifies prokaryotic 16S rRNA genes with a low possibility to amplify eukaryotic rRNA genes. DNA Res 21:217–227. https://doi.org/10.1093/dnares/dst052
Mueller RC, Balasch MM, Kuske CR (2014) Contrasting soil fungal community responses to experimental nitrogen addition using the large subunit rRNA taxonomic marker and cellobiohydrolase I functional marker. Mol Ecol 23:4406–4417. https://doi.org/10.1111/mec.12858
Nielsen UN, Prior S, Delroy B, Walker JKM, Ellsworth DS, Powell JR (2015) Response of belowground communities to short-term phosphorus addition in a phosphorus-limited woodland. Plant Soil 391:321–331. https://doi.org/10.1007/s11104-015-2432-6
Palaniyandi SA, Yang SH, Zhang L, Suh JW (2013) Effects of actinobacteria on plant disease suppression and growth promotion. Appl Microbiol Biotech 97:9621–9636. https://doi.org/10.1007/s00253-013-5206-1
Pan Y, Cassman N, de Hollander M, Mendes LW, Korevaar H, Geerts RH, van Veen JA, Kuramae EE (2014) Impact of long-term N, P, K, and NPK fertilization on the composition and potential functions of the bacterial community in grassland soil. FEMS Microbiol Ecol 90:195–205. https://doi.org/10.1111/1574-6941.12384
Peñuelas J, Poulter B, Sardans J, Ciais P, van der Velde M, Bopp L, Boucher O, Godderis Y, Hinsinger P, Llusia J, Nardin E, Vicca S, Obersteiner M, Janssens IA (2013) Human-induced nitrogen-phosphorus imbalances alter natural and managed ecosystems across the globe. Nat Commun 4: 1–10. https://doi/org/https://doi.org/10.1038/ncomms3934
Pilkingtona MG, Capornb SJM, Carrollb JA, Cresswellc N, Leed JA, Emmette BA, Bagchid R (2007) Phosphorus supply influences heathland responses to atmospheric nitrogen deposition. Environ Pollut 148:191–200. https://doi.org/10.1016/j.envpol.2006.10.034
R Core Team (2019) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna https://www.R-project.org/
Ramirez KS, Craine JM, Fierer N (2012) Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes. Glob Chang Biol 18:1918–1927. https://doi.org/10.1111/j.1365-2486.2012.02639.x
Rooney DC, Clipson NJW (2009) Phosphate addition and plant species alters microbial community structure in acidic upland grassland. Soil Microbial Ecol 57:4–13
Storer K, Coggan A, Ineson P, Hodge A (2018) Arbuscular mycorrhizal fungi reduce nitrous oxide emissions from N2O hotspots. New Phytol 220:1285–1295. https://doi.org/10.1111/nph.14931
Su JQ, Ding LJ, Xue K, Yao HY, Quensen J, Bai SJ, Wei WX, Wu JS, Zhou J, Tiedje JM (2015) Long-term balanced fertilization increases the soil microbial functional diversity in a phosphorus-limited paddy soil. Mol Ecol 24:136–150. https://doi.org/10.1111/mec.13010
Tan H, Barret M, Mooij MJ, Rice O, Morrissey JP, Dobson A, Griffiths B, O’Gara F (2013) Long-term phosphorus fertilisation increased the diversity of the total bacterial community and the phoD phosphorus mineraliser group in pasture soils. Biol Fert Soil 49:661–672. https://doi.org/10.1007/s00374-012-0755-5
Thompson K, Bent E, Abalos D, Wagner-Riddle C, Dunfield K (2016) Soil microbial communities as potential regulators of in situ N2O fluxes in annual and perennial cropping systems. Soil Biol Biochem 103:262–273. https://doi.org/10.1016/j.soilbio.2016.08.030
van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310. https://doi.org/10.1111/j.1461-0248.2007.01139.x
Vellend M, Baeten L, Becker-Scarpitta A, Boucher-Lalonde V, McCune JL, Messier J, Myers-Smith IH, Sax DF (2017) Plant biodiversity change across scales during the anthropocene. Annu Rev Plant Biol 68:563–586. https://doi.org/10.1146/annurev-arplant-042916-040949
Vicars WC, Sickman JO, Ziemann PJ (2010) Atmospheric phosphorus deposition at a montane site: size distribution, effects of wildfire, and ecological implications. Atmos Environ 44:2813–2821. https://doi.org/10.1016/j.atmosenv.2010.04.055
Wan XH, Huang ZQ, He ZM, Yu ZP, Wang MH, Davis MR, Yang YS (2015) Soil C:N ratio is the major determinant of soil microbial community structure in subtropical coniferous and broadleaf forest plantations. Plant Soil 387:103–116. https://doi.org/10.1007/s11104-014-2277-4
Wang H, Liu SR, Zhang X, Mao QG, Li XZ, You YM, Wang JX, Zheng MH, Zhang W, Lu XK, Mo JM (2018) Nitrogen addition reduces soil bacterial richness, while phosphorus addition alters community composition in an old-growth N-rich tropical forest in southern China. Soil Biol Biochem 127:22–30. https://doi.org/10.1016/j.soilbio.2018.08.022
Weber CF, Vilgalys R, 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. https://doi.org/10.3389/fmicb.2013.00078
Wen X, Xu W, Li Q, Han MJ, Tang AH, Zhang Y, Luo XS, Shen JL, Wang W, Li KH, Pan YP, Zhang L, Li WQ, Collett JL, Zhong BQ, Wang XM, Goulding K, Zhang FS (2020) Changes of nitrogen deposition in China from 1980 to 2018. Environ Int 144:106022. https://doi.org/10.1016/j.envint.2020.106022
White T, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR protocols: a guide to methods and applications. PCR protocols: a guide to methods and applications 315–322
Wu L, Wang Y, Zhang S, Wei W, Kuzyakov Y, Ding X (2021) Fertilization effects on microbial community composition and aggregate formation in saline-alkaline soil. Plant Soil. https://doi.org/10.1007/s11104-021-04909-w
Xiong J, Peng F, Sun H, Xue X, Chu H (2014) Divergent responses of soil fungi functional groups to short-term warming. Microbial Ecol 68:708–715. https://doi.org/10.1007/s00248-014-0385-6
Yan G, Xing Y, Wang J, Zhang Z, Xu L, Han S, Zhang J, Dai G, Wang Q (2018) Effects of winter snowpack and nitrogen addition on the soil microbial community in a temperate forest in northeastern China. Ecol Indic 93:602–611. https://doi.org/10.1016/j.ecolind.2018.05.048
Yang Y, Li T, Wang YQ, Cheng H, Chang SX, Liang C, An SS (2021a) Negative effects of multiple global change factors on soil microbial diversity. Soil Biol Biochem 156. https://doi.org/10.1016/j.soilbio.2021.108229
Yang X, Mariotte P, Guo J, Hautier Y, Zhang T (2021b) Suppression of arbuscular mycorrhizal fungi decreases the temporal stability of community productivity under elevated temperature and nitrogen addition in a temperate meadow. Sci Total Environ 762:143137. https://doi.org/10.1016/j.scitotenv.2020.143137
Zeng J, Liu X, Song L, Lin X, Zhang H, Shen C, Chu H (2016) Nitrogen fertilization directly affects soil bacterial diversity and indirectly affects bacterial community composition. Soil Biol Biochem 92:41–49. https://doi.org/10.1016/j.soilbio.2015.09.018
Zhang L, Fan JQ, Ding XD, He XH, Zhang FS, Feng G (2014) Hyphosphere interactions between an arbuscular mycorrhizal fungus and a phosphate solubilizing bacterium promote phytate mineralization in soil. Soil Biol Biochem 74:177–183. https://doi.org/10.1016/j.soilbio.2014.03.004
Zhang T, Guo R, Gao S, Guo JX, Sun W (2015) Responses of plant community composition and biomass production to warming and nitrogen deposition in a temperate meadow ecosystem. PLoS One 10. https://doi.org/10.1371/journal.pone.0123160
Zhang T, Yang X, Guo R, Guo J (2016) Response of AM fungi spore population to elevated temperature and nitrogen addition and their influence on the plant community composition and productivity. Sci Rep 6. https://doi.org/10.1038/srep24749
Zhao Y, Yang B, Li M, Xiao R, Rao K, Wang J, Zhang T, Guo J (2019) Community composition, structure and productivity in response to nitrogen and phosphorus additions in a temperate meadow. Sci Total Environ 654:863–871. https://doi.org/10.1016/j.scitotenv.2018.11.155
Zhou J, Jiang X, Zhou B, Zhao B, Ma M, Guan D, Li J, Chen S, Cao F, Shen D (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. https://doi.org/10.1016/j.soilbio.2015.12.012
Zhu JX, Wang QF, He NP, Smith MD, Elser JJ, Du JQ, Yuan GF, Yu GR, Yu Q (2016) Imbalanced atmospheric nitrogen and phosphorus depositions in China: implications for nutrient limitation. J Geophys Res-Biogeo 121:1605–1616. https://doi.org/10.1002/2016JG003393
Acknowledgements
This work was funded by National Natural Science Foundation of China (31770359, 32171645), Foundation of Science and Technology Commission of Jilin Province (20200201115JC) and the Fundamental Research Funds for the Central Universities (2412020ZD010). We would like to thank the anonymous reviewers for their helpful comments on the manuscript.
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Yan, Y., Sun, X., Sun, F. et al. Sensitivity of soil fungal and bacterial community compositions to nitrogen and phosphorus additions in a temperate meadow. Plant Soil 471, 477–490 (2022). https://doi.org/10.1007/s11104-021-05237-9
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DOI: https://doi.org/10.1007/s11104-021-05237-9