Abstract
This study focused on the legacy effects of 8-year application of N (in gradient of 0, 140, 280, 470, and 660 kg N ha−1 year−1) on the bacterial community diversity, interactions, and assembly processes in the wheat rhizosphere. The rhizosphere bacterial α-diversity increased with the rate of historical N input, while it did not change at N addition rates of over 280 kg N ha−1 year−1. Historical N input clearly shifted the rhizosphere bacterial community composition, and soils with more N input were more dissimilar to those without N input. The net relatedness index (NRI) and nearest taxon index (NTI) analysis revealed that the rhizosphere bacterial communities in most samples were phylogenetically clustered, and the treatments with high N (> 470 kg N ha−1 year−1) showed higher levels of clustering than those with low N (< 140 kg N ha−1 year−1), indicating more environmental selection stress in soil with higher historical N input. Increased co-occurrence network size and connectivity were accompanied by increased aboveground biomass of wheat. Overall, with the increase in historical N input, the resulting legacy effects forced the bacterial community in the rhizosphere to undergo higher environmental selection pressure, and indirectly affected the complexity of wheat rhizosphere assemblages during subsequent crop growth.
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References
Amend AS, Seifert KA, Bruns TD (2010) Quantifying microbial communities with 454 pyrosequencing: does read abundance count? Mol Ecol 19:5555–5565
Banerjee S, Kirkby CA, Schmutter D, Bissett A, Kirkegaard JA, Richardson AE (2016) Network analysis reveals functional redundancy and keystone taxa amongst bacterial and fungal communities during organic matter decomposition in an arable soil. Soil Biol Biochem 97:188–198. https://doi.org/10.1016/j.soilbio.2016.03.017
Benjamini Y, Krieger AM, Yekutieli D (2006) Adaptive linear step-up procedures that control the false discovery rate. Biometrika 93:491–507
Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486. https://doi.org/10.1016/j.tplants.2012.04.001
Bray JR, Curtis JT (1957) An ordination of the upland forest communities of southern Wisconsin. Ecol Monogr 27:325–349
Bremner J (1965) Total nitrogen. In: Black C (ed) Methods of soil analysis. American Society of Soil Science, Madison, pp 1149–1178
Bryant JA, Lamanna C, Morlon H, Kerkhoff AJ, Enquist BJ, Green JL (2008a) Colloquium paper: microbes on mountainsides: contrasting elevational patterns of bacterial and plant diversity. Proc Natl Acad Sci U S A 105(Suppl 1):11505–11511. https://doi.org/10.1073/pnas.0801920105
Bryant JA, Lamanna C, Morlon H, Kerkhoff AJ, Enquist BJ, Green JL (2008b) Microbes on mountainsides: contrasting elevational patterns of bacterial and plant diversity. Proc Natl Acad Sci U S A 105:11505–11511. https://doi.org/10.1073/pnas.0801920105
Chaparro JM, Sheflin AM, Manter DK, Vivanco JM (2012) Manipulating the soil microbiome to increase soil health and plant fertility. Biol Fertil Soils 48:489–499. https://doi.org/10.1007/s00374-012-0691-4
Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by plant development. ISME J 8:790–803. https://doi.org/10.1038/ismej.2013.196
Chung EJ, Park TS, Jeon CO, Chung YR (2012) Chitinophaga oryziterrae sp. nov., isolated from the rhizosphere soil of rice (Oryza sativa L.). Int J Syst Evol Microbiol 62:3030–3035
Cornfield A (1960) Ammonia released on treating soils with N sodium hydroxide as a possible means of predicting the nitrogen-supplying power of soils. Nature 187:260
Cuddington K (2012) Legacy effects: the persistent impact of ecological interactions. Biol Theory 6:203–210. https://doi.org/10.1007/s13752-012-0027-5
de Ridder-Duine AS, Kowalchuk GA, Klein Gunnewiek PJA, Smant W, van Veen JA, de Boer W (2005) Rhizosphere bacterial community composition in natural stands of Carex arenaria (sand sedge) is determined by bulk soil community composition. Soil Biol Biochem 37:349–357. https://doi.org/10.1016/j.soilbio.2004.08.005
de Vries FT, Griffiths RI, Bailey M, Craig H, Girlanda M, Gweon HS, Hallin S, Kaisermann A, Keith AM, Kretzschmar M, Lemanceau P, Lumini E, Mason KE, Oliver A, Ostle N, Prosser JI, Thion C, Thomson B, Bardgett RD (2018) Soil bacterial networks are less stable under drought than fungal networks. Nat Commun 9:3033–3012. https://doi.org/10.1038/s41467-018-05516-7
Delgado-Baquerizo M, Reich PB, Khachane AN, Campbell CD, Thomas N, Freitag TE, Abu Al-Soud W, Sorensen S, Bardgett RD, Singh BK (2017) It is elemental: soil nutrient stoichiometry drives bacterial diversity. Environ Microbiol 19:1176–1188. https://doi.org/10.1111/1462-2920.13642
Detheridge AP, Brand G, Fychan R, Crotty FV, Sanderson R, Griffith GW, Marley CL (2016) The legacy effect of cover crops on soil fungal populations in a cereal rotation. Agric Ecosyst Environ 228:49–61. https://doi.org/10.1016/j.agee.2016.04.022
Doncheva NT, Assenov Y, Domingues FS, Albrecht M (2012) Topological analysis and interactive visualization of biological networks and protein structures. Nat Protoc 7:670–685. https://doi.org/10.1038/nprot.2012.004
Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fitter AH (2010) Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J 4:337–345. https://doi.org/10.1038/ismej.2009.122
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 10:996
Eno CF, Blue WG, Good JM (1955) The effect of anhydrous ammonia on nematodes, fungi, bacteria, and nitrification in some Florida soils 1. Soil Sci Soc Am J 19:55–58
Fan K, Cardona C, Li Y, Shi Y, Xiang X, Shen C, Wang H, Gilbert JA, Chu H (2017) Rhizosphere-associated bacterial network structure and spatial distribution differ significantly from bulk soil in wheat crop fields. Soil Biol Biochem 113:275–284. https://doi.org/10.1016/j.soilbio.2017.06.020
Fan K, Weisenhorn P, Gilbert JA, Shi Y, Bai Y, Chu H (2018) Soil pH correlates with the co-occurrence and assemblage process of diazotrophic communities in rhizosphere and bulk soils of wheat fields. Soil Biol Biochem 121:185–192
Faust K, Raes J (2012) Microbial interactions: from networks to models. Nat Rev Microbiol 10:538–550. https://doi.org/10.1038/nrmicro2832
Ge T, Li B, Zhu Z, Hu Y, Yuan H, Dorodnikov M, Jones DL, Wu J, Kuzyakov Y (2016) Rice rhizodeposition and its utilization by microbial groups depends on N fertilization. Biol Fertil Soils 53:37–48. https://doi.org/10.1007/s00374-016-1155-z
Goberna M, Navarro-Cano JA, Valiente-Banuet A, Garcia C, Verdu M (2014) Abiotic stress tolerance and competition-related traits underlie phylogenetic clustering in soil bacterial communities. Ecol Lett 17:1191–1201. https://doi.org/10.1111/ele.12341
Greenblum S, Turnbaugh PJ, Borenstein E (2012) Metagenomic systems biology of the human gut microbiome reveals topological shifts associated with obesity and inflammatory bowel disease. Proc Natl Acad Sci U S A 109:594–599. https://doi.org/10.1073/pnas.1116053109
Gu Y, Wang Y, Lu S, Xiang Q, Yu X, Zhao K, Zou L, Chen Q, Tu S, Zhang X (2017) Long-term fertilization structures bacterial and archaeal communities along soil depth gradient in a paddy soil. Front Microbiol 8:1516. https://doi.org/10.3389/fmicb.2017.01516
Guo JH, Liu XJ, Zhang Y, Shen J, Han W, Zhang W, Christie P, Goulding K, Vitousek P, Zhang F (2010) Significant acidification in major Chinese croplands. Science 327:1008–1010
Haichar FZ, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Jm B, Heulin T, Achouak W (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230
Huang X, Zhou X, Zhang J, Cai Z (2019) Highly connected taxa located in the microbial network are prevalent in the rhizosphere soil of healthy plant. Biol Fertil Soils 55:299–312. https://doi.org/10.1007/s00374-019-01350-1
Ibekwe AM, Poss JA, Grattan SR, Grieve CM, Suarez D (2010) Bacterial diversity in cucumber (Cucumis sativus) rhizosphere in response to salinity, soil pH, and boron. Soil Biol Biochem 42:567–575. https://doi.org/10.1016/j.soilbio.2009.11.033
Jacquiod S, Franqueville L, Cécillon S, Vogel TM, Simonet P (2013) Soil bacterial community shifts after chitin enrichment: an integrative metagenomic approach. PLoS One 8:1–13
Jiang Y, Lei Y, Yang Y, Korpelainen H, Niinemets Ü, Li C (2018) Divergent assemblage patterns and driving forces for bacterial and fungal communities along a glacier forefield chronosequence. Soil Biol Biochem 118:207–216. https://doi.org/10.1016/j.soilbio.2017.12.019
Johansson JF, Paul LR, Finlay RD (2004) Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiol Ecol 48:1–13
Ju X-T, Xing G-X, Chen X-P, Zhang S-L, Zhang L-J, Liu X-J, Cui Z-L, Yin B, Christie P, Zhu Z-L (2009) Reducing environmental risk by improving N management in intensive Chinese agricultural systems. Proc Natl Acad Sci U S A 106:3041–3046
Kato S, Haruta S, Cui ZJ, Ishii M, Igarashi Y (2005) Stable coexistence of five bacterial strains as a cellulose-degrading community. Appl Environ Microbiol 71:7099–7106
Kivlin SN, Winston GC, Goulden ML, Treseder KK (2014) Environmental filtering affects soil fungal community composition more than dispersal limitation at regional scales. Fungal Ecol 12:14–25
Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glöckner FO (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41:e1–e1
Kong Y, Ling N, Xue C, Chen H, Ruan Y, Guo J, Zhu C, Wang M, Shen Q, Guo S (2019) Long-term fertilization regimes change soil nitrification potential by impacting active autotrophic ammonia oxidizers and nitrite oxidizers as assessed by DNA stable isotope probing. Environ Microbiol 21:1224–1240. https://doi.org/10.1111/1462-2920.14553
Kuzyakov Y, Xu X (2013) Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytol 198:656–669. https://doi.org/10.1111/nph.12235
Kwak MJ, Kong HG, Choi K, Kwon SK, Song JY, Lee J, Lee PA, Choi SY, Seo M, Lee HJ, Jung EJ, Park H, Roy N, Kim H, Lee MM, Rubin EM, Lee SW, Kim JF (2018) Rhizosphere microbiome structure alters to enable wilt resistance in tomato. Nat Biotechnol 36:1100–1109. https://doi.org/10.1038/nbt.4232
Leff JW, Jones SE, Prober SM, Barberan A, Borer ET, Firn JL, Harpole WS, Hobbie SE, Hofmockel KS, Knops JM, 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. Proc Natl Acad Sci U S A 112:10967–10972. https://doi.org/10.1073/pnas.1508382112
Li X, Jousset A, de Boer W, Carrion VJ, Zhang T, Wang X, Kuramae EE (2019) Legacy of land use history determines reprogramming of plant physiology by soil microbiome. ISME J 13:738–751. https://doi.org/10.1038/s41396-018-0300-0
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 C, Yao M, Stegen JC, Rui J, Li J, Li X (2017) Long-term nitrogen addition affects the phylogenetic turnover of soil microbial community responding to moisture pulse. Sci Rep UK 7:1–11. https://doi.org/10.1038/s41598-017-17736-w
Liu Y, Ge T, Ye J, Liu S, Shibistova O, Wang P, Wang J, Li Y, Guggenberger G, Kuzyakov Y, Wu J (2019) Initial utilization of rhizodeposits with rice growth in paddy soils: rhizosphere and N fertilization effects. Geoderma 338:30–39. https://doi.org/10.1016/j.geoderma.2018.11.040
Louca S, Parfrey LW, Doebeli M (2016) Decoupling function and taxonomy in the global ocean microbiome. Science 353:1272–1277
Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235
Lu L, Yin S, Liu X, Zhang W, Gu T, Shen Q, Qiu H (2013) Fungal networks in yield-invigorating and-debilitating soils induced by prolonged potato monoculture. Soil Biol Biochem 65:186–194
Lupatini M, Suleiman AK, Jacques RJ, Antoniolli ZI, de Siqueira FA, Kuramae EE, Roesch LF (2014) Network topology reveals high connectance levels and few key microbial genera within soils. Front Environ Sci 2:10
Magoc T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963. https://doi.org/10.1093/bioinformatics/btr507
Mapelli F, Marasco R, Fusi M, Scaglia B, Tsiamis G, Rolli E, Fodelianakis S, Bourtzis K, Ventura S, Tambone F, Adani F, Borin S, Daffonchio D (2018) The stage of soil development modulates rhizosphere effect along a High Arctic desert chronosequence. ISME J 12:1188–1198. https://doi.org/10.1038/s41396-017-0026-4
Marasco R, Mosqueira MJ, Fusi M, Ramond JB, Merlino G, Booth JM, Maggs-Kolling G, Cowan DA, Daffonchio D (2018) Rhizosheath microbial community assembly of sympatric desert speargrasses is independent of the plant host. Microbiome 6:215–218. https://doi.org/10.1186/s40168-018-0597-y
Mc Lean E, Watson M (1985) Soil measurements of plant-available potassium. Potassium in agriculture:277–308
Mendes LW, Kuramae EE, Navarrete AA, van Veen JA, Tsai SM (2014) Taxonomical and functional microbial community selection in soybean rhizosphere. ISME J 8:1577–1587. https://doi.org/10.1038/ismej.2014.17
Nekola JC, White PS (1999) The distance decay of similarity in biogeography and ecology. J Biogeogr 26:867–878. https://doi.org/10.1046/j.1365-2699.1999.00305.x
Nelson DW, Sommers LE (1996) Total carbon, organic carbon, and organic matter. In: Sparks DL, Page AL, Helmke PA, Loeppert RH (Eds) Methods of soil analysis. American Society of Soil Science, Madison, pp 961–1010
Olsen SR (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. US Dep Agric Circ 939:1–19
Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799. https://doi.org/10.1038/nrmicro3109
Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol 193:30–50
Raza W, Ling N, Yang L, Huang Q, Shen Q (2016) Response of tomato wilt pathogen Ralstonia solanacearum to the volatile organic compounds produced by a biocontrol strain Bacillus amyloliquefaciens SQR-9. Sci Rep 6:24856
Rousk J, Bååth 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
Schimel J (2003) The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35:549–563. https://doi.org/10.1016/s0038-0717(03)00015-4
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541
Schmalenberger A, Kertesz MA (2007) Desulfurization of aromatic sulfonates by rhizosphere bacteria: high diversity of the asfA gene. Environ Microbiol 9:535–545
Schöler A, Jacquiod S, Vestergaard G, Schulz S, Schloter M (2017) Analysis of soil microbial communities based on amplicon sequencing of marker genes. Biol Fertil Soils 53:485–489. https://doi.org/10.1007/s00374-017-1205-1
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
Shen D, Jurgens K, Beier S (2018) Experimental insights into the importance of ecologically dissimilar bacteria to community assembly along a salinity gradient. Environ Microbiol 20:1170–1184. https://doi.org/10.1111/1462-2920.14059
Shi S, Nuccio EE, Shi ZJ, He Z, Zhou J, Firestone MK (2016) The interconnected rhizosphere: high network complexity dominates rhizosphere assemblages. Ecol Lett 19:926–936. https://doi.org/10.1111/ele.12630
Tian G, Gao L, Kong Y, Hu X, Xie K, Zhang R, Ling N, Shen Q, Guo S (2017) Improving rice population productivity by reducing nitrogen rate and increasing plant density. PLoS One 12:e0182310. https://doi.org/10.1371/journal.pone.0182310
Tripathi BM, Stegen JC, Kim M, Dong K, Adams JM, Lee YK (2018) Soil pH mediates the balance between stochastic and deterministic assembly of bacteria. ISME J 12:1072–1083. https://doi.org/10.1038/s41396-018-0082-4
Vestergaard G, Schulz S, Schöler A, Schloter M (2017) Making big data smart—how to use metagenomics to understand soil quality. Biol Fertil Soils 53:479–484. https://doi.org/10.1007/s00374-017-1191-3
Vick-Majors TJ, Priscu JC, Amaral-Zettler LA (2014) Modular community structure suggests metabolic plasticity during the transition to polar night in ice-covered Antarctic lakes. ISME J 8:778–789. https://doi.org/10.1038/ismej.2013.190
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267
Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Evol Syst 33:475–505. https://doi.org/10.1146/annurev.ecolsys.33.010802.150448
Xiong Y, Xia H, Za L, Cai Xa FS (2008) Impacts of litter and understory removal on soil properties in a subtropical Acacia mangium plantation in China. Plant Soil 304:179–188. https://doi.org/10.1007/s11104-007-9536-6
Yao M, Rui J, Li J, Dai Y, Bai Y, Heděnec P, Wang J, Zhang S, Pei K, Liu C, Wang Y, Zhili H, Frouz J, Li X (2014) Rate-specific responses of prokaryotic diversity and structure to nitrogen deposition in the Leymus chinensis steppe. Soil Biol Biochem 79:81–90. https://doi.org/10.1016/j.soilbio.2014.09.009
Yuan J, Zhao J, Wen T, Zhao M, Li R, Goossens P, Huang Q, Bai Y, Vivanco JM, Kowalchuk GA, Berendsen RL, Shen Q (2018) Root exudates drive the soil-borne legacy of aboveground pathogen infection. Microbiome 6:1–12. https://doi.org/10.1186/s40168-018-0537-x
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 B, Zhang J, Liu Y, Shi P, Wei G (2018a) Co-occurrence patterns of soybean rhizosphere microbiome at a continental scale. Soil Biol Biochem 118:178–186. https://doi.org/10.1016/j.soilbio.2017.12.011
Zhang T, Chen HYH, Ruan H (2018b) Global negative effects of nitrogen deposition on soil microbes. ISME J 12:1817–1825. https://doi.org/10.1038/s41396-018-0096-y
Zhang Y, Hao X, Alexander TW, Thomas BW, Shi X, Lupwayi NZ (2018c) Long-term and legacy effects of manure application on soil microbial community composition. Biol Fertil Soils 54:269–283
Zhou J, Deng Y, Luo F, He Z, Yang Y (2011a) Phylogenetic molecular ecological network of soil microbial communities in response to elevated CO2. MBio 2. https://doi.org/10.1128/mBio.00122-11
Zhou J, Wu L, Deng Y, Zhi X, Jiang YH, Tu Q, Xie J, Van Nostrand JD, He Z, Yang Y (2011b) Reproducibility and quantitation of amplicon sequencing-based detection. ISME J 5:1303–1313. https://doi.org/10.1038/ismej.2011.11
Zhu S, 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. https://doi.org/10.1016/j.apsoil.2016.07.009
Zhu C, Tian G, Luo G, Kong Y, Guo J, Wang M, Guo S, Ling N, Shen Q (2018) N-fertilizer-driven association between the arbuscular mycorrhizal fungal community and diazotrophic community impacts wheat yield. Agric Ecosyst Environ 254:191–201. https://doi.org/10.1016/j.agee.2017.11.029
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Specially, we are grateful to Lauri Mikonranta for the helpful comments that helped us to improve the manuscript.
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This research was financially supported by the National Key Research and Development Program of China (2017YFD0200206), the Special Fund for Agro-scientific Research in the Public Interest (20150312205), the Natural Science Foundation of Jiangsu Province (BK20190543), the China Postdoctoral Science Foundation (2019M651861), the Innovative Research Team Development Plan of the Ministry of Education of China (IRT_17R56), and the Fundamental Research Funds for the Central Universities (KYT201802).
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Liu, W., Ling, N., Guo, J. et al. Legacy effects of 8-year nitrogen inputs on bacterial assemblage in wheat rhizosphere. Biol Fertil Soils 56, 583–596 (2020). https://doi.org/10.1007/s00374-020-01435-2
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DOI: https://doi.org/10.1007/s00374-020-01435-2