Abstract
Purpose
Little is known about the impact application of fertilizer and manure nutrients on the nutrient stoichiometry of crop–soil–microbe systems. We ask the question to what extent the nutrient availability in the microbe–soil–plant system may be affected by the application of fertilizers or manures.
Methods
The influence of application of inorganic fertilizers or composted manure on the concentrations of carbon (C), nitrogen (N), and phosphorus (P) and their stoichiometric ratios in soil, microbial biomass, enzymes, and plant tissues within the rhizosphere of maize was investigated in a maize–wheat rotation established for 10 years in China.
Results
The higher rate of composted manure was most effective in increasing soil C, N, and P contents and the microbial biomass. Microbes changed biomass stoichiometry instead of regulating related enzyme secretion under different nutrient supplies. Although plants and microbes showed tight but different relationships with the two nutrient sources, competition for N consistently occurred. Pearson’s inter-correlation demonstrates stable Redfield-like C:N:P fractions existed in soil properties and related enzyme activity, but was not always found in crop and microbial biomass after fertilizer and manure application.
Conclusions
The results indicate that soil microbial functioning and coupled feedback with the plants are important in maintaining the stability of fertilized/manured agricultural ecosystems.
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References
Abrar MM, Xu H, Aziz T, Sun N, Mustafa A, Aslam MW, Shah SAA, Mehmood K, Zhou B, Ma X, Chen X, Xu M (2020) Carbon, nitrogen, and phosphorus stoichiometry mediate sensitivity of carbon stabilization mechanisms along with surface layers of a Mollisol after long-term fertilization in Northeast China. J Soils Sediments 21:705–723. https://doi.org/10.1007/s11368-020-02825-7
Achbergerova L, Nahalka J (2011) Polyphosphate - an ancient energy source and active metabolic regulator. Microb Cell Factories 10:63. https://doi.org/10.1186/1475-2859-10-63
Bell C, Carrillo Y, Boot CM, Rocca JD, Pendall E, Wallenstein MD (2014) Rhizosphere stoichiometry: are C : N : P ratios of plants, soils, and enzymes conserved at the plant species-level? New Phytol 201:505–517. https://doi.org/10.1111/nph.12531
Bertrand I, Viaud V, Daufresne T, Pellerin S, Recous S (2019) Stoichiometry constraints challenge the potential of agroecological practices for the soil C storage, A review. Agron Sustain Dev 39. https://doi.org/10.1007/s13593-019-0599-6
Brookes PC, Powlson DS, Jenkinson DS (1982) Measurement of microbial biomass phosphorus in soil. Soil Biol Biochem 14:319–329. https://doi.org/10.1016/0038-0717(82)90001-3
Chen G, Liu Z, Huang YF et al (2017) Effects of different fertilizer treatments on microbial biomass, enzyme activity and related nutrients in soils of continuous cropping sugarcane field. J South Agric 46:2123–2128 http://www.nfnyxb.com/EN/Default.aspx
Chen H, Li DJ, Xiao KC, Wang KL (2018) Soil microbial processes and resource limitation in karst and non-karst forests. Funct Ecol 32:1400–1409. https://doi.org/10.1111/1365-2435.13069
Cleveland CC, Liptzin D (2007) C : N : P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85:235–252. https://doi.org/10.1007/s10533-007-9132-0
Crecchio C, Curci M, Mininni R, Ricciuti P, Ruggiero P (2001) Short-term effects of municipal solid waste compost amendments on soil carbon and nitrogen content, some enzyme activities and genetic diversity. Biol Fertil Soils 34:311–318. https://doi.org/10.1007/s003740100413
Dong CC, Wang W, Liu HY, Xu XT, Zeng H (2019) Temperate grassland shifted from nitrogen to phosphorus limitation induced by degradation and nitrogen deposition: evidence from soil extracellular enzyme stoichiometry. Ecol Indic 101:453–464. https://doi.org/10.1016/j.ecolind.2019.01.046
Dunn C, Jones TG, Girard A, Freeman C (2014) Methodologies for extracellular enzyme assays from wetland soils. Wetlands 34:9–17. https://doi.org/10.1007/s13157-013-0475-0
Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142. https://doi.org/10.1111/j.1461-0248.2007.01113.x
Elser JJ, Fagan WF, Denno RF, Dobberfuhl DR, Folarin A, Huberty A, Interlandi S, Kilham SS, McCauley E, Schulz KL, Siemann EH, Sterner RW (2000) Nutritional constraints in terrestrial and freshwater food webs. Nature 408:578–580. https://doi.org/10.1038/35046058
Fanin N, Fromin N, Buatois B, Hattenschwiler S (2013) An experimental test of the hypothesis of non-homeostatic consumer stoichiometry in a plant littermicrobe system. Ecol Lett 16:764–772. https://doi.org/10.1111/ele.12108
FAO (1998) World reference base for soil resources. World Soil Resources Rep. 84, Rome
Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364. https://doi.org/10.1890/05-1839
Fujita K, Miyabara Y, Kunito T (2019) Microbial biomass and ecoenzymatic stoichiometries vary in response to nutrient availability in an arable soil. Eur J Soil Biol 91:1–8. https://doi.org/10.1016/j.ejsobi.2018.12.005
Ghosh A, Singh AB, Kumar RV, Manna MC, Bhattacharyya R, Rahman MM, Sharma P, Rajput PS, Misra S (2020) Soil enzymes and microbial elemental stoichiometry as bio-indicators of soil quality in diverse cropping systems and nutrient management practices of Indian. Vertisols Appl Soil Ecol 145:103304. https://doi.org/10.1016/j.apsoil.2019.06.007
Huang S, Bao D, Huangfu X, Zhang F, Xu M, Jie X (2006) Effect of long-term fertilization on utilization and accumulation of phosphate nutrient in fluvo-aquic soil. Sci Agric Sin 39:102–108 http://www.chinaagrisci.com
Jiang YF, Guo X, Sun K, Rao L, Li J, Wang LK, Ye YC, Li WF (2017) Spatial variability of C-to-N ratio of farmland soil in Jiangxi Province. Huanjing Kexue 38:3840–3850. https://doi.org/10.13227/j.hjkx.201702193
Jiang YF, Guo X (2019) Stoichiometric patterns of soil carbon, nitrogen, and phosphorus in farmland of the Poyang Lake region in Southern China. J Soils Sediments 19:3476–3488. https://doi.org/10.1007/s11368-019-02317-3
Jiang YF, Rao L, Sun K, Han Y, Guo X (2018) Spatio-temporal distribution of soil nitrogen in Poyang lake ecological economic zone (South-China). Sci Total Environ 626:235–243. https://doi.org/10.1016/j.scitotenv.2018.01.087
Joergensen RG, Brookes PC (2005) Quantification of soil microbial biomass by fumigation-extraction, in: Monit. Assess. Soil Bioremediation,: pp. 281–295. https://doi.org/10.1007/3-540-28904-6_14
Joergensen RG, Mader P, Fliessbach A (2010) Long-term effects of organic farming on fungal and bacterial residues in relation to microbial energy metabolism. Biol Fertil Soils 46:303–307. https://doi.org/10.1007/s00374-009-0433-4
Kunito T, Hiruta N, Miyagishi Y, Sumi H, Moro H (2018) Changes in phosphorus fractions caused by increased microbial activity in forest soil in a short-term incubation study. Chem Speciat Bioavailab 30:9–13. https://doi.org/10.1080/09542299.2018.1433555
Lambers H, Mougel C, Jaillard B, Hinsinger P (2009) Plant-microbe-soil interactions in the rhizosphere: an evolutionary perspective. Plant Soil 321:83–115
Li J, Cooper JM, Lin ZA, Li Y, Yang X, Zhao B (2015) Soil microbial community structure and function are significantly affected by long-term organic and mineral fertilization regimes in the North China Plain. Appl. Soil Ecol 96:75–87. https://doi.org/10.1016/j.apsoil.2015.07.001
Marumoto T, Anderson JPE, Domsch KH (1982) Mineralization of nutrients from soil microbial biomass. Soil Biol Biochem 14:469–475. https://doi.org/10.1016/0038-0717(82)90106-7
McGill W, Shields J, Paul E (1975) Relation between carbon and nitrogen turnover in soil organic fractions of microbial origin. Soil Biol Biochem 7:57–63. https://doi.org/10.1016/0038-0717(75)90032-2
McGroddy ME, Daufresne T, Hedin LO (2004) Scaling of C : N : P stoichiometry in forests worldwide: Implications of terrestrial redfield-type ratios. Ecology 85:2390–2401. https://doi.org/10.1890/03-0351
Mooshammer M, Wanek W, Zechmeister-Boltenstern S, Richter A (2014) Stoichiometric imbalances between terrestrial decomposer communities and their resources: mechanisms and implications of microbial adaptations to their resources. Front Microbiol 5:10. https://doi.org/10.3389/fmicb.2014.00022
Mpanga IK, Nkebiwe PM, Kuhlmann M et al (2019) The form of N supply determines plant growth promotion by P-solubilizing microorganisms in maize. Microorganisms 7:18
Murphy J, Riley JP (1962) A modified of single solution method for the determination of phosphate in nature water. Anal Chim Acta 27:31–36. https://doi.org/10.1016/S0003-2670(00)88444-5
Olsen S Code C Watanabe F Dean L (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. Department of Agriculture Washington pp 1–9
Richardson AE, Barea JM, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339. https://doi.org/10.1007/s11104-009-9895-2
Samuel AD, Domuta C, Ciobanu C, Sandor M (2008) Field management effects on soil enzyme activities. Rom Agric Res 25:61–68. https://doi.org/10.1007/BF02854228
Singh JS, Raghubanshi AS, Singh RS, Srivastava SC (1989) Microbial biomass acts as a source of plant nutrients in dry tropical forest and savanna. Nature 338:499–500. https://doi.org/10.1038/338499a0
Sinsabaugh RL, Hill BH, Shah JJF (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795–U117. https://doi.org/10.1038/nature08632
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, Zak DR, Zeglin LH (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264. https://doi.org/10.1111/j.1461-0248.2008.01245.x
Sinsabaugh RL, Moorhead DL (1994) Resource-allocation to extracellular enzyme-production - a model for nitrogen and phosphorus control of litter decomposition. Soil Biol Biochem 26:1305–1311. https://doi.org/10.1016/0038-0717(94)90211-9
Tao L, Chu G, Liu T, Tang C, Li J, Liang Y (2014) Impacts of organic manure partial substitution for chemical fertilizer on cotton yield, soil microbial community and enzyme activities in mono-cropping system in drip irrigation condition. Acta Ecol Sin 34:6137–6146. https://doi.org/10.5846/stxb201301290184
Tischer A, Potthast K, Hamer U (2014) Land-use and soil depth affect resource and microbial stoichiometry in a tropical mountain rainforest region of southern Ecuador. Oecologia 175:375–393. https://doi.org/10.1007/s00442-014-2894-x
Wang W, Sardans J, Zeng C, Zhong C, Li Y, Penuelas J (2014) Responses of soil nutrient concentrations and stoichiometry to different human land uses in a subtropical tidal wetland. Geoderma 232:459–470. https://doi.org/10.1016/j.geoderma.2014.06.004
Wilson WA, Roach PJ, Montero M, Baroja-Fernández E, Muñoz FJ, Eydallin G, Viale AM, Pozueta-Romero J (2010) Regulation of glycogen metabolism in yeast and bacteria Fems. Microbiol Rev 34:952–985. https://doi.org/10.1111/j.1574-6976.2010.00220.x
Wutzler T, Zaehle S, Schrumpf M, Ahrens B, Reichstein M (2017) Adaptation of microbial resource allocation affects modelled long term soil organic matter and nutrient cycling. Soil Biol Biochem 115:322–336. https://doi.org/10.1016/j.soilbio.2017.08.031
Xu XF, Thornton PE, Post WM (2013) A global analysis of soil microbial biomass carbon, nitrogen and phosphorus in terrestrial ecosystems. Glob Ecol Biogeogr 22:737–749. https://doi.org/10.1111/geb.12029
Xue HL, Lan X, Liang HG, Zhang Q (2019) Characteristics and environmental factors of stoichiometric homeostasis of soil microbial biomass carbon, nitrogen and phosphorus in China. Sustainability 11
Yan WM, Zhong YQW, Liu WZ, Shangguan ZP (2021) Asymmetric response of ecosystem carbon components and soil water consumption to nitrogen fertilization in farmland. Agric Ecosyst Environ 305:107166. https://doi.org/10.1016/j.agee.2020.107166
Yuan HZ, Liu SL, Razavi BS, Zhran M, Wang J, Zhu Z, Wu J, Ge T (2019) Differentiated response of plant and microbial C: N: P stoichiometries to phosphorus application in phosphorus-limited paddy soil. Eur J Soil Biol 95:7. https://doi.org/10.1016/j.ejsobi.2019.103122
Zhang WJ, Liu KL, Wang JZ, Shao X, Xu M, Li J, Wang X, Murphy DV (2015) Relative contribution of maize and external manure amendment to soil carbon sequestration in a long-term intensive maize cropping system. Sci Rep-Uk 5. https://doi.org/10.1038/srep10791
Zhang YL, Sun CX, Chen ZH, Zhang GN, Cheng LJ, Wu ZJ (2019) Stoichiometric analyses of soil nutrients and enzymes in a Cambisol soil treated with inorganic fertilizers or manures for 26 years. Geoderma 353:382–390. https://doi.org/10.1016/j.geoderma.2019.06.026
Zhao G, Liang J, Dan J, Wang J, Qin Y, Zhang W (2011) Review of studies on relationship between soil microbes and plants. J Southwest Forestry Univ 31:83–88
Funding
This study was funded by the National Key Research and Development Program of China (2017YFD0200200) and the National Natural Science Foundation of China (41877049; 41271269).
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Yang, Y., Ji, R., Zhang, H. et al. Stoichiometric analysis of an arable crop–soil–microbe system after repeated fertilizer and compost application for 10 years. J Soils Sediments 21, 1466–1475 (2021). https://doi.org/10.1007/s11368-021-02896-0
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DOI: https://doi.org/10.1007/s11368-021-02896-0