Abstract
Purpose
Water and nutrient availability are critical factors that affect soil biological processes in agroecological systems, which are regulated by extracellular ecoenzymatic activity; however, the response of these enzymes to water and nutrient levels is poorly understood.
Methods
A 4-year field experiment with three levels of irrigation (high, 400 mm; medium, 300 mm; and low, 200 mm) and two levels of fertilization (high, 600 kg/ha P2O5 + 300 kg/ha urea; and low, 300 kg/ha P2O5 + 150 kg/ha urea) was conducted to investigate the microbial metabolic status in an arid agroecological system in China using the model of extracellular enzymatic stoichiometry.
Results
Higher C-acquisition enzyme activity and lower N-acquisition enzyme activity were observed during the crop growth stage, suggesting promoted C limitation and alleviated N limitation for microbes by the combination of medium irrigation and low fertilization. Increased microbial C limitation surged the abundance of amoA-AOA and amoA-AOB genes involved in nitrification and strengthened this process. Decreased microbial N limitation hindered the denitrification potential by reducing the abundance of the involved nirK, nirS, nosZ, and narG genes. Increased microbial C limitation was due to the elevated soil water content, which further promoted the activity of C-acquiring enzymes and facilitated microbial decomposition of organic matter. The decreased microbial N limitation was largely related to the increased soil N availability.
Conclusions
These findings suggest that a combination of medium irrigation and low fertilization is effective for organic matter decomposition, by promoting microbial C metabolism and reducing the risk of N loss via alleviation of microbial N limitation. Our results emphasize the roles of stoichiometry-regulated microbial metabolism in soil nutrient transformation and have implications for agricultural practices in arid fertigation agroecosystems.
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References
Bao SD (2008) Soil and agricultural chemistry analysis, 3rd edn. Agriculture Press, Beijing (in Chinese)
Borken W, Savage K, Davidson EA, Trumbore SE (2006) Effects of experimental drought on soil respiration and radiocarbon efflux from a temperate forest soil. Glob Change Biol 12:177–193
Bremner JM, Mulvaney CS (1982) Nitrogen-total. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis, part 2, chemical and microbial properties. Agronomy Society of America, Madison, pp 595–624
Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein MD, Weintraub MN, Zoppini A (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234
Chen H, Li D, Mao Q, Xiao K, Wang K (2019) Resource limitation of soil microbes in karst ecosystems. Sci Total Environ 650:241–248
Chen YL, Chen LY, Peng YF, Ding JZ, Li F, Yang GB, Kou D, Liu L, Fang K, Zhang BB, Wang J, Yang YH (2016) Linking microbial C:N: P stoichiometry to microbial community and abiotic factors along a 3500-km grassland transect on the Tibetan Plateau. Glob Ecol Biogeogr 25:1416–1427
Cleveland CC, Liptzin D (2007) C:N: P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85:235–252
Cui Y, Fang L, Guo X, Han F, Ju W, Ye L, Wang X, Tan W, Zhang X (2019) Natural grassland as the optimal pattern of vegetation restoration in arid and semi-arid regions: evidence from nutrient limitation of soil microbes. Sci Total Environ 648:388–397
Cui Y, Zhang Y, Duan C, Wang X, Zhang X, Ju W, Chen H, Yue S, Wang Y, Li S, Fang L (2020) Ecoenzymatic stoichiometry reveals microbial phosphorus limitation decreases the nitrogen cycling potential of soils in semi-arid agricultural ecosystems. Soil Tillage Res 197:104463
Elser JJ (2002) Biological stoichiometry from genes to ecosystems: ideas, plans, and realities. Integr Comp Biol 42:1226–1226
Elser JJ, Acharya K, Kyle M, Cotner J, Makino W, Markow T, Watts T, Hobbie S, Fagan W, Schade J, Hood J, Sterner RW (2003) Growth rate-stoichiometry couplings in diverse biota. Ecol Lett 6:936–943
Elser JJ, Dobberfuhl DR, MacKay NA, Schampel JH (1996) Organism size, life history, and N: P Stoichiometry: Toward a unified view of cellular and ecosystem processes. Bioscience 46:674–684
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
Hallin S, Jones C, Schloter M, Philippot L (2009) Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. ISME J 3:597–605
Hu H, Chen D, He J (2015) Microbial regulation of terrestrial nitrous oxide formation: understanding the biological pathways for prediction of emission rates. Fems Microbiol Rev 39:729–749
Joergensen RG (1996) The fumigation-extraction method to estimate soil microbial biomass: Calibration of the k(EC) value. Soil Biol Biochem 28:25–31
Kuypers MMM, Marchant HK, Kartal B (2018) The microbial nitrogen-cycling network. Nat Rev Microbiol 16:263–276
Luo S, Zhu L, Liu J, Bu L, Yue S, Shen Y, Li S (2015) Sensitivity of soil organic carbon stocks and fractions to soil surface mulching in semiarid farmland. Eur J Soil Biol 67:35–42
Moorhead DL, Sinsabaugh RL, Hill BH, Weintraub MN (2016) Vector analysis of ecoenzyme activities reveal constraints on coupled C, N and P dynamics. Soil Biol Biochem 93:1–7
Mori T, Ohta S, Ishizuka S, Konda R, Wicaksono A, Heriyanto J, Hardjono A (2010) Effects of phosphorus addition on N2O and NO emissions from soils of an Acacia mangium plantation. Soil Sci Plant Nutr 56:782–788
Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:678–681
Nelson DW, Sommers LE (1982) Total carbon, organic carbon, and organic matter. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis, part 2, chemical and microbial properties. Agronomy Society of America, Madison, pp 539–552
Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. Proc Natl Acad Sci USA 101:11001–11006
Romanowicz KJ, Freedman ZB, Upchurch RA, Argiroff WA, Zak DR (2016) Active microorganisms in forest soils differ from the total community yet are shaped by the same environmental factors: the in fluence of pH and soil moisture. FEMS Microbiol Ecol 73:430–440
Ru J, Zhou Y, Hui D, Zheng M, Wan S (2018) Shifts of growing-season precipitation peaks decrease soil respiration in a semiarid grassland. Glob Chang Biol 24:1001–1011
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
Schimel JP, Weintraub MN (2003) The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35:549–563
Shen HJ, Zhang QQ, Zhu SG, Duan PP, Zhang X, Wu Z, Xiong ZQ (2021) Organic substitutions aggravated microbial nitrogen limitation and decreased nitrogen-cycling gene abundances in a three-year greenhouse. J Environ Manag 288:112379
Sinsabaugh RL, Hill BH, Shah JJF (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795-U117
Sistla SA, Appling AP, Lewandowska AM, Taylor BN, Wolf AA (2015) Stoichiometric flexibility in response to fertilization along gradients of environmental and organismal nutrient richness. Oikos 124:949–959
Sun S, Badgley BD (2019) Changes in microbial functional genes within the soil metagenome during forest ecosystem restoration. Soil Biol Biochem 135:163–172
Tang Y, Zhang X, Li D, Wang H, Chen F, Fu X, Fang X, Sun X, Yu G (2016) Impacts of nitrogen and phosphorus additions on the abundance and community structure of ammonia oxidizers and denitrifying bacteria in Chinese fir plantations. Soil Biol Biochem 103:284–293
Vance E (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707
Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman DG (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–750
Wang J, Wang X, Liu G, Wang G, Wu Y, Zhang C (2020) Fencing as an effective approach for restoration of alpine meadows: Evidence from nutrient limitation of soil microbes. Geoderma 363:114148
Wang XX, Cui YX, Wang YH, Duan CJ, Niu YN, Sun RX, Shen YF, Guo XT, Fang LC (2021) Ecoenzymatic stoichiometry reveals phosphorus addition alleviates microbial nutrient limitation and promotes soil carbon sequestration in agricultural ecosystems. J Soils Sediments. https://doi.org/10.1007/s11368-021-03094-8
Xiao H, Yang H, Zhao M, Monaco TA, Rong Y, Huang D, Song Q, Zhao K, Wang D (2021) Soil extracellular enzyme activities and the abundance of nitrogen-cycling functional genes responded more to N addition than P addition in an Inner Mongolian meadow steppe. Sci Total Environ 759:143541
Xu Z, Yu G, Zhang X, He N, Wang Q, Wang S, Wang R, Zhao N, Jia Y, Wang C (2017) Soil enzyme activity and stoichiometry in forest ecosystems along the North-South Transect in eastern China (NSTEC). Soil Biol Biochem 104:152–163
Yu T, Qi R, Li D, Zhang Y, Yang M (2010) Nitrifier characteristics in submerged membrane bioreactors under different sludge retention times. Water Res 44:2823–2830
Zhang L, Wang XT, Wan WJ, Q, Liao LR, Liu GB, Zhang C (2021) Grazing exclusion reduces soil N2O emissions by regulating nirK- and nosZ-type denitrifiers in alpine meadows. J Soils Sediments 21:3753–3769
Zhang SH, Pan Y, Zhou ZH, Deng J, Zhao FZ, Guo YX, Han XH, Yang GH, Feng YZ, Ren GX, Ren CJ (2022) Resource limitation and modeled microbial metabolism along an elevation gradient. Catena 209:105807
Zhong L, Li FY, Wang Y, Zhou X, Zhou S, Gong X, Bai Y (2018) Mowing and topography effects on microorganisms and nitro gen transformation processes responsible for nitrous oxide emissions in semi-arid grassland of Inner Mongolia. J Soils Sediments 18:929–935
Zhong L, Zhou XQ, Wang YF, Li YH, Zhou ST, Bai YF, Rui YC (2017) Mixed grazing and clipping is beneficial to ecosystem recovery but may increase potential N2O emissions in a semi-arid grassland. Soil Biol Biochem 114:42–51
Funding
This work was financially supported by the West Light Foundation of Chinese Academy of Science (XAB2020YN05); Natural Science Basic Research Program of Shaanxi Province (2019KJXX-081; 2021JM-605); the National Natural Sciences Foundation of China (4177449); Under the auspices of Strategic Priority Program of the Chinese Academy of Sciences (CAS) (XDA20040200); and the Chinese Universities Scientific Fund (2452018336).
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Ye, Z., Wang, J., Li, J. et al. Ecoenzymatic stoichiometry reflects the regulation of microbial carbon and nitrogen limitation on soil nitrogen cycling potential in arid agriculture ecosystems. J Soils Sediments 22, 1228–1241 (2022). https://doi.org/10.1007/s11368-022-03142-x
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DOI: https://doi.org/10.1007/s11368-022-03142-x