Abstract
Purpose
Variation in soil microbial metabolism remains highly uncertain in predicting soil carbon (C) sequestration, and is particularly and poorly understood in agroecosystem with high soil phosphorus (P) variability.
Materials and methods
This study quantified metabolic limitation of microbes and their association with carbon use efficiency (CUE) via extracellular enzymatic stoichiometry and biogeochemical equilibrium models in field experiment employing five inorganic P gradients (0, 75, 150, 225, and 300 kg P ha−1) in farmland used to grow peas.
Results and discussion
Results showed P fertilization significantly increased soil Olsen-P and NO3−-N contents, and enzyme activities (β-1,4-glucosidase and β-D-cellobiosidase) were significantly affected by P fertilization. It indicated that P fertilization significantly decreased microbial P limitation due to the increase of soil available P. Interestingly, P application also significantly decreased microbial nitrogen (N) limitation, a phenomenon primarily attributable to increasing NO3−-N content via increasing biological N fixation within the pea field. Furthermore, P fertilization increased microbial CUE because the reduction in microbial N and P limitation leads to higher C allocation to microbial growth. Partial least squares path modeling (PLS-PM) further revealed that the reduction of microbial metabolic limitation is conducive to soil C sequestration.
Conclusions
Our study revealed that P application in agroecosystem can alleviate not only microbial P limitation but also N limitation, which further reduces soil C loss via increasing microbial CUE. This study provides important insight into better understanding the mechanisms whereby fertilization mediates soil C cycling driven by microbial metabolism in agricultural ecosystems.
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References
Aleixo S, Gama-Rodrigues AC, Gama-Rodrigues EF, Campello EFC, Silva EC, Schripsema J (2020) Can soil phosphorus availability in tropical forest systems be increased by nitrogen-fixing leguminous trees? Sci Total Environ 712. https://doi.org/10.1016/j.scitotenv.2019.136405
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
Chen H, Zhang W, Gurmesa GA, Zhu X, Li D, Mo J (2017) Phosphorus addition affects soil nitrogen dynamics in a nitrogen-saturated and two nitrogen-limited forests. Eur J Soil Sci 68:472–479. https://doi.org/10.1111/ejss.12428
Chen H, Li DJ, Zhao J, Zhang W, Xiao KC, Wang KL (2018) Nitrogen addition aggravates microbial carbon limitation: Evidence from ecoenzymatic stoichiometry. Geoderma 329:61–64. https://doi.org/10.1016/j.geoderma.2018.05.019
Cheng Y, Wang J, Sun N, Xu MG, Zhang JB, Cai ZC, Wang SQ (2018) Phosphorus addition enhances gross microbial N cycling in phosphorus-poor soils: a 15N study from two long-term fertilization experiments. Biol Fertil Soils 54:783–789. https://doi.org/10.1007/s00374-018-1294-5
Cui YX, Fang LC, Guo XB, Wang X, Zhang YJ, Li PF, Zhang XC (2018) Ecoenzymatic stoichiometry and microbial nutrient limitation in rhizosphere soil in the arid area of the northern Loess Plateau, China. Soil Biol Biochem 116:11–21. https://doi.org/10.1016/j.soilbio.2017.09.025
Cui YX, Bing HJ, Fang LC, Wu YH, Yu JL, Shen GT, Jiang M, Wang X, Zhang XC (2019) Diversity patterns of the rhizosphere and bulk soil microbial communities along an altitudinal gradient in an alpine ecosystem of the eastern Tibetan Plateau. Geoderma 338:118–127. https://doi.org/10.1016/j.geoderma.2018.11.047
Cui YX, Fang LC, Deng L, Guo XB, Han F, Ju WL, Wang X, Chen HS, Tan WF, Zhang XC (2019) Patterns of soil microbial nutrient limitations and their roles in the variation of soil organic carbon across a precipitation gradient in an arid and semi-arid region. Sci Total Environ 658:1440–1451. https://doi.org/10.1016/j.scitotenv.2018.12.289
Cui YX, Wang X, Zhang XC, Ju WL, Duan CJ, Guo XB, Wang YQ, Fang LC (2020a) Soil moisture mediates microbial carbon and phosphorus metabolism during vegetation succession in a semiarid region. Soil Biol Biochem 147. https://doi.org/10.1016/j.soilbio.2020.107814
Cui YX, Zhang YL, Duan CJ, Wang X, Zhang XC, Ju WL, Chen HS, Yue SC, Wang YQ, Li SQ, Fang LC (2020b) Ecoenzymatic stoichiometry reveals microbial phosphorus limitation decreases the nitrogen cycling potential of soils in semi-arid agricultural ecosystems. Soil Tillage Res 197. https://doi.org/10.1016/j.still.2019.104463
David IW, Remko AD, Daniel SF, Sara T (2012) smatr 3 - an R package for estimation and inference about allometric lines. Methods Ecol Evol 3:257–259
Dijkstra P, Salpas E, Fairbanks D, Miller EB, Hagerty SB, van Groenigen KJ, Hungate BA, Marks JC, Koch GW, Schwartz E (2015) High carbon use efficiency in soil microbial communities is related to balanced growth, not storage compound synthesis. Soil Biol Biochem 89:35–43. https://doi.org/10.1016/j.soilbio.2015.06.021
Feng JG, Zhu B (2019) A global meta-analysis of soil respiration and its components in response to phosphorus addition. Soil Biol Biochem 135:38–47. https://doi.org/10.1016/j.soilbio.2019.04.008
Fisk M, Santangelo S, Minick K (2015) Carbon mineralization is promoted by phosphorus and reduced by nitrogen addition in the organic horizon of northern hardwood forests. Soil Biol Biochem 81:212–218. https://doi.org/10.1016/j.soilbio.2014.11.022
Geyer KM, Kyker-Snowman E, Grandy AS, Frey SD (2016) Microbial carbon use efficiency: accounting for population, community, and ecosystem-scale controls over the fate of metabolized organic matter. Biogeochemistry 127:173–188. https://doi.org/10.1007/s10533-016-0191-y
Houlton BZ, Wang YP, Vitousek PM, Field CB (2008) A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454:327–330. https://doi.org/10.1038/nature07028
Jensen ES, Carlsson G, Hauggaard-Nielsen H (2020) Intercropping of grain legumes and cereals improves the use of soil N resources and reduces the requirement for synthetic fertilizer N: a global-scale analysis. Agron Sustain Dev 40. https://doi.org/10.1007/s13593-020-0607-x
Joergensen RG (1996) The fumigation-extraction method to estimate soil microbial biomass: calibration of the k (EC) value. Soil Biol Biochem 28:25–31. https://doi.org/10.1016/0038-0717(95)00102-6
Jones DL, Willett VB (2006) Experimental evaluation of methods to quantify dissolved organic nitrogen (DON) and dissolved organic carbon (DOC) in soil. Soil Biol Biochem 38:991–999. https://doi.org/10.1016/j.soilbio.2005.08.012
Kallenbach CM, Wallenstein MD, Schipanksi ME, Grandy AS (2019) Managing agroecosystems for soil microbial carbon use efficiency: ecological unknowns, potential outcomes, and a path forward. Front Microbiol 10. https://doi.org/10.3389/fmicb.2019.01146
Lal R (2011) Sequestering carbon in soils of agro-ecosystems. Food Policy 36:S33–S39. https://doi.org/10.1016/j.foodpol.2010.12.001
Luo RY, Fan JL, Wang WJ, Luo JF, Kuzyakov Y, He JS, Chu HY, Ding WX (2019) Nitrogen and phosphorus enrichment accelerates soil organic carbon loss in alpine grassland on the Qinghai-Tibetan Plateau. Sci Total Environ 650:303–312. https://doi.org/10.1016/j.scitotenv.2018.09.038
Ma ZZ, Zhang XC, Zheng BY, Yue SC, Zhang XC, Zhai BN, Wang ZH, Zheng W, Li ZY, Zamanian K, Razavi BS (2021) Effects of plastic and straw mulching on soil microbial P limitations in maize fields: dependency on soil organic carbon demonstrated by ecoenzymatic stoichiometry. Geoderma 388:12. https://doi.org/10.1016/j.geoderma.2021.114928
Mahmud K, Makaju S, Ibrahim R, Missaoui A (2020) Current progress in nitrogen fixing plants and microbiome research. Plants-Basel 9. https://doi.org/10.3390/plants9010097
Manzoni S, Taylor P, Richter A, Porporato A, Agren GI (2012) Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol 196:79–91. https://doi.org/10.1111/j.1469-8137.2012.04225.x
Mehnaz KR, Keitel C, Dijkstra FA (2018) Effects of carbon and phosphorus addition on microbial respiration, N2O emission, and gross nitrogen mineralization in a phosphorus-limited grassland soil. Biol Fert Soils 54:481–493. https://doi.org/10.1007/s00374-018-1274-9
Miguez-Montero MA, Valentine A, Perez-Fernandez MA (2020) Regulatory effect of phosphorus and nitrogen on nodulation and plant performance of leguminous shrubs. AoB Plants 12. https://doi.org/10.1093/aobpla/plz047
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. https://doi.org/10.1111/j.1747-0765.2010.00501.x
Olsen SR, Sommers LE (1982) Phosphorous. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis, Part 2, Chemical and Microbial Properties. Agronomy Society of America, Madison, pp 403–430
Pang J, Tibbett M, Denton MD, Lambers H, Siddique KHM, Ryan MH (2011) Soil phosphorus supply affects nodulation and N: P ratio in 11 perennial legume seedlings. Crop Pasture Sci 62:992–1001. https://doi.org/10.1071/CP11229
Poeplau C, Herrmann AM, Katterer T (2016) Opposing effects of nitrogen and phosphorus on soil microbial metabolism and the implications for soil carbon storage. Soil Biol Biochem 100:83–91. https://doi.org/10.1016/j.soilbio.2016.05.021
Reed SC, Seastedt TR, Mann CM, Suding KN, Townsend AR, Cherwin KL (2007) Phosphorus fertilization stimulates nitrogen fixation and increases inorganic nitrogen concentrations in a restored prairie. Appl Soil Ecol 36:238–242. https://doi.org/10.1016/j.apsoil.2007.02.002
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. https://doi.org/10.1016/S0038-0717(02)00074-3
Sanchez G, Trinchera L, Russolillo G (2017) Plspm: tools for partial least squares path modeling (PLS-PM). https://CRAN.R-project.org/package=plspm
Santi C, Bogusz D, Franche C (2013) Biological nitrogen fixation in non-legume plants. Ann Bot 111:743–767. https://doi.org/10.1093/aob/mct048
Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394. https://doi.org/10.1890/06-0219
Sinsabaugh RL, Hill BH, Shah JJ (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795–799. https://doi.org/10.1038/nature08632
Sinsabaugh RL, Shah JJ (2012) Ecoenzymatic stoichiometry and ecological theory. Annu Rev Ecol Evol Syst 43:313–343. https://doi.org/10.1146/annurev-ecolsys-071112-124414
Sinsabaugh RL, Manzoni S, Moorhead DL, Richter A (2013) Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling. Ecol Lett 16:930–939. https://doi.org/10.1111/ele.12113
Sinsabaugh RL, Turner BL, Talbot JM, Waring BG, Powers JS, Kuske CR, Moorhead DL, Shah JJ (2016) Stoichiometry of microbial carbon use efficiency in soils. Ecol Monogr 86:172–189. https://doi.org/10.1890/15-2110.1
Smil V (2000) Phosphorus in the environment: natural flows and human interferences. Annu Rev Energ Environ 25:53–88. https://doi.org/10.1146/annurev.energy.25.1.53
Spohn M, Chodak M (2015) Microbial respiration per unit biomass increases with carbon-to-nutrient ratios in forest soils. Soil Biol Biochem 81:128–133. https://doi.org/10.1016/j.soilbio.2014.11.008
Spohn M, Potsch EM, Eichorst SA, Woebken D, Wanek W, Richter A (2016) Soil microbial carbon use efficiency and biomass turnover in a long-term fertilization experiment in a temperate grassland. Soil Biol Biochem 97:168–175. https://doi.org/10.1016/j.soilbio.2016.03.008
Stagnari F, Maggio A, Galieni A, Pisante M (2017) Multiple benefits of legumes for agriculture sustainability: an overview. Chem Biol Technol Ag 4. https://doi.org/10.1186/s40538-016-0085-1
Thirukkumaran CM, Parkinson D (2000) Microbial respiration, biomass, metabolic quotient and litter decomposition in a lodgepole pine forest floor amended with nitrogen and phosphorous fertilizers. Soil Biol Biochem 32:59–66. https://doi.org/10.1016/S0038-0717(99)00129-7
Vesterdal L, Raulund-Rasmussen K (2002) Availability of nitrogen and phosphorus in Norway spruce forest floors fertilized with nitrogen and other essential nutrients. Soil Biol Biochem 34:1243–1251. https://doi.org/10.1016/S0038-0717(02)00064-0
Vera-Nunez JA, Infante-Santiago JP, Velasco-Velasco V, Salgado-Garcia S, Palma-Lopez DJ, Grageda-Cabrera OA, Cardenas R, Pena-Cabriales JJ (2007) Influence of P fertilization on biological nitrogen fixation in herbaceous legumes grown in acid savannah soils from the Tabasco State, Mexico. J Sustainable Agric 31:25–42. https://doi.org/10.1300/J064v31n03_04
Wang YD, Hu N, Xu MG, Li ZF, Lou YL, Chen Y, Wu CY, Wang ZL (2015) 23-year manure and fertilizer application increases soil organic carbon sequestration of a rice-barley cropping system. Biol Fertil Soils 51:583–591. https://doi.org/10.1007/s00374-015-1007-2
Wei TY, Simko V (2017) R package “corrplot”: visualization of a correlation matrix (Version 0.84). https://github.com/taiyun/corrplot
Wei XM, Zhu ZK, Liu Y, Luo Y, Deng YW, Xu XL, Liu SL, Richter A, Shibistova O, Guggenberger G, Wu JS, Ge TD (2020) C:N: P stoichiometry regulates soil organic carbon mineralization and concomitant shifts in microbial community composition in paddy soil. Biol Fert Soils 56:1093–1107. https://doi.org/10.1007/s00374-020-01468-7
Widdig M, Schleuss PM, Biederman LA, Borer ET, Crawley MJ, Kirkman KP, Seabloom EW, Wragg PD, Spohn M (2020) Microbial carbon use efficiency in grassland soils subjected to nitrogen and phosphorus additions. Soil Biol Biochem 146. https://doi.org/10.1016/j.soilbio.2020.107815
Wu Y, Chen WJ, Li Q, Guo ZQ, Li YZ, Zhao ZW, Zhai JY, Liu GB, Xue S (2021) Ecoenzymatic stoichiometry and nutrient limitation under a natural secondary succession of vegetation on the Loess Plateau, China. Land Degrad Dev 32:399–409. https://doi.org/10.1002/ldr.3723
Xiao L, Liu GB, Li P, Li Q, Xue S (2020) Ecoenzymatic stoichiometry and microbial nutrient limitation during secondary succession of natural grassland on the Loess Plateau. China Soil Tillage Res 200:9. https://doi.org/10.1016/j.still.2020.104605
Yue K, Fornara DA, Yang WQ, Peng Y, Peng CH, Liu ZL, Wu FZ (2017) Influence of multiple global change drivers on terrestrial carbon storage: additive effects are common. Ecol Lett 20:663–672. https://doi.org/10.1111/ele.12767
Zang HD, Blagodatskaya E, Wen Y, Xu XL, Dyckmans J, Kuzyakov Y (2018) Carbon sequestration and turnover in soil under the energy crop Miscanthus: repeated 13C natural abundance approach and literature synthesis. GCB Bioenergy 10:262–271. https://doi.org/10.1111/gcbb.12485
Zhao H, Sun BF, Lu F, Wang XK, Zhuang T, Zhang G, Ouyang ZY (2017) Roles of nitrogen, phosphorus, and potassium fertilizers in carbon sequestration in a Chinese agricultural ecosystem. Clim Change 142:587–596. https://doi.org/10.1007/s10584-017-1976-2
Zhang W, Xu YD, Gao DX, Wang X, Liu WC, Deng J, Han XH, Yang GH, Feng YZ, Ren GX (2019) Ecoenzymatic stoichiometry and nutrient dynamics along a revegetation chronosequence in the soils of abandoned land and Robinia pseudoacacia plantation on the Loess Plateau, China. Soil Biol Biochem 134:1–14. https://doi.org/10.1016/j.soilblo.2019.03.017
Zhang ZJ, Li HY, Hu J, Li X, He Q, Tian GM, Wang H, Wang SY, Wang B (2015) Do microorganism stoichiometric alterations affect carbon sequestration in paddy soil subjected to phosphorus input? Ecol Appl 25:866–879. https://doi.org/10.1890/14-0189.1
Zheng MH, Li DJ, Lu X, Zhu XM, Zhang W, Huang J, Fu SL, Lu XK, Mo JM (2016) Effects of phosphorus addition with and without nitrogen addition on biological nitrogen fixation in tropical legume and non-legume tree plantations. Biogeochemistry 131:65–76. https://doi.org/10.1007/s10533-016-0265-x
Zhu ZK, Zhou J, Shahbaz M, Tang HM, Liu SL, Zhang WJ, Yuan HZ, Zhou V, Alharbi H, Wu JS, Kuzyakov Y, Ge TD (2021) Microorganisms maintain C: N stoichiometric balance by regulating the priming effect in long-term fertilized soils. Appl Soil Ecol 167. https://doi.org/10.1016/j.apsoil.2021.104033
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This work was financially supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (CAS) (XDB40000000), the National Natural Science Foundation of China (41977031), and the Program of State Key Laboratory of Loess and Quaternary Geology of CAS (SKLLQGZR1803).
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Wang, X., Cui, Y., Wang, Y. et al. Ecoenzymatic stoichiometry reveals phosphorus addition alleviates microbial nutrient limitation and promotes soil carbon sequestration in agricultural ecosystems. J Soils Sediments 22, 536–546 (2022). https://doi.org/10.1007/s11368-021-03094-8
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DOI: https://doi.org/10.1007/s11368-021-03094-8