Abstract
Background and aims
Intercropping is known to have low fertilizer input but high production efficiency. However, only few studies have explored the nutrient stoichiometry of soil and microbiome under intercropping patterns to understand the mechanisms underlying the improvement in crop production by intercropping.
Methods
A field-based experiment (started in 2013) was conducted to explore the effects of intercropping of maize with peanut, soybean, gingelly, and sweet potato on soil microbial resource limitation, and the factors controlling the resource limitation were investigated by exploring functional gene abundance and soil C–N–P stoichiometry.
Results
Vector angle (indicator of microbial P limitation) was > 45° in all soil samples. Compared with monocropping, intercropping significantly decreased the vector length and angle. The RC:N-TERC:N was < 0 and the RC:P-TERC:P was > 0 in all soil samples. The RC:P-TERC:P of the monocropping was significantly higher than that of the intercropping soil. Compared with monocropping, the abundances of most of functional genes related to C degradation and fixation, N fixation, nitrification, denitrification, and P activation increased in intercropping soil. Microbial P limitation was associated more with the C–N–P stoichiometric ratios of soil and microbiome than with functional gene abundance. Soil microbial P limitation was notably related to plant N and P uptake and maize yield, regulating by soil microbial N:P, available P:C and P:N ratio.
Conclusions
This study demonstrated the mitigation of microbial P limitation by intercropping and highlighted the importance of understanding the promotion of microbial metabolisms by soil resource stoichiometry, which can help in improving maize productivity.
Similar content being viewed by others
Data Availability
All data generated or analyzed during this study are included in this published article (and its supplementary information files).
References
Achbergerova L, Nahalka J (2011) Polyphosphate an ancient energy source and active metabolic regulator. Microb Cell Fact 10:63
Ågren GI, Wetterstedt JÅM, Billberger MFK (2012) Nutrient limitation on terrestrial plant growth—modeling the interaction between nitrogen and phosphorus. New Phytol 194:953–960
Ai C, Liang G, Sun J, Wang X, Zhou W (2012) Responses of extracellular enzyme activities and microbial community in both the rhizosphere and bulk soil to longterm fertilization practices in a fluvo-aquic soil. Geoderma 173–174:330–338
Bao SD (2000) Soil and Agro-Chemistry Analysis, 3rd edn. China Agric. Press, Beijing
Bender SF, Wagg C, van der Heijden MGA (2016) An underground revolution: biodiversity and soil ecological engineering for agricultural sustainability. Trends Ecol Evol 31:440–452
Bergkemper F, Schoeler A, Engel M, Lang F, Krueger J, Schloter M, Schulz S (2016) Phosphorus depletion in forest soils shapes bacterial communities towards phosphorus recycling systems. Environ Microbiol 18:2767–2767
Brookes PC, Powlson DS, Jenkinson DS (1982) Measurement of microbial biomass phosphorus in soil. Soil Biol Biochem 14(4):319–329
Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil-nitrogen - a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17(6):837–842
Bünemann EK, Oberson A, Liebisch F, Keller F, Annaheim KE, HugueninElie O, Frossard E (2012) Rapid microbial phosphorus immobilization dominates gross phosphorus fluxes in a grassland soil with low inorganic phosphorus availability. Soil Biol Biochem 51:84–95
Cappelli SL, Domeignoz-Horta LA, Loaiza V, Laine AL (2022) Plant biodiversity promotes sustainable agriculture directly and via belowground effects. Trends Plant Sci 27:674–687
Castle SC, Sullivan BW, Knelman J, Hood E, Nemergut DR, Schmidt SK, Cleveland CC (2017) Nutrient limitation of soil microbial activity during the earliest stages of ecosystem development. Oecologia 185:513–524
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 J, Cordero I, Moorhead DL et al (2023) Trade-off between microbial carbon use efficiency and specific nutrient-acquiring extracellular enzyme activities under reduced oxygen. Soil Ecology Letters 5:220157
Cheng J, Han Z, Cong J, Yu J, Zhou J, Zhao M, Zhang YG (2021) Edaphic variables are better indicators of soil microbial functional structure than plant-related ones in subtropical broad-leaved forests. Sci Total Environ 773:145630
Cleveland CC, Liptzin D (2007) C:N: P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85:235–252
Cu STT, Hutson J, Schuller KA (2005) Mixed culture of wheat (Triticum aestivum L.) with white lupin (Lupinus albus L.) improves the growth and phosphorus nutrition of the wheat. Plant Soil 272:143–151
Cui Y, Fang L, Guo X, Wang X, Zhang Y, Li P, Zhang X (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
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 semiarid 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 and Tillage Res 197:104463
Cui J, Zhang S, Wang X, Xu X, Ai C, Liao G, Zhu P, Zhou W (2022a) Enzymatic stoichiometry reveals phosphorus limitation-induced changes in the soil bacterial communities and element cycling: Evidence from a long-term field experiment. Geoderma 426:116124
Cui Y, Bing H, Moorhead DL et al (2022b) Ecoenzymatic stoichiometry reveals widespread soil phosphorus limitation to microbial metabolism across Chinese forests. Community Earth and Environment 3:184
Cui Y, Moorhead DL, Wang X, Xu M, Wang X, Wei X, Zhu Z, Ge T, Peng S, Zhu B, Zhang X, Fang L (2022c) Decreasing microbial phosphorus limitation increases soil carbon release. Geoderma 419:115868
Curtright AJ, Tiemann LK (2021) Intercropping increases soil extracellular enzyme activity :a meta-analysis. Agr Ecosyst Environ 319:107489
de Sosa LL, Helen CG, Miles RM, Andrea S, David MC, Paul WH, Andrew B, Davey LJ (2018) Stoichiometric constraints on the microbial processing of carbon with soil depth along a riparian hillslope. Biol Fertil Soils 54:949–963
Deforest JL (2009) The influence of time, storage temperature, and substrate age on potential soil enzyme activity in acidic forest soils using MUB-linked substrates and l-dopa. Soil Biol Biochem 41:1180–1186
Duchene O, Vian JF, Celette F (2017) Intercropping with legume for agroecological cropping systems: Complementarity and facilitation processes and the importance of soil microorganisms. A Rev Agric Ecosyst Environ 240:148–161
Elser JJ, Acharya K, Kyle M, Cotner J, Makino W, Markow T et al (2003) Growth rate-stoichiometry couplings in diverse biota. Ecol Lett 6:936–943
Fanin N, Fromin N, Buatois B, H€ attenschwiler S (2013) An experimental test of the hypothesis of non-homeostatic consumer stoichiometry in a plant littermicrobe system. Ecol Lett 16:764–772
Gichangi EM, Mnkeni PNS, Brookes PC (2010) Effects of goat manure and inorganic phosphate addition on soil inorganic and microbial biomass phosphorus fractions under laboratory incubation conditions. Soil Sci Plant Nutr 55:764–771
Hartman WH, Richardson CJ (2013) Differential nutrient limitation of soil microbial Biomass and metabolic quotients (qCO2): is there a biological stoichiometry of soil microbes? PLoS ONE 8:e57127
Hauggaard-Nielsen H, Ambus P, Jensen ES (2001) Temporal and spatial distribution of roots and competition for nitrogen in pea-barley in tercrops–a field study employing 32P technique. Plant Soil 236(1):63–74
Hayden HL, Drake J, Imhof M, Oxley APA, Norng S, Mele PM (2010) The abundance of nitrogen cycle genes amoA and nifH depends on land uses and soil types in south-eastern Australia. Soil Biol Biochem 42:1774–1783
Heuck C, Weig A, Spohn M (2015) Soil microbial biomass C:N: P stoichiometry and microbial use of organic phosphorus. Soil Biol Biochem 85:119–129
Hinsinger P, Brauman A, Devau N, Gérard F, Jourdan C, Laclau JP, Le Cadre E, Jaillard B, Plassard C (2011) Acquisition of phosphorus and other poorly mobile nutrients by roots. Where do plant nutrition models fail? Plant Soil 348:29–61
Houlton BZ, Wang YP, Vitousek P, Field C (2008) A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454:327–330
Jian SY, Li JW, Chen L, Wang GS, Mayes MA, Dzentors KE, Hui DF, Luo YQ (2016) Soil extracellular enzyme activities, soil carbon and nitrogen storage under nitrogen fertilization: A meta-analysis. Soil Biol Biochem 101:32–43
Kaspari M, Powers JS (2016) Biogeochemistry and geographical ecology: embracing all twenty-five elements required to build organisms. Am Nat 188:62–73
Latati M, Bargaz A, Belarbi B, Lazali M, Benlahrech S, Tellah S, Kaci G, Drevon JJ, Ounane SM (2016) The intercropping common bean with maize improves the rhizobial efficiency, resource use and grain yield under low phosphorus availability. Eur J Agron 72:80–90
Li H, Shen J, Zhang F, Clairotte M, Drevon JJ, Cadre EL, Hinsinger P (2007) Dynamics of phosphorus fractions in the rhizosphere of common bean (Phaseolus vulgaris L.) and durum wheat (Triticum turgidum durum L.) grown in monocropping and intercropping systems. Plant Soil 312:139–150
Li B, Li YY, Wu HM, Zhang FF, Li CJ, Li XX, Lambers H, Li L (2016) Root exudates drive interspecifc facilitation by enhancing nodulation and N2 fixation. Ecology 113(23):6496–6501
Li CJ, Hofand E, Kuyper TW, Yu Y, Zhang CC, Li HG, Zhang FS, van der Werf W (2020) Syndromes of production in intercropping impact yield gains. Nature Plants 6:653–660
Luo G, Ling N, Nannipieri P, Chen H, Raza W, Wang M et al (2017) Long-term fertilisation regimes affect the composition of the alkaline phosphomonoesterase encoding microbial community of a vertisol and its derivative soil fractions. Biol Fertil Soils 53(4):375–388
Luo GW, Li L, Friman VP, Guo JJ, Guo SW, Shen QR, Ling N (2018) Organic amendments increase crop yields by improving microbe-mediated soil functioning of agroecosystems: a meta-analysis. Soil Biol Biochem 124:105–115
Luo G, Sun B, Li L, Li M, Liu M, Zhu Y et al (2019) Understanding how long-term organic amendments increase soil phosphatase activities: insight into phoD- and phoC-harboring functional microbial populations-sciencedirect. Soil Biol Biochem 139:107632
Luo GW, Xue C, Jiang QH, Xiao Y, Zhang FG, Guo SW, Shen QR, Ling N (2020) Soil carbon, nitrogen, and phosphorus cycling microbial populations and their resistance to global change depend on soil C: N: P stoichiometry. mSystems 5:e00120–e00162
Ma H, Zhou J, Ge J, Nie JW, Zhao J, Xue ZQ, Hu YG, Yang Y, Leanne P, Zhang HD, Zeng ZH (2022) Intercropping improves soil ecosystem multifunctionality through enhanced available nutrients but depends on regional factors. Plant Soil 481:71–84
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
Martin-Guay MO, Paquette A, Dupras J, Rivest D (2018) The new green revolution: sustainable intensification of agriculture by intercropping. Soil Biol Biochem 615:767–772
Mayakaduwage S, Alamgir M, Mosley L, Marschner P (2020) Phosphorus pools in sulfuric acid sulfate soils: influence of water content, ph increase and P addition. J Soil Sediment Contam 20(3):1446–1453
Moorhead DL, Rinkes ZL, Sinsabaugh RL, Weintraub MN (2013) Dynamic relationships between microbial biomass, respiration, inorganic nutrients and enzyme activities: informing enzyme-based decomposition models. Front Microbiol 4:223
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
Mooshammer M, Wanek W, Schnecker J, Wild B, Leitner S, Hofhansl F, Blochl A, Hammerle I, Frank A, Fuchslueger L, Keibinger K, Zechmeister-Boiltenstern S, Richter A (2012) Stoichiometric controls of nitrogen and phosphorus cycling in decomposing beech leaf litter. Ecology 93:770–782
Oberson A, Joner EJ (2005) Microbial turnover of phosphorus in soil. In: Turner BL, Frossard E, Baldwin DS (eds) Organic Phosphorus in the Environment. CABI, Wallingford, pp 133–164
Ostrowska A, Porębska G (2015) Assessment of the C/N ratio as an indicator of the decomposability of organic matter in forest soils. Ecological Indicator 49:104–109
Pabst H, Gerschlauer F, Kiese R, Kuzyakov Y (2016) Land use and precipitation affect organic and microbial carbon stocks and the specific metabolic quotient in soils of eleven ecosystems of Mt. Kilimanjaro Tanzania Land Degradation Dev 27:592–602
Pold G, Kwiatkowski BL, Rastetter EB, Sistla SA (2022) Sporadic P limitation constrains microbial growth and facilitates SOM accumulation in the stoichiometrically coupled, acclimating microbe–plant–soil model. Soil Biol Biochem 165:108489
Ratliff TJ, Fisk MC (2015) Phosphatase activity is related to N availability but not P availability across hardwood forests in the northeastern United States. Soil Biol Biochem 94:61–69
Ren C, Zhao F, Kang D, Yang G, Han X, Tong X, Feng Y, Ren G (2016) Linkages of C:N: P stoichiometry and bacterial community in soil following afforestation of former farmland. For Ecol Manage 376:59–66
Samaddar S, Chatterjee P, Truu J, Anandham R, Kim S, Sa T (2019) Long-term phosphorus limitation changes the bacterial community structure and functioning in paddy soils. Appl Soil Ecol 134:111–115
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
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
Sinsabaugh RL, Hill BH, Follstad Shah JJ (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795–798
Sinsabaugh RL, Manzoni S, Moorhead DL, Richter A (2013) Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling. Ecol Lett 16:930–939
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
Spohn M, Kuzyakov Y (2013) Phosphorus mineralization can be driven by microbial need for carbon. Soil Biol Biochem 61:69–75
Sterner RW, Elser JJ (2002) Ecological Stoichiometry. Princeton University Press, Princeton, Oxford
Sundareshwar PV, Morris JT, Koepfler EK, Fornwalt B (2003) Phosphorus limitation of coastal ecosystem processes. Science 299:563–565
Tang X, Bernard L, Brauman A, Daufresne T, Deleporte P, Desclaux D, Souche G, Placella SA, Hinsinger P (2014) Increase in microbial biomass and phosphorus availability in the rhizosphere of intercropped cereal and legumes under field conditions. Soil Biol Biochem 75:86–93
Tapia-Torres Y, Elser JJ, Souza V, García-Oliva F (2015) Ecoenzymatic stoichiometry at the extremes: how microbes cope in an ultra-oligotrophic desert soil. Soil Biol Biochem 87:34–42
Tian L, Zhao L, Wu X, Fang H, Zhao Y, Hu G, Yue G, Sheng Y, Wu J, Chen J, Wang Z, Li W, Zou D, Ping C-L, Shang W, Zhao Y, Zhang G (2017) Soil moisture and texture primarily control the soil nutrient stoichiometry across the Tibetan grassland. Sci Total Environ 622–623:192–202
Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass-C. Soil Biol Biochem 19(6):703–707
Wagg C, Bender SF, Widmer F, van der Heijden MG (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Nat Acad Sci USA 111:5266–5270
Wang YZ, Zhang YP, Zhang HF, Yang ZY, Zhu QR, Yan BJ, Fei JC, Rong XM, Peng JW, Luo GW (2022) Intercropping-driven nitrogen trade-off enhances maize productivity in a long-term experiment. Field Crop Res 287:108671
Waring BG, Weintraub SR, Sinsabaugh RL (2014) Ecoenzymatic stoichiometry of microbial nutrient acquisition in tropical soils. Biogeochemistry 117(1):101–113
Wilson WA, Roach PJ, Montero M, Baroja-Fernandez E, Munoz FJ, Eydallin G, Viale AM, Pozueta-Romero J (2010) Regulation of glycogen metabolism in yeast and bacteria. FEMS Microbiol Rev 34:952–985
Xu Z, Li C, Zhang CC, Yu Y, van der Werf W, Zhang FS (2020) Intercropping maize and soybean increases efficiency of land and fertilizer nitrogen use: a meta-analysis. Field Crop Res 246:107661
Yan Z, Zhou J, Yang L, Gunina A, Yang Y, Peixoto L et al (2022) Diversified cropping systems benefit soil carbon and nitrogen stocks by increasing aggregate stability: results of three fractionation methods. Sci Total Environ 824:153878–153878
Yang X, Chen X, Yang X (2019) Effect of organic matter on phosphorus adsorption and desorption in a black soil from Northeast China. Soil Tillage Res 187:85–91
Yang ZY, Zhang YP, Wang YZ, Zhang HF, Zhu QR, Yan BJ, Fei JC, Rong XM, Peng JW, Luo GW (2022) Intercropping regulation of soil phosphorus composition and microbially-driven dynamics facilitates maize phosphorus uptake and productivity improvement. Field Crop Res 287:108666
Zhai ZF, Luo M, Yang Y, Liu YX, Chen X, Zhang CW et al (2022) Trade-off between microbial carbon use efficiency and microbial phosphorus limitation under salinization in a tidal wetland. Catena. 209:105809
Zhao FZ, Ren CJ, Han XH, Yang GH, Wang J, Doughty R (2018) Changes of soil microbial and enzyme activities are linked to soil C, N and P stoichiometry in afforested ecosystems. For Ecol Manage 427:289–295
Zheng BX, Zhu YG, Sardans J, Penuelas J, Su JQ (2018) QMEC: a tool for highthroughput quantitative assessment of microbial functional potential in C, N, P, and S biogeochemical cycling. Science China Life Sciences 61:1451–1462
Zheng H, Vesterdal L, Schmidt IK, Rousk J (2022) Ecoenzymatic stoichiometry can reflect microbial resource limitation, substrate quality, or both in forest soils. Soil Biol Biochem 167:108613
Zhou Z, Wang C, Jiang L, Luo Y (2017) Trends in soil microbial communities during secondary succession. Soil Biol Biochem 115:92–99
Zhu ZK, Ge TD, Luo Y, Liu SL, Xu XL, Tong CL, Shibistova O, Guggenberger G, Wu JS (2018) Microbial stoichiometric flexibility regulates rice straw mineralization and its priming effect in paddy soil. Soil Biol Biochem 121:67–76
Acknowledgements
This work was supported by the National Natural Science Foundation of China (42107262), Key Field Research and Development Program of Hunan Province (2019NK 2021), and the Postdoctoral Research Foundation of China (2021M693384).
Author information
Authors and Affiliations
Corresponding authors
Additional information
Responsible Editor: Jihui Tian.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Yang, Z., Zhang, Y. & Luo, G. Regulation of soil C–N–P stoichiometry by intercropping mitigates microbial resource limitations and contributes to maize productivity. Plant Soil 498, 21–38 (2024). https://doi.org/10.1007/s11104-023-06251-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-023-06251-9