Abstract
Purpose
The presence and interaction of shrubs and arbuscular mycorrhizal fungi (AMF) are important for the biogeochemical cycles and sustainable development of arid and semiarid ecosystems. The regulatory mechanisms of the soil microenvironment were explored by studying microbial nutrient constraints in ecosystems.
Materials and methods
Three native shrubs were planted with and without AMF inoculation in the experimental nursery of Inner Mongolia Agricultural University. The soil chemical properties; enzyme activities related to carbon (C), nitrogen (N), and phosphorus (P) acquisition; and microbial biomass C and N were measured to determine the ecoenzymatic stoichiometries and microbial nutrient limitations of the rhizosphere soils.
Results
The ratios of ecoenzymes associated with C acquisition in the rhizospheres of Spiraea pubescens were the largest, as well as microbial C limitation. In addition, Clematis fruticosa and Amygdalus mongolica inoculated with AMF significantly increased the ratios of enzymes related to C acquisition and increased microbial C limitation in the rhizospheres of these two shrubs. The ratio of N and P acquisition enzymes showed that A. mongolica and S. pubescens were significantly lower than C. fruticosa, and the lowest microbial P limitation was found in the rhizosphere soil of C. fruticosa in the noninoculated treatment; however, there was no significant difference between shrubs in the inoculated treatment. The microbial P limitation of the shrubs with AMF inoculation could be positive, negative, or not impacted. This result indicated that AMF regulated microbial P limitation in the rhizospheres of shrubs and was closely related to the accumulation of plant biomass. Partial least squares path model analysis indicated that the main influencing factors of microbial C and P limitation were glomalin-related soil protein (GRSP) and soil available nutrients (SANU).
Conclusions
The results indicated that shrubs and AMF altered the ecoenzymatic stoichiometry of the rhizosphere soils, thus affecting soil microbial nutrient limitation through GRSP and SANU. Native shrubs with AMF inoculation can regulate soil microbial metabolism, providing a theoretical basis for vegetation restoration of degraded ecosystems in drylands.
Similar content being viewed by others
References
Achat DL, Pousse N, Nicolas M, Augusto L (2018) Nutrient remobilization in tree foliage as affected by soil nutrients and leaf life span. Ecol Monogr 88:408–428
Azcón-Aguilar C, Palenzuela J, Roldán A, Bautista S, Vallejo R, Barea JM (2003) Analysis of the mycorrhizal potential in the rhizosphere of representative plant species from desertification-threatened Mediterranean shrublands. Appl Soil Ecol 22:29–37
Barea JM, Pozo MJ, Azcón R, Azcón-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761–1778
Bolan NS, Baskaran S, Thiagarajan S (1996) An evaluation of the methods of measurement of dissolved organic carbon in soils, manures, sludges, and stream water. Commun Soil Sci Plan 27:2723–2737
Boldt-Burisch K, Naeth MA (2017) Heterogeneous soil conditions influence fungal alkaline phosphatase activity in roots of Lotus corniculatus. Appl Soil Ecol 116:55–63
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 17:837–842
Caravaca F, Barea JM, Palenzuela J, Figueroa D, Alguacil MM, Roldán A (2003) Establishment of shrub species in a degraded semiarid site after inoculation with native or allochthonous arbuscular mycorrhizal fungi. Appl Soil Ecol 22:103–111
Cavagnaro TR, Bender SF, Asghari HR, Van der Heijden MGA (2015) The role of arbuscular mycorrhizas in reducing soil nutrient loss. Trends Plant Sci 20:283–290
Chen H, Li D, Zhao J, Zhang W, Xiao K, Wang K (2018) Nitrogen addition aggravates microbial carbon limitation: evidence from ecoenzymatic stoichiometry. Geoderma 329:61–64
Ciccazzo S, Esposito A, Rolli E, Zerbe S, Daffonchio D, Brusetti L (2014) Different pioneer plant species select specific rhizosphere bacterial communities in a high mountain environment. Springerplus 3:391
Cornfield AH (1960) Ammonia released on treating soils with N sodium hydroxide as a possible means of predicting the nitrogen-supplying power of soils. Nature 187:260–261
Cui Y, Bing H, Fang L, Jiang M, Shen G, Yu J, Wang X, Zhu H, Wu Y, Zhang X (2021) Extracellular enzyme stoichiometry reveals the carbon and phosphorus limitations of microbial metabolisms in the rhizosphere and bulk soils in alpine ecosystems. Plant Soil 458:7–20
Cui Y, Fang L, Deng L, Guo X, Han F, Ju W, Wang X, Chen H, Tan W, Zhang X (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
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, Wang X, Zhang X, Ju W, Duan C, Guo X, Wang Y, Fang L (2020a) Soil moisture mediates microbial carbon and phosphorus metabolism during vegetation succession in a semiarid region. Soil Biol Biochem 147:107814
Cui Y, Zhang Y, Duan C, Wang X, Zhang X, Ju W, Chen H, Yue S, Wang Y, Li S, Fang L (2020b) Ecoenzymatic stoichiometry reveals microbial phosphorus limitation decreases the nitrogen cycling potential of soils in semi-arid agricultural ecosystems. Soil Till Res 197:104463
Deng L, Peng C, Huang C, Wang K, Liu Q, Liu Y, Hai X, Shangguan Z (2019) Drivers of soil microbial metabolic limitation changes along a vegetation restoration gradient on the Loess Plateau, China. Geoderma 353:188–200
R Development Core Team (2021) R: A language and environment for statistical computing; R Core Team: Viena, Austria. Available online: https://www.r-project.org/
Fabiańska I, Sosa-Lopez E, Bucher M (2019) The role of nutrient balance in shaping plant root-fungal interactions: facts and speculation. Curr Opin Microbiol 49:90–96
FAO (Food and Agriculture Organization of the United Nations) (2019) Trees, forests and land use in drylands: the first global assessment. Forestry Paper 184. FAO, Rome, Italy, pp. 1–2
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
Haichar FZ, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J, Heulin T, Achouak W (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230
Hernández HD, Larsen J, González-Rodríguez A, Tapia-Torres Y, De la Barrera E, Eguiarte LE, García-Oliva F (2020) Cooperation between Sporobolus airoides and associated arbuscular mycorrhizal fungi for phosphorus acquisition under drought conditions in an oligotrophic desert ecosystem. Rhizosphere 15:100225
Hill BH, Elonen CM, Jicha TM, Kolka RK, Lehto LLP, Sebestyen SD, Seifert-Monson LR (2014) Ecoenzymatic stoichiometry and microbial processing of organic matter in northern bogs and fens reveals a common P-limitation between peatland types. Biogeochemistry 120:203–224
Holátko J, Brtnický M, Kučerík J, Kotianová M, Elbl J, Kintl A, Kynický J, Benada O, Datta R, Jansa J (2021) Glomalin – Truths, myths, and the future of this elusive soil glycoprotein. Soil Biol Biochem 153:108116
Jiang Y, Lei Y, Qin W, Korpelainen H, Li C (2019) Revealing microbial processes and nutrient limitation in soil through ecoenzymatic stoichiometry and glomalin-related soil proteins in a retreating glacier forefield. Geoderma 338:313–324
Jiang Y, Wang W, Xie Q, Liu N, Liu L, Wang D, Zhang X, Yang C, Chen X, Tang D, Wang E (2017) Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science 356:1172–1175
Joergensen RG, Mueller T (1996) The fumigation-extraction method to estimate soil microbial biomass: Calibration of the kEN value. Soil Biol Biochem 28:33–37
Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phytol 163:459–480
Jones DL, Kielland K, Sinclair FL, Dahlgren RA, Newsham KK, Farrar JF, Murphy DV (2009) Soil organic nitrogen mineralization across a global latitudinal gradient. Glob Biogeochem Cycles 23:GB1016
Lareen A, Burton F, Schäfer P (2016) Plant root-microbe communication in shaping root microbiomes. Plant Mol Biol 90:575–587
Lerat S, Lapointe L, Gutjahr S, Piché Y, Vierheilig H (2003) Carbon partitioning in a split-root system of arbuscular mycorrhizal plants is fungal and plant species dependent. New Phytol 157:589–595
Luo L, Gu J (2018) Nutrient limitation status in a subtropical mangrove ecosystem revealed by analysis of enzymatic stoichiometry and microbial abundance for sediment carbon cycling. Int Biodeter Biodegr 128:3–10
Mcgonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501
Mebius LJ (1960) A rapid method for the determination of organic carbon in soil. Anal Chim Acta 22:120–124
Muñoz-Rojas M, Erickson TE, Dixon KW, Merritt DJ (2016) Soil quality indicators to assess functionality of restored soils in degraded semiarid ecosystems. Restor Ecol 24:1–10
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 4:1–12
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
Municipal government office (2019) Nature and Geography. Hohhot: Municipal government office. http://www.huhhot.gov.cn/mlqc/qcgk/zrdl/. Accessed 31 Oct 2020 (in Chinese)
Olsen SR, Sommers LE (1982) Phosphorous. In: Page AL, Miller RH, Keeney DR (Eds.) Methods of Soil Analysis, Part 2, Chemical and Microbial Properties. Madison Wisconsin pp 403–430
Querejeta JI, Allen MF, Alguacil MM, Roldán A (2007) Plant isotopic composition provides insight into mechanisms underlying growth stimulation by AM fungi in a semiarid environment. Funct Plant Biol 34:683–691
Reynolds JF, Smith DMS, Lambin EF, Turner BL II, Mortimore M, Batterbury SPJ, Downing TE, Dowlatabadi H, Fernández RJ, Herrick JE, Huber-Sannwald E, Jiang H, Leemans R, Lynam T, Maestre FT, Ayarza M, Walker B (2007) Global desertification: Building a science for dryland development. Science 316:847–851
Rodríguez-Caballero G, Caravaca F, Fernández-González AJ, Alguacil MM, Fernández-López M, Roldán A (2017) Arbuscular mycorrhizal fungi inoculation mediated changes in rhizosphere bacterial community structure while promoting revegetation in a semiarid ecosystem. Sci Total Environ 584–585:838–848
Roth R, Paszkowski U (2017) Plant carbon nourishment of arbuscular mycorrhizal fungi. Curr Opin Plant Biol 39:50–56
Sanchez G, Trinchera L, Russolillo G (2017) plspm: Tools for partial least squares path modeling (PLS-PM). R package version plspm 0.4.9. Retrieved from http://CRAN.R-project.org/package=plspm
Singh AK, Rai A, Pandey V, Singh N (2017) Contribution of glomalin to dissolve organic carbon under different land uses and seasonality in dry tropics. J Environ Manage 192:142–149
Sinsabaugh RL, Follstad SJJ (2012) Ecoenzymatic stoichiometry and ecological theory. Annu Rev Ecol Evol Syst 43:313–343
Sinsabaugh RL, Hill BH, Shah JJF (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795–798
Sinsabaugh RL, Klug MJ, Collins HP, Yeager PE, Petersen SO (1999) Characterizing soil microbial communities. In: Robertson GP, Coleman D, Bledsoe CS, Sollins P (eds) Standard soil methods for long-term ecological research. Oxford University Press, New York, pp 329–333
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, 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
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic press, New York, pp 147–157
Sterner RW, Elser JJ (2002) Stoichiometry and homeostasis. In: Sterner RW, Elser JJ (eds) Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere. Princeton University Press, Princeton, NJ, USA, pp 1–43
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
Toljander JF, Lindahl BD, Paul LR, Elfstrand M, Finlay RD (2007) Influence of arbuscular mycorrhizal mycelial exudates on soil bacterial growth and community structure. FEMS Microbiol Ecol 61:295–304
Van der Heijden MG, Bardgett RD, Van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310
Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707
Veresoglou SD, Chen B, Rillig MC (2012) Arbuscular mycorrhiza and soil nitrogen cycling. Soil Biol Biochem 46:53–62
Vives-Peris V, Molina L, Segura A, Gómez-Cadenas A, Pérez-Clemente RM (2018) Root exudates from citrus plants subjected to abiotic stress conditions have a positive effect on rhizobacteria. J Plant Physiol 228:208–217
Wright SF, Upadhyaya A (1998) A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi. Plant Soil 198:97–107
Wu Q, H X, Zou Y, He K, Sun Y, Cao M (2012) Spatial distribution of glomalin-related soil protein and its relationships with root mycorrhization, soil aggregates, carbohydrates, activity of protease and β-glucosidase in the rhizosphere of Citrus unshiu. Soil Biol Biochem 45:181–183
Xu H, Shao H, Lu Y (2019) Arbuscular mycorrhiza fungi and related soil microbial activity drive carbon mineralization in the maize rhizosphere. Ecotox Environ Safe 182:109476
Yao Y, Shao M, Fu X, Wang X, Wei X (2019) Effects of shrubs on soil nutrients and enzymatic activities over a 0–100 cm soil profile in the desert-loess transition zone. CATENA 174:362–370
Zhang L, Xu M, Liu Y, Zhang F, Hodge A, Feng Gu (2016) Carbon and phosphorus exchange may enable cooperation between an arbuscular mycorrhizal fungus and a phosphate-solubilizing bacterium. New Phytol 210:1022–1032
Zhou Z, Wang C, Jiang L, Luo Y (2017) Trends in soil microbial communities during secondary succession. Soil Biol Biochem 115:92–99
Acknowledgements
We are grateful to the Ecological Restoration Laboratory of Heilongjiang University for providing the AMF inoculum.
Funding
This work was funded by the National Natural Science Foundation of China (41761055), the China Postdoctoral Science Foundation (2018M643778XB), and the Science and Technology Planning Project of Inner Mongolia (2020GG0029 and 2020GG0075).
Author information
Authors and Affiliations
Corresponding authors
Additional information
Responsible Editor: Qiaoyun Huang
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
About this article
Cite this article
Liu, T., Hao, L., Bai, S. et al. Ecoenzymatic stoichiometry and microbial nutrient limitation of shrub rhizosphere soils in response to arbuscular mycorrhizal fungi inoculation. J Soils Sediments 22, 594–606 (2022). https://doi.org/10.1007/s11368-021-03096-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11368-021-03096-6