Skip to main content
SpringerLink
Log in

Decoupling of soil organic carbon and nutrient mineralization across plant communities as affected by microbial stoichiometry

  • Original Paper
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

Abstract

To investigate the effects of shrubification—the global phenomena of an increase of shrubs in grasslands—on C, N, and P cycles, the changes in soil organic C, N, and P mineralization in an alpine meadow were compared across five plant communities: grasses and four shrub species–dominated patches. The nutrient content and stoichiometry (C:N:P) of leaves, litter, microbial biomass, and soil organic matter (SOM) were analyzed during vegetation season. Net rates of N and P mineralization were measured in situ in the top 20 cm of soil throughout the growing season, and organic C mineralization was determined under controlled conditions. Microbial C:N, C:P, and N:P ratios in the top 20 cm generally decreased with increasing plant size (height combined with crown diameter), associated with greater input of litter with lower C:nutrient ratios under shrubs. The net N and P mineralization rates in soil under shrubs were about 3- to sevenfold and 4- to 15-fold faster, respectively, compared with those under grasses. The increase in organic C mineralization under shrubs compared with that under grasses was much smaller than the increase of N or P mineralization under shrubs. This indicates faster turnover of nutrients than C leading to decoupling of organic C and nutrient mineralization across plant communities by shrubification. The C:N, C:P, and N:P ratios of organic pools mineralized in soil decreased with increasing plant size, but increased with respective microbial C:N, C:P, and N:P ratios across plant communities. This indicates that specific SOM pools were mineralized depending on plant communities and microbial stoichiometry in soil. Consequently, the decoupling of organic C and nutrient mineralization across plant communities is driven by microbial stoichiometry and increases by shrubification.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

Data presented in this paper can be obtained by sending a written request to the corresponding author.

References

  • Achat DL, Bakker MR, Zeller B, Pellerin S, Bienaimé S, Morel C (2010) Long-term organic phosphorus mineralization in Spodosols under forests and its relation to carbon and nitrogen mineralization. Soil Biol Biochem 42:1479–1490

    Article  CAS  Google Scholar 

  • Baer SG, Church JM, Williard KWJ, Groninger JW (2006) Changes in intrasystem N cycling from N2-fixing shrub encroachment in grassland: multiple positive feedbacks. Agric Ecosyst Environ 115:174–182

    Article  CAS  Google Scholar 

  • Bao S (2000) Soil agrochemical analysis. China Agricultural Press, Beijing

    Google Scholar 

  • Berg B, McClaugherty C (2008) Plant litter: decomposition, humus formation, carbon sequestration, 2nd edn. Springer-Verlag, Berlin Heidelberg

    Book  Google Scholar 

  • Binkley D, Giardina C, Bashkin MA (2000) Soil phosphorus pools and supply under the influence of Eucalyptus saligna and nitrogen-fixing Albizia facaltaria. For Ecol Manag 128:241–247

    Article  Google Scholar 

  • Blagodatsky A, Richter O (1998) Microbial growth in soil and nitrogen turnover: a theoretical model considering the activity state of microorganisms. Soil Biol Biochem 30:1743–1755

    Article  CAS  Google Scholar 

  • Brandt JS, Haynes MA, Kuemmerle T, Waller DM, Radeloff VC (2013) Regime shift on the roof of the world: Alpine meadows converting to shrublands in the southern Himalayas. Biol Conserv 158:116–127

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Bunemann EK, Augstburger S, Frossard E (2016) Dominance of either physicochemical or biological phosphorus cycling processes in temperate forest soils of contrasting phosphate availability. Soil Biol Biochem 101:85–95

    Article  CAS  Google Scholar 

  • Camenzind T, Grenz KP, Lehmann J, Rillig MC (2021) Soil fungal mycelia have unexpectedly flexible stoichiometric C: N and C: P ratios. Ecol Lett 24:208–218

    Article  PubMed  Google Scholar 

  • Carboni M, Gueguen M, Barros C, Georges D, Boulangeat I, Douzet R, Dullinger S, Klonner G, van Kleunen M, Essl F (2017) Simulating plant invasion dynamics in mountain ecosystems under global change scenarios. Glob Change Biol 24:e289–e302

    Article  Google Scholar 

  • Chandregowda MH, Murthy K, Bagchi S (2018) Woody shrubs increase soil microbial functions and multifunctionality in a tropical semi-arid grazing ecosystem. J Arid Environ 155:65–72

    Article  Google Scholar 

  • Chen J, Seven J, Zilla T, Dippold MA, Blagodatskaya E, Kuzyakov Y (2019) Microbial C:N: P stoichiometry and turnover depend on nutrients availability in soil: A 14C, 15N and 33P triple labelling study. Soil Biol Biochem 131:206–216

    Article  CAS  Google Scholar 

  • Clark JS (1990) Landscape interactions among nitrogen mineralization, species composition, and long-term fire frequency. Biogeochemistry 11:1–22

    Article  Google Scholar 

  • Clayton J, Lemanski K, Bonkowski M (2021) Shifts in soil microbial stoichiometry and metabolic quotient provide evidence for a critical tipping point at 1% soil organic carbon in an agricultural post-mining chronosequence. Biol Fertil Soils 57:435–446

    Article  CAS  Google Scholar 

  • Cui J, Zhu ZK, Xu XL, Liu SL, Jones DL, Kuzyakov Y, Shibistova O, Wu JS, Ge TD (2020) Carbon and nitrogen recycling from microbial necromass to cope with C: N stoichiometric imbalance by priming. Soil Biol Biochem 142:107720

    Article  CAS  Google Scholar 

  • Díaz-Raviña M, Acea MJ, Carballas T (1995) Seasonal changes in microbial biomass and nutrient flush in forest soils. Biol Fertil Soils 19:220–226

    Article  Google Scholar 

  • Ehtesham E, Bengtson P (2017) Decoupling of soil carbon and nitrogen turnover partly explains increased net ecosystem production in response to nitrogen fertilization. Sci Rep 7:46286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eldridge DJ, Ding J (2020) Remove or retain: ecosystem effects of woody encroachment and removal are linked to plant structural and functional traits. New Phytol 229:2637–2646

    Article  PubMed  CAS  Google Scholar 

  • Eldridge DJ, Bowker MA, Maestre FT, Roger E, Reynolds JF, Whitford WG (2011) Impacts of shrub encroachment on ecosystem structure and functioning: towards a global synthesis. Ecol Lett 14:709–722

    Article  PubMed  PubMed Central  Google Scholar 

  • Elser JJ, Urabe J (1999) The stoichiometry of consumer-driven nutrient recycling: theory, observation, and consequences. Ecology 80:735–751

    Article  Google Scholar 

  • Elser JJ, Acharya K, Kyle M, Cotner J, Makino W, Markow T, Watts T, Hobbie S, Fagan W, Schade J (2003) Growth rate-stoichiometry couplings in diverse biota. Ecol Lett 6:936–943

    Article  Google Scholar 

  • Enríquez S, Duarte CM, Sand-Jensen K (1993) Patterns in decomposition rates among photosynthetic organisms: the importance of detritus C:N: P content. Oecologia 94:457–471

    Article  PubMed  Google Scholar 

  • Ettema CH, Wardle DA (2002) Spatial soil ecology. Trends Ecol Evol 17:177–183

    Article  Google Scholar 

  • Fang Y, Singh BP, Collins D, Armstrong R, Zwieten LV, Tavakkoli E (2020) Nutrient stoichiometry and labile carbon content of organic amendments control microbial biomass and carbon-use efficiency in a poorly structured sodic-subsoil. Biol Fertil Soils 56:219–233

    Article  CAS  Google Scholar 

  • Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364

    Article  PubMed  Google Scholar 

  • Gao XL, Li XG, Zhao L, Kuzyakov Y (2019) Regulation of soil phosphorus cycling in grasslands by shrubs. Soil Biol Biochem 133:1–11

    Article  CAS  Google Scholar 

  • Ge T, Luo Y, Singh BP (2020) Resource stoichiometric and fertility in soil. Biol Fertil Soils 56:1091–1092

    Article  Google Scholar 

  • Hernandez RR, Debenport SJ, Leewis MCCE, Ndoye F, Nkenmogne KIE, Soumare A, Thuita M, Gueye M, Miambi E, Chapuis-Lardy L, Diedhiou I, Dick RP (2015) The native shrub, Piliostigma reticulatum, as an ecological “resource island” for mango trees in the Sahel. Agric Ecosyst Environ 204:51–61

    Article  CAS  Google Scholar 

  • He JL, Li XG (2016) Potentilla fruticosa has a greater capacity to translocate phosphorus from the lower to upper soils than herbaceous grasses in an alpine meadow. Agric Ecosyst Environ 228:19–29

    Article  CAS  Google Scholar 

  • Hicks LC, Lajtha K, Rousk J (2021) Nutrient limitation may induce microbial mining for resources from persistent soil organic matter. Ecology 102:e03328

    Article  PubMed  Google Scholar 

  • Hicks LC, Leizeagal A, Rousk K, Michelsen A, Rousk J (2020) Simulated rhizosphere deposits induce microbial N-mining that may accelerate shrubification in the subarctic. Ecology 101:e03094

    Article  PubMed  Google Scholar 

  • HilleRisLambers R, Rietkerk M, van den Bosch F, Prins HHT, de Kroon H (2001) Vegetation pattern formation in semi-arid grazing systems. Ecology 82:50–61

    Article  Google Scholar 

  • Hopkins DW, Sparrow AD, Shillam LL, English LC, Dennis PG, Novis P, Elberling B, Gregorich EG, Greenfield LG (2008) Enzymatic activities and microbial communities in an Antarctic dry valley soil: responses to C and N supplementation. Soil Biol Biochem 40:2130–2136

    Article  CAS  Google Scholar 

  • Howison RA, Olff H, van de Koppel J, Smit C (2017) Biotically driven vegetation mosaics in grazing ecosystems: the battle between bioturbation and biocompaction. Ecol Monogr 87:363–378

    Article  Google Scholar 

  • Khan KS, Joergensen RG (2012) Relationships between P fractions and the microbial biomass in soils under different land use management. Geoderma 173:274–281

    Article  CAS  Google Scholar 

  • Kuzyakov Y, Mason-Jones K (2018) Viruses in soil: nano-scale undead drivers of microbial life, biogeochemical turnover and ecosystem functions. Soil Biol Biochem 127:305–317

    Article  CAS  Google Scholar 

  • Liu XJA, Hayer M, Mau RL, Schwartz E, Dijkstra P, Hungate BA (2021) Substrate stoichiometric regulation of microbial respiration and community dynamics across four different ecosystems. Soil Biol Biochem 163:108458

    Article  CAS  Google Scholar 

  • Lu RK (2000) Soil and agrochemical analysis methods. China Agricultural Science & Technology Press, Beijing

    Google Scholar 

  • Lu X, Liang E, Camarero JJ, Ellison AM (2021) An unusually high shrubline on the Tibetan Plateau. Ecology 102:e03310

    Article  PubMed  Google Scholar 

  • Mooshammer M, Wanek W, Schnecker J, Wild B, Leitner S, Hofhansl F, Blochl A, Hammerle I, Frank AH, Fuchslueger L (2012) Stoichiometric controls of nitrogen and phosphorus cycling in decomposing beech leaf litter. Ecology 93:770–782

    Article  PubMed  Google Scholar 

  • 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 5:22

    Article  PubMed  PubMed Central  Google Scholar 

  • Morel C, Tiessen H, Stewart JWB (1996) Correction for P-sorption in the measurement of soil microbial biomass P by CHCl3 fumigation. Soil Biol Biochem 28:1699–1706

    Article  CAS  Google Scholar 

  • Mou XM, Wu YN, Niu ZQ, Jia B, Guan ZH, Chen J, Li H, Cui HY, Kuzyakov Y, Li XG (2020) Soil phosphorus accumulation changes with decreasing temperature along a 2300 m altitude gradient. Agric Ecosyst Environ 301:107050

    Article  CAS  Google Scholar 

  • Murphy CJ, Baggs EM, Morley N, Wall DP, Paterson E (2015) Rhizosphere priming can promote mobilisation of N-rich compounds from soil organic matter. Soil Biol Biochem 81:236–243

    Article  CAS  Google Scholar 

  • Nannipieri P, Trasar-Cepeda C, Dick RP (2018) Soil enzyme activity: a brief history and biochemistry as a basis for appropriate interpretations and meta-analysis. Biol Fertil Soils 54:11–19

    Article  CAS  Google Scholar 

  • Nelson DW, Sommers LE (1982) Total carbon, organic carbon and organic matter, second ed. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis, part 2, chemical and microbiological properties agronomy monograph, vol 9. American Society of Agronomy Inc, Madison, pp 539–579

    Google Scholar 

  • Ren C, Chen J, Deng J, Zhao FZ, Han XH, Yang GH, Tong XG, Feng YZ, Shelton S, Ren GX (2017) Response of microbial diversity to C:N: P stoichiometry in fine root and microbial biomass following afforestation. Biol Fertil Soils 53:457–468

    Article  CAS  Google Scholar 

  • Rousk K, Michelsen A, Rousk J (2016) Microbial control of soil organic matter mineralization responses to labile carbon in subarctic climate change treatments. Glob Change Biol 22:4150–4161

    Article  Google Scholar 

  • Schleuss PM, Widdig M, Biederman LA, Borer ET, Crawley MJ, Kirkman KP, Seabloom EW, Wragg PD, Spohn M (2021) Microbial substrate stoichiometry governs nutrient effects on nitrogen cycling in grassland soils. Soil Biol Biochem 155:108168

    Article  CAS  Google Scholar 

  • Schroeder J, Jannoura R, Beuschel R, Pfeiffer B, Dyckmans J, Murugan R, Chavannavar S, Wachendorf C, Joergensen RG (2020) Carbon use efficiency and microbial functional diversity in a temperate Luvisol and a tropical Nitisol after millet litter and N addition. Biol Fertil Soils 56:1139–1150

    Article  CAS  Google Scholar 

  • Sistla AA, Schimel JP (2012) Stoichiometric flexibility as a regulator of carbon and nutrient cycling in terrestrial ecosystems under change. New Phytol 196:68–78

    Article  CAS  PubMed  Google Scholar 

  • Song M, Yu L, Fu S, Korpelainen H, Li C (2020) Stoichiometric flexibility and soil bacterial communities respond to nitrogen fertilization and neighbor competition at the early stage of primary succession. Biol Fertil Soils 56:1121–1135

    Article  CAS  Google Scholar 

  • Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton

    Google Scholar 

  • Stock S, Köster M, Dippold MA, Najera F, Merino-Guzman C, Matus F, Boy J, Merino C, Spielvogel S, Gorbushina A (2019) Environmental drivers and stoichiometric constraints on enzyme activities in soils from rhizosphere to continental scales. Geoderma 337:973–982

    Article  CAS  Google Scholar 

  • Tabatabai MA, Bremner JM (1972) Assay of urease activity in soils. Soil Biol Biochem 4:479–487

    Article  CAS  Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass-C. Soil Biol Biochem 19:703–707

    Article  CAS  Google Scholar 

  • Wang L, Chen Y, Zhou Y, Xu Z, Tan B, You C, Zhang L, Li H, Zheng H, Guo L, Wang L, Huang Y, Zhang J, Liu Y (2021a) Environmental conditions and litter nutrients are key determinants of soluble C, N, and P release during litter mixture decomposition. Soil till Res 209:104928

    Article  Google Scholar 

  • Wang G, Gao Q, Yang Y, Hobbie SE, Reich PB, Zhou J (2021b) Soil enzymes as indicators of soil function: a step toward greater realism in microbial ecological modeling. Glob Change Biol 28:1935–1950

    Article  CAS  Google Scholar 

  • Wang J, Wu Y, Li J, He Q, Bing H (2021c) Soil enzyme stoichiometry is tightly linked to microbial community composition in successional ecosystems after glacier retreat. Soil Biol Biochem 162:108429

    Article  CAS  Google Scholar 

  • Wei X, Zhu Z, Liu Y, Luo Y, Deng Y, Xu X, Liu S, Richter A, Shibistova O, Guggenberger G, Wu J, Ge T (2020) C:N: P stoichiometry regulates soil organic carbon mineralization and concomitant shifts in microbial community composition in paddy soil. Biol Fertil Soils 56:1093–1107

    Article  CAS  Google Scholar 

  • Yang YH, Fang JY, Tang YH, Ji CJ, Zheng CY, He JS, Zhu B (2008) Storage, patterns and controls of soil organic carbon in the Tibetan grasslands. Glob Chang Biol 14:1592–1599

    Article  Google Scholar 

  • Zechmeister-Boltenstern S, Keiblinger KM, Mooshammer M, Peňuelas J, Richter A, Sardans J, Wanek W (2015) The application of ecological stoichiometry to plant–microbial–soil organic matter transformations. Ecol Monogr 85:133–155

    Article  Google Scholar 

  • Zhang W, Xu Y, Gao D, Wang X, Liu W, Deng J, Han X, Yang G, Feng Y, Ren G (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

    Article  CAS  Google Scholar 

  • Zhao YN, Mou XM, Wei M, Li XG (2021) Effect of vegetation mosaic on spatial heterogeneity of soil organic carbon mineralization and nitrification in an alpine meadow. Appl Soil Ecol 165:104007

    Article  Google Scholar 

  • Zhou Y, Boutton TW, Wu XB (2018) Soil phosphorus does not keep pace with soil carbon and nitrogen accumulation following woody encroachment. Glob Change Biol 24:1992–2007

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank the Lanzhou University Research Station of Alpine Meadow and Wetland Ecosystems for supporting the field sampling and measurements. YK is grateful for the support provided by the RUDN University Strategic Academic Leadership Program. The authors highly appreciate the constructive comments from the anonymous reviewers and Editor Paolo Nannipieri, which have greatly helped improve the quality of this paper.

Funding

This work was financed by the National Natural Science Foundation of China (41571279).

Author information

Authors and Affiliations

  1. State Key Laboratory of Grassland and Agro-Ecosystems, College of Ecology, Lanzhou University, 222 South Tianshui Road, Lanzhou, 730000, China

    Jie Chen, Bin Jia, Shu Gang, Yawen Li, Fen-Can Li, Xiao Ming Mou & Xiao Gang Li

  2. Department of Soil Science of Temperate Ecosystems, Department of Agricultural Soil Science, University of Goettingen, 37077, Göttingen, Germany

    Yakov Kuzyakov

  3. Peoples’ Friendship University of Russia (RUDN University), 117198, Moscow, Russia

    Yakov Kuzyakov

Authors
  1. Jie Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bin Jia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shu Gang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yawen Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fen-Can Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiao Ming Mou
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yakov Kuzyakov
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xiao Gang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xiao Gang Li.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

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.

Supplementary file1 (DOCX 1279 KB)

Rights and permissions

Springer Nature or its licensor 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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, J., Jia, B., Gang, S. et al. Decoupling of soil organic carbon and nutrient mineralization across plant communities as affected by microbial stoichiometry. Biol Fertil Soils 58, 693–706 (2022). https://doi.org/10.1007/s00374-022-01655-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-022-01655-8

Keywords

Search

Navigation