Skip to main content

Advertisement

Log in

Carbon storage and plant-soil linkages among soil aggregates as affected by nitrogen enrichment and mowing management in a meadow grassland

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

Soil aggregates constitute spatially-separated microbial habitats and architectural units for biogeochemical reactions. However, little is known about how aggregates varying in size can affect soil carbon (C) storage and mediate the direction of plant-soil interactions.

Methods

In a meadow steppe, we assessed soil aggregate C storage affected by nitrogen (N) addition and mowing and to what degree plant-soil interactions differed among soil aggregate-size classes.

Results

Nitrogen addition increased plant biomass, soil C concentration in macroaggregates and relative abundance of bacteria, but decreased fungal relative abundance and the activity of oxidative enzymes. However, mowing counteracted N effects on plant productivity and enzyme activity. In macroaggregates, close linkages with plant biomass and species richness were found for soil available nutrients and ratio of fungi to bacteria (F:B ratio). In contrast, strong physical protection and restricted fungal dominance and activity contributed to C stabilization in microaggregates, where plant community and soil properties were less linked with each other.

Conclusions

Our study clearly demonstrated that stronger plant-soil linkages occurred in macro- vs. microaggregates. This linkage was associated with a rise in plant biomass and soil C accumulation but a drop in F:B ratio in macroaggregates under N addition.

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

Access this article

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

Similar content being viewed by others

Data availability

Data sets can be obtained from the corresponding author.

References

  • Aciego Pietri JA, Brookes PC (2009) Substrate inputs and pH as factors controlling microbial biomass, activity and community structure in an arable soil. Soil Biol Biochem 41:1396–1405

    CAS  Google Scholar 

  • Bååth E, Anderson TH (2003) Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biol Biochem 35:955–963

    Google Scholar 

  • Bach EM, Williams RJ, Hargreaves SK, Yang F, Hofmockel KS (2018) Greatest soil microbial diversity found in micro-habitats. Soil Biol Biochem 118:217–226

    CAS  Google Scholar 

  • Bergkemper F, Schöler A, Engel M, Lang F, Krüger J, Schloter M, Schulz S (2016) Phosphorus depletion in forest soils shapes bacterial communities towards phosphorus recycling systems. Environ Microbiol 18:1988–2000

    CAS  PubMed  Google Scholar 

  • Bicharanloo B, Shirvan MB, Keitel C, Dijkstra FA (2020) Rhizodeposition mediates the effect of nitrogen and phosphorous availability on microbial carbon use efficiency and turnover rate. Soil Biol Biochem 107705

  • Bossio DA, Scow KM (1998) Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. Microb Ecol 35:265–278

    CAS  PubMed  Google Scholar 

  • Cantarel AA, Pommier T, Desclos-Theveniau M, Diquélou S, Dumont M, Grassein F, Kastl EM, Grigulis K, Laîné P, Lavorel S, Lemauviel-Lavenant S (2015) Using plant traits to explain plant-microbe relationships involved in nitrogen acquisition. Ecology 96:788–799

    PubMed  Google Scholar 

  • Čapek P, Manzoni S, Kaštovská E, Wild B, Diáková K, Bárta J, Schnecker J, Biasi C, Martikainen PJ, Alves RJE, Guggenberger G (2018) A plant-microbe interaction framework explaining nutrient effects on primary production. Nat Ecol Evol 2:1588–1596

    PubMed  Google Scholar 

  • Chen J, Luo Y, Van Groenigen KJ, Hungate BA, Cao J, Zhou X, Wang R (2018) A keystone microbial enzyme for nitrogen control of soil carbon storage. Sci Adv 4:eaaq1689

  • Chen Y, Liu X, Hou Y, Zhou S, Zhu B (2020) Particulate organic carbon is more vulnerable to nitrogen addition than mineral-associated organic carbon in soil of an alpine meadow. Plant Soil. https://doi.org/10.1007/s11104-019-04279-4

  • de Vries FT, Shade A (2013) Controls on soil microbial community stability under climate change. Front Microbiol 4:265

    PubMed  PubMed Central  Google Scholar 

  • de Vries FT, Griffiths RI, Bailey M, Craig H, Girlanda M, Gweon HS, Hallin S, Kaisermann A, Keith AM, Kretzschmar M, Lemanceau P (2018) Soil bacterial networks are less stable under drought than fungal networks. Nat Commun 9:3033

    PubMed  PubMed Central  Google Scholar 

  • Dorodnikov M, Blagodatskaya E, Blagodatsky S, Fangmeier A, Kuzyakov Y (2009) Stimulation of r- vs. K-selected microorganisms by elevated atmospheric CO2 depends on soil aggregate size. FEMS Microbiol Ecol 69:43–52

    CAS  PubMed  Google Scholar 

  • Ebrahimi A, Or D (2016) Microbial community dynamics in soil aggregates shape biogeochemical gas fluxes from soil profiles-upscaling an aggregate biophysical model. Glob Chang Biol 22:3141–3156

    PubMed  Google Scholar 

  • Ebrahimi A, Or D (2018) Dynamics of soil biogeochemical gas emissions shaped by remolded aggregate sizes and carbon configurations under hydration cycles. Glob Chang Biol 24:e378–e392

    PubMed  Google Scholar 

  • Farrer EC, Suding KN (2016) Teasing apart plant community responses to N enrichment: the roles of resource limitation, competition and soil microbes. Ecol Lett 19:1287–1296

    PubMed  Google Scholar 

  • Feng X, Wang R, Yu Q, Cao Y, Zhang Y, Yang L, Dijkstra FA, Jiang Y (2019) Decoupling of plant and soil metal nutrients as affected by nitrogen addition in a meadow steppe. Plant Soil 443:337–351

    CAS  Google Scholar 

  • Fierer N, Strickland MS, Liptzin D, Bradford MA, Cleveland CC (2009) Global patterns in belowground communities. Ecol Lett 12:1238–1249

    PubMed  Google Scholar 

  • Frostegård Å, Bååth E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22:59–65

    Google Scholar 

  • Glinski J (2018) Soil physical conditions and plant roots. CRC Press, Boca Raton

    Google Scholar 

  • Grosso F, Bååth E, De Nicola F (2016) Bacterial and fungal growth on different plant litter in Mediterranean soils: effects of C/N ratio and soil pH. Appl Soil Ecol 108:1–7

    Google Scholar 

  • Gunina A, Kuzyakov Y (2014) Pathways of litter C by formation of aggregates and SOM density fractions: implications from 13C natural abundance. Soil Biol Biochem 71:95–104

    CAS  Google Scholar 

  • Guo Q, Yan L, Korpelainen H, Niinemets Ü, Li C (2019) Plant-plant interactions and N fertilization shape soil bacterial and fungal communities. Soil Biol Biochem 128:127–138

    CAS  Google Scholar 

  • Gupta VV, Germida JJ (2015) Soil aggregation: influence on microbial biomass and implications for biological processes. Soil Biol Biochem 80:A3–A9

    CAS  Google Scholar 

  • Harris D, Horwáth WR, van Kessel C (2001) Acid fumigation of soils to remove carbonates prior to total organic carbon or carbon-13 isotopic analysis. Soil Sci Soc Am J 65:1853–1856

    CAS  Google Scholar 

  • Helfrich M, Ludwig B, Thoms C, Gleixner G, Flessa H (2015) The role of soil fungi and bacteria in plant litter decomposition and macroaggregate formation determined using phospholipid fatty acids. Appl Soil Ecol 96:261–264

    Google Scholar 

  • IUSS Working Group WRB (2015) World reference base for soil resources 2014, update 2015: International soil classification system for naming soils and creating legends for soil maps. FAO, Rome, p 192

  • Jenkinson DS, Brookes PC, Powlson DS (2004) Measuring soil microbial biomass. Soil Biol Biochem 36:5–7

    CAS  Google Scholar 

  • Jian S, Li J, Chen J, Wang G, Mayes MA, Dzantor KE, Hui D, Luo Y (2016) Soil extracellular enzyme activities, soil carbon and nitrogen storage under nitrogen fertilization: A meta-analysis. Soil Biol Biochem 101:32–43

    CAS  Google Scholar 

  • Jiang Y, Qian H, Wang X, Chen L, Liu M, Li H, Sun B (2018) Nematodes and microbial community affect the sizes and turnover rates of organic carbon pools in soil aggregates. Soil Biol Biochem 119:22–31

    CAS  Google Scholar 

  • Lange M, Eisenhauer N, Sierra CA, Bessler H, Engels C, Griffiths RI, Mellado-Vázquez PG, Malik AA, Roy J, Scheu S, Steinbeiss S (2015) Plant diversity increases soil microbial activity and soil carbon storage. Nat Commun 6:6707

    CAS  PubMed  Google Scholar 

  • Li F, Peng Y, Zhang D, Yang G, Fang K, Wang G, Wang J, Yu J, Zhou G, Yang Y (2019) Leaf area rather than photosynthetic rate determines the response of ecosystem productivity to experimental warming in an alpine steppe. J Geophys Res-Biogeo 124:2277–2287

    Google Scholar 

  • Liang C, Amelung W, Lehmann J, Kästner M (2019) Quantitative assessment of microbial necromass contribution to soil organic matter. Glob Chang Biol 25:3578–3590

    PubMed  Google Scholar 

  • Liu N, Kan H, Yang G, Zhang Y (2015) Changes in plant, soil, and microbes in a typical steppe from simulated grazing: explaining potential change in soil C. Ecol Monogr 85:269–286

    Google Scholar 

  • Liu K, Han T, Huang J, Huang Q, Li D, Hu Z, Yu X, Muhammad Q, Ahmed W, Hu H, Zhang H (2019) Response of soil aggregate-associated potassium to long-term fertilization in red soil. Geoderma 352:160–170

    CAS  Google Scholar 

  • Meidute S, Demoling F, Bååth E (2008) Antagonistic and synergistic effects of fungal and bacterial growth in soil after adding different carbon and nitrogen sources. Soil Biol Biochem 40:2334–2343

    CAS  Google Scholar 

  • Miller M, Palojärvi A, Rangger A, Reeslev M, Kjøller A (1998) The use of fluorogenic substrates to measure fungal presence and activity in soil. Appl Environ Microbiol 64:613–617

    CAS  PubMed  PubMed Central  Google Scholar 

  • Moreau D, Pivato B, Bru D, Busset H, Deau F, Faivre C, Matejicek A, Strbik F, Philippot L, Mougel C (2015) Plant traits related to nitrogen uptake influence plant-microbe competition. Ecology 96:2300–2310

    PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Negassa WC, Guber AK, Kravchenko AN, Marsh TL, Hildebrandt B, Rivers ML (2015) Properties of soil pore space regulate pathways of plant residue decomposition and community structure of associated bacteria. PLoS One 10:e0123999

    PubMed  PubMed Central  Google Scholar 

  • Olsen SR, Watanabe FS, Cosper HR, Larson WE, Nelson LB (1954) Residual phosphorus availability in long-time rotations on calcareous soils. Soil Sci 78:141–152

    CAS  Google Scholar 

  • Olsson PA, Bååth E, Jakobsen I, Söderström B (1995) The use of phospholipid and neutral lipid fatty acids to estimate biomass of arbuscular mycorrhizal fungi in soil. Mycol Res 99:623–629

    CAS  Google Scholar 

  • Prommer J, Walker TW, Wanek W, Braun J, Zezula D, Hu Y, Hofhansl F, Richter A (2020) Increased microbial growth, biomass, and turnover drive soil organic carbon accumulation at higher plant diversity. Glob Chang Biol 26:669–681

    PubMed  Google Scholar 

  • Rillig MC, Muller LA, Lehmann A (2017) Soil aggregates as massively concurrent evolutionary incubators. ISME J 11:1943–1948

    PubMed  PubMed Central  Google Scholar 

  • Sarker JR, Singh BP, Cowie AL, Fang Y, Collins D, Badgery W, Dalal RC (2018) Agricultural management practices impacted carbon and nutrient concentrations in soil aggregates, with minimal influence on aggregate stability and total carbon and nutrient stocks in contrasting soils. Soil Till Res 178:209–223

    Google Scholar 

  • Schutter ME, Dick RP (2002) Microbial community profiles and activities among aggregates of winter fallow and cover-cropped soil. Soil Sci Soc Am J 66:142–153

    CAS  Google Scholar 

  • Six J, Callewaert P, Lenders S, De Gryze S, Morris SJ, Gregorich EG, Paul EA, Paustian K (2002) Measuring and understanding carbon storage in afforested soils by physical fractionation. Soil Sci Soc Am J 66:1981–1987

    CAS  Google Scholar 

  • Smith AP, Marín-Spiotta E, de Graaff MA, Balser TC (2014) Microbial community structure varies across soil organic matter aggregate pools during tropical land cover change. Soil Biol Biochem 77:292–303

    CAS  Google Scholar 

  • Soares M, Rousk J (2019) Microbial growth and carbon use efficiency in soil: links to fungal-bacterial dominance, SOC-quality and stoichiometry. Soil Biol Biochem 131:195–205

    CAS  Google Scholar 

  • Tabatabai M (1994) Soil enzymes, in: Methods of soil analysis, part 2: microbiological and biochemical properties, edited by: Mickelson SH, Bifham JM, Soil Science Society of America, Inc., Madison, pp775–833

  • Tian Q, Liu N, Bai W, Li L, Chen J, Reich PB, Yu Q, Guo D, Smith MD, Knapp AK, Cheng W (2016) A novel soil manganese mechanism drives plant species loss with increased nitrogen deposition in a temperate steppe. Ecology 97:65–74

    PubMed  Google Scholar 

  • Tisdall JM, Oades J (1982) Organic matter and water-stable aggregates in soils. J Soil Sci 33:141–163

    CAS  Google Scholar 

  • Totsche KU, Amelung W, Gerzabek MH, Guggenberger G, Klumpp E, Knief C, Lehndorff E, Mikutta R, Peth S, Prechtel A, Ray N (2018) Microaggregates in soils. J Plant Nutr Soil Sci 181:104–136

    CAS  Google Scholar 

  • Trivedi P, Delgado-Baquerizo M, Jeffries TC, Trivedi C, Anderson IC, Lai K, McNee M, Flower K, Pal Singh B, Minkey D, Singh BK (2017) Soil aggregation and associated microbial communities modify the impact of agricultural management on carbon content. Environ Microbiol 19:3070–3086

    CAS  PubMed  Google Scholar 

  • van der Wal A, De Boer W (2017) Dinner in the dark: illuminating drivers of soil organic matter decomposition. Soil Biol Biochem 105:45–48

    Google Scholar 

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

    CAS  Google Scholar 

  • Waldrop MP, Holloway JM, Smith DB, Goldhaber MB, Drenovsky RE, Scow KM, Dick R, Howard D, Wylie B, Grace JB (2017) The interacting roles of climate, soils, and plant production on soil microbial communities at a continental scale. Ecology 98:1957–1967

    CAS  PubMed  Google Scholar 

  • Wang X, Yost RS, Linquist BA (2001) Soil aggregate size affects phosphorus desorption from highly weathered soils and plant growth. Soil Sci Soc Am J 65:139–146

    CAS  Google Scholar 

  • Wang R, Dorodnikov M, Yang S, Zhang Y, Filley TR, Turco RF, Zhang Y, Xu Z, Li H, Jiang Y (2015) Responses of enzymatic activities within soil aggregates to 9-year nitrogen and water addition in a semi-arid grassland. Soil Biol Biochem 81:159–167

    CAS  Google Scholar 

  • Wang R, Dorodnikov M, Dijkstra FA, Yang S, Xu Z, Li H, Jiang Y (2017) Sensitivities to nitrogen and water addition vary among microbial groups within soil aggregates in a semiarid grassland. Biol Fertil Soils 53:129–140

    CAS  Google Scholar 

  • Wang B, Brewer PE, Shugart HH, Lerdau MT, Allison SD (2019a) Soil aggregates as biogeochemical reactors and implications for soil–atmosphere exchange of greenhouse gases-A concept. Glob Chang Biol 25:373–385

    Google Scholar 

  • Wang J, Song B, Ma F, Tian D, Li Y, Yan T, Quan Q, Zhang F, Li Z, Wang B, Gao Q (2019b) Nitrogen addition reduces soil respiration but increases the relative contribution of heterotrophic component in an alpine meadow. Funct Ecol 33:2239–2253

    Google Scholar 

  • Wei C, Yu Q, Bai E, Lü X, Li Q, Xia J, Kardol P, Liang W, Wang Z, Han X (2013) Nitrogen deposition weakens plant-microbe interactions in grassland ecosystems. Glob Chang Biol 19:3688–3697

    PubMed  Google Scholar 

  • Xiao W, Chen X, Jing X, Zhu B (2018) A meta-analysis of soil extracellular enzyme activities in response to global change. Soil Biol Biochem 123:21–32

    CAS  Google Scholar 

  • Yang S, Liu W, Qiao C, Wang J, Deng M, Zhang B, Liu L (2019a) The decline in plant biodiversity slows down soil carbon turnover under increasing nitrogen deposition in a temperate steppe. Funct Ecol 33:1362–1372

    Google Scholar 

  • Yang C, Liu N, Zhang Y (2019b) Soil aggregates regulate the impact of soil bacterial and fungal communities on soil respiration. Geoderma 337:444–452

    CAS  Google Scholar 

  • Yang S, Xu Z, Wang R, Zhang Y, Yao F, Zhang Y, Turco RF, Jiang Y, Zou H, Li H (2017) Variations in soil microbial community composition and enzymatic activities in response to increased N deposition and precipitation in Inner Mongolian grassland. Appl Soil Ecol 119:275–285

    Google Scholar 

  • Yue K, Peng Y, Peng C, Yang W, Peng X, Wu F (2016) Stimulation of terrestrial ecosystem carbon storage by nitrogen addition: a meta-analysis. Sci Rep-UK 6:19895

    CAS  Google Scholar 

  • Zak DR, Holmes WE, White DC, Peacock AD, Tilman D (2003) Plant diversity, soil microbial communities, and ecosystem function: are there any links? Ecology 84:2042–2050

    Google Scholar 

  • Zhang N, Wan S, Guo J, Han G, Gutknecht J, Schmid B, Yu L, Liu W, Bi J, Wang Z, Ma K (2015) Precipitation modifies the effects of warming and nitrogen addition on soil microbial communities in northern Chinese grasslands. Soil Biol Biochem 89:12–23

    CAS  Google Scholar 

  • Zhu J, He N, Wang Q, Yuan G, Wen D, Yu G, Jia Y (2015) The composition, spatial patterns, and influencing factors of atmospheric wet nitrogen deposition in Chinese terrestrial ecosystems. Sci Total Environ 511:777–785

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (31770525 and 31870441) and the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA23080400). Ruzhen Wang was grateful for the support from the Youth Innovation Promotion Association CAS (Y9QCH121YY). JS and JP research was supported by the European Research Council Synergy grant ERC-2013-SyG 610028-IMBALANCE-P, the Spanish Government grant CGL2016-79835-P and the Catalan Government grant SGR 2017-1005. We are grateful to the three anonymous referees for their helpful and constructive comments on an early version of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yong Jiang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible Editor: Zucong Cai.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 531 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, R., Wu, H., Sardans, J. et al. Carbon storage and plant-soil linkages among soil aggregates as affected by nitrogen enrichment and mowing management in a meadow grassland. Plant Soil 457, 407–420 (2020). https://doi.org/10.1007/s11104-020-04749-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-020-04749-0

Keywords

Navigation