Skip to main content

Advertisement

Log in

Contrasting priming effect intensities and drivers in single and repeated glucose additions to a forest soil receiving long-term N fertilization

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

Abstract

Soil nitrogen (N) availability plays an important role in regulating priming effects (PE). In this study, we aimed to investigate the effects of long-term N fertilization on PE under single and more frequent additions of labile carbon (C) inputs (13C-labeled glucose). The soils collected from a 6-year-long inorganic N fertilization experiment in a subtropical Phyllostachys edulis forest in China were incubated at a constant temperature of 25 °C for 90 days. Regardless of the mode of glucose addition, the cumulative primed C was lower in the previously fertilized soil and showed a positive relationship with soil pH and peroxidase activity. When comparing the amount of cumulative primed C and the remaining added glucose-C after 90 days of incubation, the fertilized soil had a higher net C increase than the control. These results indicate that atmospheric N deposition and N fertilization might reduce the PE caused by labile organic matter inputs, thereby increasing soil organic C sequestration. The effect of N fertilization on PE under a single glucose addition (reduced by 11%) was smaller than that of repeated additions (reduced by 24%). Previously fertilized soil with a single glucose addition exhibited higher microbial P deficiency, which had a negative impact on PE; in contrast, in soil with repeated glucose additions, higher abundance of Gram-positive bacteria contributed to the negative PE. As such, the frequency of glucose addition affects the intensity and regulation of soil PE. Regardless of the N fertilization treatment, soil with a single glucose addition exhibited stronger PE but lower soil net C increases than those with repeated additions, which might be related to higher microbial activities. Collectively, our findings provide insights regarding soil PE in subtropical forests under the combined effects of increasing N deposition and glucose 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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Data availability

The data presented in this study are available on request from the corresponding author.

References

  • Ackerman D, Millet DB, Chen X (2019) Global estimates of inorganic nitrogen deposition across four decades. Global Biogeochem Cy 33:100–107

    Article  CAS  Google Scholar 

  • Aye NS, Butterly CR, Sale PWG, Tang C (2017) Residue addition and liming history interactively enhance mineralization of native organic carbon in acid soils. Biol Fertil Soils 53:61–75

    Article  CAS  Google Scholar 

  • Aylward GH, Finlay TJV (1974) SI chemical data, 2nd edn. John Wiley and Sons, Hong Kong

    Google Scholar 

  • Bååth E, Nilsson LO, Goransson H, Wallander H (2004) Can the extent of degradation of soil fungal mycelium during soil incubation be used to estimate ectomycorrhizal biomass in soil? Soil Biol Biochem 36:2105–2109

    Article  Google Scholar 

  • Bartoń K (2020) MuMIn: multi-model inference. R Package Version 1(43):17. https://CRAN.R-project.org/package=MuMIn. Accessed June 2022

  • Bei S, Li X, Kuyper TW, Chadwick DR, Zhang J (2022) Nitrogen availability mediates the priming effect of soil organic matter by preferentially altering the straw carbon-assimilating microbial community. Sci Total Environ 815:152882

    Article  CAS  PubMed  Google Scholar 

  • Blagodatskaya E, Kuzyakov Y (2008) Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review. Biol Fertil Soils 45:115–131

    Article  Google Scholar 

  • Blagodatskaya EV, Blagodatsky SA, Anderson TH, Kuzyakov Y (2007) Priming effects in Chernozem induced by glucose and N in relation to microbial growth strategies. Appl Soil Ecol 37:95–105

    Article  Google Scholar 

  • Camenzind T, Hattenschwiler S, Treseder KK, Lehmann A, Rillig MC (2018) Nutrient limitation of soil microbial processes in tropical forests. Ecol Monogr 88:4–21

    Article  Google Scholar 

  • Cleveland C, Liptzin D (2007) C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85:235–252

    Article  Google Scholar 

  • Cleveland CC, Townsend AR (2006) Nutrient additions to a tropical rain forest drive substantial soil carbon dioxide losses to the atmosphere. Proc Natl Acad Sci USA 103:10316–10321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Craine JM, Morrow C, Fierer N (2007) Microbial nitrogen limitation increases decomposition. Ecology 88:2105–2113

    Article  PubMed  Google Scholar 

  • Cui J, Zhu Z, Xu X, Liu S, Jones DL, Kuzyakov Y, Shibistova O, Wu J, Ge T (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 

  • Cui Y, Moorhead DL, Wang X, Xu M, Wang X, Wei X, Zhu Z, Ge T, Peng S, Zhu B, Zhang X, Fang L (2022) Decreasing microbial phosphorus limitation increases soil carbon release. Geoderma 419:115868

    Article  CAS  Google Scholar 

  • Denef K, Bubenheim H, Lenhart K, Vermeulen J, Van Cleemput O, Boeckx P, Muller C (2007) Community shifts and carbon translocation within metabolically-active rhizosphere microorganisms in grasslands under elevated CO2. Biogeosciences 4:769–779

    Article  CAS  Google Scholar 

  • Dijkstra FA, Carrillo Y, Pendall E, Morgan JA (2013) Rhizosphere priming: a nutrient perspective. Front Microbiol 4:1–8

    Article  Google Scholar 

  • Dimassia B, Marya B, Fontaineb S, Perveenb N, Cohanc JP (2014) Effect of nutrients availability and long-term tillage on priming effect and soil C mineralization. Soil Biol Biochem 78:332–339

    Article  Google Scholar 

  • Dong S, Brooks D, Jones MD, Grayston SJ (2007) A method for linking in situ activities of hydrolytic enzymes to associated organisms in forest soils. Soil Biol Biochem 39:2414–2419

    Article  CAS  Google Scholar 

  • Fan Y, Lin F, Yang L, Zhong X, Wang M, Zhou J, Chen Y, Yang Y (2018) Decreased soil organic P fraction associated with ectomycorrhizal fungal activity to meet increased P demand under N application in a subtropical forest ecosystem. Biol Fertil Soils 54:149–161

    Article  CAS  Google Scholar 

  • Fang YY, Nazaries L, Singh BK, Singh BP (2018) Microbial mechanisms of carbon priming effects revealed during the interaction of crop residue and nutrient inputs in contrasting soils. Glob Chang Biol 24:2775–2790

    Article  PubMed  Google Scholar 

  • Feng J, Zhu B (2021) Global patterns and associated drivers of priming effect in response to nutrient addition. Soil Biol Biochem 153:108118

    Article  CAS  Google Scholar 

  • Fontaine S, Henault C, Amor A, Bdioui N, Bloor JMG, Maire V, Mary B, Revaillot S, Maron PA (2011) Fungi mediate long term sequestration of carbon and nitrogen in soil through their priming effect. Soil Biol Biochem 43:86–96

    Article  CAS  Google Scholar 

  • Fontaine S, Mariotti A, Abbadie L (2003) The priming effect of organic matter: a question of microbial competition? Soil Biol Biochem 35:837–843

    Article  CAS  Google Scholar 

  • García-Palacios P, Gross N, Gaitán J, Maestre FT (2018) Climate mediates the biodiversity–ecosystem stability relationship globally. Proc Natl Acad Sci USA 115:8400–8405

    Article  PubMed  PubMed Central  Google Scholar 

  • German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD (2011) Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem 43:1387–1397

    Article  CAS  Google Scholar 

  • Gnankambary Z, Ilstedt U, Nyberg G, Hien V, Malmer A (2008) Nitrogen and phosphorus limitation of soil microbial respiration in two tropical agroforestry parklands in the south-Sudanese zone of Burkina Faso: the effects of tree canopy and fertilization. Soil Biol Biochem 40:350–359

    Article  CAS  Google Scholar 

  • Guenet B, Neill C, Bardoux G, Abbadie L (2010) Is there a linear relationship between priming effect intensity and the amount of organic matter input? Appl Soil Ecol 46:436–442

    Article  Google Scholar 

  • Hou E, Luo Y, Kuang Y, Chen C, Lu X, Jiang L, Luo X, Wen D (2020) Global meta-analysis shows pervasive phosphorus limitation of aboveground plant production in natural terrestrial ecosystems. Nat Commun 11:637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joergensen RG (2022) Phospholipid fatty acids in soil—drawbacks and future prospects. Biol Fertil Soils 58:1–6

    Article  CAS  Google Scholar 

  • Jones DL, Cooledge EC, Hoyle FC, Grifths RI, Murphy DV (2019) pH and exchangeable aluminum are major regulators of microbial energy flow and carbon use efficiency in soil microbial communities. Soil Biol Biochem 138:107584

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Kaspari M, Garcia MN, Harms KE, Santana M, Wright SJ, Yavitt JB (2008) Multiple nutrients limit litterfall and decomposition in a tropical forest. Ecol Lett 11:35–43

    Article  PubMed  Google Scholar 

  • Keith A, Singh B, Singh BP (2011) Interactive priming of biochar and labile organic matter mineralization in a smectite-rich soil. Environ Sci Technol 45:9611–9618

    Article  CAS  PubMed  Google Scholar 

  • Kuzyakov Y, Friedel JK, Stahr K (2000) Review of mechanisms and quantification of priming effects. Soil Biol Biochem 32:1485–1498

    Article  CAS  Google Scholar 

  • Lang M, Cai ZC, Chang SX (2011) Effects of land use type and incubation temperature on greenhouse gas emissions from Chinese and Canadian soils. J Soils Sed 11:15–24

    Article  CAS  Google Scholar 

  • Li Q, Lv J, Peng C, Xiang W, Xiao W, Song X (2021) Nitrogen-addition accelerates phosphorus cycling and changes phosphorus use strategy in a subtropical Moso bamboo forest. Environ Res 16:024023

    CAS  Google Scholar 

  • Li Q, Song X, Gu H, Gao F (2016) Nitrogen deposition and management practices increase soil microbial biomass carbon but decrease diversity in Moso bamboo plantations. Sci Rep 6:1–11

    Google Scholar 

  • Liu XJA, Finley BK, Mau RL, Schwartz E, Dijkstra P, Bowker MA, Hungate BA (2020) The soil priming effect: consistent across ecosystems, elusive mechanisms. Soil Biol Biochem 140:107617

    Article  CAS  Google Scholar 

  • Liu XJA, Sun J, Mau RL, Finley BK, Compson ZG, van Gestel N, Brown JR, Schwartz E, Dijkstra P, Hungate BA (2017) Labile carbon input determines the direction and magnitude of the priming effect. Appl Soil Ecol 109:7–13

    Article  Google Scholar 

  • Lyu M, Nie Y, Giardina CP, Vadeboncoeur MA, Ren Y, Fu Z, Wang M, Jin C, Liu X, Xie J (2019) Litter quality and site characteristics interact to affect the response of priming effect to temperature in subtropical forests. Funct Ecol 33:2226–2238

    Article  Google Scholar 

  • Malik AA, Martiny JBH, Brodie EL, Martiny AC, Treseder KK, Allison SD (2020) Defining trait-based microbial strategies with consequences for soil carbon cycling under climate change. ISME J 14:1–9

    Article  CAS  PubMed  Google Scholar 

  • Mau RL, Dijkstra P, Schwartz E, Koch BJ, Hungate BA (2018) Warming induced changes in soil carbon and nitrogen influence priming responses in four ecosystems. Appl Soil Ecol 124:110–116

    Article  Google Scholar 

  • Mau RL, Liu CM, Aziz M, Schwartz E, Dijkstra P, Marks JC, Price LB, Keim P, Hungate BA (2015) Linking soil bacterial biodiversity and soil carbon stability. ISME J 9:1477–1480

    Article  CAS  PubMed  Google Scholar 

  • McGill WB, Cole CV (1981) Comparative aspects of cycling of organic C, N, S and P through soil organic matter. Geoderma 26:267–286

    Article  CAS  Google Scholar 

  • Mehnaz KR, Corneo PE, Keitel C, Dijkstra FA (2019) Carbon and phosphorus addition effects on microbial carbon use efficiency, soil organic matter priming, gross nitrogen mineralization and nitrous oxide emission from soil. Soil Biol Biochem 134:175–186

    Article  CAS  Google Scholar 

  • Mooshammer M, 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 

  • Mori T, Lu X, Aoyagi R, Mo J (2018) Reconsidering the phosphorus limitation of soil microbial activity in tropical forests. Funct Ecol 32:1145–1154

    Article  Google Scholar 

  • Mori T, Ohta S, Ishizuka S, Konda R, Wicaksono A, Heriyanto J, Hardjono A (2013) Effects of phosphorus application on root respiration and heterotrophic microbial respiration in Acacia mangium plantation soil. Tropics 22:113–118

    Article  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 

  • Nottingham AT, Turner BL, Stott AW, Tanner EVJ (2015) Nitrogen and phosphorus constrain labile and stable carbon turnover in lowland tropical forest soils. Soil Biol Biochem 80:26–33

    Article  CAS  Google Scholar 

  • Olsen SR, Sommers LE (1982) Phosphorous. In: Page AL, Miller RH, Keeney DR (eds) Methods of Soil Analysis, Part 2, Chemical and Microbial Properties, vol 9. Agronomy Society of America, Agronomy Monograph, Madison, WI, pp 403–430

    Google Scholar 

  • Pennanen T, Liski J, Bååth E, Kitunen V, Uotila J, Westman CJ, Fritze H (1999) Structure of the microbial communities in coniferous forest soils in relation to site fertility and stand development stage. Microb Ecol 38:168–179

    Article  CAS  PubMed  Google Scholar 

  • Peñuelas J, Poulter B, Sardans J, Ciais P, van der Velde M, Bopp L, Boucher O, Godderis Y, Hinsinger P, Llusia J, Nardin E, Vicca S, Obersteiner M, Janssens IA (2013) Human-induced nitrogen–phosphorus imbalances alter natural and managed ecosystems across the globe. Nat Commun 4:1–10

    Article  Google Scholar 

  • Peñuelas J, Sardans JJS (2022) The global nitrogen-phosphorus imbalance. Science 375:266–267

    Article  PubMed  Google Scholar 

  • Perveen N, Barot S, Maire V, Cotrufo MF, Shahzad T, Blagodatskaya E, Stewart CE, Ding W, Siddiq MR, Dimassi B, Mary B, Fontaine S (2019) Universality of priming effect: An analysis using thirty five soils with contrasted properties sampled from five continents. Soil Biol Biochem 134:162–171

    Article  CAS  Google Scholar 

  • Phillips RP, Finzi AC, Bernhardt ES (2011) Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol Lett 14:187–194

    Article  PubMed  Google Scholar 

  • Qiao N, Schaefer D, Blagodatskaya E, Zou X, Xu X, Kuzyakov Y (2014) Labile carbon retention compensates for CO2 released by priming in forest soils. Glob Chang Biol 20:1943–1954

    Article  PubMed  Google Scholar 

  • Qiao N, Xu X, Hu Y, Blagodatskaya E, Liu Y, Schaefer D, Kuzyakov Y (2016) Carbon and nitrogen additions induce distinct priming effects along an organic-matter decay continuum. Sci Rep 6:19865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rasul M, Cho J, Shin HS, Hur J (2022) Biochar-induced priming effects in soil via modifying the status of soil organic matter and microflora: a review. Sci Total Environ 805:150304

    Article  CAS  PubMed  Google Scholar 

  • Razanamalala K, Razafimbelo T, Maron PA, Ranjard L, Chemidlin N, Lelièvre M, Dequiedt S, Ramaroson VH, Marsden C, Becquer T, Trap J, Blanchart E, Bernard L (2018) Soil microbial diversity drives the priming effect along climate gradients: a case study in Madagascar. ISME J 12:451–462

    Article  PubMed  Google Scholar 

  • Reay DS, Dentener F, Smith P, Grace J, Feely RA (2008) Global nitrogen deposition and carbon sinks. Nat Geosci 1:430–437

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Shahbaz M, Kumar A, Kuzyakov Y, Börjesson G, Blagodatskaya E (2018) Priming effects induced by glucose and decaying plant residues on SOM decomposition: a three-source 13C/14C partitioning study. Soil Biol Biochem 121:138–146

    Article  CAS  Google Scholar 

  • Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404

    Article  CAS  Google Scholar 

  • Tang B, Rocci KS, Lehmann A, Rillig MC (2023) Nitrogen increases soil organic carbon accrual and alters its functionality. Glob Chang Biol 25:2325–2337

    Google Scholar 

  • Tavi NM, Martikainen PJ, Lokko K, Kontro M, Wild B, Richter A, Biasi C (2013) Linking microbial community structure and allocation of plant-derived carbon in an organic agricultural soil using 13CO2 pulse-chase labelling combined with 13C-PLFA profiling. Soil Biol Biochem 58:207–215

    Article  CAS  Google Scholar 

  • Tian P, Liu S, Wang Q, Sun T, Blagodatskaya E (2019) Organic N deposition favours soil C sequestration by decreasing priming effect. Plant Soil 445:439–451

    Article  CAS  Google Scholar 

  • Turner BL, Wrigh SJ (2014) The response of microbial biomass and hydrolytic enzymes to a decade of nitrogen, phosphorus, and potassium addition in a lowland tropical rain forest. Biogeochemistry 117:115–130

    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 

  • Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions. Ecol Appl 20:5–15

    Article  PubMed  Google Scholar 

  • Wan D, Ma MK, Peng N, Luo XS, Chen WL, Cai P, Wu L, Pan H, Chen J, Yu G, Huang Q (2021) Effects of long-term fertilization on calcium-associated soil organic carbon: Implications for C sequestration in agricultural soils. Sci Total Environ 772:145037

    Article  CAS  PubMed  Google Scholar 

  • Wang Q, Chen L, Yang Q, Sun T, Li C (2019) Different effects of single versus repeated additions of glucose on the soil organic carbon turnover in a temperate forest receiving long-term N addition. Geoderma 341:59–67

    Article  CAS  Google Scholar 

  • Wang X, Li S, Zhu B, Homyak PM, Chen G, Yao X, Wu D, Yang Z, Lyu M, Yang Y (2023) Long-term nitrogen deposition inhibits soil priming effects by enhancing phosphorus limitation in a subtropical forest. Glob Chang Biol 29:4081–4093

    Article  CAS  PubMed  Google Scholar 

  • Webster R, Lark RM (2019) Analysis of variance in soil research: examining the assumptions. Eur J Soil Sci 70:990–1000

    Article  Google Scholar 

  • Wei Y, Xiong X, Ryo M, Badgery WB, Bi Y, Yang G, Zhang Y, Liu N (2022) Repeated litter inputs promoted stable soil organic carbon formation by increasing fungal dominance and carbon use efficiency. Biol Fertil Soils 58:619–631

    Article  CAS  Google Scholar 

  • Xiao Q, Huang Y, Wu L, Tian Y, Wang Q, Wang B, Xu M, Zhang W (2021) Long-term manuring increases microbial carbon use efficiency and mitigates priming effect via alleviated soil acidification and resource limitation. Biol Fertil Soils 57:925–934

    Article  CAS  Google Scholar 

  • Yu G, Zhao H, Chen J, Zhang T, Cai Z, Zhou G, Li Z, Qiu Z, Wu Z (2020) Soil microbial community dynamics mediate the priming effects caused by in situ decomposition of fresh plant residues. Sci Total Environ 737:139708

    Article  CAS  PubMed  Google Scholar 

  • Zeng Q, Fan Y, Zhang Q, Yuan X, Lin K, Zhou J, Lin H, Xie H, Cui J, Wu Y, Chen Y (2022) Differential factors determine the response of soil P fractions to N deposition in wet and dry seasons in a subtropical Moso bamboo forest. Plant Soil 1–19. https://doi.org/10.1007/s11104-022-05768-9

  • Zhang J, Sayer EJ, Zhou J, Li Y, Li Y, Li Z, Wang F (2021a) Long-term fertilization modifies the mineralization of soil organic matter in response to added substrate. Sci Total Environ 798:149341

    Article  CAS  PubMed  Google Scholar 

  • Zhang Q, Cheng L, Feng J, Mei K, Zeng Q, Zhu B, Chen Y (2021b) Nitrogen addition stimulates priming effect in a subtropical forest soil. Soil Biol Biochem 160:108339

    Article  CAS  Google Scholar 

  • Zhang Z, Wang W, Qi J, Zhang H, Tao F, Zhang R (2019) Priming effects of soil organic matter decomposition with addition of different carbon substrates. J Soils Sed 19:1171–1178

    Article  CAS  Google Scholar 

  • Zhao X, Tian Q, Huang L, Lin Q, Wu J, Liu F (2022) Fine-root functional trait response to nitrogen deposition across forest ecosystems: a meta-analysis. Sci Total Environ 844:157111

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was supported by the Natural Science Foundation of Fujian Province (No. 2020J01142 and 2020J01397).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yuehmin Chen.

Ethics declarations

Conflict of interest

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

ESM 1

(DOCX 1.08 mb)

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zeng, Q., Liu, Y., Zhang, Q. et al. Contrasting priming effect intensities and drivers in single and repeated glucose additions to a forest soil receiving long-term N fertilization. Biol Fertil Soils 60, 53–68 (2024). https://doi.org/10.1007/s00374-023-01762-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-023-01762-0

Keywords

Navigation