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Long-term bare fallow soil reveals the temperature sensitivity of priming effect of the relatively stabilized soil organic matter

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Abstract

Background and aims

Priming effect (PE) plays an important role in modifying the decomposition of soil organic matter (SOM), but large uncertainties remain in the temperature effect on PE mainly due to the variation in SOM stability.

Methods

We tested the temperature effect on PE of the relatively stabilized SOM by incubating soils collected from a bare fallow (representing the relatively stabilized SOM) and its adjacent old field (containing both stabilized SOM and labile SOM) at 10 and 20 °C for 815 days. We used a natural 13C abundance tracer method for measuring the PE.

Results

Positive PE was observed in all treatment combinations when maize leaf litter was added. The temperature sensitivity of PE in the bare fallow soil and the old field soil was quite different: increasing temperature significantly enhanced the magnitude of PE in the bare fallow soil, but had no effect on it in the old field soil. The increase of microbial biomass C by litter addition was higher in the bare fallow soil than in the old field soil. Furthermore, for litter-treated soil, temperature increase significantly increased net N mineralization rate throughout the incubation in the bare fallow soil, but had minor effect on it in the old field soil at the end of incubation.

Conclusions

Overall, this study demonstrates that PE of the relatively stabilized SOM is sensitive to temperature, which may be mainly driven by greater microbial growth and demand for N.

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Abbreviations

PE:

priming effect

C:

carbon

CO2:

carbon dioxide

SOC:

soil organic carbon

SOM:

soil organic matter

N:

nitrogen

MBC:

microbial biomass carbon

DOC:

dissolved organic carbon

C/N:

the ratio of carbon to nitrogen

NNM:

net nitrogen mineralization

WHC:

water-holding capacity

References

  • Allison SD, Vitousek PM (2005) Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biol Biochem 37:937–944

    Article  CAS  Google Scholar 

  • Anderson DW, Paul EA (1984) Organo-mineral complexes and their study by radiocarbon dating. Soil Sci Soc Am J 48:298–301

    Article  CAS  Google Scholar 

  • Barré P, Eglin T, Christense BT, Ciais P, Houot S, Kätterer T, van Oort F, Peylin P, Poulton PR, Romanenkov V, Chenu C (2010) Quantifying and isolating stable soil organic carbon using long-term bare fallow experiments. Biogeosciences 7:3839–3850

    Article  Google Scholar 

  • Blagodatsky S, Blagodatskaya E, Yuyukina T, Kuzyakov Y (2010) Model of apparent and real priming effects: Linking microbial activity with soil organic matter decomposition. Soil Biol Biochem 42:1275–1283

    Article  CAS  Google Scholar 

  • Cardinael R, Eglin T, Guenet B, Neill C, Houot S, Chenu C (2015) Is priming effect a significant process for long-term SOC dynamics? Analysis of a 52-years old experiment. Biogeochemistry 123:203–219

    Article  CAS  Google Scholar 

  • Chen R, Senbayram M, Blagodatsky S, Myachina O, Dittert K, Lin X, Blagodatskaya E, Kuzyakov Y (2013) Soil C and N availability determine the priming effect: Microbial N mining and stoichiometric decomposition theories. Glob Change Biol 20:2356–2367

    Article  Google Scholar 

  • Cheng W (1996) Measurement of rhizosphere respiration and organic matter decomposition using natural 13C. Plant Soil 183:263–268

    Article  CAS  Google Scholar 

  • Cheng W, Johnson DW, Fu S (2003) Rhizosphere effects on decomposition: controls of plant species, phenology, and fertilization. Soil Sci Soc Am J 67:1418–1427

    Article  CAS  Google Scholar 

  • Cheng W, Parton WJ, Gonzalez-Meler MA, Phillips R, Asao S, Mcnickle GG, Brzostek E, Jastrow JD (2014) Synthesis and modeling perspectives of rhizosphere priming. New Phytol 201:31–44

    Article  CAS  PubMed  Google Scholar 

  • Conant RT, Drijber RA, Haddix ML, Parton WJ, Paul EA, Plante AF, Six J, Steinweg JM (2008) Sensitivity of organic matter decomposition to warming varies with its quality. Glob Change Biol 14:868–877

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–173

    Article  CAS  PubMed  Google Scholar 

  • Demyan MS, Rasche F, Schulz E, Breulmann M, Müller T, Cadisch G (2012) Use of specific peaks obtained by diffuse reflectance Fourier transform mid-infrared spectroscopy to study the composition of organic matter in a Haplic Chernozem. Eur J Soil Sci 63:189–199

    Article  CAS  Google Scholar 

  • Derrien D, Plain C, Courty P-E, Gelhaye L, Moerdijk-Poortvliet TCW, Thomas F, Versini A, Zeller B, Koutika L-S, Boschker HTS, Epron D (2014) Does the addition of labile substrate destabilise old soil organic matter? Soil Biol Biochem 76:149–160

    Article  CAS  Google Scholar 

  • Dijkstra P, Thomas SC, Heinrich PL, Koch GW, Schwartz E, Hungate BA (2011) Effect of temperature on metabolic activity of intact microbial communities: Evidence for altered metabolic pathway activity but not for increased maintenance respiration and reduced carbon use efficiency. Soil Biol Biochem 43:2023–2031

    Article  CAS  Google Scholar 

  • Duboc O, Zehetner F, Djukic I, Tatzber M, Berger TW, Gerzabek MH (2012) Decomposition of European beech and Black pine foliar litter along an Alpine elevation gradient: Mass loss and molecular characteristics. Geoderma 189–190:522–531

    Article  Google Scholar 

  • Erhagen B, Ilstedt U, Nilsson MB (2015) Temperature sensitivity of heterotrophic soil CO2 production increases with increasing carbon substrate uptake rate. Soil Biol Biochem 80:45–52

    Article  CAS  Google Scholar 

  • Fang Y, 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 Change Biol 24:2775–2790

    Article  Google Scholar 

  • Feng J, Tang M, Zhu B (2021) Soil priming effect and its responses to nutrient addition along a tropical forest elevation gradient. Glob Change Biol. https://doi.org/10.1111/gcb.15587

    Article  Google Scholar 

  • Fontaine S, Barot S, Barre P, Bdioui N, Mary B, Rumpel C (2007) Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature 450:10–14

    Article  Google Scholar 

  • Fontaine S, Henault C, Aamor 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 

  • Frøseth RB, Bleken MA (2015) Effect of low temperature and soil type on the decomposition rate of soil organic carbon and clover leaves, and related priming effect. Soil Biol Biochem 80:156–166

    Article  Google Scholar 

  • Ghee C, Neilson R, Hallett PD, Robinson D, Paterson E (2013) Priming of soil organic matter mineralisation is intrinsically insensitive to temperature. Soil Biol Biochem 66:20–28

    Article  CAS  Google Scholar 

  • Guenet B, Juarez S, Bardoux G, Abbadie L, Chenu C (2012) Evidence that stable C is as vulnerable to priming effect as is more labile C in soil. Soil Biol Biochem 52:43–48

    Article  CAS  Google Scholar 

  • Guenet B, Camino-Serrano M, Ciais P, Tifafi M, Maignan F, Soong JL, Janssens IA (2018) Impact of priming on global soil carbon stocks. Glob Change Biol 24:1873–1883

    Article  Google Scholar 

  • Henneron L, Kardol P, Wardle DA, Cros C, Fontaine S (2020) Rhizosphere control of soil nitrogen cycling: a key component of plant economic strategies. New Phytol 228:1269–1282

    Article  CAS  PubMed  Google Scholar 

  • Hopkins FM, Torn MS, Trumbore SE (2012) Warming accelerates decomposition of decades-old carbon in forest soils. Proc Natl Acad Sci USA 109:1753–1761

    Article  Google Scholar 

  • Hopkins FM, Filley TR, Gleixner G, Lange M, Top SM, Trumbore SE (2014) Increased belowground carbon inputs and warming promote loss of soil organic carbon through complementary microbial responses Francesca. Soil Biol Biochem 76:57–69

    Article  CAS  Google Scholar 

  • Hou Y, Chen Y, Chen X, He K, Zhu B (2019) Changes in soil organic matter stability with depth in two alpine ecosystems on the Tibetan Plateau. Geoderma 351:153–162

    Article  CAS  Google Scholar 

  • Jenkinson DS, Harkness DD, Vance ED, Adams DE, Harrison AF (1992) Calculating net primary production and annual input of organic-matter to soil from the amount and radiocarbon content of soil organic-matter. Soil Biol Biochem 24:295–308

    Article  Google Scholar 

  • Jenkinson DS, Rayner JH (1977) The turnover of soil organic matter in some of the Rothamsted classical experiments. Soil Sci 123:298–305

    Article  CAS  Google Scholar 

  • Kirschbaum MUF (2004) Soil respiration under prolonged soil warming: are rate reductions caused by acclimation or substrate loss? Glob Change Biol 10:1870–1877

    Article  Google Scholar 

  • Kuzyakov Y, Subbotina I, Chen H, Bogomolova I, Xu X (2009) Black carbon decomposition and incorporation into soil microbial biomass estimated by 14C labelling. Soil Biology Biochemistry 41:210–219

    Article  CAS  Google Scholar 

  • Kuzyakov Y (2010) Priming effects: Interactions between living and dead organic matter. Soil Biol Biochem 42:1363–1371

    Article  CAS  Google Scholar 

  • Lal R (2008) Carbon sequestration. Philos Trans R Soc B: Biol Sci 363:815–830

    Article  CAS  Google Scholar 

  • Lefèvre R, Barré P, Moyano FE, Christensen BT, Bardoux G, Eglin T, Girardin C, Houot S, Kätterer T, van Oort F, Chenu C (2014) Higher temperature sensitivity for stable than for labile soil organic carbon – Evidence from incubations of long-term bare fallow soils. Glob Change Biol 20:633–640

    Article  Google Scholar 

  • Lenka S, Trivedi P, Singh B, Singh BP, Pendall E, Bass A, Lenka NK (2019) Effect of crop residue addition on soil organic carbon priming as influenced by temperature and soil properties. Geoderma 347:70–79

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Liang Y, Han X, Song C, Li H (2011) Impacts of returning organic materials on soil labile organic carbon fractions redistribution of Mollisol in Northeast China. Sci Agric Sin 44:3565–3574

    CAS  Google Scholar 

  • Lin J, Zhu B, Cheng W (2015) Decadally cycling soil carbon is more sensitive to warming than faster-cycling soil carbon. Glob Change Biol 21:4602–4612

    Article  Google Scholar 

  • Liu Q, Xu X, Wang H, Blagodatskaya E, Kuzyakov Y (2019) Dominant extracellular enzymes in priming of SOM decomposition depend on temperature. Geoderma 343:187–195

    Article  CAS  Google Scholar 

  • Lu J, Dijkstra FA, Wang P, Cheng W (2018) Rhizosphere priming of grassland species under different water and nitrogen conditions: a mechanistic hypothesis of C-N interactions. Plant Soil 429:303–319

    Article  CAS  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 

  • 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 

  • Nocentini C, Guenet B, Mattia ED, Certini G, Bardoux G, Rumpel C (2010) Charcoal mineralisation potential of microbial inocula from burned and unburned forest soil with and without substrate addition. Soil Biol Biochem 42:1472–1478

    Article  CAS  Google Scholar 

  • Nunan N, Lerch TZ, Pouteau V, Mora P, Changey F, Kätterer T, Giusti-Miller S, Herrmann AM (2015) Metabolising old soil carbon: Simply a matter of simple organic matter? Soil Biol Biochem 88:128–136

    Article  CAS  Google Scholar 

  • Paterson E, Sim A, Osborne SM, Murray PJ (2011) Long-term exclusion of plant-inputs to soil reduces the functional capacity of microbial communities to mineralise recalcitrant root-derived carbon sources. Soil Biol Biochem 43:1873–1880

    Article  CAS  Google Scholar 

  • Perveen N, Barot S, Alvarez G, Klumpp K, Martin R, Rapaport A, Herfurth D, Louault F, Fontaine S (2014) Priming effect and microbial diversity in ecosystem functioning and response to global change: a modeling approach using the SYMPHONY model. Glob Change Biol 20:1174–1190

    Article  Google Scholar 

  • Senesi N, D’Orazio V, Ricca G (2003) Humic acids in the first generation of EUROSOILS. Geoderma 116:325–344

    Article  CAS  Google Scholar 

  • Shahbaz M, Kuzyakov Y, Sanaullah M, Heitkamp F, Zelenev V, Kumar A, Blagodatskaya E (2017) Microbial decomposition of soil organic matter is mediated by quality and quantity of crop residues: mechanisms and thresholds. Biol Fertil Soils 53:287–301

    Article  CAS  Google Scholar 

  • Smidt E, Meissl K (2007) The applicability of Fourier transform infrared (FT-IR) spectroscopy in waste management. Waste Manag 27:268–276

    Article  CAS  PubMed  Google Scholar 

  • Smolander A, Kitunen V (2002) Soil microbial activities and characteristics of dissolved organic C and N in relation to tree species. Soil Biol Biochem 34:651–660

    Article  CAS  Google Scholar 

  • Soil Survey Staff (1999) Soil Taxonomy. A basic system of soil classification for making and interpreting soil surveys, 2nd end. Agricultural Handbook 436. Natural Resources Conservation Service. USDA, Washington DC, pp 869

  • Song M, Jiang J, Xu X, Shi P (2011) Correlation between CO2 efflux and net nitrogen mineralization and its response to external C or N supply in an Alpine meadow soil. Pedosphere 21:666–675

    Article  CAS  Google Scholar 

  • Stevenson FJ (1994) Humus chemistry: genesis, composition, reactions, 2nd end. Wiley, New York

  • Tatzber M, Mutsch F, Mentler A, Leitgeb E, Englisch M, Gerzabek MH (2010) Determination of organic and inorganic carbon in forest soil samples by mid-infrared spectroscopy and partial least squares regression. Appl Spectrosc 64:1167–1175

    Article  CAS  PubMed  Google Scholar 

  • Thiessen S, Gleixner G, Wutzler T, Reichstein M (2013) Both priming and temperature sensitivity of soil organic matter decomposition depend on microbial biomass – An incubation study. Soil Biol Biochem 57:739–748

    Article  CAS  Google Scholar 

  • Tian Q, Wang X, Wang D, Wang M, Liao C, Yang X, Liu F (2017) Decoupled linkage between soil carbon and nitrogen mineralization among soil depths in a subtropical mixed forest. Soil Biol Biochem 109:135–144

    Article  CAS  Google Scholar 

  • Trumbore SE, Vogel JS, Southon JR (1989) AMS 14C measurements of fraction- ated soil organic matter: an approach to deciphering the soil carbon cycle. Radiocarbon 31:644–654

    Article  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 

  • Vestergård M, Reinsch S, Bengtson P, Ambus P, Christensen S (2016) Enhanced priming of old, not new soil carbon at elevated atmospheric CO2. Soil Biol Biochem 100:140–148

    Article  Google Scholar 

  • Xiao C, Guenet B, Zhou Y, Su J, Janssens IA (2015) Priming of soil organic matter decomposition scales linearly with microbial biomass response to litter input in steppe vegetation. Oikos 124:649–657

    Article  CAS  Google Scholar 

  • You M, He P, Dai S, Burger M, Li L (2021) Priming effect of stable C pool in soil and its temperature sensitivity. Geoderma 401:115216

    Article  CAS  Google Scholar 

  • Zhang X, Han X, Yu W, Wang P, Cheng W (2017) Priming effects on labile and stable soil organic carbon decomposition: Pulse dynamics over two years. PLoS ONE 12:e0184978

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Zhu B, Yu F, Cheng W (2021) Plant inputs mediate the linkage between soil carbon and net nitrogen mineralization. Sci Total Environ 790:148208

    Article  CAS  PubMed  Google Scholar 

  • Zhu B, Cheng W (2011) Rhizosphere priming effect increases the temperature sensitivity of soil organic matter decomposition. Glob Change Biol 17:2172–2183

    Article  Google Scholar 

  • Zhu B, Gutknecht JLM, Herman DJ, Keck DC, Firestone MK, Cheng W (2014) Rhizosphere priming effects on soil carbon and nitrogen mineralization. Soil Biol Biochem 76:183–192

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (31470625, 41630755 and 31988102), and the Natural Science Foundation of Zhejiang Province (LQ20D030001). We are also grateful to the anonymous reviewers and the handling editor for their insightful and constructive comments which improved the manuscript.

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Authors and Affiliations

  1. Institute of Wetland Ecology & Clone Ecology, Zhejiang Provincial Key Laboratory of Plant Evolutionary Ecology and Conservation, Taizhou University, Taizhou, 318000, China

    Xiuwei Zhang & Fei-Hai Yu

  2. Key Laboratory of Forest Ecology and Management, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, 110016, China

    Xiuwei Zhang & Peng Wang

  3. Institute of Ecology, College of Urban and Environmental Sciences, Key Laboratory for Earth Surface Processes of the Ministry of Education, Peking University, Beijing, 100871, China

    Biao Zhu

  4. Department of Environmental Studies, University of California, Santa Cruz, CA, 95064, USA

    Weixin Cheng

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  1. Xiuwei Zhang
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  2. Biao Zhu
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  3. Fei-Hai Yu
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  4. Peng Wang
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Correspondence to Xiuwei Zhang or Biao Zhu.

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Zhang, X., Zhu, B., Yu, FH. et al. Long-term bare fallow soil reveals the temperature sensitivity of priming effect of the relatively stabilized soil organic matter. Plant Soil 488, 57–70 (2023). https://doi.org/10.1007/s11104-021-05260-w

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