Adding glucose at a uniform amount or according to soil organic carbon content does not cause significant differences in soil priming effects across a broad grassland transect

Abstract

Inputs of plant carbon (C) may modify the decomposition of soil organic C (SOC) through a phenomenon known as priming effect. Glucose is often used to simulate plant C input in priming effect experiments, but whether adding glucose based on whole soil or as a proportion of SOC result in variations in estimating the magnitude and drivers of priming effects is poorly understood. Here, we collected soil samples from 10 sites along an approximately 2000 km grassland transect inInner Mongolia, China. Subsequently, in a 30-day laboratory incubation experiment, ¹³C-labeled glucose was added to the soil using two methods (i.e., relative to soil C or soil mass): glucose-C=2% SOC and 0.4 mg glucose-C g^‒1 soil. This allowed us to investigate the potential impact of different glucose addition methods on assessing the priming effect. The results showed that different glucose addition methods did not cause significant differences in the overall cumulative priming effect. When glucose was added at a rate of glucose-C=2% SOC, the priming effect mechanism aligned with the co-metabolism hypothesis, with SOM stability (represented by content of soil minerals and (clay+silt) %) being the primary driver. When the glucose was added at a rate of 0.4 mg glucose-C g^‒1 soil, the priming effect mechanism was supported by the nutrient mining hypothesis, and SOM stability was also the main controlling factor of the priming effect. These findings suggest that different glucose addition methods may not cause significant differences in the magnitude of soil priming effect or its primary driving factor, but may lead to variation in understanding the main mechanism behind the priming effect.

Graphical abstract

Keywords

soil carbon / large-scale priming effect / glucose addition / Carbon-13 / priming effect driver / mechanism of priming effect

Highlight

	● Glucose-induced soil priming effect was studied along a 2000-km grassland transect.
	● Glucose addition amount was based on soil organic carbon or soil mass.
	● Soil priming effect was not different between these two addition methods.
	● SOM stability was the primary factor for soil priming effect in these two methods.
	● The mechanisms of soil priming effect were inconsistent between these two methods.

References

[1] Araújo, M.S.B., Schaefer, C.E.R., Sampaio, E.V.S.B., 2004. Soil phosphorus fractions from toposequences of semi-arid Latosols and Luvisols in northeastern Brazil. Geoderma119, 309–321.

[2] Basile-Doelsch, I., Balesdent, J., Pellerin, S., 2020. Reviews and syntheses: the mechanisms underlying carbon storage in soil. Biogeosciences17, 5223–5242.

[3] Bastida, F., García, C., Fierer, N., Eldridge, D.J., Bowker, M.A., Abades, S., Alfaro, F.D., Asefaw Berhe, A., Cutler, N.A., Gallardo, A., García-Velázquez, L., Hart, S.C., Hayes, P.E., Hernández, T., Hseu, Z.Y., Jehmlich, N., Kirchmair, M., Lambers, H., Neuhauser, S., Peña-Ramírez, V.M., Pérez, C.A., Reed, S.C., Santos, F., Siebe, C., Sullivan, B.W., Trivedi, P., Vera, A., Williams, M.A., Luis Moreno, J., Delgado-Baquerizo, M., 2019. Global ecological predictors of the soil priming effect. Nature Communications10, 3481.

[4] Bastida, F., Torres, I.F., Hernández, T., Bombach, P., Richnow, H.H., García, C., 2013. Can the labile carbon contribute to carbon immobilization in semiarid soils? Priming effects and microbial community dynamics. Soil Biology and Biochemistry57, 892–902.

[5] Bernal, B., McKinley, D.C., Hungate, B.A., White, P.M., Mozdzer, T.J., Megonigal, J.P., 2016. Limits to soil carbon stability; Deep, ancient soil carbon decomposition stimulated by new labile organic inputs. Soil Biology and Biochemistry98, 85–94.

[6] Bernard, L., Basile-Doelsch, I., Derrien, D., Fanin, N., Fontaine, S., Guenet, B., Karimi, B., Marsden, C., Maron, P.A., 2022. Advancing the mechanistic understanding of the priming effect on soil organic matter mineralisation. Functional Ecology36, 1355–1377.

[7] Blagodatskaya, Е., Kuzyakov, Y., 2008. Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review. Biology and Fertility of Soils45, 115–131.

[8] Blagodatskaya, E., Yuyukina, T., Blagodatsky, S., Kuzyakov, Y., 2011. Three-source-partitioning of microbial biomass and of CO₂ efflux from soil to evaluate mechanisms of priming effects. Soil Biology and Biochemistry43, 778–786.

[9] Blagodatskaya, E.V., Blagodatsky, S.A., Anderson, T.H., Kuzyakov, Y., 2007. Priming effects in Chernozem induced by glucose and N in relation to microbial growth strategies. Applied Soil Ecology37, 95–105.

[10] Bradford, M.A., Wieder, W.R., Bonan, G.B., Fierer, N., Raymond, P.A., Crowther, T.W., 2016. Managing uncertainty in soil carbon feedbacks to climate change. Nature Climate Change6, 751–758.

[11] Chen, L.Y., Liu, L., Qin, S.Q., Yang, G.B., Fang, K., Zhu, B., Kuzyakov, Y., Chen, P.D., Xu, Y.P., Yang, Y.H., 2019. Regulation of priming effect by soil organic matter stability over a broad geographic scale. Nature Communications10, 5112.

[12] Chen, R.R., Senbayram, M., Blagodatsky, S., Myachina, O., Dittert, K., Lin, X.G., Blagodatskaya, E., Kuzyakov. Y., 2014. Soil C and N availability determine the priming effect: microbial N mining and stoichiometric decomposition theories. Global Change Biology20, 2356–2367.

[13] Cheng, W.X., 1999. Rhizosphere feedbacks in elevated CO₂. Tree Physiology19, 313–320.

[14] Ciesielski, H., Sterckeman, T., Santerne, M., Willery, J.P., 1997. A comparison between three methods for the determination of cation exchange capacity and exchangeable cations in soils. Agronomie17, 9–16.

[15] Collignon, C., Ranger, J., Turpault, M.P., 2012. Seasonal dynamics of Al- and Fe-bearing secondary minerals in an acid forest soil: influence of Norway spruce roots (Picea abies (L. ) Karst.). European Journal of Soil Science63, 592–602.

[16] Craine, J.M., Morrow, C., Fierer, N., 2007. Microbial nitrogen limitation increases decomposition. Ecology88, 2105–2113.

[17] Fanin, N., Alavoine, G., Bertrand, I., 2020. Temporal dynamics of litter quality, soil properties and microbial strategies as main drivers of the priming effect. Geoderma377, 114576.

[18] Feng, J.G., Tang, M., Zhu, B., 2021. Soil priming effect and its responses to nutrient addition along a tropical forest elevation gradient. Global Change Biology27, 2793–2806.

[19] Friedlingstein, P., O'Sullivan, M., Jones, M.W., Andrew, R.M., Hauck, J., Olsen, A., Peters, G.P., Peters, W., Pongratz, J., Sitch, S., Le Quéré, C., Canadell, J.G., Ciais, P., Jackson, R.B., Alin, S., Aragão, L.E.O.C., Arneth, A., Arora, V., Bates, N.R., Becker, M., Benoit-Cattin, A., Bittig, H.C., Bopp, L., Bultan, S., Chandra, N., Chevallier, F., Chini, L.P., Evans, W., Florentie, L., Forster, P.M., Gasser, T., Gehlen, M., Gilfillan, D., Gkritzalis, T., Gregor, L., Gruber, N., Harris, I., Hartung, K., Haverd, V., Houghton, R.A., Ilyina, T., Jain, A.K., Joetzjer, E., Kadono, K., Kato, E., Kitidis, V., Korsbakken, J.I., Landschützer, P., Lefèvre, N., Lenton, A., Lienert, S., Liu, Z., Lombardozzi, D., Marland, G., Metzl, N., Munro, D.R., Nabel, J.E.M.S., Nakaoka, S.I., Niwa, Y., O'brien, K., Ono, T., Palmer, P.I., Pierrot, D., Poulter, B., Resplandy, L., Robertson, E., Rödenbeck, C., Schwinger, J., Séférian, R., Skjelvan, I., Smith, A.J.P., Sutton, A.J., Tanhua, T., Tans, P.P., Tian, H.Q., Tilbrook, B., van der Werf, G., Vuichard, N., Walker, A.P., Wanninkhof, R., Watson, A.J., Willis, D., Wiltshire, A.J., Yuan, W.P., Yue, X., Zaehle, S., 2020. Global carbon budget 2020. Earth System Science Data12, 3269–3340.

[20] Gelsomino, A., Petrovičová, B., Zaffina, F., Peruzzi, A., 2010. Chemical and microbial properties in a greenhouse loamy soil after steam disinfestation alone or combined with CaO addition. Soil Biology and Biochemistry42, 1091–1100.

[21] German, D.P., Weintraub, M.N., Grandy, A.S., Lauber, C.L., Rinkes, Z.L., Allison, S.D., 2011. Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biology and Biochemistry43, 1387–1397.

[22] Guttières, R., Nunan, N., Raynaud, X., Lacroix, G., Barot, S., Barré, P., Girardin, C., Guenet, B., Lata, J.C., Abbadie, L., 2021. Temperature and soil management effects on carbon fluxes and priming effect intensity. Soil Biology and Biochemistry153, 108103.

[23] Hamer, U., Marschner, B., 2005. Priming effects in different soil types induced by fructose, alanine, oxalic acid and catechol additions. Soil Biology and Biochemistry37, 445–454.

[24] Harris, D., Horwáth, W.R., van Kessel, C., 2001. Acid fumigation of soils to remove carbonates prior to total organic carbon or carbon-13 isotopic analysis. Soil Science Society of America Journal65, 1853–1856.

[25] Hu, Y.L., Feng, J.G., Zhang, S., Luo, Z.K., Zhu, B., 2025. Depth-dependent regulations of soil priming effects along a 2000 km grassland transect. Soil Biology and Biochemistry202, 109696.

[26] ISSS, 1929. Minutes of the first commission meetings, international congress of soil science. In: Proceedings of Congress of the International Society of Soil Science. Washington215–220.

[27] Jenkinson, D.S., Brookes, P.C., Powlson, D.S., 2004. Measuring soil microbial biomass. Soil Biology and Biochemistry36, 5–7.

[28] Jing, X., Chen, X., Tang, M., Ding, Z.J., Jiang, L., Li, P., Ma, S.H., Tian, D., Xu, L.C., Zhu, J.X., Ji, C.J., Shen, H.H., Zheng, C.Y., Fang, J.Y., Zhu, B., 2017. Nitrogen deposition has minor effect on soil extracellular enzyme activities in six Chinese forests. Science of the Total Environment607–608, 806–815.

[29] Karhu, K., Alaei, S., Li, J., Merilä, P., Ostonen, I., Bengtson, P., 2022. Microbial carbon use efficiency and priming of soil organic matter mineralization by glucose additions in boreal forest soils with different C:N ratios. Soil Biology and Biochemistry167, 108615.

[30] Kuzyakov, Y., 2010. Priming effects: interactions between living and dead organic matter. Soil Biology and Biochemistry42, 1363–1371.

[31] Kuzyakov, Y., Bol, R., 2006. Sources and mechanisms of priming effect induced in two grassland soils amended with slurry and sugar. Soil Biology and Biochemistry38, 747–758.

[32] Kuzyakov, Y., Friedel, J.K., Stahr, K., 2000. Review of mechanisms and quantification of priming effects. Soil Biology and Biochemistry32, 1485–1498.

[33] Liu, X.J.A., Finley, B.K., Mau, R.L., Schwartz, E., Dijkstra, P., Bowker, M.A., Hungate, B.A., 2020. The soil priming effect: consistent across ecosystems, elusive mechanisms. Soil Biology and Biochemistry140, 107617.

[34] Liu, X.J.A., Hayer, M., Mau, R.L., Schwartz, E., Dijkstra, P., Hungate, B.A., 2021. Substrate stoichiometric regulation of microbial respiration and community dynamics across four different ecosystems. Soil Biology and Biochemistry163, 108458.

[35] Liu, X.J.A., Sun, J.R., Mau, R.L., Finley, B.K., Compson, Z.G., van Gestel, N., Brown, J.R., Schwartz, E., Dijkstra, P., Hungate, B.A., 2017. Labile carbon input determines the direction and magnitude of the priming effect. Applied Soil Ecology109, 7–13.

[36] Luo, Z.K., Wang, E.L., Sun, O.J., 2016. A meta-analysis of the temporal dynamics of priming soil carbon decomposition by fresh carbon inputs across ecosystems. Soil Biology and Biochemistry101, 96–103.

[37] Mo, F., Ren, C.J., Yu, K.L., Zhou, Z.H., Phillips, R.P., Luo, Z.K., Zhang, Y.Y., Dang, Y.T., Han, J., Ye, J.S., Vinay, N., Liao, Y.C., Xiong, Y.C., Wen, X.X., 2022. Global pattern of soil priming effect intensity and its environmental drivers. Ecology103, e3790.

[38] Morrissey, E.M., Mau, R.L., Schwartz, E., McHugh, T.A., Dijkstra, P., Koch, B.J., Marks, J.C., Hungate, B.A., 2017. Bacterial carbon use plasticity, phylogenetic diversity and the priming of soil organic matter. The ISME Journal11, 1890–1899.

[39] Paterson, E., Sim, A., 2013. Soil-specific response functions of organic matter mineralization to the availability of labile carbon. Global Change Biology19, 1562–1571.

[40] Perveen, N., Barot, S., Maire, V., Cotrufo, M.F., Shahzad, T., Blagodatskaya, E., Stewart, C.E., Ding, W.X., Siddiq, M.R., 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 Biology and Biochemistry134, 162–171.

[41] Qiao, N., Schaefer, D., Blagodatskaya, E., Zou, X.M., Xu, X.L., Kuzyakov, Y., 2014. Labile carbon retention compensates for CO₂ released by priming in forest soils. Global Change Biology20, 1943–1954.

[42] R Core Team, 2021. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria [Online].

[43] Razanamalala, K., Razafimbelo, T., Maron, P.A., Ranjard, L., Chemidlin, N., Lelièvre, M., Dequiedt, S., Ramaroson, V.H., 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. The ISME Journal12, 451–462.

[44] Ren, C.J., Mo, F., Zhou, Z.H., Bastida, F., Delgado-Baquerizo, M., Wang, J.Y., Zhang, X.Y., Luo, Y.Q., Griffis, T.J., Han, X.H., Wei, G.H., Wang, J., Zhong, Z.K., Feng, Y.Z., Ren, G.X., Wang, X.J., Yu, K.L., Zhao, F.Z., Yang, G.H., Yuan, F.H., 2022a. The global biogeography of soil priming effect intensity. Global Ecology and Biogeography31, 1679–1687.

[45] Ren, C.J., Wang, J.Y., Bastida, F., Delgado-Baquerizo, M., Yang, Y.H., Wang, J., Zhong, Z.K., Zhou, Z.H., Zhang, S.H., Guo, Y.X., Zhou, S., Wei, G.H., Han, X.H., Yang, G.H., Zhao, F.Z., 2022b. Microbial traits determine soil C emission in response to fresh carbon inputs in forests across biomes. Global Change Biology28, 1516–1528.

[46] Rukshana, F., Butterly, C.R., Xu, J.M., Baldock, J.A., Tang. C., 2013. Soil organic carbon contributes to alkalinity priming induced by added organic substrates. Soil Biology and Biochemistry65, 217–226.

[47] Schiedung, M., Don, A., Beare, M.H., Abiven, S., 2023. Soil carbon losses due to priming moderated by adaptation and legacy effects. Nature Geoscience16, 909–914.

[48] Shi, X.Z., Yu, D.S., Xu, S.X., Warner, E.D., Wang, H.J., Sun, W.X., Zhao, Y.C., Gong, Z.T., 2010. Cross-reference for relating Genetic Soil Classification of China with WRB at different scales. Geoderma155, 344–350.

[49] Siles, J.A., Díaz-López, M., Vera, A., Eisenhauer, N., Guerra, C.A., Smith, L.C., Buscot, F., Reitz, T., Breitkreuz, van den Hoogen, J., Crowther, T.W., Orgiazzi, A., Kuzyakov, Y., Delgado-Baquerizo, M., Bastida, F., 2022. Priming effects in soils across Europe. Global Change Biology28, 2146–2157.

[50] Sinsabaugh, R.L., Lauber, C.L., Weintraub, M.N., Ahmed, B., Allison, S.D., Crenshaw, C., Contosta, A.R., Cusack, D., Frey, S., Gallo, M.E., Gartner, T.B., Hobbie, S.E., Holland, K., Keeler, B.L., Powers, J.S., Stursova, M., Takacs-Vesbach, C., Waldrop, M.P., Wallenstein, M.D., Zak, D.R., Zeglin. L. H., 2008. Stoichiometry of soil enzyme activity at global scale. Ecology Letters11, 1252–1264.

[51] Tian, Q.X., Yang, X.L., Wang, X.G., Liao, C., Li, Q.X., Wang, M., Wu, Y., Liu, F., 2016. Microbial community mediated response of organic carbon mineralization to labile carbon and nitrogen addition in topsoil and subsoil. Biogeochemistry128, 125–139.

[52] Treat, C.C., Wollheim, W.M., Varner, R.K., Grandy, A.S., Talbot, J., Frolking, S., 2014. Temperature and peat type control CO₂ and CH₄ production in Alaskan permafrost peats. Global Change Biology20, 2674–2686.

[53] Vance, E.D., Brookes, P.C., Jenkinson, D.S., 1987. An extraction method for measuring soil microbial biomass C. Soil Biology and Biochemistry19, 703–707.

[54] Wu, L., Xu, H., Xiao, Q., Huang, Y.P., Suleman, M.M., Zhu, P., Kuzyakov, Y., Xu, X.L., Xu, M.G., Zhang, W.J., 2020. Soil carbon balance by priming differs with single versus repeated addition of glucose and soil fertility level. Soil Biology and Biochemistry148, 107913.

[55] Yang, S.Y., Angst, G., Jandová, K., Kukla, J., Meador, T.B., Paterson, E., Jílková, V., 2023. Early- and later-stage priming effects induced by spruce root fractions are regulated by substrate availability, stoichiometry and C input. Geoderma437, 116610.

[56] Zhao, F.Z., Wang, J.Y., Li, Y., Xu, X.F., He, L.Y., Wang, J., Ren, C.J., Guo, Y.X., 2022. Microbial functional genes driving the positive priming effect in forest soils along an elevation gradient. Soil Biology and Biochemistry165, 108498.

RIGHTS & PERMISSIONS

Higher Education Press