Persistent soil organic carbon is more susceptible to the priming effect than labile soil organic carbon

Abstract

As the dominant soil organic carbon (SOC) pool, persistent SOC with a longer turnover time plays a more important role in climate change mitigation in the long term than labile SOC. However, our understanding of the susceptibility of persistent relative to labile SOC to the priming effect caused by simple C is still elusive at a global scale. We conducted a meta-analysis and employed a first-order kinetic decomposition model to assess priming effects induced by simple C such as simple sugars (e.g., glucose) and low-molecular-weight organic acids (e.g., oxalic acid). We found that simple C addition significantly stimulated the decomposition of persistent SOC by on average 66.2% across all ecosystems, i.e., an overall positive priming effect, but did not significantly stimulate labile SOC decomposition with a large variation. The priming effect on persistent SOC increased initially and then decreased with soil C to nitrogen ratio with a threshold at a ratio of ~20, i.e., the microbial stoichiometric decomposition hypothesis. A similar trend was observed with pH increasing, and the threshold was at pH ~6.0. In contrast, the priming effect on labile SOC was mainly influenced by soil nitrogen content. We highlight the high susceptibility of persistent SOC to the priming effect globally, and soil characteristics affecting microbial decomposition activity may play an important role. Our findings advance our knowledge on the potential mechanisms underlying priming effect on distinct SOC pools, which can aid in improving the prediction of dynamics of SOC pools in the presence of plant C inputs.

Graphical abstract

Keywords

soil carbon persistence / soil organic carbon decomposition / first-order kinetic model / microbial carbon availability / stoichiometric decomposition hypothesis

Highlight

	● We used a first-order kinetic decomposition model to assess priming effect on SOC.
	● Persistent SOC exhibited a significant positive priming effect by simple C addition.
	● There was no significant priming effect on labile SOC.
	● There was no difference in priming effect on persistent SOC among ecosystems.
	● Soil C to N ratio and pH regulated priming effects among ecosystems.

References

[1] Balesdent, J., Mariotti, A., Guillet, B., 1987. Natural ¹³C abundance as a tracer for studies of soil organic matter dynamics. Soil Biology and Biochemistry19, 25–30.

[2] 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.

[3] 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.

[4] Collins, H.P., Elliott, E.T., Paustian, K., Bundy, L.G., Dick, W.A., Huggins, D.R., Smucker, A.J.M., Paul, E.A., 2000. Soil carbon pools and fluxes in long-term corn belt agroecosystems. Soil Biology and Biochemistry32, 157–168.

[5] Cotrufo, M.F., Soong, J.L., Horton, A.J., Campbell, E.E., Haddix, M., Wall, D.H., Parton, W.J., 2015. Formation of soil organic matter via biochemical and physical pathways of litter mass loss. Nature Geoscience8, 776–779.

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

[7] Davidson, E.A., Janssens, I.A., 2006. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature440, 165–173.

[8] Dungait, J.A.J., Hopkins, D.W., Gregory, A.S., Whitmore, A.P., 2012. Soil organic matter turnover is governed by accessibility not recalcitrance. Global Change Biology18, 1781–1796.

[9] Fang, Y.Y., Nazaries, L., Singh, B.K., Singh, B.P., 2018. Microbial mechanisms of carbon priming effects revealed during the interaction of crop residue and nutrient inputs in contrasting soils. Global Change Biology24, 2775–2790.

[10] Favaro, A., Singh, B., Warren, C., Dijkstra, F.A., 2025. Differences between priming and rhizosphere priming effects: concepts and mechanisms. Soil Biology and Biochemistry205, 109769.

[11] 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.

[12] Fontaine, S., Mariotti, A., Abbadie, L., 2003. The priming effect of organic matter: a question of microbial competition. Soil Biology and Biochemistry35, 837–843.

[13] Georgiou, K., Koven, C.D., Riley, W.J., Torn, M.S., 2015. Toward improved model structures for analyzing priming: potential pitfalls of using bulk turnover time. Global Change Biology21, 4298–4302.

[14] 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 Biology and Biochemistry52, 43–48.

[15] Gunina, A., Kuzyakov, Y., 2022. From energy to (soil organic) matter. Global Change Biology28, 2169–2182.

[16] Hedges, L.V., Gurevitch, J., Curtis, P.S., 1999. The meta-analysis of response ratios in experimental ecology. Ecology80, 1150–1156.

[17] Henneron, L., Balesdent, J., Alvarez, G., Barré, P., Baudin, F., Basile-Doelsch, I., Cécillon, L., Fernandez-Martinez, A., Hatté, C., Fontaine, S., 2022. Bioenergetic control of soil carbon dynamics across depth. Nature Communications13, 7676.

[18] Hessen, D.O., Ågren, G.I., Anderson, T.R., Elser, J.J., de Ruiter, P.C., 2004. Carbon sequestration in ecosystems: the role of stoichiometry. Ecology85, 1179–1192.

[19] Huo, C.F., Liang, J.Y., Zhang, W.D., Wang, P., Cheng, W.X., 2022. Priming effect and its regulating factors for fast and slow soil organic carbon pools: a meta-analysis. Pedosphere32, 140–148.

[20] Huo, C.F., Luo, Y.Q., Cheng, W.X., 2017. Rhizosphere priming effect: a meta-analysis. Soil Biology and Biochemistry111, 78–84.

[21] Jilling, A., Keiluweit, M., Gutknecht, J.L.M., Grandy, A.S., 2021. Priming mechanisms providing plants and microbes access to mineral-associated organic matter. Soil Biology and Biochemistry158, 108265.

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

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

[24] Lehmann, J., Kleber, M., 2015. The contentious nature of soil organic matter. Nature528, 60–68.

[25] Li, H., Bölscher, T., Winnick, M., Tfaily, M.M., Cardon, Z.G., Keiluweit, M., 2021. Simple plant and microbial exudates destabilize mineral-associated organic matter via multiple pathways. Environmental Science & Technology55, 3389–3398.

[26] Liang, J.Y., Li, D.J., Shi, Z., Tiedje, J.M., Zhou, J.Z., Schuur, E.A.G., Konstantinidis, K.T., Luo, Y.Q., 2015. Methods for estimating temperature sensitivity of soil organic matter based on incubation data: a comparative evaluation. Soil Biology and Biochemistry80, 127–135.

[27] Liang, J.Y., Qi, X., Souza, L., Luo, Y.Q., 2016. Processes regulating progressive nitrogen limitation under elevated carbon dioxide: a meta-analysis. Biogeosciences13, 2689–2699.

[28] Liang, J.Y., Zhou, Z.H., Huo, C.F., Shi, Z., Cole, J.R., Huang, L., Konstantinidis, K.T., Li, X.M., Liu, B., Luo, Z.K., Penton, C.R., Schuur, E.A.G., Tiedje, J.M., Wang, Y.P., Wu, L.Y., Xia, J.Y., Zhou, J.Z., Luo, Y.Q., 2018. More replenishment than priming loss of soil organic carbon with additional carbon input. Nature Communications9, 3175.

[29] Lu, M., Zhou, X.H., Yang, Q., Li, H., Luo, Y.Q., Fang, C.M., Chen, J.K., Yang, X., Li, B., 2013. Responses of ecosystem carbon cycle to experimental warming: a meta-analysis. Ecology94, 726–738.

[30] Luo, Z.K., Baldock, J., Wang, E.L., 2017. Modelling the dynamic physical protection of soil organic carbon: insights into carbon predictions and explanation of the priming effect. Global Change Biology23, 5273–5283.

[31] Michel, J., Brostaux, Y., Longdoz, B., Vanderschuren, H., Delaplace, P., 2025. What if publication bias is the rule and net carbon loss from priming the exception. Soil11, 755–762.

[32] 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.

[33] Phillips, R.P., Finzi, A.C., Bernhardt, E.S., 2011. Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO₂ fumigation. Ecology Letters14, 187–194.

[34] Qin, S.Q., Chen, L.Y., Fang, K., Zhang, Q.W., Wang, J., Liu, F.T., Yu, J.C., Yang, Y.H., 2019. Temperature sensitivity of SOM decomposition governed by aggregate protection and microbial communities. Science Advances5, eaau1218.

[35] R Core Team, 2018. R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.

[36] Rosenberg, M.S., 2005. The file-drawer problem revisited: a general weighted method for calculating fail-safe numbers in meta-analysis. Evolution59, 464–468.

[37] Rothstein, H.R., Sutton, A.J., Borenstein, M., 2005. Publication Bias in Meta-Analysis: Prevention, Assessment and Adjustments. Chichester, UK: Wiley-Blackwell.

[38] Rumpel, C., Kögel-Knabner, I., 2011. Deep soil organic matter—a key but poorly understood component of terrestrial C cycle. Plant and Soil338, 143–158.

[39] Schmidt, M.W.I., Torn, M.S., Abiven, S., Dittmar, T., Guggenberger, G., Janssens, I.A., Kleber, M., Kögel-Knabner, I., Lehmann, J., Manning, D.A.C., Nannipieri, P., Rasse, D.P., Weiner, S., Trumbore, S.E., 2011. Persistence of soil organic matter as an ecosystem property. Nature478, 49–56.

[40] Shahzad, T., Rashid, M.I., Maire, V., Barot, S., Perveen, N., Alvarez, G., Mougin, C., Fontaine, S., 2018. Root penetration in deep soil layers stimulates mineralization of millennia-old organic carbon. Soil Biology and Biochemistry124, 150–160.

[41] Smith, P., Fang, C.M., Dawson, J.J.C., Moncrieff, J.B., 2008. Impact of global warming on soil organic carbon. Advances in Agronomy97, 1–43.

[42] Sokol, N.W., Bradford, M.A., 2019. Microbial formation of stable soil carbon is more efficient from belowground than aboveground input. Nature Geoscience12, 46–53.

[43] Su, J., Zhang, H.Y., Han, X.G., Lv, R.F., Liu, L., Jiang, Y., Li, H., Kuzyakov, Y., Wei, C.Z., 2023. 5300-Year-old soil carbon is less primed than young soil organic matter. Global Change Biology29, 260–275.

[44] Sun, Z.L., Liu, S.G., Zhang, T.A., Zhao, X.C., Chen, S., Wang, Q.K., 2019. Priming of soil organic carbon decomposition induced by exogenous organic carbon input: a meta-analysis. Plant and Soil443, 463–471.

[45] Tian, D.S., Niu, S.L., 2015. A global analysis of soil acidification caused by nitrogen addition. Environmental Research Letters10, 024019.

[46] Torn, M.S., Kleber, M., Zavaleta, E.S., Zhu, B., Field, C.B., Trumbore, S.E., 2013. A dual isotope approach to isolate soil carbon pools of different turnover times. Biogeosciences10, 8067–8081.

[47] van Groenigen, K.J., Qi, X., Osenberg, C.W., Luo, Y.Q., Hungate, B.A., 2014. Faster decomposition under increased atmospheric CO₂ limits soil carbon storage. Science344, 508–509.

[48] van Groenigen, K.J., Xia, J.Y., Osenberg, C.W., Luo, Y.Q., Hungate, B.A., 2015. Application of a two-pool model to soil carbon dynamics under elevated CO₂. Global Change Biology21, 4293–4297.

[49] Wang, C.Q., Kuzyakov, Y., 2024. Soil organic matter priming: the pH effects. Global Change Biology30, e17349.

[50] Wild, B., Monteux, S., Wendler, B., Hugelius, G., Keuper, F., 2023. Circum-Arctic peat soils resist priming by plant-derived compounds. Soil Biology and Biochemistry180, 109012.

[51] Xiang, D.F., Wang, G.S., Tian, J., Li, W.Y., 2023. Global patterns and edaphic-climatic controls of soil carbon decomposition kinetics predicted from incubation experiments. Nature Communications14, 2171.

[52] Xu, S.W., Delgado-Baquerizo, M., Kuzyakov, Y., Wu, Y., Liu, L.H., Yang, Y.Y., Li, Y.Y., Yu, Y.X., Zhu, B., Yao, H.Y., 2024. Positive soil priming effects are the rule at a global scale. Global Change Biology30, e17502.

[53] Xu, T., White, L., Hui, D.F., Luo, Y.Q., 2006. Probabilistic inversion of a terrestrial ecosystem model: analysis of uncertainty in parameter estimation and model prediction. Global Biogeochemical Cycles20, GB2007.

[54] Yan, S.B., Yin, L.M., Dijkstra, F.A., Wang, P., Cheng, W.X., 2023. Priming effect on soil carbon decomposition by root exudate surrogates: a meta-analysis. Soil Biology and Biochemistry178, 108955.

[55] Zhang, Q.F., Feng, J.G., Li, J., Huang, C.Y., Shen, Y.W., Cheng, W.X., Zhu, B., 2023. A distinct sensitivity to the priming effect between labile and stable soil organic carbon. New Phytologist237, 88–99.

[56] Zhang, X.W., Han, X.Z., Yu, W.T., Wang, P., Cheng, W.X., 2017. Priming effects on labile and stable soil organic carbon decomposition: pulse dynamics over two years. PLoS One12, e0184978.

[57] Zhou, G.Y., Zhou, X.H., Nie, Y.Y., Bai, S.H., Zhou, L.Y., Shao, J.J., Cheng, W.S., Wang, J.W., Hu, F.Q., Fu, Y.L., 2018. Drought-induced changes in root biomass largely result from altered root morphological traits: evidence from a synthesis of global field trials. Plant, Cell & Environment41, 2589–2599.

[58] Zhou, J., Guillaume, T., Wen, Y., Blagodatskaya, E., Shahbaz, M., Zeng, Z.H., Peixoto, L., Zang, H.D., Kuzyakov, Y., 2022. Frequent carbon input primes decomposition of decadal soil organic matter. Soil Biology and Biochemistry175, 108850.

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