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Soil carbon losses due to priming moderated by adaptation and legacy effects

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Abstract

Increasing soil organic carbon contents contributes to global climate change mitigation. However, new plant inputs can enhance the mineralization of native soil organic carbon by the positive priming effect, which may counterbalance the sequestration of new carbon. Here we use soils from a 20 year chronosequence of inverted pasture soils (reciprocal translocation of topsoil and subsoil to >1 m) to study the dynamics of soil organic carbon in topsoils and subsoils. We evaluated the root-induced priming effect by differentiating native soil organic carbon from 13C root-derived carbon in a 6 month incubation experiment. We found that the addition of fresh root-derived carbon caused positive priming of native soil organic carbon in new topsoils (109 ± 27% additional respiration compared with controls without roots) and subsoils (331 ± 84%) after inversion. This effect was temporary for new topsoils as they accumulated soil organic carbon and adapted to high carbon inputs within a few years, leading to no priming in the long term. In contrast, buried topsoils became more sensitive to root carbon inputs over time, demonstrating how the legacy of high carbon inputs mediates the magnitude of priming (50% to 390% after 20 years of inversion). Overall, carbon losses with priming never exceeded new root-derived carbon inputs. We conclude that priming is a temporary reaction to additional carbon, which attenuates when soils adapt to high carbon inputs within a few years to decades.

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Fig. 1: SOC contents, microbial biomass and respiration of native SOC.
Fig. 2: Priming effect with roots in topsoils and subsoils.
Fig. 3: Allocation of root-derived C within fractions.
Fig. 4: Gains in root-derived C and loss of native SOC with net balance.

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Data availability

All data are available via Zenodo at https://doi.org/10.5281/zenodo.7304562.

References

  1. Batjes, N. H. Harmonized soil property values for broad-scale modelling (WISE30sec) with estimates of global soil carbon stocks. Geoderma 269, 61–68 (2016).

    Google Scholar 

  2. Jobbágy, B. E. G. & Jackson, R. The vertical distribution of soil organic carbon and its relation to climate and vegetation. Belowgr. Process. Glob. Change 10, 423–436 (2000).

    Google Scholar 

  3. Paustian, K. et al. Climate-smart soils. Nature 532, 49–57 (2016).

    Google Scholar 

  4. Minasny, B. et al. Soil carbon 4 per mille. Geoderma 292, 59–86 (2017).

    Google Scholar 

  5. Bossio, D. A. et al. The role of soil carbon in natural climate solutions. Nat. Sustain. 3, 391–398 (2020).

  6. Amelung, W. et al. Towards a global-scale soil climate mitigation strategy. Nat. Commun. 11, 5427 (2020).

    Google Scholar 

  7. Lützow, M. V. et al. Stabilization of organic matter in temperate soils: mechanisms and their relevance under different soil conditions—a review. Eur. J. Soil Sci. 57, 426–445 (2006).

    Google Scholar 

  8. Schmidt, M. W. I. et al. Persistence of soil organic matter as an ecosystem property. Nature 478, 49–56 (2011).

    Google Scholar 

  9. Peixoto, L. et al. Deep-rooted perennial crops differ in capacity to stabilize C inputs in deep soil layers. Sci. Rep. 12, 5952 (2022).

    Google Scholar 

  10. Thorup-Kristensen, K. et al. Digging deeper for agricultural resources, the value of deep rooting. Trends Plant Sci. 25, 406–417 (2020).

    Google Scholar 

  11. Button, E. S. et al. Deep-C storage: biological, chemical and physical strategies to enhance carbon stocks in agricultural subsoils. Soil Biol. Biochem. 170, 108697 (2022).

    Google Scholar 

  12. Kuzyakov, Y., Friedel, J. K. & Stahr, K. Review of mechanisms and quantification of priming effects. Soil Biol. Biochem. 14, 382–395 (2000).

    Google Scholar 

  13. Blagodatskaya, Е & Kuzyakov, Y. 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 (2008).

    Google Scholar 

  14. Guttières, R. et al. Temperature and soil management effects on carbon fluxes and priming effect intensity. Soil Biol. Biochem. 153, 108103 (2021).

    Google Scholar 

  15. Chen, L. et al. Regulation of priming effect by soil organic matter stability over a broad geographic scale. Nat. Commun. 10, 5112 (2019).

    Google Scholar 

  16. Lyu, M. et al. Simulated leaf litter addition causes opposite priming effects on natural forest and plantation soils. Biol. Fertil. Soils 54, 925–934 (2018).

    Google Scholar 

  17. Siles, J. A. et al. Priming effects in soils across Europe. Glob. Change Biol. 28, 2146–2157 (2022).

  18. Luo, Z., Wang, E. & Sun, O. J. A meta-analysis of the temporal dynamics of priming soil carbon decomposition by fresh carbon inputs across ecosystems. Soil Biol. Biochem. 101, 96–103 (2016).

    Google Scholar 

  19. Bastida, F. et al. Global ecological predictors of the soil priming effect. Nat. Commun. 10, 3481 (2019).

    Google Scholar 

  20. Gaudel, G. et al. Meta-analysis of the priming effect on native soil organic carbon in response to glucose amendment across soil depths. Plant Soil 479, 107–124 (2022).

    Google Scholar 

  21. Fontaine, S. et al. Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature 450, 277–280 (2007).

    Google Scholar 

  22. Fontaine, S., Bardoux, G., Abbadie, L. & Mariotti, A. Carbon input to soil may decrease soil carbon content. Ecol. Lett. 7, 314–320 (2004).

    Google Scholar 

  23. Bernard, L. et al. Advancing the mechanistic understanding of the priming effect on soil organic matter mineralisation. Funct. Ecol. 36, 1355–1377 (2022).

    Google Scholar 

  24. Guenet, B. et al. Impact of priming on global soil carbon stocks. Glob. Change Biol. 24, 1873–1883 (2018).

    Google Scholar 

  25. Wordell-Dietrich, P., Don, A. & Helfrich, M. Controlling factors for the stability of subsoil carbon in a Dystric Cambisol. Geoderma 304, 40–48 (2017).

    Google Scholar 

  26. Hicks Pries, C. E. et al. Root litter decomposition slows with soil depth. Soil Biol. Biochem. 125, 103–114 (2018).

    Google Scholar 

  27. Kuzyakov, Y. Review: factors affecting rhizosphere priming effects. J. Plant Nutr. Soil Sci. 15, 382–395 (2002).

    Google Scholar 

  28. Kuzyakov, Y. & Blagodatskaya, E. Microbial hotspots and hot moments in soil: concept & review. Soil Biol. Biochem. 83, 184–199 (2015).

    Google Scholar 

  29. Huo, C., Luo, Y. & Cheng, W. Rhizosphere priming effect: a meta-analysis. Soil Biol. Biochem. 111, 78–84 (2017).

    Google Scholar 

  30. Dijkstra, F. A., Zhu, B. & Cheng, W. Root effects on soil organic carbon: a double‐edged sword. N. Phytol. 230, 60–65 (2021).

    Google Scholar 

  31. Kuzyakov, Y. & Razavi, B. S. Rhizosphere size and shape: temporal dynamics and spatial stationarity. Soil Biol. Biochem. 135, 343–360 (2019).

    Google Scholar 

  32. Kleber, M. et al. Dynamic interactions at the mineral-organic matter interface. Nat. Rev. Earth Environ. 2, 402–421 (2021).

    Google Scholar 

  33. Sokol, N. W. et al. Life and death in the soil microbiome: how ecological processes influence biogeochemistry. Nat. Rev. Microbiol. 20, 415–430 (2022).

    Google Scholar 

  34. Sokol, N. W. & Bradford, M. A. Microbial formation of stable soil carbon is more efficient from belowground than aboveground input. Nat. Geosci. 12, 46–53 (2019).

    Google Scholar 

  35. Jilling, A., Keiluweit, M., Gutknecht, J. L. M. & Grandy, A. S. Priming mechanisms providing plants and microbes access to mineral-associated organic matter. Soil Biol. Biochem. 158, 108265 (2021).

    Google Scholar 

  36. Schiedung, M., Tregurtha, C. S., Beare, M. H., Thomas, S. M. & Don, A. Deep soil flipping increases carbon stocks of New Zealand grasslands. Glob. Change Biol. 25, 2296–2309 (2019).

    Google Scholar 

  37. Alcántara, V., Don, A., Vesterdal, L., Well, R. & Nieder, R. Stability of buried carbon in deep-ploughed forest and cropland soils - implications for carbon stocks. Sci. Rep. 7, 5511 (2017).

    Google Scholar 

  38. Pereira, R. C. et al. Evidence for soil carbon enhancement through deeper mouldboard ploughing at pasture renovation on a Typic Fragiaqualf. Soil Res. 56, 182–191 (2018).

    Google Scholar 

  39. Kirschbaum, M. U. F. et al. Sequestration of soil carbon by burying it deeper within the profile: A theoretical exploration of three possible mechanisms. Soil Biol. Biochem. 163, 108432 (2021).

    Google Scholar 

  40. Alcántara, V., Don, A., Well, R. & Nieder, R. Deep ploughing increases agricultural soil organic matter stocks. Glob. Change Biol. 22, 2939–2956 (2016).

    Google Scholar 

  41. Sanaullah, M. et al. How do microbial communities in top- and subsoil respond to root litter addition under field conditions? Soil Biol. Biochem. 103, 28–38 (2016).

    Google Scholar 

  42. Cookson, W. R., Beare, M. H. & Wilson, P. E. Effects of prior crop residue management on microbial properties and crop residue decomposition. Appl. Soil Ecol. 7, 179–188 (1998).

    Google Scholar 

  43. Don, A., Böhme, I. H., Dohrmann, A. B., Poeplau, C. & Tebbe, C. C. Microbial community composition affects soil organic carbon turnover in mineral soils. Biol. Fertil. Soils 53, 445–456 (2017).

    Google Scholar 

  44. Lehmann, J. et al. Persitence of soil organic carbon caused by functional complexity. Nat. Geosci. 13, 529–534 (2020).

    Google Scholar 

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

    Google Scholar 

  46. Kögel-Knabner, I. et al. Organo-mineral associations in temperate soils: integrating biology, mineralogy, and organic matter chemistry. J. Plant Nutr. Soil Sci. 171, 61–82 (2008).

    Google Scholar 

  47. Lehmann, J. & Kleber, M. The contentious nature of soil organic matter. Nature 528, 60–68 (2015).

    Google Scholar 

  48. Gregorich, E. G., Beare, M. H., McKim, U. F. & Skjemstad, J. O. Chemical and biological characteristics of physically uncomplexed organic matter. Soil Sci. Soc. Am. J. 70, 975–985 (2006).

    Google Scholar 

  49. Villarino, S. H., Pinto, P., Jackson, R. B. & Piñeiro, G. Plant rhizodeposition: a key factor for soil organic matter formation in stable fractions. Sci. Adv. 7, eabd3176 (2021).

    Google Scholar 

  50. Poeplau, C., Don, A. & Schneider, F. Roots are key to increasing the mean residence time of organic carbon entering temperate agricultural soils. Glob. Change Biol. 27, 4921–4934 (2021).

    Google Scholar 

  51. Fossum, C. et al. Belowground allocation and dynamics of recently fixed plant carbon in a California annual grassland. Soil Biol. Biochem. 165, 108519 (2022).

    Google Scholar 

  52. Sanderman, J., Creamer, C., Baisden, W. T., Farrell, M. & Fallon, S. Greater soil carbon stocks and faster turnover rates with increasing agricultural productivity. Soil 3, 1–16 (2017).

    Google Scholar 

  53. Angst, G., Kögel-Knabner, I., Kirfel, K., Hertel, D. & Mueller, C. W. Spatial distribution and chemical composition of soil organic matter fractions in rhizosphere and non-rhizosphere soil under European beech (Fagus sylvatica L.). Geoderma 264, 179–187 (2016).

    Google Scholar 

  54. Shi, A. et al. Substrate spatial heterogeneity reduces soil microbial activity. Soil Biol. Biochem. 152, 108068 (2021).

    Google Scholar 

  55. Nunan, N., Leloup, J., Ruamps, L. S., Pouteau, V. & Chenu, C. Effects of habitat constraints on soil microbial community function. Sci. Rep. 7, 4280 (2017).

    Google Scholar 

  56. Inagaki, T. M. et al. Microscale spatial distribution and soil organic matter persistence in top and subsoil. Soil Biol. Biochem. 178, 108921 (2023).

    Google Scholar 

  57. Lawrence‐Smith, E. J. et al. Full inversion tillage during pasture renewal to increase soil carbon storage: New Zealand as a case study. Glob. Change Biol. 27, 1998–2010 (2021).

    Google Scholar 

  58. Thomas, S. M., Beare, M. H. & Rietveld, V. Changes in soil quality following humping/hollowing and flipping of pakihi soils on the West Coast, South Island New Zealand. In Proceedings of the New Zealand Grassland Association 265–270 (New Zealand Grassland Association, 2007).

  59. Anderson, J. P. E. & Domsch, K. H. A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biol. Biochem. 10, 215–221 (1978).

    Google Scholar 

  60. Heinemeyer, O., Insam, H., Kaiser, E. A. & Walenzik, G. Soil microbial biomass and respiration measurements: an automated technique based on infra-red gas analysis. Plant Soil 195, 191–195 (1989).

    Google Scholar 

  61. Kaiser, E. A., Mueller, T., Joergensen, R. G., Insam, H. & Heinemeyer, O. Evaluation of methods to estimate the soil microbial biomass and the relationship with soil texture and organic matter. Soil Biol. Biochem. 24, 675–683 (1992).

    Google Scholar 

  62. Studer, M. S. et al. The MICE facility–a new tool to study plant–soil C cycling with a holistic approach. Isot. Environ. Health Stud. 53, 286–297 (2017).

    Google Scholar 

  63. Wollum, A. G. & Gomez, J. E. A conductivity method for measuring microbially evolved carbon dioxide. Ecology 51, 155–156 (1970).

    Google Scholar 

  64. Zimmermann, M., Leifeld, J., Schmidt, M. W. I., Smith, P. & Fuhrer, J. Measured soil organic matter fractions can be related to pools in the RothC model. Eur. J. Soil Sci. 58, 658–667 (2007).

    Google Scholar 

  65. Poeplau, C. et al. Reproducibility of a soil organic carbon fractionation method to derive RothC carbon pools. Eur. J. Soil Sci. 64, 735–746 (2013).

    Google Scholar 

  66. Abiven, S. & Andreoli, R. Charcoal does not change the decomposition rate of mixed litters in a mineral cambisol: a controlled conditions study. Biol. Fertil. Soils 47, 111–114 (2011).

    Google Scholar 

  67. Coplen, T. B. Guidelines and recommended terms for expression of stable-isotope-ratio and gas-ratio measurement results. Rapid Commun. Mass Spectrom. 25, 2538–2560 (2011).

    Google Scholar 

  68. R Studio (R Core Team, 2021).

  69. Hothorn, T. et al. Multcomp package: simultaneous inference in general parametric models. R package version 1.4-17 (2021).

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Acknowledgements

This work was funded by the Swiss National Science Foundation under project no. 200021_178768 (M.S. and S.A.) and by the European Union’s Horizon 2020 research and innovation programme as part of the EJPSoil project under grant agreement no. 862695 (A.D.). Additional support was provided by the Sustainable Agroecosystem programme at the New Zealand Institute for Plant and Food Research, with funding from the Strategic Science Investment Funded provided by the New Zealand Ministry for Business, Innovation and Employment (M.H.B). We thank C. Tregurtha and F. Hegewald for assistance with the soil sampling and S.-L. Bellè for his support in the laboratory. We also thank the soil organic matter group at the Thünen Institute of Climate-Smart Agriculture and the Research group on Organic Matter in soil and sediments at the Ecole Normale Supérieure Paris (ROMENS) for discussions and comments on earlier versions of the manuscript.

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M.S. conceptualized and designed the experiment with A.D., M.H.B. and S.A. M.S. conducted the experiment and performed all laboratory analyses. M.S. conducted the data analysis and wrote the manuscript with contributions from all authors. All authors approved the final version of the manuscript.

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Correspondence to Marcus Schiedung or Samuel Abiven.

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Extended data

Extended Data Fig. 1 Soil inversion and input of labelled roots.

Concept of soil inversion (a) showing the non-inverted soil with SOC-rich topsoil. The inversion brings the former topsoil in the new subsoil and a new topsoil in created consisting of former subsoil. Set up of pre-incubation and growth of ryegrass under 13C enriched environment (10 atm%) to achieve highly labelled root input (b). The ryegrass seeds were placed on a 2 mm nylon mesh (black dotted line) to allow germination into the soil. After 22 days, aboveground biomass was removed directly at the mesh and soils were mixed prior to the division into the four replicates (equal weight) used for the closed jar incubation (c). The roots were cut during homogenization into 0.5-1 cm large pieces. The respired CO2 was trapped in NaOH traps to determine the total respiration by conductivity. By determining the isotopic composition of the trapped CO2 (precipitated as SrCO3), the contribution of native SOC and root-derived C was calculated (see method section). The isotopic signature of the rood-derived C allowed to trace it in the soils and within SOC fraction separated as particulate organic matter (POM) and mineral associated organic matter (MAOM; divided in sand & aggregate ( > 63 µm) and silt & clay ( < 63 µm) particle sizes).

Extended Data Fig. 2 Total CO2 production six months of incubation.

The cumulative total CO2-C production is shown per mass of soil (a & b) and the specific production is given per total SOC, including native SOC and root-derived C (c & d). All values are presented with the standard error of the mean of incubation replicates (n = 4, also shown as circles). Significant differences between the years since inversion were identified by analysis of variance (ANOVA) and p-values were computed on a 95% pairwise confidence interval with a post hoc-test (Tukey) and a Bonferroni multiplicity adjustment as indicated by letters (p < 0.05). All p-values are presented in Supplementary Table S6 and S7. The cumulative fluxes over the incubation time are shown in Supplementary Fig. S1.

Extended Data Fig. 3 Native SOC and root-derived C specific CO2 production.

Cumulative CO2 production over six months as native SOC specific [mg CO2-Cnative SOC (g native SOC)-1] respiration (a), root-derived C specific [mg CO2-Croot-derived SOC (g root-derived C)-1] (b) respiration and proportion of root-derived C (CO2-Croot-derived) of total respired CO2-C at each timestep (c) for topsoil and subsoils. Error bars indicate the propagated standard error of the mean over the days of incubation of the incubation replicates (n = 4).

Extended Data Fig. 4 Priming effect in inverted soils with roots.

Additional native SOC respiration of inverted soils (3-20 years) with fitted two-tailed linear regression over time since inversion for topsoils (a; R² = 0.66, p < 0.001) and subsoils (b; R² = 0.14, p = 0.09). Grey linear model for subsoils (b; R² = 0.96, p < 0.001) shows the fit excluding the soil inverted seven years ago.

Extended Data Fig. 5 Incubated root-derived C in particulate organic matter.

Proportion of root-derived C remained after the incubation in the particulate organic matter (POM) fraction. The proportion of root derived C after the growth (pre-incubation) and before the incubation are shown in Supplementary Table S2. Linear models with time since inversion are shown in Supplementary Fig. S5.

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Supplementary Figs. 1–4 and Tables 1–7.

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Schiedung, M., Don, A., Beare, M.H. et al. Soil carbon losses due to priming moderated by adaptation and legacy effects. Nat. Geosci. 16, 909–914 (2023). https://doi.org/10.1038/s41561-023-01275-3

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