Soil organic carbon stabilization by organic amendments through iron gate and enzyme latch mechanisms

1. IPCC. Climate Change 2022: Mitigation of Climate Change. Contribution of Working Group III to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change (Cambridge University Press, 2022).

2. Liu, Y. et al. Rice paddy soils are a quantitatively important carbon store according to a global synthesis. Commun. Earth Environ. 2, 154 (2021).

   Google Scholar 

3. Beillouin, D. et al. A global meta-analysis of soil organic carbon in the Anthropocene. Nat. Commun. 14, 3700 (2023).

   Google Scholar 

4. Ma, S. et al. Response of soil aggregation and associated organic carbon to organic amendment and its controls: a global meta-analysis. Catena 237, 107774 (2024).

   Google Scholar 

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

   Google Scholar 

6. Tisdall, J. M. & Oades, J. M. Organic matter and water-stable aggregates in soils. J. Soil Sci. 33, 141–163 (1982).

   Google Scholar 

7. Six, J., Bossuyt, H., Degryze, S. & Denef, K. A history of research on the link between (micro)aggregates, soil biota, and soil organic matter dynamics. Soil Tillage Res., Adv. Soil Struct. Res. 79, 7–31 (2004).

   Google Scholar 

8. Totsche, K. U. et al. Microaggregates in soils. J. Plant Nutr. Soil Sci. 181, 104–136 (2018).

   Google Scholar 

9. Wang, C., Li, R., Liu, X. & Gao, P. Iron-driven organic carbon sequestration in arid saline-alkali soils: mechanisms of Fe-C coupling via reactive iron oxides and microaggregate stabilization. Geoderma 465, 117655 (2026).

   Google Scholar 

10. Kleber, M. et al. In Advances in Agronomy (ed. Sparks, D. L.) 1–140 (Academic Press, 2015).

11. Xiao, K. Q. et al. Introducing the soil mineral carbon pump. Nat. Rev. Earth Environ. 4, 135–136 (2023).

    Google Scholar 

12. Wu, D., Wu, L., Liu, K., Shang, J. & Zhang, W. Contrasting effects of iron oxides on soil organic carbon accumulation in paddy and upland fields under long-term fertilization. J. Environ. Manag. 369, 122286 (2024).

    Google Scholar 

13. Jia, N., Li, L., Guo, H. & Xie, M. Important role of Fe oxides in global soil carbon stabilization and stocks. Nat. Commun. 15, 10318 (2024).

    Google Scholar 

14. Zhu, J. H. et al. Mineral–enzyme interactions drive soil organic carbon accumulation and stabilization in permafrost. Environ. Sci. Technol. 59, 27824–27835 (2025).

    Google Scholar 

15. Jiang, Z. et al. Conversion from double-rice to maize-rice increases iron-bound organic carbon by “iron gate” and “enzyme latch” mechanisms. Soil Tillage Res. 211, 105014 (2021).

    Google Scholar 

16. Ma, S. et al. Organic amendment increases soil carbon sequestration by altering carbon stabilization pathways within soil aggregates. Soil Tillage Res. 256, 106868 (2026).

    Google Scholar 

17. Li, J., Yang, Y., Wen, J., Mo, F. & Liu, Y. Continuous manure application strengthens the associations between soil microbial function and crop production: Evidence from a 7-year multisite field experiment on the Guanzhong Plain. Agric. Ecosyst. Environ. 338, 108082 (2022).

    Google Scholar 

18. Huang, X. iaolei, Jia, Z., Jiao, X., Wang, J. & Huang, X. uefang Long-term manure applications to increase carbon sequestration and macroaggregate-stabilized carbon. Soil Biol. Biochem. 174, 108827 (2022).

    Google Scholar 

19. Wang, X. et al. Organic amendments drive shifts in microbial community structure and keystone taxa which increase C mineralization across aggregate size classes. Soil Biol. Biochem. 153, 108062 (2021).

    Google Scholar 

20. Lehmann, J. et al. Biochar in climate change mitigation. Nat. Geosci. 14, 883–892 (2021).

    Google Scholar 

21. Castellini, M., Giglio, L., Niedda, M., Palumbo, A. D. & Ventrella, D. Impact of biochar addition on the physical and hydraulic properties of a clay soil. Soil Tillage Res. 154, 1–13 (2015).

    Google Scholar 

22. Liu, S. et al. Response of soil carbon dioxide fluxes, soil organic carbon and microbial biomass carbon to biochar amendment: a meta-analysis. GCB Bioenergy 8, 392–406 (2016).

    Google Scholar 

23. Zhang, S. et al. Linking soil carbon availability, microbial community composition and enzyme activities to organic carbon mineralization of a bamboo forest soil amended with pyrogenic and fresh organic matter. Sci. Total Environ. 801, 149717 (2021).

    Google Scholar 

24. Lan, X. et al. Effects of long-term manure substitution regimes on soil organic carbon composition in a red paddy soil of southern China. Soil Tillage Res. 221, 105395 (2022).

    Google Scholar 

25. Jia, Z. et al. Rejuvenation of iron oxides enhances carbon sequestration by the ‘iron gate’ and ‘enzyme latch’ mechanisms in a rice-wheat cropping system. Sci. Total Environ. 839, 156209 (2022).

    Google Scholar 

26. Lalonde, K., Mucci, A., Ouellet, A. & Gélinas, Y. Preservation of organic matter in sediments promoted by iron. Nature 483, 198–200 (2012).

    Google Scholar 

27. Freeman, C., Ostle, N. & Kang, H. An enzymic “latch” on a global carbon store. Nature 409, 149–149 (2001).

    Google Scholar 

28. Sinsabaugh, R. L., Hill, B. H. & Follstad Shah, J. J. Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462, 795–798 (2009).

    Google Scholar 

29. Burns, R. G. et al. Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol. Biochem. 58, 216–234 (2013).

    Google Scholar 

30. Lin, Y. et al. Long-term manure application increases soil organic matter and aggregation, and alters microbial community structure and keystone taxa. Soil Biol. Biochem. 134, 187–196 (2019).

    Google Scholar 

31. Wu, Q. et al. Biochar co-application mitigated the stimulation of organic amendments on soil respiration by decreasing microbial activities in an infertile soil. Biol. Fertil. Soils 57, 793–807 (2021).

    Google Scholar 

32. Tian, L. & Shi, W. Soil peroxidase regulates organic matter decomposition through improving the accessibility of reducing sugars and amino acids. Biol. Fertil. Soils 50, 785–794 (2014).

    Google Scholar 

33. Xin, P., Zhang, Y., Jiang, N., Chen, Z. & Chen, L. Neutral soil pH conditions favor the inhibition of phenol on hydrolase activities and soil organic carbon mineralization. Eur. J. Soil Biol. 121, 103621 (2024).

    Google Scholar 

34. He, Z. et al. Effects of biochar particle size on sorption and desorption behavior of NH4+-N. Ind. Crops Prod. 189, 115837 (2022).

    Google Scholar 

35. Zhu, X., Chen, B., Zhu, L. & Xing, B. Effects and mechanisms of biochar-microbe interactions in soil improvement and pollution remediation: a review. Environ. Pollut. 227, 98–115 (2017).

    Google Scholar 

36. Palansooriya, K. N. et al. Soil amendments for immobilization of potentially toxic elements in contaminated soils: a critical review. Environ. Int. 134, 105046 (2020).

    Google Scholar 

37. Yi, Q. et al. Temporal physicochemical changes and transformation of biochar in a rice paddy: Insights from a 9-year field experiment. Sci. Total Environ. 721, 137670 (2020).

    Google Scholar 

38. Li, T. et al. Weakening of the ‘enzymatic latch’ mechanism following long-term fertilization in a minerotrophic peatland. Soil Biol. Biochem. 136, 107528 (2019).

    Google Scholar 

39. Schimel, J. P. & Weintraub, M. N. The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol. Biochem. 35, 549–563 (2003).

    Google Scholar 

40. Cotrufo, M. F., Wallenstein, M. D., Boot, C. M., Denef, K. & Paul, E. The Microbial Efficiency-Matrix Stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Glob. Change Biol. 19, 988–995 (2013).

    Google Scholar 

41. Cotrufo, M. F., Haddix, M. L., Kroeger, M. E. & Stewart, C. E. The role of plant input physical-chemical properties, and microbial and soil chemical diversity on the formation of particulate and mineral-associated organic matter. Soil Biol. Biochem. 168, 108648 (2022).

    Google Scholar 

42. Liang, C., Schimel, J. P. & Jastrow, J. D. The importance of anabolism in microbial control over soil carbon storage. Nat. Microbiol 2, 17105 (2017).

    Google Scholar 

43. Chen, N. et al. Active iron phases regulate the abiotic transformation of organic carbon during redox fluctuation cycles of paddy soil. Environ. Sci. Technol. 55, 14281–14293 (2021).

    Google Scholar 

44. Yu, G. H. & Kuzyakov, Y. Fenton chemistry and reactive oxygen species in soil: abiotic mechanisms of biotic processes, controls and consequences for carbon and nutrient cycling. Earth-Sci. Rev. 214, 103525 (2021).

    Google Scholar 

45. Wen, Y. L. et al. Organic amendments stimulate co-precipitation of ferrihydrite and dissolved organic matter in soils. Geoderma 402, 115352 (2021).

    Google Scholar 

46. Giannetta, B. et al. Iron speciation in organic matter fractions isolated from soils amended with biochar and organic fertilizers. Environ. Sci. Technol. 54, 5093–5101 (2020).

    Google Scholar 

47. He, H. et al. Microbially driven iron cycling facilitates organic carbon accrual in decadal biochar-amended soil. Environ. Sci. Technol. 58, 12430–12440 (2024).

    Google Scholar 

48. Weng, Z. et al. Microspectroscopic visualization of how biochar lifts the soil organic carbon ceiling. Nat. Commun. 13, 5177 (2022).

    Google Scholar 

49. Tian, Y. & Lu, S. Amorphous iron oxides protect aggregate-associated organic carbon from microbial utilization and decomposition evidenced from the natural abundance of 13C. Soil Tillage Res. 227, 105623 (2023).

    Google Scholar 

50. Wen, Y., Xiao, J., Goodman, B. A. & He, X. Effects of organic amendments on the transformation of Fe (Oxyhydr)oxides and soil organic carbon storage. Front. Earth Sci. 7, 257 (2019).

    Google Scholar 

51. Kalu, S. et al. Biochar reduced the mineralization of native and added soil organic carbon: evidence of negative priming and enhanced microbial carbon use efficiency. Biochar 6, 7 (2024).

    Google Scholar 

52. Liu, L., Zheng, N., Yu, Y., Zheng, Z. & Yao, H. Soil carbon and nitrogen cycles driven by iron redox: a review. Sci. Total Environ. 918, 170660 (2024).

    Google Scholar 

53. Zhang, W. et al. Rice-crayfish farming system promote subsoil microbial residual carbon accumulation and stabilization by mediating microbial metabolism process. Sci. Total Environ. 946, 174188 (2024).

    Google Scholar 

54. Song, X. et al. Towards a better understanding of the role of Fe cycling in soil for carbon stabilization and degradation. carbon res 1, 5 (2022).

    Google Scholar 

55. Shi, L. et al. Extracellular electron transfer mechanisms between microorganisms and minerals. Nat. Rev. Microbiol. 14, 651–662 (2016).

    Google Scholar 

56. Litchman, E. et al. Refocusing the microbial rare biosphere concept through a functional lens. Trends Ecol. Evol. 39, 923–936 (2024).

    Google Scholar 

57. Liu, Y. et al. Rare keystone taxa drive soil microbial stability in low-temperature peatlands of China. Appl. Soil Ecol. 213, 106290 (2025).

    Google Scholar 

58. IUSS Working Group WRB. World Reference Base for Soil Resources 2022. World Soil Resources Reports 103 (FAO, 2022).

59. Bach, E. M., Williams, R. J., Hargreaves, S. K., Yang, F. & Hofmockel, K. S. Greatest soil microbial diversity found in micro-habitats. Soil Biol. Biochem. 118, 217–226 (2018).

    Google Scholar 

60. Gunina, A. & Kuzyakov, Y. Pathways of litter C by formation of aggregates and SOM density fractions: Implications from 13C natural abundance. Soil Biol. Biochem. 71, 95–104 (2014).

    Google Scholar 

61. Marx, M.-C., Wood, M. & Jarvis, S. C. A microplate fluorimetric assay for the study of enzyme diversity in soils. Soil Biol. Biochem. 33, 1633–1640 (2001).

    Google Scholar 

62. Wang, Y., Wang, H., He, J. S. & Feng, X. Iron-mediated soil carbon response to water-table decline in an alpine wetland. Nat. Commun. 8, 15972 (2017).

    Google Scholar 

63. Mehra, O. P. & Jackson, M. L. In Clays and Clay Minerals (ed. Ingerson, E.) 317–327 (Pergamon, 2013).

64. McKeague, J. A. & Day, J. H. Dithionite- and oxalate-extractable Fe and Al as aids in differentiating various classes of soils. Can. J. Soil. Sci. 46, 13–22 (1966).

    Google Scholar 

65. Li, D., Liu, C.-M., Luo, R., Sadakane, K. & Lam, T.-W. MEGAHIT: an ultra-fast singlenode solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 31, 1674–1676 (2015).

    Google Scholar 

66. Li, W., Jaroszewski, L. & Godzik, A. Clustering of highly homologous sequences to reduce the size of large protein databases. Bioinformatics 17, 282–283 (2001).

    Google Scholar 

67. Kanehisa, M., Sato, Y., Furumichi, M., Morishima, K. & Tanabe, M. New approach for understanding genome variations in KEGG. Nucleic Acids Res. 47, D590–D595 (2019).

    Google Scholar 

68. Xie, C. et al. Kobas 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res. 39, W316–W322 (2011).

    Google Scholar 

Download references