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Minor effects of nutrient additions on soil microbial carbon use efficiency

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Abstract

The carbon use efficiency (CUE) of soil microbes is defined as the proportion of assimilated carbon (C) allocated to microbial growth than lost through respiration. CUE is a critical parameter in soil C cycling, and its response to external nutrient inputs (including nitrogen [N], phosphorus [P], and combined NP) could determine the change of soil C pool. However, the general pattern of CUE response to nutrient addition remains unclear. By conducting a global meta-analysis of 427 observations, we found that the nutrient addition had no significant overall effect on CUE, whether in the overall nutrient addition experiments or in experiments with different types of nutrient addition. The response of CUE to N addition was regulated by duration, with long-term addition (>10 year) leading to a decrease in CUE. We identified the aridity index as the most important predictor influencing CUE in response to N addition, while ecosystem type was the most key variable for CUE response to both P and NP additions. Global predictions showed future N inputs tends to enhance CUE across most regions, especially in cropland ecosystems. Overall, the effect of nutrient addition on CUE was relatively minor, providing key microbial evidence for understanding future soil C dynamics.

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Data availability

The data that support the findings of this study are openly available in figshare at https://doi.org/10.6084/m9.figshare.30702806.

Code availability

The code that support the findings of this study are openly available in figshare at https://doi.org/10.6084/m9.figshare.30702806.

References

  1. Davidson, E. A. & Janssens, I. A. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440, 165–173 (2006).

    Google Scholar 

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

    Google Scholar 

  3. Friedlingstein, P. et al. Global carbon budget 2023. Earth Syst. Sci. Data 15, 5301–5369 (2023).

    Google Scholar 

  4. Pries, H. C. E., Castanha, C., Porras, R. & Torn, M. The whole-soil carbon flux in response to warming. Science 355, 1420–1423 (2017).

    Google Scholar 

  5. Chen, Y. et al. Whole-soil warming leads to substantial soil carbon emission in an alpine grassland. Nat. Commun. 15, 4489 (2024).

    Google Scholar 

  6. Allison, S. D., Wallenstein, M. D. & Bradford, M. A. Soil-carbon response to warming dependent on microbial physiology. Nat. Geosci. 3, 336–340 (2010).

    Google Scholar 

  7. Liang, C., Schimel, J. P. & Jastrow, J. D. The importance of anabolism in microbial control over soil carbon storage. Nat. Microbiol. 2, 1–6 (2017).

    Google Scholar 

  8. 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 

  9. Camenzind, T., Mason-Jones, K., Mansour, I., Rillig, M. C. & Lehmann, J. Formation of necromass-derived soil organic carbon determined by microbial death pathways. Nat. Geosci. 16, 115–122 (2023).

    Google Scholar 

  10. Sinsabaugh, R. L., Manzoni, S., Moorhead, D. L. & Richter, A. Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling. Ecol. Lett. 16, 930–939 (2013).

    Google Scholar 

  11. Tao, F. et al. Microbial carbon use efficiency promotes global soil carbon storage. Nature 618, 981–985 (2023).

    Google Scholar 

  12. Nottingham, A. T., Meir, P., Velasquez, E. & Turner, B. L. Soil carbon loss by experimental warming in a tropical forest. Nature 584, 234–237 (2020).

    Google Scholar 

  13. Schimel, J. Modeling ecosystem-scale carbon dynamics in soil: the microbial dimension. Soil Biol. Biochem. 178, 108948 (2023).

    Google Scholar 

  14. Pan, Y. et al. Enhanced atmospheric phosphorus deposition in Asia and Europe in the past two decades. Atmos. Ocean. Sci. Lett. 14, 100051 (2021).

    Google Scholar 

  15. Malik, A. et al. Drivers of global nitrogen emissions. Environ. Res. Lett. 17, 015006 (2022).

    Google Scholar 

  16. Zhu, J. X. et al. Changing patterns of global nitrogen deposition driven by socio-economic development. Nat. Commun. 16, 46 (2025).

    Google Scholar 

  17. Peñuelas, J., Sardans, J., Rivas-ubach, A. & Janssens, I. A. The human-induced imbalance between C, N and P in Earth’s life system. Glob. Change Biol. 18, 3–6 (2012).

    Google Scholar 

  18. LeBauer, D. S. & Treseder, K. K. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89, 371–379 (2008).

    Google Scholar 

  19. Zemunik, G., Turner, B. L., Lambers, H. & Laliberté, E. Diversity of plant nutrient-acquisition strategies increases during long-term ecosystem development. Nat. plants 1, 1–4 (2015).

    Google Scholar 

  20. Li, Y., Hou, L. Y., Song, B., Yang, L. Y. & Li, L. H. Effects of increased nitrogen and phosphorus deposition on offspring performance of two dominant species in a temperate steppe ecosystem. Sci. Rep. 7, 40951 (2017).

    Google Scholar 

  21. Bobbink, R. et al. Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol. Appl. 20, 30–59 (2010).

    Google Scholar 

  22. Tulloss, E. M. & Cadenasso, M. L. The effect of nitrogen deposition on plant performance and community structure: is it life stage specific?. PloS ONE 11, e0156685 (2016).

    Google Scholar 

  23. Chen, Y., Liu, X., Hou, Y. H., Zhou, S. R. & Zhu, B. Particulate organic carbon is more vulnerable to nitrogen addition than mineral-associated organic carbon in soil of an alpine meadow. Plant Soil 458, 93–103 (2021).

    Google Scholar 

  24. Wang, X. D. et al. Globally nitrogen addition alters soil microbial community structure, but has minor effects on soil microbial diversity and richness. Soil Biol. Biochem. 179, 108982 (2023).

    Google Scholar 

  25. Janssens, I. et al. Reduction of forest soil respiration in response to nitrogen deposition. Nat. Geosci. 3, 315–322 (2010).

    Google Scholar 

  26. Riggs, C. E. & Hobbie, S. E. Mechanisms driving the soil organic matter decomposition response to nitrogen enrichment in grassland soils. Soil Biol. Biochem. 99, 54–65 (2016).

    Google Scholar 

  27. Crowther, T. W. et al. Sensitivity of global soil carbon stocks to combined nutrient enrichment. Ecol. Lett. 22, 936–945 (2019).

    Google Scholar 

  28. Luo, R. Y. et al. Nutrient addition reduces carbon sequestration in a Tibetan grassland soil: disentangling microbial and physical controls. Soil Biol. Biochem. 144, 107764 (2020).

    Google Scholar 

  29. Keeler, B. L., Hobbie, S. E. & Kellogg, L. E. Effects of long-term nitrogen addition on microbial enzyme activity in eight forested and grassland sites: implications for litter and soil organic matter decomposition. Ecosystems 12, 1–15 (2009).

    Google Scholar 

  30. Zheng, X. Y. et al. Interactions between nitrogen and phosphorus in modulating soil respiration: a meta-analysis. Sci. Total Environ. 905, 167346 (2023).

    Google Scholar 

  31. Hou, E. Q. et al. Latitudinal patterns of terrestrial phosphorus limitation over the globe. Ecol. Lett. 24, 1420–1431 (2021).

    Google Scholar 

  32. Widdig, M. et al. Microbial carbon use efficiency in grassland soils subjected to nitrogen and phosphorus additions. Soil Biol. Biochem. 146, 107815 (2020).

    Google Scholar 

  33. Feng, X. H. et al. Nitrogen input enhances microbial carbon use efficiency by altering plant-microbe-mineral interactions. Glob. Change Biol. 28, 4845–4860 (2022).

    Google Scholar 

  34. Duan, P. P., Wang, K. L. & Li, D. J. Nitrogen addition effects on soil mineral-associated carbon differ between the valley and slope in a subtropical karst forest. Geoderma 430, 116357 (2023).

    Google Scholar 

  35. Kuske, C. R. et al. Simple measurements in a complex system: soil community responses to nitrogen amendment in a Pinus taeda forest. Ecosphere 10, e02687 (2019).

    Google Scholar 

  36. Cui, J. et al. Carbon and nitrogen recycling from microbial necromass to cope with C:N stoichiometric imbalance by priming. Soil Biol. Biochem. 142, 107720 (2020).

    Google Scholar 

  37. Strickland, M. S. & Rousk, J. Considering fungal:bacterial dominance in soils-Methods, controls, and ecosystem implications. Soil Biol. Biochem. 42, 1385–1395 (2010).

    Google Scholar 

  38. Kallenbach, C. M., Frey, S. D. & Grandy, A. S. Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls. Nat. Commun. 7, 13630 (2016).

    Google Scholar 

  39. Miao, Y. C. et al. Lower microbial carbon use efficiency reduces cellulose-derived carbon retention in soils amended with compost versus mineral fertilizers. Soil Biol. Biochem. 156, 108227 (2021).

    Google Scholar 

  40. Chen, J. et al. Microbial C:N:P stoichiometry and turnover depend on nutrients availability in soil: A 14C, 15N and 33P triple labelling study. Soil Biol. Biochem. 131, 206–216 (2019).

    Google Scholar 

  41. Fang, Y. Y. et al. Nutrient stoichiometry and labile carbon content of organic amendments control microbial biomass and carbon-use efficiency in a poorly structured sodic-subsoil. Biol. Fertil. Soils 56, 219–233 (2020).

    Google Scholar 

  42. Barcelos, J. P. Q., Mariano, E., Jones, D. L. & Rosolem, C. A. Topsoil and subsoil C and N turnover are affected by superficial lime and gypsum application in the short-term. Soil Biol. Biochem. 163, 108456 (2021).

    Google Scholar 

  43. Cui, H., He, C., Zheng, W. W., Jiang, Z. H. & Yang, J. P. Effects of nitrogen addition on rhizosphere priming: the role of stoichiometric imbalance. Sci. Total Environ. 914, 169731 (2024).

    Google Scholar 

  44. Silva-Sánchez, A., Soares, M. & Rousk, J. Testing the dependence of microbial growth and carbon use efficiency on nitrogen availability, pH, and organic matter quality. Soil Biol. Biochem. 134, 25–35 (2019).

    Google Scholar 

  45. Wang, Q. Q. et al. Soil pH and phosphorus availability regulate sulphur cycling in an 82-year-old fertilised grassland. Soil Biol. Biochem. 194, 109436 (2024).

    Google Scholar 

  46. Hu, J. X., Huang, C. D., Zhou, S. X. & Kuzyakov, Y. Nitrogen addition to soil affects microbial carbon use efficiency: meta-analysis of similarities and differences in 13C and 18O approaches. Glob. Change Biol. 28, 4977–4988 (2022).

    Google Scholar 

  47. Zhang, Q. F. et al. Effect of field warming on soil microbial carbon use efficiency—a meta-analysis. Soil Biol. Biochem. 197, 109531 (2024).

    Google Scholar 

  48. Lian, J. S., Li, G. H., Zhang, J. F. & Massart, S. Nitrogen fertilization affected microbial carbon use efficiency and microbial resource limitations via root exudates. Sci. Total Environ. 950, 174933 (2024).

    Google Scholar 

  49. Ma, Z. B. et al. Long-term green manuring increases soil carbon sequestration via decreasing qCO2 caused by lower microbial phosphorus limitation in a dry land field. Agric. Ecosyst. Environ. 374, 109142 (2024).

    Google Scholar 

  50. Hicks, L. C., Yuan, M. Y., Brangarí, A., Rousk, K. & Rousk, J. Increased above- and belowground plant input can both trigger microbial nitrogen mining in subarctic tundra soils. Ecosystems 25, 105–121 (2022).

    Google Scholar 

  51. Neurauter, M., Yuan, M., Hicks, L. C. & Rousk, J. Soil microbial resource limitation along a subarctic ecotone from birch forest to tundra heath. Soil Biol. Biochem. 177, 108919 (2023).

    Google Scholar 

  52. Su, Z. X. & Shangguan, Z. P. Nitrogen addition decreases the soil cumulative priming effect and favours soil net carbon gains in Robinia pseudoacacia plantation soil. Geoderma 433, 116444 (2023).

    Google Scholar 

  53. Mehnaz, K. R., Corneo, P. E., Keitel, C. & Dijkstra, F. A. Carbon and phosphorus addition effects on microbial carbon use efficiency, soil organic matter priming, gross nitrogen mineralization and nitrous oxide emission from soil. Soil Biol. Biochem. 134, 175–186 (2019).

    Google Scholar 

  54. Geyer, K. M., Dijkstra, P., Sinsabaugh, R. & Frey, S. D. Clarifying the interpretation of carbon use efficiency in soil through methods comparison. Soil Biol. Biochem. 128, 79–88 (2019).

    Google Scholar 

  55. Ziegler, S. E. & Billings, S. A. Soil nitrogen status as a regulator of carbon substrate flows through microbial communities with elevated CO2. J. Geophys. Res. Biogeosciences 116, G01011 (2011).

    Google Scholar 

  56. Spohn, M. Element cycling as driven by stoichiometric homeostasis of soil microorganisms. Basic Appl. Ecol. 17, 471–478 (2016).

    Google Scholar 

  57. Poeplau, C. et al. Increased microbial anabolism contributes to soil carbon sequestration by mineral fertilization in temperate grasslands. Soil Biol. Biochem. 130, 167–176 (2019).

    Google Scholar 

  58. Bond-Lamberty, B., Bailey, V. L., Chen, M., Gough, C. M. & Vargas, R. Globally rising soil heterotrophic respiration over recent decades. Nature 560, 80–83 (2018).

    Google Scholar 

  59. Liu, W. X., Zhang, Z. & Wan, S. Q. Predominant role of water in regulating soil and microbial respiration and their responses to climate change in a semiarid grassland. Glob. Change Biol. 15, 184–195 (2009).

    Google Scholar 

  60. Choi, R. T., Reed, S. C. & Tucker, C. L. Multiple resource limitation of dryland soil microbial carbon cycling on the Colorado Plateau. Ecology 103, e3671 (2022).

    Google Scholar 

  61. Morris, K. A., Richter, A., Migliavacca, M. & Schrumpf, M. Growth of soil microbes is not limited by the availability of nitrogen and phosphorus in a Mediterranean oak-savanna. Soil Biol. Biochem. 169, 108680 (2022).

    Google Scholar 

  62. Li, J. W., Wang, G. S., Allison, S. D., Mayes, M. A. & Luo, Y. Q. Soil carbon sensitivity to temperature and carbon use efficiency compared across microbial-ecosystem models of varying complexity. Biogeochemistry 119, 67–84 (2014).

    Google Scholar 

  63. Manning, D. W., Rosemond, A. D., Gulis, V., Benstead, J. P. & Kominoski, J. S. Nutrients and temperature additively increase stream microbial respiration. Glob. Change Biol. 24, e233–e247 (2018).

    Google Scholar 

  64. Potapov, P. et al. Global maps of cropland extent and change show accelerated cropland expansion in the twenty-first century. Nat. Food 3, 19–28 (2022).

    Google Scholar 

  65. Pittelkow, C. M. et al. Productivity limits and potentials of the principles of conservation agriculture. Nature 517, 365–368 (2015).

    Google Scholar 

  66. Xu, P. et al. Fertilizer management for global ammonia emission reduction. Nature 626, 792–798 (2024).

    Google Scholar 

  67. Ren, C., He, L. & Rosa, L. Integrated irrigation and nitrogen optimization is a resource-efficient adaptation strategy for US maize and soybean production. Nat. Food 6, 389–400 (2025).

    Google Scholar 

  68. Harpole, W. S. et al. Addition of multiple limiting resources reduces grassland diversity. Nature 537, 93–96 (2016).

    Google Scholar 

  69. Cotrufo, M. F. & Lavallee, J. M. Soil organic matter formation, persistence, and functioning: a synthesis of current understanding to inform its conservation and regeneration. Adv. Agron. 172, 1–66 (2022).

    Google Scholar 

  70. Hedges, L. V., Gurevitch, J. & Curtis, P. S. The meta-analysis of response ratios in experimental ecology. Ecology 80, 1150–1156 (1999).

    Google Scholar 

  71. Fryda, T. et al. h2o: R interface for the ‘H2O’ scalable machine learning platform. R package version 3.44.0.3 https://CRAN.R-project.org/package=h2o (2024).

  72. Ziehn, T. et al. CSIRO ACCESS-ESM1.5 model output prepared for CMIP6 ScenarioMIP ssp585. Version 20241220. Earth System Grid Federation https://doi.org/10.22033/ESGF/CMIP6.4333 (2019).

  73. FAO & IIASA. Global agro-ecological zoning version 5 (GAEZ v5) model documentation https://github.com/un-fao/gaezv5/wiki (2025).

  74. R Development Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing https://www.R-project.org (2025).

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Acknowledgements

The authors thank the Subject editor and three anonymous reviewers for their insightful comments and suggestions. We sincerely thank all the scientists whose data were included in this meta-analysis. This study was financially supported by the National Natural Science Foundation of China (32301426 and 32571907), the China Postdoctoral Science Foundation (2022M720252 and 2024T170025).

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  1. These authors contributed equally: Ying Chen, Yawen Lu.

Authors and Affiliations

  1. Zhejiang Tiantong Forest Ecosystem National Observation and Research Station, Institute of Eco-Chongming, Zhejiang Zhoushan Island Ecosystem Observation and Research Station, School of Ecological and Environmental Sciences, East China Normal University, Shanghai, China

    Ying Chen, Siyuan Gao & Huiying Liu

  2. College of Chemistry and Life Science, Suzhou University of Science and Technology, Suzhou, China

    Yawen Lu

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  1. Ying Chen
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Contributions

Y.C. and Y.L. conceived the idea; Y.C. and Y.L. collected the data with the help from S.G.; Y.C., Y.L., and H.L. analyzed the data; Y.C. and Y.L. wrote the manuscript with input from all authors.

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Correspondence to
Ying Chen.

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Communications Earth and Environment thanks Marcio F. A. Leite and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Primary Handling Editors: Yi Jiao, Somaparna Ghosh A peer review file is available.

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Chen, Y., Lu, Y., Gao, S. et al. Minor effects of nutrient additions on soil microbial carbon use efficiency.
Commun Earth Environ (2025). https://doi.org/10.1038/s43247-025-03096-1

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