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Agricultural subsoil microbiomes and functions exhibit lower resistance to global change than topsoils in Chinese agroecosystems

Nature Food volume 6, pages 375–388 (2025)Cite this article

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Abstract

Soils play a critical role in supporting agricultural production. Subsoils, below 20 cm, underpin fundamental agroecosystem sustainability traits including soil carbon storage, climate regulation and water provision. However, little is known about the ecological stability of subsoils in response to global change. Here we conducted a microcosm experiment to determine whether subsoils were more sensitive to global changes across 40 agricultural ecosystems in China, in combination with a multiple global change factor experiment and an in situ field study. We found that subsoils exhibited greater fluctuation in species diversity, community composition, and complexity of microbial networks and ecosystem functions than topsoils, indicating lower resistance to global changes. Soil biodiversity was a major driver of ecosystem resistance, surpassing climate and soil parameters. A reciprocal microorganism transplant experiment showed that microorganisms isolated from the topsoil are more resistant to global changes than those from subsoil. Our study emphasizes that subsoil ecosystems are sensitive to global changes, underscoring the importance of including subsoils in predictions of agricultural sustainability and crop productivity under changing environmental conditions.

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Fig. 1: A conceptual diagram of the ecological resistance of topsoil and subsoil.
Fig. 2: The resistance of soil organisms and functions to global change in agroecosystems.
Fig. 3: The community resistance and temporal resistance of topsoils and subsoils.
Fig. 4: Links between soil biodiversity and resistance to global change in agroecosystems.
Fig. 5: The functional resistance of topsoils and subsoils derived from the microorganism reciprocal transplant experiment.
Fig. 6: The construction of integrated co-occurrence networks and the relationships between soil biodiversity, negative associations, network complexity, resistant phylotypes and resistance to global change.
Fig. 7: Conceptual model linking soil biodiversity to ecological resistance.

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Data availability

The raw sequence data reported in this paper have been deposited in the Beijing Institute of Genomics (BIG) Data Center, Chinese Academy of Sciences, under BioProject accession numbers PRJCA019230 and PRJCA019239 and are publicly accessible at http://bigd.big.ac.cn/gsa. The microbial abundance table is available via GitHub at https://github.com/Pong2021/soil-resistance.git. The taxonomy information of 16S rRNA and 18S rRNA is available in the Silva database (https://www.arb-silva.de/) and the Protist Ribosomal Reference database (https://pr2-database.org/). Source data are provided with this paper.

Code availability

The R script is available via GitHub at https://github.com/Pong2021/soil-resistance.git.

References

  1. Crowther, T. W. et al. The global soil community and its influence on biogeochemistry. Science 365, eaav0550 (2019).

    Article  CAS  PubMed  Google Scholar 

  2. 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).

    Article  CAS  Google Scholar 

  3. Soong, J. L. et al. Five years of whole-soil warming led to loss of subsoil carbon stocks and increased CO2 efflux. Sci. Adv. 7, eabd1343 (2021).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  4. Delgado-Baquerizo, M. et al. Multiple elements of soil biodiversity drive ecosystem functions across biomes. Nat. Ecol. Evol. 4, 210–220 (2020).

    Article  PubMed  Google Scholar 

  5. Silver, W. L., Perez, T., Mayer, A. & Jones, A. R. The role of soil in the contribution of food and feed. Philos. Trans. R. Soc. B 376, 20200181 (2021).

    Article  CAS  Google Scholar 

  6. Maxwell, S. L., Fuller, R. A., Brooks, T. M. & Watson, J. E. J. N. N. Biodiversity: the ravages of guns, nets and bulldozers. Nature 536, 143–145 (2016).

    Article  ADS  CAS  PubMed  Google Scholar 

  7. Zhou, Z., Wang, C. & Luo, Y. Meta-analysis of the impacts of global change factors on soil microbial diversity and functionality. Nat. Commun. 11, 3072 (2020).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  8. Tian, J. et al. Microbial metabolic response to winter warming stabilizes soil carbon. Glob. Change Biol. 27, 2011–2028 (2021).

    Article  ADS  CAS  Google Scholar 

  9. Feng, Q., An, C., Chen, Z. & Wang, Z. Can deep tillage enhance carbon sequestration in soils? A meta-analysis towards GHG mitigation and sustainable agricultural management. Renew. Sustain. Energy Rev. 133, 110293 (2020).

    Article  CAS  Google Scholar 

  10. Harrison, R. B., Footen, P. W. & Strahm, B. D. Deep soil horizons: contribution and importance to soil carbon pools and in assessing whole-ecosystem response to management and global change. For. Sci. 57, 67–76 (2011).

    Google Scholar 

  11. Schlaepfer, D. R. et al. Climate change reduces extent of temperate drylands and intensifies drought in deep soils. Nat. Commun. 8, 14196 (2017).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  12. Soong, J. L., Phillips, C. L., Ledna, C., Koven, C. D. & Torn, M. S. CMIP5 models predict rapid and deep soil warming over the 21st century. J. Geophys. Res. Biogeosci. 125, e2019JG005266 (2020).

    Article  ADS  Google Scholar 

  13. Siebers, N. et al. Subsoils—a sink for excess fertilizer P but a minor contribution to P plant nutrition: evidence from long-term fertilization trials. Environ. Sci. Eur. 33, 60 (2021).

    Article  CAS  Google Scholar 

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

    Article  ADS  Google Scholar 

  15. Ives, A. R. & Carpenter, S. R. Stability and diversity of ecosystems. Science 317, 58–62 (2007).

    Article  ADS  CAS  PubMed  Google Scholar 

  16. Pimm, S. L. The complexity and stability of ecosystems. Nature 307, 321–326 (1984).

    Article  ADS  Google Scholar 

  17. Pennekamp, F. et al. Biodiversity increases and decreases ecosystem stability. Nature 563, 109–112 (2018).

    Article  ADS  CAS  PubMed  Google Scholar 

  18. Isbell, F. et al. Biodiversity increases the resistance of ecosystem productivity to climate extremes. Nature 526, 574–577 (2015).

    Article  ADS  CAS  PubMed  Google Scholar 

  19. Wang, Z. et al. Environmental stability impacts the differential sensitivity of marine microbiomes to increases in temperature and acidity. ISME J. 15, 19–28 (2021).

    Article  CAS  PubMed  Google Scholar 

  20. de Bello, F. et al. Functional trait effects on ecosystem stability: assembling the jigsaw puzzle. Trends Ecol. Evol. 36, 822–836 (2021).

    Article  PubMed  Google Scholar 

  21. Philippot, L., Griffiths, B. S. & Langenheder, S. Microbial community resilience across ecosystems and multiple disturbances. Microbiol. Mol. Biol. Rev. 85, e00026-20 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  ADS  Google Scholar 

  23. MacDougall, A. S., McCann, K. S., Gellner, G. & Turkington, R. Diversity loss with persistent human disturbance increases vulnerability to ecosystem collapse. Nature 494, 86–89 (2013).

    Article  ADS  CAS  PubMed  Google Scholar 

  24. Galand, P. E., Pereira, O., Hochart, C., Auguet, J. C. & Debroas, D. A strong link between marine microbial community composition and function challenges the idea of functional redundancy. ISME J. 12, 2470–2478 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Allison, S. D. & Martiny, J. B. H. Resistance, resilience, and redundancy in microbial communities. Proc. Natl Acad. Sci. USA 105, 11512–11519 (2008).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  26. Louca, S. et al. Function and functional redundancy in microbial systems. Nat. Ecol. Evol. 2, 936–943 (2018).

    Article  PubMed  Google Scholar 

  27. Sáez-Sandino, T. et al. The soil microbiome governs the response of microbial respiration to warming across the globe. Nat. Clim. Change 13, 1382–1387 (2023).

    Article  ADS  Google Scholar 

  28. Delgado-Baquerizo, M. et al. Soil microbial communities drive the resistance of ecosystem multifunctionality to global change in drylands across the globe. Ecol. Lett. 20, 1295–1305 (2017).

    Article  PubMed  Google Scholar 

  29. Ratzke, C., Barrere, J. & Gore, J. Strength of species interactions determines biodiversity and stability in microbial communities. Nat. Ecol. Evol. 4, 376–383 (2020).

    Article  PubMed  Google Scholar 

  30. Pastore, A. I., Barabás, G., Bimler, M. D., Mayfield, M. M. & Miller, T. E. The evolution of niche overlap and competitive differences. Nat. Ecol. Evol. 5, 330–337 (2021).

    Article  PubMed  Google Scholar 

  31. Hibbing, M. E., Fuqua, C., Parsek, M. R. & Peterson, S. B. Bacterial competition: surviving and thriving in the microbial jungle. Nat. Rev. Microbiol. 8, 15–25 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Pontrelli, S. et al. Metabolic cross-feeding structures the assembly of polysaccharide degrading communities. Sci. Adv. 8, eabk3076 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Fritts, R. K. et al. Enhanced nutrient uptake is sufficient to drive emergent cross-feeding between bacteria in a synthetic community. ISME J. https://doi.org/10.1038/s41396-020-00737-5 (2020).

  34. Coyte, K. Z., Schluter, J. & Foster, K. R. The ecology of the microbiome: networks, competition, and stability. Science 350, 663–666 (2015).

    Article  ADS  CAS  PubMed  Google Scholar 

  35. Gorter, F. A., Manhart, M. & Ackermann, M. Understanding the evolution of interspecies interactions in microbial communities. Philos. Trans. R. Soc. B 375, 20190256 (2020).

    Article  CAS  Google Scholar 

  36. Urgoiti, J. et al. No complementarity no gain—net diversity effects on tree productivity occur once complementarity emerges during early stand development. Ecol. Lett. https://doi.org/10.1111/ele.13959 (2022).

  37. Michalet, R., Delerue, F., Liancourt, P. & Pugnaire, F. I. Are complementarity effects of species richness on productivity the strongest in species-rich communities? J. Ecol. 109, 2038–2046 (2021).

    Article  Google Scholar 

  38. Hartmann, M. & Six, J. Soil structure and microbiome functions in agroecosystems. Nat. Rev. Earth Environ. 4, 4–18 (2022).

    Article  ADS  Google Scholar 

  39. Wilpiszeski, R. L. et al. Soil aggregate microbial communities: towards understanding microbiome interactions at biologically relevant scales. Appl. Environ. Microbiol. 85, e00324–00319 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Hassani, M. A., Durán, P. & Hacquard, S. Microbial interactions within the plant holobiont. Microbiome 6, 58 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  41. Berg, G. & Smalla, K. Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol. Ecol. 68, 1–13 (2009).

    Article  CAS  PubMed  Google Scholar 

  42. Tang, B., Man, J., Lehmann, A. & Rillig, M. C. Arbuscular mycorrhizal fungi benefit plants in response to major global change factors. Ecol. Lett. 26, 2087–2097 (2023).

    Article  PubMed  Google Scholar 

  43. Salome, C., Nunan, N., Pouteau, V., Lerch, T. Z. & Chenu, C. Carbon dynamics in topsoil and in subsoil may be controlled by different regulatory mechanisms. Glob. Change Biol. 16, 416–426 (2010).

    Article  ADS  Google Scholar 

  44. Rillig, M. C. et al. The role of multiple global change factors in driving soil functions and microbial biodiversity. Science 366, 886–890 (2019).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  45. Wagg, C., Dudenhöffer, J.-H., Widmer, F. & van der Heijden, M. G. A. Linking diversity, synchrony and stability in soil microbial communities. Funct. Ecol. 32, 1280–1292 (2018).

    Article  Google Scholar 

  46. Wagg, C. et al. Diversity and asynchrony in soil microbial communities stabilizes ecosystem functioning. eLife 10, e62813 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Zhang, J. et al. Harnessing the plant microbiome to promote the growth of agricultural crops. Microbiol. Res. 245, 126690 (2021).

    Article  ADS  CAS  PubMed  Google Scholar 

  48. Doak, D. F. et al. The statistical inevitability of stability–diversity relationships in community ecology. Am. Nat. 151, 264–276 (1998).

    Article  CAS  PubMed  Google Scholar 

  49. IPCC Climate Change 2014: Synthesis Report (eds Core Writing Team, Pachauri, R. K. & Meyer L. A.) (IPCC, 2014).

  50. Ryser, R., Hirt, M. R., Häussler, J., Gravel, D. & Brose, U. Landscape heterogeneity buffers biodiversity of simulated meta-food-webs under global change through rescue and drainage effects. Nat. Commun. 12, 4716 (2021).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  51. Stoeck, T. et al. Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Mol. Ecol. 19, 21–31 (2010).

    Article  CAS  PubMed  Google Scholar 

  52. Oliverio, A. M. et al. The global-scale distributions of soil protists and their contributions to belowground systems. Sci. Adv. 6, eaax8787 (2020).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  53. Garland, G. et al. A closer look at the functions behind ecosystem multifunctionality: a review. J. Ecol. https://doi.org/10.1111/1365-2745.13511 (2020).

  54. Orwin, K. H. & Wardle, D. A. New indices for quantifying the resistance and resilience of soil biota to exogenous disturbances. Soil Biol. Biochem. 36, 1907–1912 (2004).

    Article  CAS  Google Scholar 

  55. Baert, J. M., De Laender, F., Sabbe, K. & Janssen, C. R. Biodiversity increases functional and compositional resistance, but decreases resilience in phytoplankton communities. Ecology 97, 3433–3440 (2016).

    Article  PubMed  Google Scholar 

  56. Jiao, S., Lu, Y. & Wei, G. Soil multitrophic network complexity enhances the link between biodiversity and multifunctionality in agricultural systems. Glob. Change Biol. 28, 140–153 (2022).

    Article  CAS  Google Scholar 

  57. Carlson, M. L., Flagstad, L. A., Gillet, F. & Mitchell, E. A. D. Community development along a proglacial chronosequence: are above-ground and below-ground community structure controlled more by biotic than abiotic factors? J. Ecol. 98, 1084–1095 (2010).

    Article  Google Scholar 

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Acknowledgements

This work was supported by the National Science Foundation for Excellent Young Scholars of China (grant number: 42122050; S.J.), National Science Foundation of China (grant number: 42077222; S.J.), National Key Research and Development Program of China (grant number: 2021YFD1900500; S.J.), the Fundamental Research Funds for the Central Universities and Joint Fund of the National Natural Science Foundation of China (grant number: U21A2029; G.W.) and US National Science Foundation (grant DBI-1759892; J.M.T.).

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Authors and Affiliations

  1. State Key Laboratory for Crop Stress Resistance and High-Efficiency Production, Shaanxi Key Laboratory of Agricultural and Environmental Microbiology, College of Life Sciences, Northwest A&F University, Yangling, People’s Republic of China

    Ziheng Peng, Yu Liu, Xiaomeng Li, Haibo Pan, Yining An, Hang Gao, Jiejun Qi, Jiamin Gao, Gehong Wei & Shuo Jiao

  2. Plant–Soil Interactions Group, Agroscope, Zurich, Switzerland

    Marcel G. A. van der Heijden

  3. Department of Plant and Microbial Biology, University of Zurich, Zurich, Switzerland

    Marcel G. A. van der Heijden

  4. Interdisciplinary Research Center for Soil Microbial Ecology and Land Sustainable Productivity in Dry Areas, Northwest A&F University, Yangling, People’s Republic of China

    Xun Qian & James M. Tiedje

  5. Center for Microbial Ecology, Michigan State University, East Lansing, MI, USA

    James M. Tiedje

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Contributions

All authors contributed intellectual input and assistance to this study and the paper preparation. Z.P. conducted the survey collection, analysed the data and wrote the original draft. S.J. and G.W. conceived and designed the experiments. Y.L., H.P., X.L., Y.A., H.G., J.Q. and J.G. contributed to survey collection and sample processing. Z.P. and Y.L. contributed to the multifactor experiments, temporal variability experiment and microorganism reciprocal transplant experiment. S.J., M.v.d.H., X.Q., J.M.T. and G.W. reviewed and edited the draft.

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Correspondence to Shuo Jiao.

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Nature Food thanks Cameron Wagg, Gaowen Yang and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Peng, Z., van der Heijden, M.G.A., Liu, Y. et al. Agricultural subsoil microbiomes and functions exhibit lower resistance to global change than topsoils in Chinese agroecosystems. Nat Food 6, 375–388 (2025). https://doi.org/10.1038/s43016-024-01106-7

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