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Microbial controls over soil priming effects under chronic nitrogen and phosphorus additions in subtropical forests

The ISME Journal volume 17, pages 2160–2168 (2023)Cite this article

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Abstract

The soil priming effect (PE), defined as the modification of soil organic matter decomposition by labile carbon (C) inputs, is known to influence C storage in terrestrial ecosystems. However, how chronic nutrient addition, particularly in leguminous and non-leguminous forests, will affect PE through interaction with nutrient (e.g., nitrogen and phosphorus) availability is still unclear. Therefore, we collected soils from leguminous and non-leguminous subtropical plantations across a suite of historical nutrient addition regimes. We added 13C-labeled glucose to investigate how background soil nutrient conditions and microbial communities affect priming and its potential microbial mechanisms. Glucose addition increased soil organic matter decomposition and prompted positive priming in all soils, regardless of dominant overstory tree species or fertilizer treatment. In non-leguminous soil, only combined nitrogen and phosphorus addition led to a higher positive priming than the control. Conversely, soils beneath N-fixing leguminous plants responded positively to P addition alone, as well as to joint NP addition compared to control. Using DNA stable-isotope probing, high-throughput quantitative PCR, enzyme assays and microbial C substrate utilization, we found that positive PE was associated with increased microbial C utilization, accompanied by an increase in microbial community activity, nutrient-related gene abundance, and enzyme activities. Our findings suggest that the balance between soil available N and P effects on the PE,  was dependent on rhizosphere microbial community composition. Furthermore, these findings highlight the roles of the interaction between plants and their symbiotic microbial communities in affecting soil priming and improve our understanding of the potential microbial pathways underlying soil PEs.

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Fig. 1: SOM-derived CO2 and priming effects in different treatments.
Fig. 2: Principal co-ordinates analysis (PCoA) of the response ratio (RR) of bacterial and fungal communities among treatments (LP = leguminous plant, NLP = non-leguminous plant, CK = no nitrogen or phosphorus addition, N = nitrogen addition, P = phosphorus addition, and NP = nitrogen and phosphorus addition).
Fig. 3: Correlation between priming effect, soil and microbial properties.
Fig. 4: Conceptual diagram depicting factors and mechanisms underlying the soil priming effect.

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Data availability

The sequencing raw data are deposited in the NCBI Short Read Archive database under accession numbers PRJNA884088 and PRJNA884089.

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Acknowledgements

This study was supported by the National Natural Science Foundation of China (42207262 and 42177289) and the China Postdoctoral Science Foundation (2021M703135). JS was supported by Spanish Government grant. JP and JS were supported by the Spanish Government grants PID2020-115770RB-I00 and TED2021-132627B-I00 funded by MCIN, AEI/10.13039/501100011033 and the European NextGenerationEU/PRTR, the Fundación Ramón Areces grant CIVP20A6621, and the Catalan government project SGR2021-01333.

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Authors and Affiliations

  1. Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems & CAS Engineering Laboratory for Vegetation Ecosystem Restoration on Islands and Coastal Zones, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, 510650, China

    Jian Li, Zhan-Feng Liu, Wei Zhang, Jing Zhang & Donghai Wu

  2. Key Laboratory of Urban Environment and Health, Ningbo Observation and Research Station, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen, 361021, China

    Jian Li, Ming-Kang Jin & Yong-Guan Zhu

  3. Zhejiang Key Laboratory of Urban Environmental Processes and Pollution Control, CAS Haixi Industrial Technology Innovation Center in Beilun, Ningbo, 315830, China

    Jian Li, Ming-Kang Jin & Yong-Guan Zhu

  4. Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Guangzhou, 510650, China

    Zhan-Feng Liu, Jing Zhang & Donghai Wu

  5. School of Biological Sciences, University of Western Australia, Perth, WA, WA6009, Australia

    Hans Lambers

  6. Department of Plant Nutrition, College of Resources and Environmental Sciences; National Academy of Agriculture Green Development; Key Laboratory of Plan-Soil Interactions, Ministry of Education, China Agricultural University, Beijing, 100193, China

    Hans Lambers

  7. Department of Biological Sciences, Tennessee State University, Nashville, TN, TN37209, USA

    Dafeng Hui

  8. Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, 110016, China

    Chao Liang

  9. CSIC, Global Ecology Unit, CREAF-CSIC-UAB, Bellaterra, 08193, Barcelona, Catalonia, Spain

    Jordi Sardans & Josep Peñuelas

  10. CREAF, Cerdanyola del Vallès, 08193, Barcelona, Catalonia, Spain

    Jordi Sardans & Josep Peñuelas

  11. Department of Ecology & Evolutionary Biology, Cornell University, Ithaca, NY, 14850, USA

    Daniel F. Petticord & David W. Frey

  12. State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, 100085, China

    Yong-Guan Zhu

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  1. Jian Li
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Contributions

ZFL, YGZ, and JL conceptualized the study and led the writing of the manuscript. JL, MKJ, WZ, and JZ performed the study and analyzed the data. HL, DFH, CL, DHW, JS, JP, DFP, and DWF contributed substantially to manuscript revisions. All authors reviewed and edited the manuscript.

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Correspondence to Zhan-Feng Liu or Yong-Guan Zhu.

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Li, J., Liu, ZF., Jin, MK. et al. Microbial controls over soil priming effects under chronic nitrogen and phosphorus additions in subtropical forests. ISME J 17, 2160–2168 (2023). https://doi.org/10.1038/s41396-023-01523-9

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