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Land use conversion increases network complexity and stability of soil microbial communities in a temperate grassland

The ISME Journal volume 17, pages 2210–2220 (2023)Cite this article

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Abstract

Soils harbor highly diverse microbial communities that are critical to soil health, but agriculture has caused extensive land use conversion resulting in negative effects on critical ecosystem processes. However, the responses and adaptations of microbial communities to land use conversion have not yet been understood. Here, we examined the effects of land conversion for long-term crop use on the network complexity and stability of soil microbial communities over 19 months. Despite reduced microbial biodiversity in comparison with native tallgrass prairie, conventionally tilled (CT) cropland significantly increased network complexity such as connectivity, connectance, average clustering coefficient, relative modularity, and the number of species acting at network hubs and connectors as well as resulted in greater temporal variation of complexity indices. Molecular ecological networks under CT cropland became significantly more robust and less vulnerable, overall increasing network stability. The relationship between network complexity and stability was also substantially strengthened due to land use conversion. Lastly, CT cropland decreased the number of relationships between network structure and environmental properties instead being strongly correlated to management disturbances. These results indicate that agricultural disturbance generally increases the complexity and stability of species “interactions”, possibly as a trade-off for biodiversity loss to support ecosystem function when faced with frequent agricultural disturbance.

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Fig. 1: Temporal dynamics of soil microbial networks.
Fig. 2: The relative contributions of different ecological processes to the observed network links.
Fig. 3: Temporal dynamics of network stability.
Fig. 4: Associations between network indices, environmental properties, and management.

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Code availability

16S rRNA gene sequences were deposited to the Sequence Read Archive (SRA) under the project accession number PRJNA954023. The R scripts and Python 3 scripts were adapted from the publicly available code on GitHub at https://github.com/Mengting-Maggie-Yuan/warming-network-complexity-stability with the identifier https://doi.org/10.5281/zenodo.4383469.

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Acknowledgements

This study was funded by the USDA National Institute of Food and Agriculture (NIFA) award 2016-68002-24967. It was also supported in part by the USDA-ARS Office of National Programs (Project number: 3070-21610-003-00D) and USDA-LTAR (Long-Term Agroecosystem Research) Network. USDA is an equal opportunity provider and employer. Computing for this project was performed at the OU Supercomputing Center for Education & Research (OSCER) at the University of Oklahoma (OU).

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Author notes

  1. Carolyn R. Cornell

    Present address: Department of Civil and Environmental Engineering, Rice University, Houston, TX, USA

  2. These authors contributed equally: Carolyn R. Cornell, Ya Zhang.

Authors and Affiliations

  1. Department of Microbiology and Plant Biology, University of Oklahoma, Norman, OK, USA

    Carolyn R. Cornell, Ya Zhang, Daliang Ning, Naijia Xiao, Xiangming Xiao & Jizhong Zhou

  2. Institute for Environmental Genomics, University of Oklahoma, Norman, OK, USA

    Carolyn R. Cornell, Ya Zhang, Daliang Ning, Naijia Xiao & Jizhong Zhou

  3. USDA, Agricultural Research Service, Oklahoma and Central Plains Agricultural Research Center, El Reno, OK, USA

    Pradeep Wagle

  4. School of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, Ok, USA

    Jizhong Zhou

  5. School of Computer Science, University of Oklahoma, Norman, OK, USA

    Jizhong Zhou

  6. Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, USA

    Jizhong Zhou

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Contributions

JZ and XX designed research; CRC collected soil samples; PW provided site data; CRC and YZ performed research; CRC, YZ, DN, and NX analyzed data; CRC and YZ wrote paper; DN, NX, PW, JZ, and XX reviewed and edited paper.

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Correspondence to Jizhong Zhou.

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Cornell, C.R., Zhang, Y., Ning, D. et al. Land use conversion increases network complexity and stability of soil microbial communities in a temperate grassland. ISME J 17, 2210–2220 (2023). https://doi.org/10.1038/s41396-023-01521-x

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