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Microbial keystone taxa drive succession of plant residue chemistry

The ISME Journal volume 17, pages 748–757 (2023)Cite this article

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Abstract

Managing above-ground plant carbon inputs can pave the way toward carbon neutrality and mitigating climate change. Chemical complexity of plant residues largely controls carbon sequestration. There exist conflicting opinions on whether residue chemistry diverges or converges after long-term decomposition. Moreover, whether and how microbial communities regulate residue chemistry remains unclear. This study investigated the decomposition processes and residue composition dynamics of maize straw and wheat straw and related microbiomes over a period of 9 years in three climate zones. Residue chemistry exhibited a divergent-convergent trajectory during decomposition, that is, the residue composition diverged during the 0.5–3 year period under the combined effect of straw type and climate and then converged to an array of common compounds during the 3–9 year period. Chemical divergence during the first 2–3 years was primarily driven by the changes in extracellular enzyme activity influenced by keystone taxa-guided bacterial networks, and the keystone taxa belonged to Alphaproteobacteria, particularly Rhizobiales. After 9 years, microbial assimilation became dominant, leading to chemical convergence, and fungi, particularly Chaetomium, were the main contributors to microbial assimilation. Overall, this study demonstrated that keystone taxa regulate the divergent-convergent trajectory in residue chemistry.

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Fig. 1: Decomposition patterns of wheat and maize straw residues represented by mass remaining and O-alkyl/alkyl ratio.
Fig. 2: Principal coordinate analyses and divergence index based on Bray-Curtis distances.
Fig. 3: Extracellular enzyme activity and microbial necromass abundance in maize straw and wheat straw residues after decomposition for 0.5 year, 2 years, and 9 years.
Fig. 4: The co-occurrence networks of bacterial and fungal communities in straw residues during different periods of decomposition.
Fig. 5: The effects of abiotic and biotic factors on the divergence of residue chemical composition as estimated using the structural equation model.
Fig. 6: The importance of keystone taxa in extracellular enzyme activity.

Data availability

MiSeq sequencing data and metagenomic sequencing data have been deposited in the NCBI Sequence Read Archive under the SRA accessions of SRP312985 and SRP417783, respectively. All other data generated or analyzed during this study are included in this article and/or its supplementary information files.

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Acknowledgements

We gratefully thank Dr. Xudong Zhang’s lab for their assistance in amino sugar analysis. We appreciate the experiment management and sampling assistance from staffs in Hailun, Fengqiu and Yingtan Research Stations. This work is financially supported by the National Key R&D Program (2022YFD1900600), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA28030102), the Science Foundation of the Chinese Academy of Sciences (ISSASIP2211), National Natural Science Foundation of China (31930070), and the China Agriculture Research System of MOF and MARA (CARS-22, CARS-52).

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Authors and Affiliations

  1. State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, China

    Xiaoyue Wang, Yuji Jiang, Qing Bian, Yuting Liang, Yan Chen & Bo Sun

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

    Chao Liang

  3. Department of Chemistry and Biochemistry, Old Dominion University, 4541 Hampton Boulevard, Norfolk, VA, 23529, USA

    Jingdong Mao

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  1. Xiaoyue Wang
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Contributions

B.S designed the field experiment. X.W., J.M., Y.J., Q.B., and Y.L. for their assistance in soil sampling and responsible for performing the field experiments. X.W. contributed the data analysis. X.W, C.L., and B.S. wrote the manuscript. All authors discussed the results and commented on the manuscript.

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Correspondence to Chao Liang or Bo Sun.

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Wang, X., Liang, C., Mao, J. et al. Microbial keystone taxa drive succession of plant residue chemistry. ISME J 17, 748–757 (2023). https://doi.org/10.1038/s41396-023-01384-2

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