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Plant–microbe interactions underpin contrasting enzymatic responses to wetland drainage

Nature Climate Change volume 14, pages 1078–1086 (2024)Cite this article

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Abstract

The carbon storage of wetlands is related to inhibited enzyme activity (particularly phenol oxidase) under oxygen-deprived conditions. However, phenol oxidase response to field drainage is highly uncertain, constraining our ability to predict wetland carbon–climate feedbacks. Here, using literature data, laboratory simulations and a pair-wise survey of 30 diverse wetlands experiencing long-term (15–55 years) drainage across China, we show that while short-term drainage generally leads to increased phenol oxidative activity, its response to long-term drainage diverges in Sphagnum versus non-Sphagnum wetlands. In non-Sphagnum wetlands, long-term drainage is linked to increased plant secondary metabolites and decreased phenol oxidase-producing microbes, while in Sphagnum wetlands, drainage is linked to replacement of antimicrobial Sphagnum by vascular plants and increased phenol oxidative activity with cascading effects on hydrolytic enzymes. Our findings highlight that trait-based plant dynamics are pivotal to decipher wetland carbon dynamics and feedback to climate change under shifting hydrological regimes.

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Fig. 1: Sampling sites and experimental design.
Fig. 2: Response of phenol oxidative activity to wetland drainage.
Fig. 3: Soil microbes related to phenol oxidase production.
Fig. 4: Plant metabolites and their links with phenol oxidase-producing microbes.
Fig. 5: Pathways regulating enzymatic response to long-term drainage.

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Data availability

All data supporting the findings are available via Figshare at https://doi.org/10.6084/m9.figshare.26038639 (ref. 64).

Code availability

Data analysis was carried out using R v.4.1.3, which is publicly available at https://www.r-project.org. The supporting code is available via Figshare at https://doi.org/10.6084/m9.figshare.25604109 (ref. 65).

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Acknowledgements

This study was supported financially by the National Natural Science Foundation of China (grant nos. 42025303, 31988102, 42230501). We thank Plant Science Facility of the Institute of Botany, Chinese Academy of Sciences for their help in sample analysis. We thank Natural Reserves in Dajiuhu, Jinchuan, Niangningshan, Dapingjing, Xundian, Wuyiling, Qizimei, Erxianyan, Aershan, Mohe, Panguhe, Honghe, Naolihe, Qixinghe, Xingkaihu, Zoige, Ruoergai, Caohai, Eeerguna, Shaliuhe, Luanhaizi, Jiuquan, Dongtinghu and Poyanghu for support in soil sampling. We also acknowledge data support from the National Earth System Science Data Center, National Science & Technology Infrastructure of China (http://www.geodata.cn/).

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Authors and Affiliations

  1. State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, Beijing, China

    Yunpeng Zhao, Chengzhu Liu, Enze Kang, Xingqi Li & Xiaojuan Feng

  2. China National Botanical Garden, Beijing, China

    Yunpeng Zhao, Chengzhu Liu, Enze Kang, Xingqi Li & Xiaojuan Feng

  3. University of Chinese Academy of Sciences, Beijing, China

    Yunpeng Zhao, Chengzhu Liu, Enze Kang, Xingqi Li, Ye Deng & Xiaojuan Feng

  4. CAS Key Laboratory for Environmental Biotechnology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, China

    Ye Deng

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Contributions

X.F. and Y.Z. designed this study. Y.Z. conducted soil sampling and analytical measurements with help from C.L. and X.L. Y.Z. and X.F. analysed the data with help from E.K. and Y.D. Y.Z. and X.F. wrote the paper with input from all other authors.

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Correspondence to Xiaojuan Feng.

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Nature Climate Change thanks Hojeong Kang, Yuan Wen and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 β-Glucosidase activity.

a, Response of β-glucosidase activity to long-term drainage (0‒20 cm). b, Spearman’s correlation between phenol oxidative activity and β-glucosidase activity. The violin plots show the distribution of data. The dots mark the value of samples. The solid lines in violin plots mark the median of each dataset. The signs of plus (+), minus (–) and cross (×) represent significant increase, decrease and no change after drainage at the level of P = 0.05 (t-test), respectively. Error bars in bar graph represent standard error of mean (n = 4). Solid lines in correlation analysis represent the linear regressions (n = 240; P < 0.05). The shaded areas represent the 95% confidence intervals.

Extended Data Fig. 2 The abundance of β-glucosidase-producing functional genes.

a, Spearman’s correlations of the abundance of β-glucosidase-producing functional genes with β-glucosidase activity in Sphagnum (n = 84) and non-Sphagnum wetlands (n = 96), respectively. b, Site-weighted response ratio (RR++) of the abundance of β-glucosidase-producing functional genes in the drained relative to waterlogged soils in Sphagnum (n = 84) and non-Sphagnum wetlands (n = 96), respectively. Solid lines in a indicate linear regressions (P < 0.05). The shaded areas represent the 95% confidence intervals. Error bars in bar graph represent 95% confidence interval. If the 95% CI did not overlap with zero, the response was considered to be significant.

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Supplementary Text 1–5, Figs. 1–15 and Tables 1–3.

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Zhao, Y., Liu, C., Kang, E. et al. Plant–microbe interactions underpin contrasting enzymatic responses to wetland drainage. Nat. Clim. Chang. 14, 1078–1086 (2024). https://doi.org/10.1038/s41558-024-02101-3

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