Earthworms and warming alter methane uptake and methane-cycling microbial community in meadow soil

Highlights

● Earthworms significantly reduced soil CH₄ uptake at both temperatures, and warming significantly promoted soil CH₄ uptake.

● Earthworms significantly altered methanotroph community, and warming significantly altered methanogen community, and their interaction had a significant influence on both methanogen and methanotroph communities.

● Soil properties exhibited a negative impact on CH₄ uptake, while the α-diversity of methanotrophs was associated with enhanced CH₄ uptake.

● Dissolved organic carbon (DOC) was identified as the most essential factor in forecasting soil CH₄ uptake.

Abstract

The function and service of biologically driven ecosystems are undergoing significant changes due to climate warming. Earthworms play a crucial role as soil engineer by modulating the effects of climate change on soil nutrient cycle through alterations to biotic and abiotic soil conditions. However, there is currently a scarcity of information regarding the impacts of earthworms and warming on soil CH₄ uptake and their associated microbial mechanisms. This study conducted a 61-day microcosm experiment to investigate the impact of warming (temperature rise from 14.2 °C to 17.2 °C) and the presence of earthworms (Eisenia fetida and Moniligaster japonicus) on soil CH₄ uptake. We employed gas chromatography and high-throughput sequencing to investigate the fluctuations in soil CH₄ uptake and the microbial communities involved in methane cycling. Compared to low temperature conditions (14.2 °C), we observed that warming significantly increased soil CH₄ uptake in all treatments (non-earthworm: 51.85%; Eisenia fetida: 50.88%; Moniligaster japonicus: 71.78%). Both Eisenia fetida and Moniligaster japonicus significantly reduced soil CH₄ uptake at two temperatures compared to the non-earthworm treatment. Nevertheless, no significant impacts were found on soil CH₄ uptake due to the interactions between earthworms and warming. The methanotroph communities exhibited notable variations among earthworm treatments, whereas the methanogenic communities displayed significant differences among temperature treatments. The interaction between earthworm and warming also resulted in noticeable variations in both methanogenic and methanotrophic communities. The FAPROTAX analysis revealed that earthworms and warming altered relative abundance of methanogens and methanotroph associated with CH₄ cycle functions. Soil properties exhibited a negative impact on CH₄ uptake, with DOC identified as the most crucial variable in predicting soil CH₄ uptake, while the α-diversity of methanotrophs was associated with enhanced CH₄ uptake. This study emphasized the crucial role of soil fauna in adjusting soil greenhouse gas emissions under the context of global warming.

Graphical abstract

Keywords

endogeic earthworms / epigeic earthworms / greenhouse gas emissions / Illumina sequencing / network analysis

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Author contributions

Yujuan Kang: Data curation, Writing–original draft. Haitao Wu: Supervision, writing–review and editing. Qiang Guan: Investigation. Zhongsheng Zhang: Investigation. Wenfeng Wang: Investigation.

Declaration of competing interest

The authors have disclosed that there are no known financial or personal ties that could have swayed the research presented in this paper, and they report no conflicts of interest.

Acknowledgements

This research received funding from the National Natural Science Foundation of China under Grant No. U20A2083, and from the Science and Technology Development Program of Jilin Province under Grant Nos. JL2022-12, 20210509037RQ, and 20230101348JC.

Electronic supplementary material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s42832-024-0255-1 and is accessible for authorized users.

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