Extreme summers impact cropland and grassland soil microbiomes

Abstract

Abstract The increasing frequency of extreme weather events highlights the need to understand how soil microbiomes respond to such disturbances. Here, metagenomics was used to investigate the effects of future climate scenarios (+0.6 °C warming and altered precipitation) on soil microbiomes during the summers of 2014–2019. Unexpectedly, Central Europe experienced extreme heatwaves and droughts during 2018–2019, causing significant impacts on the structure, assembly, and function of soil microbiomes. Specifically, the relative abundance of Actinobacteria (bacteria), Eurotiales (fungi), and Vilmaviridae (viruses) was significantly increased in both cropland and grassland. The contribution of homogeneous selection to bacterial community assembly increased significantly from 40.0% in normal summers to 51.9% in extreme summers. Moreover, genes associated with microbial antioxidant (Ni-SOD), cell wall biosynthesis (glmSMU, murABCDEF), heat shock proteins (GroES/GroEL, Hsp40), and sporulation (spoIID, spoVK) were identified as potential contributors to drought-enriched taxa, and their expressions were confirmed by metatranscriptomics in 2022. The impact of extreme summers was further evident in the taxonomic profiles of 721 recovered metagenome-assembled genomes (MAGs). Annotation of contigs and MAGs suggested that Actinobacteria may have a competitive advantage in extreme summers due to the biosynthesis of geosmin and 2-methylisoborneol. Future climate scenarios caused a similar pattern of changes in microbial communities as extreme summers, but to a much lesser extent. Soil microbiomes in grassland showed greater resilience to climate change than those in cropland. Overall, this study provides a comprehensive framework for understanding the response of soil microbiomes to extreme summers.