Soil Microbial Adaptations to Climate Disturbance: Integrated Multi-Omics Insights from Permafrost and Arid Ecosystems

Abstract

Climate change is intensifying temperature and precipitation variability, challenging microbial communities and ecosystem functioning. Interactions between microbiomes and metabolites are central to biogeochemical cycling, yet how these interactions drive greenhouse gas emissions during ecosystem transitions remains poorly understood. To address this, we applied an integrated multi-omics approach—combining metagenomics, metatranscriptomics, and metabolomics—across two climate-sensitive ecosystems: thawing permafrost peatlands and monsoon-influenced arid soils.In Stordalen Mire, Sweden, we analyzed microbial and metabolite composition along a permafrost thaw gradient using genome-resolved metagenomics and high-resolution Fourier transform ion cyclotron resonance mass spectrometry (FT-ICR-MS), guided by community assembly theory. We found divergent assembly processes between microbial taxa and metabolites in response to the same environmental drivers, challenging assumptions in trait-based microbial models. Feature-level analysis revealed associations between microbial taxa, metabolite profiles, and variations in porewater CO₂ and CH₄, highlighting the importance of microbe–metabolite interactions in greenhouse gas flux. We investigated arid soil microbial communities, which endure extreme and rapidly fluctuating environmental conditions, particularly during monsoon transitions. Contrary to the assumption of widespread dormancy, our multi-omics analyses show that microbial populations remain metabolically active, exhibiting dynamic functional redundancy. Communities rapidly reconfigure gene expression and metabolite profiles in response to moisture and nutrient pulses. This functional plasticity enables continuous ecosystem processes and reveals a resilience strategy previously underappreciated in arid soils. Furthermore, we observed consistent partitioning of metabolic functions across ecological preference groups, supporting ecosystem functioning despite environmental extremes. Altogether, our findings demonstrate that microbial responses to climate perturbations are shaped by distinct, ecosystem-specific processes linking microbial function, metabolite dynamics, and environmental change. By integrating high-resolution molecular tools with ecological theory, this work provides new insight into the metabolic mechanisms driving ecosystem resilience and greenhouse gas emissions, offering a predictive framework for understanding microbial contributions to climate feedbacks in a warming world.