Compartment-specific archaeal responses to alpine wetland grasslandification reveal distinct taxonomic, functional, and network reorganization across soil-root interfacial continua.

Introduction: Alpine wetland ecosystems on the Qinghai-Tibetan Plateau are critical carbon sinks experiencing grasslandification due to anthropogenic activities and climate change. While microbial dynamics underpin ecosystem processes, archaeal community dynamics across soil-root compartments remain poorly understood.

Objectives: This study aimed to elucidate how archaeal diversity, community structure, assembly mechanisms, and functional potential respond to grasslandification across soil depths (0-10 cm and 10-20 cm) and root compartments associated with three dominant plant species along a gradient from alpine wetland meadow to degraded meadow on the QTP.

Methods: We estimated archaeal diversity and assembly at soil-root interfaces using 16S rRNA high-throughput sequencing, ecological modeling (βNTI, co-occurrence networks), functional inference (PICRUSt2/FAPROTAX), and structure equation modeling (SEM) to estimate drivers.

Results: Soil degradation, marked by declining soil water content, soil organic carbon, and total nitrogen, drove compartment-specific archaeal responses. Bulk soils showed decreased α-diversity and network complexity with grasslandification dominated by Thaumarchaeota, whereas Euryarchaeota increased significantly in root compartments during degradation. Functional predictions revealed a transition from nitrification and carbon oxidation processes in the wetland meadow to enhanced methanogenesis in the degraded meadow. Stochastic processes governed community assembly in surface soils and root compartments, while deterministic filtering dominated deeper soils in the wetland meadow. The integrative analyses, including Mantel test, SEM, and PERMANOVA, revealed the combined influence of abiotic and biotic factors structuring archaeal communities, network associations, and predicted functions.

Conclusions: This study demonstrates that grasslandification drives a transition from carbon storage towards methane-emitting processes. Notably, plant roots form microbial refugia that maintain complex archaeal interactions even under degraded conditions, highlighting the importance of incorporating plant-microbe interactions into conservation strategies for alpine wetland ecosystems.