Hydrothermal regimes regulate microbiome patterns across vertical profile and their responses to alpine permafrost degradation

Abstract Deciphering microbiomes across vertical profiles is critical for understanding biogeochemical cycling and potential biosafety hazards associated with permafrost degradation under climate warming. However, knowledge about microbiome patterns over key profile layers in response to degradation remains limited in the Qinghai–Tibet Plateau. Using metagenomic data obtained from 150 samples of six 15 m-depth alpine permafrost cores along a degradation gradient, we analyzed microbial community structure and functional potential across different main-layers, including the active, frozen fringe, and frozen layers. We found the recovered microbial and functional diversity decreased with profile depth, and declined only in the active layer as permafrost degraded. Interestingly, Pithoviridae, Caulimoviridae , and virulence factors related to adhesion, biofilm formation, and immune regulation were enriched in the frozen fringe layer, along with increasing relative abundance of Lavidaviridae under the degradation. Along the degradation gradient, carbohydrate-active enzymes diversity decreased in the active layer, while the ratio of nitrite reductase genes to nitrous oxide reductase genes increased in the active and the frozen fringe layers. Hydrothermal regimes emerged as the primary controls shaping microbiome distributions across the vertical profile and along the degradation gradient. Notably, hydrothermal and microbiome attributes jointly regulated carbon/nitrogen loss during the degradation. Taken together, these findings offer crucial insights into microbiome patterns, carbon/nitrogen loss and biosecurity concerning permafrost degradation under global warming.