Fast and persistent responses of alpine permafrost microbial communities to in situ warming

Global warming in mid-latitude alpine regions results in permafrost thawing, together with greater availability of carbon and nutrients in soils and frequent freeze–thaw cycles. Yet it is unclear how these multifactorial changes will shape the 1 m-deep permafrost microbiome in the future, and how this will in turn modulate microbially-mediated feedbacks between mountain soils and climate (e.g. soil CO₂ emissions). To unravel the responses of the alpine permafrost microbiome to in situ warming, we established a three-year experiment in a permafrost monitoring summit in the Alps. Specifically, we simulated conditions of warming by transplanting permafrost soils from a depth of 160 cm either to the active-layer topsoils in the north-facing slope or in the warmer south-facing slope, near the summit. qPCR-based and amplicon sequencing analyses indicated an augmented microbial abundance in the transplanted permafrost, driven by the increase in copiotrophic prokaryotic taxa (e.g. Noviherbaspirillum and Massilia) and metabolically versatile psychrotrophs (e.g. Tundrisphaera and Granulicella); which acclimatized to the changing environment and potentially benefited from substrates released upon thawing. Metabolically restricted Patescibacteria lineages vastly decreased with warming, as reflected in the loss of α-diversity in the transplanted soils. Ascomycetous sapro-pathotrophs (e.g. Tetracladium) and a few lichenized fungi (e.g. Aspicilia) expanded in the transplanted permafrost, particularly in soils transplanted to the warmer south-facing slope, replacing basidiomycetous yeasts (e.g. Glaciozyma). The transplantation-induced loosening of microbial association networks in the permafrost could potentially indicate lesser cooperative interactions between neighboring microorganisms. Broader substrate-use microbial activities measured in the transplanted permafrost could relate to altered soil C dynamics. The three-year simulated warming did not, however, enhance heterotrophic respiration, which was limited by the carbon-depleted permafrost conditions. Collectively, our quantitative findings suggest the vulnerability of the alpine permafrost microbiome to warming, which might improve predictions on microbially-modulated transformations of mountain soil ecosystems under the future climate.