Permafrost thawing by soil transplantation alters the functional genetic potential of the alpine permafrost microbiome

Abstract

Global warming has led to permafrost thawing in mid-latitude alpine regions, resulting in greater availability of carbon (C) and nutrients in soils. However, how these changes will impact the functional genetic potential of permafrost soil microbiomes, and subsequently, how they will influence the microbially mediated feedback of mountain soils under climate change remains unknown. To help answer this question, we conducted a permafrost thawing experiment on the north-facing slope near the summit of Muot da Barba Peider (2979 m above sea level) in the Swiss Alps. Specifically, we transplanted permafrost soils from a depth of 160 cm to the active-layer topsoils (0–18 cm) and incubated the soils in situ for three years. Using shotgun metagenomics, we found that transplantation significantly altered the gene structure of the permafrost microbiome, with changes occurring in the short term (< one year) and remaining stable over time. Transplanted soils exhibited an enhanced functional genetic potential, particularly for genes related to “Information storage and processing”, “Cellular processes and signaling” and “Metabolism” functions, which suggests increased cellular processes and metabolism. Carbohydrate-active enzymes involved in the degradation of both labile (such as starch) and recalcitrant (such as lignin) C substrates were enriched in transplanted soils, indicating an enhanced C-degradation potential. Nitrogen (N)-cycling genes related to the degradation and synthesis of N compounds, denitrification, assimilation and dissimilatory nitrate reduction were overrepresented in the transplanted soil, pointing to enhanced N assimilation and transformation potential. Our study elucidates how the permafrost microbiome may functionally respond to warming in the European Alps. This research complements observations from Tibetan and Arctic regions, improving our understanding of functional changes in thawing permafrost globally.