Paleoclimatic Legacies Help Explain Microbial Carbon Use Efficiency in Thawing Permafrost

Microbial decomposition in thawing permafrost mobilizes one of Earth’s largest organic carbon reservoirs, releasing CO2 that amplifies global warming. This carbon–climate feedback depends strongly on microbial carbon use efficiency (CUE)─the ratio of biomass carbon synthesis to total carbon uptake, which governs the balance between carbon retention and respiratory loss. Although permafrost carbon and microbial communities developed thousands of years ago, how paleoclimatic legacies shape permafrost CUE remains unresolved. Here, by integrating 18O–H2O labeling with amplicon and metagenomic sequencing across a ∼1000-km transect on the Tibetan Plateau, we show that mid-Holocene paleoclimate outperforms contemporary drivers in explaining spatial variation in permafrost CUE. Sites with drier and more variable paleoclimates exhibited lower CUE (0.17 ± 0.07) than wetter and more climatically stable sites (0.43 ± 0.08). This lower CUE was linked to two pathways: geochemical constraints involving reduced nutrient availability and stronger phosphorus limitation, and microbial adaptations reflected in communities enriched in metabolically costly stress-tolerance and recalcitrant carbon-acquisition traits. Collectively, these paleoclimatic legacies accounted for 70% of CUE variation, underscoring the critical role of paleoclimate in shaping the vulnerability of permafrost carbon to respiratory loss upon thawing. Incorporating these millennial-scale legacies into Earth system models could improve projections of future permafrost carbon feedbacks.