Asymmetric winter warming reduces microbial carbon use efficiency and growth more than symmetric year-round warming in alpine soils.

Asymmetric seasonal warming trends are evident across terrestrial ecosystems, with winter temperatures rising more than summer ones. Yet, the impact of such asymmetric seasonal warming on soil microbial carbon metabolism and growth remains poorly understood. Using O isotope labeling, we examined the effects of a decade-long experimental seasonal warming on microbial carbon use efficiency (CUE) and growth in alpine grassland ecosystems. Moreover, the quantitative stable isotope probing with O-HO was employed to evaluate taxon-specific bacterial growth in these ecosystems. Results show that symmetric year-round warming decreased microbial growth rate by 31% and CUE by 22%. Asymmetric winter warming resulted in a further decrease in microbial growth rate of 27% and microbial CUE of 59% compared to symmetric year-round warming. Long-term warming increased microbial carbon limitations, especially under asymmetric winter warming. Long-term warming suppressed the growth rates of most bacterial genera, with asymmetric winter warming having a stronger inhibition on the growth rates of specific genera (e.g., , , , , and ) compared to symmetric year-round warming. Bacterial growth was phylogenetically conserved, but this conservation diminished under warming conditions, primarily due to shifts in bacterial physiological states rather than the number of bacterial species and community composition. Overall, long-term warming escalated microbial carbon limitations, decreased microbial growth and CUE, with asymmetric winter warming having a more pronounced effect. Understanding these impacts is crucial for predicting soil carbon cycling as global warming progresses.