Long-term warming reduces surface soil organic carbon by reducing mineral-associated carbon rather than “free” particulate carbon

Soils in alpine ecosystems store a large amount of carbon. However, the responses of soil organic carbon (SOC) to long-term warming and the microbial mechanisms underlying SOC dynamics remain poorly understood. Here, we investigated the effects of 20-year warming (1997–2017) on SOC pools in an alpine shrubland on the Qinghai-Tibetan Plateau. We analyzed the plant and microbial communities, as well as soil chemistry, particularly the SOC of bulk soil and its two physical fractions. Warming did not alter plant biomass (either above- or below-ground). However, warming decreased overall microbial biomass carbon and nitrogen, the biomass of fungi (indicated by phospholipid fatty acids, amino sugars, and OTU richness), and potential activities of hydrolytic enzymes (especially β-1,4-glucosidase), in the surface 0–10 cm soil. Moreover, warming reduced the SOC in bulk soil (by 21%) and the heavy fraction (by 25%), but did not change the SOC in the light fraction. Importantly, there were strong positive correlations between the SOC in bulk soil and in the heavy fraction with the total microbial and fungal necromass, suggesting that the warming-induced loss of soil carbon was mainly due to the suppression of the microbial pathway of soil carbon formation. In deeper layers (10–50 cm) of the shrubland, however, warming (to a much lower degree than that in the surface soil) had only a minor effect on soil carbon pools and the microbial community. A global meta-analysis further showed that warming on average did not significantly change the SOC in different fractions (bulk SOC, active C, and stable C) in the surface soil. Taken together, these results show that long-term warming leads to significant loss of surface soil carbon (mostly in the mineral-associated heavy fraction), likely due to suppressing the microbial (particularly fungal) pathway to soil carbon formation and/or stimulating the utilization of stable soil carbon (i.e. heavy fraction) by microbes in the alpine shrubland.