Microbial metabolisms determine soil priming effect induced by organic inputs

Soil microorganisms are essential in determining soil organic carbon (C) decomposition via the priming effect. However, the understanding of microbial-driven priming effects is hampered by the poor understanding of microbial metabolisms in response to different organic inputs. Based on a meta-analysis encompassing 449 experimental comparisons globally, we investigated the differences in priming effects induced by two types of substrates: sugars and lipids. Coupled with the stable isotope probing combined with metagenomics (SIP-metagenomics), an incubation with ¹³C-labeled glucose or glycerol (proxy of sugar or lipid products) was further conducted to investigate the priming effect and the underlying microbial mechanisms, e.g., the core bacteria taxa and their metabolism. Firstly, meta-analysis showed, at a global scale, sugars induced a significantly higher priming effect compared to lipids. Secondly, incubation experiments with these low-molecular-weight substrates further demonstrated that sugar-derived compounds stimulated greater bacterial diversity and enriched genes encoding glycoside hydrolases, resulting in a stronger priming effect. In contrast, bacterial communities utilizing lipid-derived compounds were dominated by Bacillus species, exhibiting genes associated with metabolite synthesis processes (e.g., glycosyl transferases, GTs) while concurrently depleting genes related to extracellular enzyme production (e.g., glycoside hydrolases, GHs), which collectively resulted in a weaker priming effect. This study underscores that the substrate selected bacteria taxa and their metabolisms, particularly the balance between anabolism and catabolism, play a key role in regulating the magnitude of the priming effect.