AI-2-mediated quorum sensing marks the ecological transition from collective cooperation to individual survival...

Quorum sensing (QS) is a central system reflecting microbial collective behavior; however, its role in shaping functional microbial communities within complex solid-state fermentation matrices such as Daqu remains insufficiently understood. Here, we integrated amplicon sequencing, metagenomics, proteomics, and metabolomics to investigate autoinducer-2 (AI-2)-mediated quorum sensing dynamics during Daqu storage. Storage induced a directional succession of the microbial community, revealing two distinct ecological stages. The rapid adjustment stage (0-2 months) was characterized by strong homogeneous selection and rapid species turnover, whereas the slow stabilization stage (3-9 months) was dominated by gradual shifts in microbial relative abundances. Notably, the LuxS/AI-2 pathway, the only QS system detected during Daqu storage, declined rapidly and then stabilized, coinciding with the transition between the two ecological stages. During the early stage, the core QS protein LuxS was tightly associated with the dominant taxon Lactobacillaceae and the methyl donor S-adenosylmethionine, forming a synergistic functional module. In contrast, during the late stage, LuxS became decoupled from stress-tolerant taxa and showed weakened associations with resistance-related metabolic networks. This shift was accompanied by a metabolic transition, with carbon flux gradually redirected from active glycolysis toward the pentose phosphate pathway and amino acid biosynthesis during later stages. Collectively, these findings demonstrate that temporal modulation of the LuxS/AI-2 quorum sensing system represents a critical regulatory node reflecting the transition of the Daqu microbial community from cooperative growth to stress-resilient survival, ultimately shaping metabolic phenotypes and ecosystem functions during storage.