Extracellular vesicles as structured vectors of quorum sensing signals influence aquatic microbial communities

Abstract Quorum sensing (QS) orchestrates collective microbial behaviors and functional acclimatization through chemical communication. However, QS in natural waters is challenged by dilution, alkaline hydrolysis, and enzymatic degradation of freely dissolved autoinducers. Here, we demonstrate that extracellular vesicles (EVs) act as selective, durable, and protective vectors for QS signal molecules under environmental stresses. Specifically, EVs preferentially package hydrophobic acyl‑homoserine lactones, concentrate them locally, and shield them from alkaline hydrolysis, and exhibiting long-distance transport. In addition, EVs possess specific affinity to recipients, thus influencing microbial community. Field investigation via multi-omics showed that EV abundance covaried with salinity, nutrients, chlorophyll a, and biomass, which were validated by culture experiments. Our statistical framework demonstrated that organisms producing moderate EV levels contributed significantly to maintaining community stability and ecosystem functions. Distinctively within this group, QS-active species (including Burkholderiaceae, Pseudomonadaceae, Rhodobacteraceae, Roseobacteraceae, Flavobacteriaceae etc.) emerge as key drivers facilitating these crucial ecological roles. Furthermore, metaproteomics of field EVs reveal QS receptor and synthesis proteins, suggesting coordinated transport of signals and proteins, which indicate new routes for QS crosstalk, particularly for taxa bearing luxR/I solos. Our results show that moderately generated EVs are the potentially important QS signal carriers and ecological regulation hubs in natural waters.