Diverse quorum sensing systems regulate microbial communication and biogeochemical processes in deep-sea cold seeps

Abstract Background Quorum sensing is a fundamental chemical communication mechanism that enables microorganisms to coordinate behavior and adapt to environmental conditions. However, its contribution in deep-sea cold seep ecosystems, where diverse microbial communities and frequent communication occur, remains poorly understood. In this study, we aimed to elucidate the occurrence and potential ecological roles of quorum sensing in cold seeps. Results We analyzed 170 metagenomes and 33 metatranscriptomes from 17 global cold seep sites, identifying 299,355 quorum sensing genes from the cold seep non-redundant gene catalog. These genes represent 34 types across six quorum sensing systems, with distribution patterns influenced by sediment depth and seep type. A total of 32,500 quorum sensing genes were identified in 3576 metagenome-assembled genomes from 12 archaeal and 108 bacterial phyla, revealing a complex network of intraspecies and interspecies communication. Microbial groups involved in key metabolic processes, such as sulfate-reducing bacteria, anaerobic methanotrophic archaea, diazotrophs, and organohalide reducers, were extensively regulated by quorum sensing, influencing biogeochemical cycles in cold seeps. Phylogenetic analysis and protein domain identification highlighted the involvement of key quorum sensing-related proteins (e.g., PDE, RpfC/G, CahR, and LuxR) in modulating microbial behaviors, such as motility and chemotaxis. Heterologous expression further confirmed the activity of representative LuxI-R pairs, and metabolomic profiling suggested the presence of putative quorum sensing inhibitors in cold seep sediments. Conclusions Overall, these findings highlight the complexity and significance of quorum sensing in microbial interactions, ecological adaptation, and biogeochemical cycling within cold seep ecosystems, advancing our understanding of microbial communication in the deep biosphere. Video Abstract