Sponges harbor a remarkable diversity of microbial symbionts in an enclosed niche where signal molecules can accumulate and enable cell-cell interaction, such as quorum sensing (QS). QS signal molecules were here detected in approximately half of the sponge species investigated in this study. While bacteria capable of QS have been isolated from marine sponges, it is unclear whether they are important members of the holobiont. Using metagenomics on the microbial fraction of the holobiont we identified the eight known N-acyl-homoserine lactone (AHL) QS systems in the microbiome of Theonella swinhoei. The most prevalent AHL-QS system, designated tswIR, was novel, shown to be associated with an alphaproteobacterium of the Rhodobacterales order, and was validated by metabolic analysis of sponge extracts, PCR amplification from species specific groups, and heterologous expression. Taxonomic affiliation using assembled 16S rRNA markers, combined with the presence of sponge-specific features such as ankyrin-like domains, tetratricopeptide repeats, and restriction-modification systems point at the likely symbiotic nature of this novel QS system harboring bacterium.
