Biodiversity affects the exometabolomes of four benthic functional groups in coral reefs

Abstract Coral reef organisms associate with diverse microorganisms as holobionts. The microbial and biochemical properties of these holobionts extend beyond the physical boundary of the organisms into the surrounding environment. This dynamic zone called the aura-biome may mediate and be mediated by interactions between species in the reef. However, the factors such as the surrounding species that shape the biomolecules present in the aura-biome remain largely unknown. Here, we manipulated the reef species composition and biodiversity in a controlled aquarium experiment and analyzed the exometabolomes of seven species from four functional groups using LC–MS/MS of water samples in the aura-biome of the organisms. We show that biodiversity of neighboring species affects the exometabolome of stony corals, soft corals, macroalgae, and sponges. Exometabolomes were most distinct in organisms in high and low complexity polyculture compared to the empty controls, while exometabolomes of organisms in monoculture were indistinguishable from controls, indicating that surrounding reef species triggered the release of biomolecules. Exometabolomes were specific with distinct patterns between the four functional groups and species within groups. These differences between benthic reef species persisted under varying biodiversity treatments. We annotated 20 compounds from the exometabolomes, 15 of which belonged to ten classes of natural products, with known effects ranging from competition to antifouling. Our data demonstrate that reef species have distinct metabolite auras, which are dynamically adapted to the surrounding species diversity, implicating them in the understudied water-mediated interactions between species. It is therefore essential to understand the composition of reef metabolites in aura-biomes and the factors shaping them to understand their role in mediating organismal interactions and nutrient cycling in coral reef ecosystems.