Metabolic interactions between coral animal and endolithic bacterial communities

Coral skeletons constitute sources of nutrients and energy for holobiont. Although bacteria predominate in endolithic microbiomes of corals, their ecological functions have long been masked by those of symbiotic microalgae. In the skeleton of Isopora palifera, previous studies showed the absence of microalgae and a green layer dominated by green sulfur bacteria. This system, which excludes a contribution from microalgae, provides a perfect model for studying the role of endolithic bacteria in corals. Using this model, we examined the metabolite profile and translocation of organic matter between coral tissue and skeleton. Chromatography-time-of-flight-mass spectrometry and ultra-high-performance liquid chromatography tandem mass spectrometry revealed distinct metabolic profiles in tissue and different skeletal layers. A stable isotope incubation experiment further demonstrated ¹³C translocation between tissue and the green layer, but no translocation of ¹⁵N. These findings suggest communication between the two compartments that is generally carbon-based, possibly in the form of carbohydrates and bioactive compounds, such as corticosterone and domoic acid. Nevertheless, some nitrogenous compounds appear to have an endolithic source, indicating a possible contribution of the skeleton to coral animal. Notably, antibiotic treatment greatly increased ¹⁵N translocation in the tissue but not in the green layer. This highlights an important role of bacteria in nitrogen cycling in the holobiont and in establishing the nitrogen-limiting green layer. Altogether, this study provides the first data about coral skeletal metabolomes. Based on these findings, we propose a model of interactions between coral animal and skeletal bacterial communities, offering a new perspective on the ecological role of endolithic bacteria in corals.