The giant barrel sponge Xestospongia muta takes up dissolved organic matter from benthic cyanobacterial mats

With the decline of reef-building corals, other organisms are taking over Caribbean reefs, including sponges and benthic cyanobacterial mats (BCM). Sponges take up dissolved organic matter (DOM), but the sources and chemical characteristics of DOM taken up by sponges are unknown. One likely DOM source is benthic autotrophs, including BCM, which are prolific producers of DOM. We tested the hypothesis that sponges take up BCM-derived DOM using laboratory experiments in which seawater samples were collected before and after sequential incubations of BCM and small individuals of the giant barrel sponge Xestospongia muta. The concentration of DOC and relative abundance of individual features in the high resolution mass spectra using untargeted metabolomics were determined for each sample. There was a significant increase in DOC after BCM incubations, followed by a significant decrease after sponge incubations. These changes were mirrored in single feature relative abundances, with 2101 out of 3667 features significantly enriched during BCM incubations, and 54% of these (1142) depleted during sponge incubations. Among BCM-enriched and sponge-depleted features, many were halogenated, some were known BCM-derived secondary metabolites (e.g., carriebowmide, barbamide), and others matched unidentified sponge-depleted features from seawater samples collected on the reef. To our knowledge, this is the first report that sponges take up BCM exudates, including some that were detectable in reef DOM, revealing a path of molecules from source to sink through their environment. The BCM exudates taken up by sponges may be used as a food source or incorporated into sponge secondary metabolites for holobiont maintenance or chemical defenses.