Resolving Symbiodiniaceae diversity across coral microhabitats and reef niches

Dinoflagellates of the family Symbiodiniaceae are main symbionts of diverse marine animals. A large diversity of Symbiodiniaceae also occur beyond the bounds of their multicellular hosts, occupying environmental niches on coral reefs. The link between spatial diversity at ecosystem scale to microhabitats of Symbiodiniaceae within the coral holobiont are largely unknown. Using ITS2 amplicon sequencing, we compared Symbiodiniaceae communities across four environments (seawater, near-reef and distant sediments, and turf algae mats) and two coral microhabitats (tissue and mucus) on a coral reef in the Red Sea. Analysis of ITS2 sequences revealed that coral and environmental habitats were both dominated by the genera Symbiodinium, Cladocopium, and Durusdinium, but environmental habitats additionally harbored Fugacium, Gerakladium, and Halluxium. Each environmental habitat harbored a distinct Symbiodiniaceae community, with 14-27 % exclusive ITS2 sequences. Nonetheless, 17 ITS2 sequences were shared among all habitat types and were variants defining nearly half of the ITS2 type profiles used to further resolve Symbiodiniaceae identity of coral-based communities. Tissues and surface mucus layers of 49 coral colonies from 17 genera had largely identical Symbiodiniaceae communities. Together with the large difference between environmental Symbiodiniaceae communities and those in the mucus, our results indicate a clear barrier between host-associated and environmental Symbiodiniaceae communities marked by only few shared complete type profiles under normal conditions. It remains to be determined how Symbiodiniaceae community dynamics between coral microhabitats and environmental reservoirs change during coral bleaching events. Monitoring coral colonies after mucus sampling confirmed its suitability for repeated long-term monitoring of coral-associated Symbiodiniaceae communities.