Comparing Symbiodiniaceae diversity across unicellular hosts, multicellular hosts, and environmental reservoirs

Symbiodiniaceae dinoflagellates are the primary photosymbionts in reef ecosystems, crucial for reef productivity. Although they are widely recognized as symbionts of animals such as corals and clams, they can occupy a broad range of reef niches, including water, sediment, and macroalgae. Understanding their ecology is typically hampered by their horizontal acquisition. Combining evidence from multiple sample types collected at the same location has the potential to address this issue, but such analyses are surprisingly rare. Here, we analysed Symbiodiniaceae communities across 74 environmental and host samples in one reef flat in Okinawa, Japan. We detected ten Symbiodiniaceae genera or genus-level clades using the ITS2 marker metabarcoding, including Clade J, previously known only from Okinotori Island, Japan. Cladocopium, Symbiodinium, and Durusdinium dominated multicellular hosts (hexacorals and Tridacna). In contrast, foraminiferal hosts were dominated by Cladocopium or genus-specific Freudenthalidium, Fugacium, and Miliolidium. Symbiont communities were mostly specific to the host genera. Water samples, with higher proportions of Durusdinium and free-living Symbiodinium, were distinct from macroalgae and sediment samples. The latter did not differ significantly from each other and contained Freudenthalidium, Fugacium, Miliolidium, Clade I, and Clade J. Only three ITS2 variants were shared across all sample categories, but many variants were unique to hosts or habitats. We highlight that both unicellular and multicellular hosts harbor specific endosymbiont types, with lower diversity than in the surrounding environment. Our results imply that host diversity, availability, and environmental context jointly structure photosymbiont communities at fine spatial scales within coral reef ecosystems.