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In the present study, we developed and validated an experimental life support system (ELSS) designed to investigate coral reef associated bacterial communities. The microcosms in the ELSS consisted of coral reef sediment, synthetic seawater, and specimens of five benthic reef species. These included two hard corals Montipora digitata and Montipora capricornis, a soft coral Sarcophyton glaucum, a zoanthid Zoanthus sp., and a sponge Chondrilla sp.. Physicochemical parameters and bacterial communities in the ELSS were similar to those observed at shallow coral reef sites. Sediment bacterial evenness and higher taxonomic composition were more similar to natural-type communities at days 29 and 34 than at day 8 after transfer to the microcosms, suggesting microbial stabilization after an initial recovery period. Biotopes were compositionally distinct but shared a number of ASVs. At day 34, sediment specific ASVs were found in hosts and visa versa. Transplantation significantly altered the bacterial community composition of M. digitata and Chondrilla sp., suggesting microbial adaptation to altered environmental conditions. Altogether, our results support the suitability of the ELSS developed in this study as a model system to investigate coral reef associated bacterial communities using multi-factorial experiments., (© 2024. The Author(s).)

Microbially induced calcification is an ancient, community-driven mineralisation process that produces different types of microbialites. Symbiolites are photosynthesis-induced microbialites, formed by calcifying co-cultures of dinoflagellates from the family Symbiodiniaceae and bacteria. Symbiolites encase the calcifying community as endolithic cells, pointing at an autoendolithic niche of symbiotic dinoflagellates, and provide a rare opportunity to study the role of bacteria in bacterial-algal calcification, as symbiodiniacean cultures display either distinct symbiolite-producing (SP) or non-symbiolite-producing (NP) phenotypes. Using Illumina sequencing, we found that the bacterial communities of SP and NP cultures differed significantly in the relative abundance of 23 genera, 14 families, and 2 phyla. SP cultures were rich in biofilm digesters from the phylum Planctomycetes and their predicted metagenomes were enriched in orthologs related to biofilm formation. In contrast, NP cultures were dominated by biofilm digesters from the Bacteroidetes, and were inferred as enriched in proteases and nucleases. Functional assays confirmed the potential of co-cultures and bacterial isolates to produce biofilms and point at acidic polysaccharides as key stimulators for mineral precipitation. Hence, bacteria appear to influence symbiolite formation primarily through their biofilm-producing and modifying activity and we anticipate that symbiolite formation, as a low-complexity in vitro model, will significantly advance our understanding of photosynthesis-induced microbial calcification processes.

Dinoflagellates of the genus Symbiodinium are commonly recognized as invertebrate endosymbionts that are of central importance for the functioning of coral reef ecosystems. However, the endosymbiotic phase within Symbiodinium life history is inherently tied to a more cryptic free-living (ex hospite) phase that remains largely unexplored. Here we show that free-living Symbiodinium spp. in culture commonly form calcifying bacterial-algal communities that produce aragonitic spherulites and encase the dinoflagellates as endolithic cells. This process is driven by Symbiodinium photosynthesis but occurs only in partnership with bacteria. Our findings not only place dinoflagellates on the map of microbial-algal organomineralization processes but also point toward an endolithic phase in the Symbiodinium life history, a phenomenon that may provide new perspectives on the biology and ecology of Symbiodinium spp. and the evolutionary history of the coral-dinoflagellate symbiosis.