Abstract
Symbiodiniaceae algae are often photosymbionts of reef-building corals. The establishment of their symbiosis resembles a microbial infection where eukaryotic pattern recognition receptors (e.g. lectins) are thought to recognize a specific range of taxon-specific microbial-associated molecular patterns (e.g. glycans). The present study used the sea anemone, Exaiptasia diaphana and three species of Symbiodiniaceae (the homologous Breviolum minutum, the heterologous-compatible Cladocopium goreaui and the heterologous-incompatible Fugacium kawagutii) to compare the surface glycomes of three symbionts and explore the role of glycan–lectin interactions in host–symbiont recognition and establishment of symbiosis. We identified the nucleotide sugars of the algal cells, then examined glycans on the cell wall of the three symbiont species with monosaccharide analysis, lectin array technology and fluorescence microscopy of the algal cell decorated with fluorescently tagged lectins. Armed with this inventory of possible glycan moieties, we then assayed the ability of the three Symbiodiniaceae to colonize aposymbiotic E. diaphana after modifying the surface of one of the two partners. The Symbiodiniaceae cell-surface glycome varies among algal species. Trypsin treatment of the alga changed the rate of B. minutum and C. goreaui uptake, suggesting that a protein-based moiety is an essential part of compatible symbiont recognition. Our data strongly support the importance of D-galactose (in particular β-D-galactose) residues in the establishment of the cnidarian–dinoflagellate symbiosis, and we propose a potential involvement of L-fucose, D-xylose and D-galacturonic acid in the early steps of this mutualism.
Highlights
Symbiodiniaceae are single-celled alveolate protists of the phylum Dinoflagellata
We hypothesized that the compatible symbionts (B. minutum and C. goreaui) have similar cell-surface structures that fit the lock-and-key mechanism of the host and are different from the ones on the cell surface of incompatible algae (F. kawagutii)
The B. minutum culture was isolated from the E. diaphana anemones mentioned above [27], while C. goreaui and F. kawagutii were obtained from the Australian Institute of Marine Science (AIMS) where they were originally isolated from the Great Barrier Reef (GBR)-sourced corals Acrocopora tenuis and Pocillopora damicornis, respectively
Summary
Symbiodiniaceae are single-celled alveolate protists of the phylum Dinoflagellata. Dinoflagellates inhabit temperate and tropical areas as phototrophs, heterotrophs, parasites and symbionts, but the Symbiodiniaceae are most widely recognized as intracellular photosymbionts of reef-building corals [1]. We hypothesized that the compatible symbionts (B. minutum and C. goreaui) have similar cell-surface structures that fit the lock-and-key mechanism of the host and are different from the ones on the cell surface of incompatible algae (F. kawagutii) Based on this concept, we explored and compared the composition of the three Symbiodiniaceae cell surfaces. Three replicates for each Symbiodiniaceae species were diluted and subsequently analysed on an ICS 6,000 (Dionex Corporation, Sunnyvale, CA) essentially as described in Rautengarten et al 2014 [32], with the innovative methods [31], was adopted to profile the cell surface of these Symbiodiniaceae In this way, we created a list of potential molecular candidates, that we strategically altered to investigate their role(s) during the first stages of symbiosis. Standards comprised Lfucose, L-rhamnose, L-arabinose, C-galactose, D-galactose, D-xylose, Dgalacturonic acid, D-glucuronic acid, N-acetylgalactosamine and N-
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