Cell surface carbohydrates of symbiotic dinoflagellates and their role in the establishment of cnidarian–dinoflagellate symbiosis

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.

Heat Stress of Algal Partner Hinders Colonization Success and Alters the Algal Cell Surface Glycome in a Cnidarian-Algal Symbiosis

“…High-mannoside glycans are the most abundant type of N-glycan in B. minutum , but increasing the abundance of high-mannoside glycans with inhibitors for glycan maturation pathways can decrease the colonization capacity of B. minutum ( 12 ). Similarly, Tortorelli et al ( 13 ) found higher abundances of high-mannoside glycans as measured by lectin array in nonnative species of algae, Cladocopium goreaui , and Fugacium kawagutii , compared to B. minutum , suggesting that an overabundance of high-mannoside glycans can inhibit symbiosis. The second-most abundant group of N-glycans in B. minutum are galactosylated glycans ( 12 ).…”

“…The second-most abundant group of N-glycans in B. minutum are galactosylated glycans ( 12 ). These glycans are less abundant in nonnative species of algae, Symbiodinium pilosum , C. goreaui , and F. kawagutii , as measured by lectin array compared to B. minutum ( 11 , 13 ). This supports the hypothesis that galactosylation is a marker for a compatible symbiont in Aiptasia ( 11 , 13 ).…”

“…These glycans are less abundant in nonnative species of algae, Symbiodinium pilosum , C. goreaui , and F. kawagutii , as measured by lectin array compared to B. minutum ( 11 , 13 ). This supports the hypothesis that galactosylation is a marker for a compatible symbiont in Aiptasia ( 11 , 13 ). Sialylated glycans have also been detected in Symbiodiniaceae in several recent studies, but their role in symbiosis remains unclear, and their abundance is low ( 11 – 13 ).…”

“…Cell surface glycans from one partner are recognized by lectins from the other partner, allowing microbes to invade hosts, modulate immunity, or evade host detection altogether ( 7 ). In cnidarian-algal symbiosis, molecular manipulation of Symbiodiniaceae glycans or host lectins alters colonization dynamics, suggesting that glycan-lectin interactions are critical for interpartner recognition during the onset of symbiosis ( 8 – 13 ). Glycan lectin interactions may be involved in interpartner specificity because different Symbiodiniaceae species maintain distinct surface glycomes ( 11 , 13 , 14 ).…”

“…In cnidarian-algal symbiosis, molecular manipulation of Symbiodiniaceae glycans or host lectins alters colonization dynamics, suggesting that glycan-lectin interactions are critical for interpartner recognition during the onset of symbiosis ( 8 – 13 ). Glycan lectin interactions may be involved in interpartner specificity because different Symbiodiniaceae species maintain distinct surface glycomes ( 11 , 13 , 14 ). In addition, glycan-lectin signaling may also play a role in maintaining symbiosis because both lectins and glycans are present within the symbiosome even after initial colonization ( 15 – 17 ).…”