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

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posted on 27.01.2022, 01:00 authored by G Tortorelli, C Rautengarten, Tony BacicTony Bacic, G Segal, B Ebert, SK Davy, MJH van Oppen, GI McFadden
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.

Funding

This research was funded by the Australian Government through the Australian Research Council Discovery Project DP160101539 and DP210100639. GT acknowledges receipt of the University of Melbourne International Research Scholarship and Fee Remission Scholarship, and the Botany Foundation at the University of Melbourne for awarding the Ethel McLennan prize that supported Symbiodiniaceae monosaccharide and lectin array analyses. GIMcF and MJHvO acknowledge Australian Research Council Discovery Grant DP160101539. MJHvO acknowledges Australian Research Council Laureate Fellowship FL180100036. BE acknowledges an ARC Future Fellowship Award FT160100276, Discovery Grant DP180102630 and support from the University of Melbourne Botany Foundation. CR acknowledges the financial aid of an Albert Shimmins COVID-19 support fund. We thank Joshua Heazlewood and Alfie Hao for the sugar nucleotide and the monosaccharide component analyses. We thank Virginia Weis, John Parkinson, Paige Mandelare and Kruti Patel for the support in the preparation of lectin array samples. We thank Ellie Cho from the Biological Optical Microscopy Platform (BOMP) at the University of Melbourne for assistance with confocal microscopy. We thank Kevin Bairos-Novak, Patrick Buerger and Wing Chan for the help with bioinformatics.

History

Publication Date

01/01/2022

Journal

ISME Journal

Volume

16

Issue

1

Pagination

(p. 190-199)

Publisher

Springer

ISSN

1751-7362

Rights Statement

© 2022 Springer Nature Limited. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article ’ s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article ’ s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons. org/licenses/by/4.0/.