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N-Linked Surface Glycan Biosynthesis, Composition, Inhibition, and Function in Cnidarian-Dinoflagellate Symbiosis

  • Host Microbe Interactions
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Abstract

The success of symbioses between cnidarian hosts (e.g., corals and sea anemones) and micro-algal symbionts hinges on the molecular interactions that govern the establishment and maintenance of intracellular mutualisms. As a fundamental component of innate immunity, glycan-lectin interactions impact the onset of marine endosymbioses, but our understanding of the effects of cell surface glycome composition on symbiosis establishment remains limited. In this study, we examined the canonical N-glycan biosynthesis pathway in the genome of the dinoflagellate symbiont Breviolum minutum (family Symbiodiniaceae) and found it to be conserved with the exception of the transferase GlcNAc-TII (MGAT2). Using coupled liquid chromatography-mass spectrometry (LC-MS/MS), we characterized the cell surface N-glycan content of B. minutum, providing the first insight into the molecular composition of surface glycans in dinoflagellates. We then used the biosynthesis inhibitors kifunensine and swainsonine to alter the glycan composition of B. minutum. Successful high-mannose enrichment via kifunensine treatment resulted in a significant decrease in colonization of the model sea anemone Aiptasia (Exaiptasia pallida) by B. minutum. Hybrid glycan enrichment via swainsonine treatment, however, could not be confirmed and did not impact colonization. We conclude that functional Golgi processing of N-glycans is critical for maintaining appropriate cell surface glycan composition and for ensuring colonization success by B. minutum.

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Acknowledgments

We thank Shumpei Maruyama, Sarah Howey, Milan Sengthrep, Tyler Coleman, Kyle Petersen, Darian Thompson, and Kenneth Moller for their assistance in algal and animal maintenance. In addition, we thank Allison Ehrlich, Jamie Pennington, and the Environmental and Molecular Toxicology Department at Oregon State University for technical support in flow cytometry.

Funding

This research was funded by the National Science Foundation (NSF IOS-1557804 to V.M.W and S.L.).

Author information

Authors and Affiliations

  1. Department of Integrative Biology, Oregon State University, Corvallis, OR, USA

    Trevor R. Tivey, John Everett Parkinson & Virginia M. Weis

  2. Department of Entomology, Cornell University, Ithaca, NY, USA

    Trevor R. Tivey

  3. Department of Integrative Biology, University of South Florida, Tampa, FL, USA

    John Everett Parkinson

  4. Department of Chemistry, Oregon State University, Corvallis, OR, USA

    Paige E. Mandelare, Donovon A. Adpressa & Sandra Loesgen

  5. Whitney Laboratory for Marine Bioscience and Department of Chemistry, University of Florida, St. Augustine, FL, USA

    Paige E. Mandelare & Sandra Loesgen

  6. Analytical Research & Development, Merck & Co. Inc., Boston, MA, USA

    Donovon A. Adpressa

  7. Department of Chemistry and Biochemistry, Texas Tech University, Lubbock, TX, USA

    Wenjing Peng, Xue Dong & Yehia Mechref

Authors
  1. Trevor R. Tivey
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  2. John Everett Parkinson
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  3. Paige E. Mandelare
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  4. Donovon A. Adpressa
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  5. Wenjing Peng
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  6. Xue Dong
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  7. Yehia Mechref
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  8. Virginia M. Weis
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  9. Sandra Loesgen
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Corresponding authors

Correspondence to Trevor R. Tivey or Sandra Loesgen.

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Tivey, T.R., Parkinson, J.E., Mandelare, P.E. et al. N-Linked Surface Glycan Biosynthesis, Composition, Inhibition, and Function in Cnidarian-Dinoflagellate Symbiosis. Microb Ecol 80, 223–236 (2020). https://doi.org/10.1007/s00248-020-01487-9

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  • DOI: https://doi.org/10.1007/s00248-020-01487-9

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