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N-Linked Surface Glycan Biosynthesis, Composition, Inhibition, and Function in Cnidarian-Dinoflagellate Symbiosis
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...
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Published in: | Microbial ecology 2020-07, Vol.80 (1), p.223-236 |
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description | 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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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.</description><identifier>ISSN: 0095-3628</identifier><identifier>EISSN: 1432-184X</identifier><identifier>DOI: 10.1007/s00248-020-01487-9</identifier><identifier>PMID: 31982929</identifier><language>eng</language><publisher>New York: Springer Science + Business Media</publisher><subject>Algae ; Biomedical and Life Sciences ; Biosynthesis ; Cell surface ; Chemical composition ; Colonization ; Corals ; Dinoflagellates ; Ecology ; Genomes ; Geoecology/Natural Processes ; Glycan ; Golgi apparatus ; HOST MICROBE INTERACTIONS ; Immunity ; Innate immunity ; Life Sciences ; Liquid chromatography ; Mannose ; Marine invertebrates ; Mass spectrometry ; Mass spectroscopy ; Microbial Ecology ; Microbiology ; Microorganisms ; Molecular interactions ; N-glycans ; Nature Conservation ; Polysaccharides ; Symbionts ; Symbiosis ; Water Quality/Water Pollution</subject><ispartof>Microbial ecology, 2020-07, Vol.80 (1), p.223-236</ispartof><rights>Springer Science+Business Media, LLC, part of Springer Nature 2020</rights><rights>Springer Science+Business Media, LLC, part of Springer Nature 2020.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c441t-abdb19f424c6534650c28181277648ed614b2319ea2ec93f53a450cc3aef8e973</citedby><cites>FETCH-LOGICAL-c441t-abdb19f424c6534650c28181277648ed614b2319ea2ec93f53a450cc3aef8e973</cites><orcidid>0000-0003-1090-564X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/48740011$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/48740011$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>314,780,784,27923,27924,58237,58470</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31982929$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Tivey, Trevor R.</creatorcontrib><creatorcontrib>Parkinson, John Everett</creatorcontrib><creatorcontrib>Mandelare, Paige E.</creatorcontrib><creatorcontrib>Adpressa, Donovon A.</creatorcontrib><creatorcontrib>Peng, Wenjing</creatorcontrib><creatorcontrib>Dong, Xue</creatorcontrib><creatorcontrib>Mechref, Yehia</creatorcontrib><creatorcontrib>Weis, Virginia M.</creatorcontrib><creatorcontrib>Loesgen, Sandra</creatorcontrib><title>N-Linked Surface Glycan Biosynthesis, Composition, Inhibition, and Function in Cnidarian-Dinoflagellate Symbiosis</title><title>Microbial ecology</title><addtitle>Microb Ecol</addtitle><addtitle>Microb Ecol</addtitle><description>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. 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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.</description><subject>Algae</subject><subject>Biomedical and Life Sciences</subject><subject>Biosynthesis</subject><subject>Cell surface</subject><subject>Chemical composition</subject><subject>Colonization</subject><subject>Corals</subject><subject>Dinoflagellates</subject><subject>Ecology</subject><subject>Genomes</subject><subject>Geoecology/Natural Processes</subject><subject>Glycan</subject><subject>Golgi apparatus</subject><subject>HOST MICROBE INTERACTIONS</subject><subject>Immunity</subject><subject>Innate immunity</subject><subject>Life Sciences</subject><subject>Liquid chromatography</subject><subject>Mannose</subject><subject>Marine invertebrates</subject><subject>Mass spectrometry</subject><subject>Mass spectroscopy</subject><subject>Microbial 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Ecol</addtitle><date>2020-07-01</date><risdate>2020</risdate><volume>80</volume><issue>1</issue><spage>223</spage><epage>236</epage><pages>223-236</pages><issn>0095-3628</issn><eissn>1432-184X</eissn><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. 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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.</abstract><cop>New York</cop><pub>Springer Science + Business Media</pub><pmid>31982929</pmid><doi>10.1007/s00248-020-01487-9</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0003-1090-564X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Algae Biomedical and Life Sciences Biosynthesis Cell surface Chemical composition Colonization Corals Dinoflagellates Ecology Genomes Geoecology/Natural Processes Glycan Golgi apparatus HOST MICROBE INTERACTIONS Immunity Innate immunity Life Sciences Liquid chromatography Mannose Marine invertebrates Mass spectrometry Mass spectroscopy Microbial Ecology Microbiology Microorganisms Molecular interactions N-glycans Nature Conservation Polysaccharides Symbionts Symbiosis Water Quality/Water Pollution |
title | N-Linked Surface Glycan Biosynthesis, Composition, Inhibition, and Function in Cnidarian-Dinoflagellate Symbiosis |
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