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

Corals owe their ecological success to their symbiotic relationship with dinoflagellate algae (family Symbiodiniaceae). While the negative effects of heat stress on this symbiosis are well studied, how heat stress affects the onset of symbiosis and symbiont specificity is less explored. In this work...

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Autores principales: Maruyama, Shumpei, Mandelare-Ruiz, Paige E., McCauley, Mark, Peng, Wenjing, Cho, Byeong Gwan, Wang, Junyao, Mechref, Yehia, Loesgen, Sandra, Weis, Virginia M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9241721/
https://www.ncbi.nlm.nih.gov/pubmed/35639004
http://dx.doi.org/10.1128/spectrum.01567-22
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author Maruyama, Shumpei
Mandelare-Ruiz, Paige E.
McCauley, Mark
Peng, Wenjing
Cho, Byeong Gwan
Wang, Junyao
Mechref, Yehia
Loesgen, Sandra
Weis, Virginia M.
author_facet Maruyama, Shumpei
Mandelare-Ruiz, Paige E.
McCauley, Mark
Peng, Wenjing
Cho, Byeong Gwan
Wang, Junyao
Mechref, Yehia
Loesgen, Sandra
Weis, Virginia M.
author_sort Maruyama, Shumpei
collection PubMed
description Corals owe their ecological success to their symbiotic relationship with dinoflagellate algae (family Symbiodiniaceae). While the negative effects of heat stress on this symbiosis are well studied, how heat stress affects the onset of symbiosis and symbiont specificity is less explored. In this work, we used the model sea anemone, Exaiptasia diaphana (commonly referred to as Aiptasia), and its native symbiont, Breviolum minutum, to study the effects of heat stress on the colonization of Aiptasia by algae and the algal cell-surface glycome. Heat stress caused a decrease in the colonization of Aiptasia by algae that were not due to confounding variables such as algal motility or oxidative stress. With mass spectrometric analysis and lectin staining, a thermally induced enrichment of glycans previously found to be associated with free-living strains of algae (high-mannoside glycans) and a concomitant reduction in glycans putatively associated with symbiotic strains of algae (galactosylated glycans) were identified. Differential enrichment of specific sialic acid glycans was also identified, although their role in this symbiosis remains unclear. We also discuss the methods used to analyze the cell-surface glycome of algae, evaluate current limitations, and provide suggestions for future work in algal-coral glycobiology. Overall, this study provided insight into how stress may affect the symbiosis between cnidarians and their algal symbionts by altering the glycome of the symbiodinian partner. IMPORTANCE Coral reefs are under threat from global climate change. Their decline is mainly caused by the fragility of their symbiotic relationship with dinoflagellate algae which they rely upon for their ecological success. To better understand coral biology, researchers used the sea anemone, Aiptasia, a model system for the study of coral-algal symbiosis, and characterized how heat stress can alter the algae's ability to communicate to the coral host. This study found that heat stress caused a decline in algal colonization success and impacted the cell surface molecules of the algae such that it became more like that of nonsymbiotic species of algae. This work adds to our understanding of the molecular signals involved in coral-algal symbiosis and how it breaks down during heat stress.
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spelling pubmed-92417212022-06-30 Heat Stress of Algal Partner Hinders Colonization Success and Alters the Algal Cell Surface Glycome in a Cnidarian-Algal Symbiosis Maruyama, Shumpei Mandelare-Ruiz, Paige E. McCauley, Mark Peng, Wenjing Cho, Byeong Gwan Wang, Junyao Mechref, Yehia Loesgen, Sandra Weis, Virginia M. Microbiol Spectr Research Article Corals owe their ecological success to their symbiotic relationship with dinoflagellate algae (family Symbiodiniaceae). While the negative effects of heat stress on this symbiosis are well studied, how heat stress affects the onset of symbiosis and symbiont specificity is less explored. In this work, we used the model sea anemone, Exaiptasia diaphana (commonly referred to as Aiptasia), and its native symbiont, Breviolum minutum, to study the effects of heat stress on the colonization of Aiptasia by algae and the algal cell-surface glycome. Heat stress caused a decrease in the colonization of Aiptasia by algae that were not due to confounding variables such as algal motility or oxidative stress. With mass spectrometric analysis and lectin staining, a thermally induced enrichment of glycans previously found to be associated with free-living strains of algae (high-mannoside glycans) and a concomitant reduction in glycans putatively associated with symbiotic strains of algae (galactosylated glycans) were identified. Differential enrichment of specific sialic acid glycans was also identified, although their role in this symbiosis remains unclear. We also discuss the methods used to analyze the cell-surface glycome of algae, evaluate current limitations, and provide suggestions for future work in algal-coral glycobiology. Overall, this study provided insight into how stress may affect the symbiosis between cnidarians and their algal symbionts by altering the glycome of the symbiodinian partner. IMPORTANCE Coral reefs are under threat from global climate change. Their decline is mainly caused by the fragility of their symbiotic relationship with dinoflagellate algae which they rely upon for their ecological success. To better understand coral biology, researchers used the sea anemone, Aiptasia, a model system for the study of coral-algal symbiosis, and characterized how heat stress can alter the algae's ability to communicate to the coral host. This study found that heat stress caused a decline in algal colonization success and impacted the cell surface molecules of the algae such that it became more like that of nonsymbiotic species of algae. This work adds to our understanding of the molecular signals involved in coral-algal symbiosis and how it breaks down during heat stress. American Society for Microbiology 2022-05-31 /pmc/articles/PMC9241721/ /pubmed/35639004 http://dx.doi.org/10.1128/spectrum.01567-22 Text en Copyright © 2022 Maruyama et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Maruyama, Shumpei
Mandelare-Ruiz, Paige E.
McCauley, Mark
Peng, Wenjing
Cho, Byeong Gwan
Wang, Junyao
Mechref, Yehia
Loesgen, Sandra
Weis, Virginia M.
Heat Stress of Algal Partner Hinders Colonization Success and Alters the Algal Cell Surface Glycome in a Cnidarian-Algal Symbiosis
title Heat Stress of Algal Partner Hinders Colonization Success and Alters the Algal Cell Surface Glycome in a Cnidarian-Algal Symbiosis
title_full Heat Stress of Algal Partner Hinders Colonization Success and Alters the Algal Cell Surface Glycome in a Cnidarian-Algal Symbiosis
title_fullStr Heat Stress of Algal Partner Hinders Colonization Success and Alters the Algal Cell Surface Glycome in a Cnidarian-Algal Symbiosis
title_full_unstemmed Heat Stress of Algal Partner Hinders Colonization Success and Alters the Algal Cell Surface Glycome in a Cnidarian-Algal Symbiosis
title_short Heat Stress of Algal Partner Hinders Colonization Success and Alters the Algal Cell Surface Glycome in a Cnidarian-Algal Symbiosis
title_sort heat stress of algal partner hinders colonization success and alters the algal cell surface glycome in a cnidarian-algal symbiosis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9241721/
https://www.ncbi.nlm.nih.gov/pubmed/35639004
http://dx.doi.org/10.1128/spectrum.01567-22
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