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Using Aiptasia as a Model to Study Metabolic Interactions in Cnidarian-Symbiodinium Symbioses

The symbiosis between cnidarian hosts and microalgae of the genus Symbiodinium provides the foundation of coral reefs in oligotrophic waters. Understanding the nutrient-exchange between these partners is key to identifying the fundamental mechanisms behind this symbiosis, yet has proven difficult gi...

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Autores principales: Rädecker, Nils, Raina, Jean-Baptiste, Pernice, Mathieu, Perna, Gabriela, Guagliardo, Paul, Kilburn, Matt R., Aranda, Manuel, Voolstra, Christian R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5864895/
https://www.ncbi.nlm.nih.gov/pubmed/29615919
http://dx.doi.org/10.3389/fphys.2018.00214
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author Rädecker, Nils
Raina, Jean-Baptiste
Pernice, Mathieu
Perna, Gabriela
Guagliardo, Paul
Kilburn, Matt R.
Aranda, Manuel
Voolstra, Christian R.
author_facet Rädecker, Nils
Raina, Jean-Baptiste
Pernice, Mathieu
Perna, Gabriela
Guagliardo, Paul
Kilburn, Matt R.
Aranda, Manuel
Voolstra, Christian R.
author_sort Rädecker, Nils
collection PubMed
description The symbiosis between cnidarian hosts and microalgae of the genus Symbiodinium provides the foundation of coral reefs in oligotrophic waters. Understanding the nutrient-exchange between these partners is key to identifying the fundamental mechanisms behind this symbiosis, yet has proven difficult given the endosymbiotic nature of this relationship. In this study, we investigated the respective contribution of host and symbiont to carbon and nitrogen assimilation in the coral model anemone Aiptaisa. For this, we combined traditional measurements with nanoscale secondary ion mass spectrometry (NanoSIMS) and stable isotope labeling to investigate patterns of nutrient uptake and translocation both at the organismal scale and at the cellular scale. Our results show that the rate of carbon and nitrogen assimilation in Aiptasia depends on the identity of the host and the symbiont. NanoSIMS analysis confirmed that both host and symbiont incorporated carbon and nitrogen into their cells, implying a rapid uptake and cycling of nutrients in this symbiotic relationship. Gross carbon fixation was highest in Aiptasia associated with their native Symbiodinium communities. However, differences in fixation rates were only reflected in the δ(13)C enrichment of the cnidarian host, whereas the algal symbiont showed stable enrichment levels regardless of host identity. Thereby, our results point toward a “selfish” character of the cnidarian—Symbiodinium association in which both partners directly compete for available resources. Consequently, this symbiosis may be inherently instable and highly susceptible to environmental change. While questions remain regarding the underlying cellular controls of nutrient exchange and the nature of metabolites involved, the approach outlined in this study constitutes a powerful toolset to address these questions.
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spelling pubmed-58648952018-04-03 Using Aiptasia as a Model to Study Metabolic Interactions in Cnidarian-Symbiodinium Symbioses Rädecker, Nils Raina, Jean-Baptiste Pernice, Mathieu Perna, Gabriela Guagliardo, Paul Kilburn, Matt R. Aranda, Manuel Voolstra, Christian R. Front Physiol Physiology The symbiosis between cnidarian hosts and microalgae of the genus Symbiodinium provides the foundation of coral reefs in oligotrophic waters. Understanding the nutrient-exchange between these partners is key to identifying the fundamental mechanisms behind this symbiosis, yet has proven difficult given the endosymbiotic nature of this relationship. In this study, we investigated the respective contribution of host and symbiont to carbon and nitrogen assimilation in the coral model anemone Aiptaisa. For this, we combined traditional measurements with nanoscale secondary ion mass spectrometry (NanoSIMS) and stable isotope labeling to investigate patterns of nutrient uptake and translocation both at the organismal scale and at the cellular scale. Our results show that the rate of carbon and nitrogen assimilation in Aiptasia depends on the identity of the host and the symbiont. NanoSIMS analysis confirmed that both host and symbiont incorporated carbon and nitrogen into their cells, implying a rapid uptake and cycling of nutrients in this symbiotic relationship. Gross carbon fixation was highest in Aiptasia associated with their native Symbiodinium communities. However, differences in fixation rates were only reflected in the δ(13)C enrichment of the cnidarian host, whereas the algal symbiont showed stable enrichment levels regardless of host identity. Thereby, our results point toward a “selfish” character of the cnidarian—Symbiodinium association in which both partners directly compete for available resources. Consequently, this symbiosis may be inherently instable and highly susceptible to environmental change. While questions remain regarding the underlying cellular controls of nutrient exchange and the nature of metabolites involved, the approach outlined in this study constitutes a powerful toolset to address these questions. Frontiers Media S.A. 2018-03-16 /pmc/articles/PMC5864895/ /pubmed/29615919 http://dx.doi.org/10.3389/fphys.2018.00214 Text en Copyright © 2018 Rädecker, Raina, Pernice, Perna, Guagliardo, Kilburn, Aranda and Voolstra. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Rädecker, Nils
Raina, Jean-Baptiste
Pernice, Mathieu
Perna, Gabriela
Guagliardo, Paul
Kilburn, Matt R.
Aranda, Manuel
Voolstra, Christian R.
Using Aiptasia as a Model to Study Metabolic Interactions in Cnidarian-Symbiodinium Symbioses
title Using Aiptasia as a Model to Study Metabolic Interactions in Cnidarian-Symbiodinium Symbioses
title_full Using Aiptasia as a Model to Study Metabolic Interactions in Cnidarian-Symbiodinium Symbioses
title_fullStr Using Aiptasia as a Model to Study Metabolic Interactions in Cnidarian-Symbiodinium Symbioses
title_full_unstemmed Using Aiptasia as a Model to Study Metabolic Interactions in Cnidarian-Symbiodinium Symbioses
title_short Using Aiptasia as a Model to Study Metabolic Interactions in Cnidarian-Symbiodinium Symbioses
title_sort using aiptasia as a model to study metabolic interactions in cnidarian-symbiodinium symbioses
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5864895/
https://www.ncbi.nlm.nih.gov/pubmed/29615919
http://dx.doi.org/10.3389/fphys.2018.00214
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