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Symbiont population control by host-symbiont metabolic interaction in Symbiodiniaceae-cnidarian associations

In cnidarian-Symbiodiniaceae symbioses, algal endosymbiont population control within the host is needed to sustain a symbiotic relationship. However, the molecular mechanisms that underlie such population control are unclear. Here we show that a cnidarian host uses nitrogen limitation as a primary m...

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Autores principales: Xiang, Tingting, Lehnert, Erik, Jinkerson, Robert E., Clowez, Sophie, Kim, Rick G., DeNofrio, Jan C., Pringle, John R., Grossman, Arthur R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6949306/
https://www.ncbi.nlm.nih.gov/pubmed/31913264
http://dx.doi.org/10.1038/s41467-019-13963-z
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author Xiang, Tingting
Lehnert, Erik
Jinkerson, Robert E.
Clowez, Sophie
Kim, Rick G.
DeNofrio, Jan C.
Pringle, John R.
Grossman, Arthur R.
author_facet Xiang, Tingting
Lehnert, Erik
Jinkerson, Robert E.
Clowez, Sophie
Kim, Rick G.
DeNofrio, Jan C.
Pringle, John R.
Grossman, Arthur R.
author_sort Xiang, Tingting
collection PubMed
description In cnidarian-Symbiodiniaceae symbioses, algal endosymbiont population control within the host is needed to sustain a symbiotic relationship. However, the molecular mechanisms that underlie such population control are unclear. Here we show that a cnidarian host uses nitrogen limitation as a primary mechanism to control endosymbiont populations. Nitrogen acquisition and assimilation transcripts become elevated in symbiotic Breviolum minutum algae as they reach high-densities within the sea anemone host Exaiptasia pallida. These same transcripts increase in free-living algae deprived of nitrogen. Symbiotic algae also have an elevated carbon-to-nitrogen ratio and shift metabolism towards scavenging nitrogen from purines relative to free-living algae. Exaiptasia glutamine synthetase and glutamate synthase transcripts concomitantly increase with the algal endosymbiont population, suggesting an increased ability of the host to assimilate ammonium. These results suggest algal growth and replication in hospite is controlled by access to nitrogen, which becomes limiting for the algae as their population within the host increases.
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spelling pubmed-69493062020-01-10 Symbiont population control by host-symbiont metabolic interaction in Symbiodiniaceae-cnidarian associations Xiang, Tingting Lehnert, Erik Jinkerson, Robert E. Clowez, Sophie Kim, Rick G. DeNofrio, Jan C. Pringle, John R. Grossman, Arthur R. Nat Commun Article In cnidarian-Symbiodiniaceae symbioses, algal endosymbiont population control within the host is needed to sustain a symbiotic relationship. However, the molecular mechanisms that underlie such population control are unclear. Here we show that a cnidarian host uses nitrogen limitation as a primary mechanism to control endosymbiont populations. Nitrogen acquisition and assimilation transcripts become elevated in symbiotic Breviolum minutum algae as they reach high-densities within the sea anemone host Exaiptasia pallida. These same transcripts increase in free-living algae deprived of nitrogen. Symbiotic algae also have an elevated carbon-to-nitrogen ratio and shift metabolism towards scavenging nitrogen from purines relative to free-living algae. Exaiptasia glutamine synthetase and glutamate synthase transcripts concomitantly increase with the algal endosymbiont population, suggesting an increased ability of the host to assimilate ammonium. These results suggest algal growth and replication in hospite is controlled by access to nitrogen, which becomes limiting for the algae as their population within the host increases. Nature Publishing Group UK 2020-01-08 /pmc/articles/PMC6949306/ /pubmed/31913264 http://dx.doi.org/10.1038/s41467-019-13963-z Text en © The Author(s) 2020 Open Access 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/.
spellingShingle Article
Xiang, Tingting
Lehnert, Erik
Jinkerson, Robert E.
Clowez, Sophie
Kim, Rick G.
DeNofrio, Jan C.
Pringle, John R.
Grossman, Arthur R.
Symbiont population control by host-symbiont metabolic interaction in Symbiodiniaceae-cnidarian associations
title Symbiont population control by host-symbiont metabolic interaction in Symbiodiniaceae-cnidarian associations
title_full Symbiont population control by host-symbiont metabolic interaction in Symbiodiniaceae-cnidarian associations
title_fullStr Symbiont population control by host-symbiont metabolic interaction in Symbiodiniaceae-cnidarian associations
title_full_unstemmed Symbiont population control by host-symbiont metabolic interaction in Symbiodiniaceae-cnidarian associations
title_short Symbiont population control by host-symbiont metabolic interaction in Symbiodiniaceae-cnidarian associations
title_sort symbiont population control by host-symbiont metabolic interaction in symbiodiniaceae-cnidarian associations
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6949306/
https://www.ncbi.nlm.nih.gov/pubmed/31913264
http://dx.doi.org/10.1038/s41467-019-13963-z
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