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Coral endosymbiont growth is enhanced by metabolic interactions with bacteria

Bacteria are key contributors to microalgae resource acquisition, competitive performance, and functional diversity, but their potential metabolic interactions with coral microalgal endosymbionts (Symbiodiniaceae) have been largely overlooked. Here, we show that altering the bacterial composition of...

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Autores principales: Matthews, Jennifer L., Khalil, Abeeha, Siboni, Nachshon, Bougoure, Jeremy, Guagliardo, Paul, Kuzhiumparambil, Unnikrishnan, DeMaere, Matthew, Le Reun, Nine M., Seymour, Justin R., Suggett, David J., Raina, Jean-Baptiste
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10611727/
https://www.ncbi.nlm.nih.gov/pubmed/37891154
http://dx.doi.org/10.1038/s41467-023-42663-y
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author Matthews, Jennifer L.
Khalil, Abeeha
Siboni, Nachshon
Bougoure, Jeremy
Guagliardo, Paul
Kuzhiumparambil, Unnikrishnan
DeMaere, Matthew
Le Reun, Nine M.
Seymour, Justin R.
Suggett, David J.
Raina, Jean-Baptiste
author_facet Matthews, Jennifer L.
Khalil, Abeeha
Siboni, Nachshon
Bougoure, Jeremy
Guagliardo, Paul
Kuzhiumparambil, Unnikrishnan
DeMaere, Matthew
Le Reun, Nine M.
Seymour, Justin R.
Suggett, David J.
Raina, Jean-Baptiste
author_sort Matthews, Jennifer L.
collection PubMed
description Bacteria are key contributors to microalgae resource acquisition, competitive performance, and functional diversity, but their potential metabolic interactions with coral microalgal endosymbionts (Symbiodiniaceae) have been largely overlooked. Here, we show that altering the bacterial composition of two widespread Symbiodiniaceae species, during their free-living stage, results in a significant shift in their cellular metabolism. Indeed, the abundance of monosaccharides and the key phytohormone indole-3-acetic acid (IAA) were correlated with the presence of specific bacteria, including members of the Labrenzia (Roseibium) and Marinobacter genera. Single-cell stable isotope tracking revealed that these two bacterial genera are involved in reciprocal exchanges of carbon and nitrogen with Symbiodiniaceae. We identified the provision of IAA by Labrenzia and Marinobacter, and this metabolite caused a significant growth enhancement of Symbiodiniaceae. By unravelling these interkingdom interactions, our work demonstrates how specific bacterial associates fundamentally govern Symbiodiniaceae fitness.
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spelling pubmed-106117272023-10-29 Coral endosymbiont growth is enhanced by metabolic interactions with bacteria Matthews, Jennifer L. Khalil, Abeeha Siboni, Nachshon Bougoure, Jeremy Guagliardo, Paul Kuzhiumparambil, Unnikrishnan DeMaere, Matthew Le Reun, Nine M. Seymour, Justin R. Suggett, David J. Raina, Jean-Baptiste Nat Commun Article Bacteria are key contributors to microalgae resource acquisition, competitive performance, and functional diversity, but their potential metabolic interactions with coral microalgal endosymbionts (Symbiodiniaceae) have been largely overlooked. Here, we show that altering the bacterial composition of two widespread Symbiodiniaceae species, during their free-living stage, results in a significant shift in their cellular metabolism. Indeed, the abundance of monosaccharides and the key phytohormone indole-3-acetic acid (IAA) were correlated with the presence of specific bacteria, including members of the Labrenzia (Roseibium) and Marinobacter genera. Single-cell stable isotope tracking revealed that these two bacterial genera are involved in reciprocal exchanges of carbon and nitrogen with Symbiodiniaceae. We identified the provision of IAA by Labrenzia and Marinobacter, and this metabolite caused a significant growth enhancement of Symbiodiniaceae. By unravelling these interkingdom interactions, our work demonstrates how specific bacterial associates fundamentally govern Symbiodiniaceae fitness. Nature Publishing Group UK 2023-10-27 /pmc/articles/PMC10611727/ /pubmed/37891154 http://dx.doi.org/10.1038/s41467-023-42663-y Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/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/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Matthews, Jennifer L.
Khalil, Abeeha
Siboni, Nachshon
Bougoure, Jeremy
Guagliardo, Paul
Kuzhiumparambil, Unnikrishnan
DeMaere, Matthew
Le Reun, Nine M.
Seymour, Justin R.
Suggett, David J.
Raina, Jean-Baptiste
Coral endosymbiont growth is enhanced by metabolic interactions with bacteria
title Coral endosymbiont growth is enhanced by metabolic interactions with bacteria
title_full Coral endosymbiont growth is enhanced by metabolic interactions with bacteria
title_fullStr Coral endosymbiont growth is enhanced by metabolic interactions with bacteria
title_full_unstemmed Coral endosymbiont growth is enhanced by metabolic interactions with bacteria
title_short Coral endosymbiont growth is enhanced by metabolic interactions with bacteria
title_sort coral endosymbiont growth is enhanced by metabolic interactions with bacteria
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10611727/
https://www.ncbi.nlm.nih.gov/pubmed/37891154
http://dx.doi.org/10.1038/s41467-023-42663-y
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