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Reef-building corals farm and feed on their photosynthetic symbionts

Coral reefs are highly diverse ecosystems that thrive in nutrient-poor waters, a phenomenon frequently referred to as the Darwin paradox(1). The energy demand of coral animal hosts can often be fully met by the excess production of carbon-rich photosynthates by their algal symbionts(2,3). However, t...

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Autores principales: Wiedenmann, Jörg, D’Angelo, Cecilia, Mardones, M. Loreto, Moore, Shona, Benkwitt, Cassandra E., Graham, Nicholas A. J., Hambach, Bastian, Wilson, Paul A., Vanstone, James, Eyal, Gal, Ben-Zvi, Or, Loya, Yossi, Genin, Amatzia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10468396/
https://www.ncbi.nlm.nih.gov/pubmed/37612503
http://dx.doi.org/10.1038/s41586-023-06442-5
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author Wiedenmann, Jörg
D’Angelo, Cecilia
Mardones, M. Loreto
Moore, Shona
Benkwitt, Cassandra E.
Graham, Nicholas A. J.
Hambach, Bastian
Wilson, Paul A.
Vanstone, James
Eyal, Gal
Ben-Zvi, Or
Loya, Yossi
Genin, Amatzia
author_facet Wiedenmann, Jörg
D’Angelo, Cecilia
Mardones, M. Loreto
Moore, Shona
Benkwitt, Cassandra E.
Graham, Nicholas A. J.
Hambach, Bastian
Wilson, Paul A.
Vanstone, James
Eyal, Gal
Ben-Zvi, Or
Loya, Yossi
Genin, Amatzia
author_sort Wiedenmann, Jörg
collection PubMed
description Coral reefs are highly diverse ecosystems that thrive in nutrient-poor waters, a phenomenon frequently referred to as the Darwin paradox(1). The energy demand of coral animal hosts can often be fully met by the excess production of carbon-rich photosynthates by their algal symbionts(2,3). However, the understanding of mechanisms that enable corals to acquire the vital nutrients nitrogen and phosphorus from their symbionts is incomplete(4–9). Here we show, through a series of long-term experiments, that the uptake of dissolved inorganic nitrogen and phosphorus by the symbionts alone is sufficient to sustain rapid coral growth. Next, considering the nitrogen and phosphorus budgets of host and symbionts, we identify that these nutrients are gathered through symbiont ‘farming’ and are translocated to the host by digestion of excess symbiont cells. Finally, we use a large-scale natural experiment in which seabirds fertilize some reefs but not others, to show that the efficient utilization of dissolved inorganic nutrients by symbiotic corals established in our laboratory experiments has the potential to enhance coral growth in the wild at the ecosystem level. Feeding on symbionts enables coral animals to tap into an important nutrient pool and helps to explain the evolutionary and ecological success of symbiotic corals in nutrient-limited waters.
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spelling pubmed-104683962023-09-01 Reef-building corals farm and feed on their photosynthetic symbionts Wiedenmann, Jörg D’Angelo, Cecilia Mardones, M. Loreto Moore, Shona Benkwitt, Cassandra E. Graham, Nicholas A. J. Hambach, Bastian Wilson, Paul A. Vanstone, James Eyal, Gal Ben-Zvi, Or Loya, Yossi Genin, Amatzia Nature Article Coral reefs are highly diverse ecosystems that thrive in nutrient-poor waters, a phenomenon frequently referred to as the Darwin paradox(1). The energy demand of coral animal hosts can often be fully met by the excess production of carbon-rich photosynthates by their algal symbionts(2,3). However, the understanding of mechanisms that enable corals to acquire the vital nutrients nitrogen and phosphorus from their symbionts is incomplete(4–9). Here we show, through a series of long-term experiments, that the uptake of dissolved inorganic nitrogen and phosphorus by the symbionts alone is sufficient to sustain rapid coral growth. Next, considering the nitrogen and phosphorus budgets of host and symbionts, we identify that these nutrients are gathered through symbiont ‘farming’ and are translocated to the host by digestion of excess symbiont cells. Finally, we use a large-scale natural experiment in which seabirds fertilize some reefs but not others, to show that the efficient utilization of dissolved inorganic nutrients by symbiotic corals established in our laboratory experiments has the potential to enhance coral growth in the wild at the ecosystem level. Feeding on symbionts enables coral animals to tap into an important nutrient pool and helps to explain the evolutionary and ecological success of symbiotic corals in nutrient-limited waters. Nature Publishing Group UK 2023-08-23 2023 /pmc/articles/PMC10468396/ /pubmed/37612503 http://dx.doi.org/10.1038/s41586-023-06442-5 Text en © The Author(s) 2023, corrected publication 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Wiedenmann, Jörg
D’Angelo, Cecilia
Mardones, M. Loreto
Moore, Shona
Benkwitt, Cassandra E.
Graham, Nicholas A. J.
Hambach, Bastian
Wilson, Paul A.
Vanstone, James
Eyal, Gal
Ben-Zvi, Or
Loya, Yossi
Genin, Amatzia
Reef-building corals farm and feed on their photosynthetic symbionts
title Reef-building corals farm and feed on their photosynthetic symbionts
title_full Reef-building corals farm and feed on their photosynthetic symbionts
title_fullStr Reef-building corals farm and feed on their photosynthetic symbionts
title_full_unstemmed Reef-building corals farm and feed on their photosynthetic symbionts
title_short Reef-building corals farm and feed on their photosynthetic symbionts
title_sort reef-building corals farm and feed on their photosynthetic symbionts
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10468396/
https://www.ncbi.nlm.nih.gov/pubmed/37612503
http://dx.doi.org/10.1038/s41586-023-06442-5
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