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Reef-building corals farm and feed on their photosynthetic symbionts

Reef-building corals farm and feed on their photosynthetic symbionts
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 paradox1. The energy demand of coral animal hosts can often be fully met by the excess production of carbon-rich photosynthates by their algal symbionts2,3. However, the understanding of mechanisms that enable corals to acquire the vital nutrients nitrogen and phosphorus from their symbionts is incomplete4,5,6,7,8,9. 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.

Animals, Anthozoa/growth & development, Ecosystem, Nitrogen/metabolism, Phosphorus/metabolism, Symbiosis/physiology, Photosynthesis, Birds/physiology
0028-0836
1018–1024
Wiedenmann, Jörg
ad445af2-680f-4927-90b3-589ac9d538f7
D’Angelo, Cecilia
0d35b03b-684d-43aa-a57a-87212ab07ee1
Mardones, M. Loreto
58972563-9548-4d03-97df-0dbbd7970009
Moore, Shona
18f99ddc-911c-4ad8-bea5-12e384d799fc
Benkwitt, Cassandra E.
323cfd7d-00a7-4ddd-9c0c-a43466536869
Graham, Nicholas A.J.
4eda0d3e-7ad0-4d61-8cc8-656c2f666526
Hambach, Bastian
d144b919-bc71-4793-89ee-7fdfdb7762bb
Wilson, Paul A.
f940a9f0-fa5a-4a64-9061-f0794bfbf7c6
Vanstone, James
16b95649-7244-4829-a00c-021723af3640
Eyal, Gal
da83d991-4ed9-44de-b90d-272036b54ad0
Ben-Zvi, Or
dce6a933-bca5-4e91-abf8-25d51c448835
Loya, Yossi
26f27801-394c-4428-a9dd-1423f3d5b457
Genin, Amatzia
6654d1bd-fc2e-4b76-8de9-220dbe4d3b85
Wiedenmann, Jörg
ad445af2-680f-4927-90b3-589ac9d538f7
D’Angelo, Cecilia
0d35b03b-684d-43aa-a57a-87212ab07ee1
Mardones, M. Loreto
58972563-9548-4d03-97df-0dbbd7970009
Moore, Shona
18f99ddc-911c-4ad8-bea5-12e384d799fc
Benkwitt, Cassandra E.
323cfd7d-00a7-4ddd-9c0c-a43466536869
Graham, Nicholas A.J.
4eda0d3e-7ad0-4d61-8cc8-656c2f666526
Hambach, Bastian
d144b919-bc71-4793-89ee-7fdfdb7762bb
Wilson, Paul A.
f940a9f0-fa5a-4a64-9061-f0794bfbf7c6
Vanstone, James
16b95649-7244-4829-a00c-021723af3640
Eyal, Gal
da83d991-4ed9-44de-b90d-272036b54ad0
Ben-Zvi, Or
dce6a933-bca5-4e91-abf8-25d51c448835
Loya, Yossi
26f27801-394c-4428-a9dd-1423f3d5b457
Genin, Amatzia
6654d1bd-fc2e-4b76-8de9-220dbe4d3b85

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 and Genin, Amatzia (2023) Reef-building corals farm and feed on their photosynthetic symbionts. Nature, 620, 1018–1024. (doi:10.1038/s41586-023-06442-5).

Record type: Article

Abstract

Coral reefs are highly diverse ecosystems that thrive in nutrient-poor waters, a phenomenon frequently referred to as the Darwin paradox1. The energy demand of coral animal hosts can often be fully met by the excess production of carbon-rich photosynthates by their algal symbionts2,3. However, the understanding of mechanisms that enable corals to acquire the vital nutrients nitrogen and phosphorus from their symbionts is incomplete4,5,6,7,8,9. 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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Accepted/In Press date: 17 July 2023
e-pub ahead of print date: 23 August 2023
Published date: 31 August 2023
Additional Information: A correction has been attached to this output located at https://www.nature.com/articles/s41586-023-06584-6 and https://doi.org/10.1038/s41586-023-06584-6
Keywords: Animals, Anthozoa/growth & development, Ecosystem, Nitrogen/metabolism, Phosphorus/metabolism, Symbiosis/physiology, Photosynthesis, Birds/physiology

Identifiers

Local EPrints ID: 481555
URI: http://eprints.soton.ac.uk/id/eprint/481555
ISSN: 0028-0836
PURE UUID: e537b4f8-7356-416d-b964-11c14b1f2ba5
ORCID for Jörg Wiedenmann: ORCID iD orcid.org/0000-0003-2128-2943
ORCID for Bastian Hambach: ORCID iD orcid.org/0000-0003-4546-5672
ORCID for Paul A. Wilson: ORCID iD orcid.org/0000-0001-6425-8906

Catalogue record

Date deposited: 01 Sep 2023 17:02
Last modified: 13 Jul 2024 01:48

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Contributors

Author: M. Loreto Mardones
Author: Shona Moore
Author: Cassandra E. Benkwitt
Author: Nicholas A.J. Graham
Author: Bastian Hambach ORCID iD
Author: Paul A. Wilson ORCID iD
Author: James Vanstone
Author: Gal Eyal
Author: Or Ben-Zvi
Author: Yossi Loya
Author: Amatzia Genin

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