A carbon-nitrogen negative feedback loop underlies the repeated evolution of cnidarian–Symbiodiniaceae symbioses

Abstract Symbiotic associations with Symbiodiniaceae have evolved independently across a diverse range of cnidarian taxa including reef-building corals, sea anemones, and jellyfish, yet the molecular mechanisms underlying their regulation and repeated evolution are still elusive. Here, we show that...

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Published inNature communications Vol. 14; no. 1; p. 6949
Main Authors Cui, Guoxin, Mi, Jianing, Moret, Alessandro, Menzies, Jessica, Zhong, Huawen, Li, Angus, Hung, Shiou-Han, Al-Babili, Salim, Aranda, Manuel
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group 01.11.2023
Nature Publishing Group UK
Nature Portfolio
Subjects
Algae
Amino acids
Ammonium
Animals
Biosynthesis
Carbohydrates
Carbon
Cnidaria
Control systems
Control theory
Coral reefs
Corals
Dietary supplements
Evolution
Feedback
Feedback loops
Glutamate-ammonia ligase
Glutamine
Molecular modelling
Negative feedback
Nitrogen
Photosynthates
Symbiodiniaceae
Symbionts
Symbiosis
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Summary:Abstract Symbiotic associations with Symbiodiniaceae have evolved independently across a diverse range of cnidarian taxa including reef-building corals, sea anemones, and jellyfish, yet the molecular mechanisms underlying their regulation and repeated evolution are still elusive. Here, we show that despite their independent evolution, cnidarian hosts use the same carbon-nitrogen negative feedback loop to control symbiont proliferation. Symbiont-derived photosynthates are used to assimilate nitrogenous waste via glutamine synthetase–glutamate synthase-mediated amino acid biosynthesis in a carbon-dependent manner, which regulates the availability of nitrogen to the symbionts. Using nutrient supplementation experiments, we show that the provision of additional carbohydrates significantly reduces symbiont density while ammonium promotes symbiont proliferation. High-resolution metabolic analysis confirmed that all hosts co-incorporated glucose-derived 13 C and ammonium-derived 15 N via glutamine synthetase–glutamate synthase-mediated amino acid biosynthesis. Our results reveal a general carbon-nitrogen negative feedback loop underlying these symbioses and provide a parsimonious explanation for their repeated evolution.
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ISSN:2041-1723
2041-1723
DOI:10.1038/s41467-023-42582-y