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

Guoxin Cui (), Jianing Mi, Alessandro Moret, Jessica Menzies, Huawen Zhong, Angus Li, Shiou-Han Hung, Salim Al-Babili and Manuel Aranda ()
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Guoxin Cui: King Abdullah University of Science and Technology (KAUST), Biological and Environmental Science and Engineering Division, Red Sea Research Center
Jianing Mi: King Abdullah University of Science and Technology (KAUST), Biological and Environmental Science and Engineering Division, the BioActives Lab, Center for Desert Agriculture
Alessandro Moret: King Abdullah University of Science and Technology (KAUST), Biological and Environmental Science and Engineering Division, Red Sea Research Center
Jessica Menzies: King Abdullah University of Science and Technology (KAUST), Biological and Environmental Science and Engineering Division, Red Sea Research Center
Huawen Zhong: King Abdullah University of Science and Technology (KAUST), Biological and Environmental Science and Engineering Division, Red Sea Research Center
Angus Li: King Abdullah University of Science and Technology (KAUST), Biological and Environmental Science and Engineering Division, Red Sea Research Center
Shiou-Han Hung: King Abdullah University of Science and Technology (KAUST), Biological and Environmental Science and Engineering Division, Red Sea Research Center
Salim Al-Babili: King Abdullah University of Science and Technology (KAUST), Biological and Environmental Science and Engineering Division, the BioActives Lab, Center for Desert Agriculture
Manuel Aranda: King Abdullah University of Science and Technology (KAUST), Biological and Environmental Science and Engineering Division, Red Sea Research Center

Nature Communications, 2023, vol. 14, issue 1, 1-12

Abstract: 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 13C and ammonium-derived 15N 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.

Date: 2023
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DOI: 10.1038/s41467-023-42582-y

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