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

Author

Listed:
  • 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
    The Second Affiliated Hospital of Guangzhou University of Chinese Medicine)

  • 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
    King Abdullah University of Science and Technology (KAUST), Biological and Environmental Science and Engineering Division, the Plant Science Program)

  • Manuel Aranda

    (King Abdullah University of Science and Technology (KAUST), Biological and Environmental Science and Engineering Division, Red Sea Research Center)

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.

Suggested Citation

  • Guoxin Cui & Jianing Mi & Alessandro Moret & Jessica Menzies & Huawen Zhong & Angus Li & Shiou-Han Hung & Salim Al-Babili & Manuel Aranda, 2023. "A carbon-nitrogen negative feedback loop underlies the repeated evolution of cnidarian–Symbiodiniaceae symbioses," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42582-y
    DOI: 10.1038/s41467-023-42582-y
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    References listed on IDEAS

    as
    1. Guoxin Cui & Yi Jin Liew & Yong Li & Najeh Kharbatia & Noura I Zahran & Abdul-Hamid Emwas & Victor M Eguiluz & Manuel Aranda, 2019. "Host-dependent nitrogen recycling as a mechanism of symbiont control in Aiptasia," PLOS Genetics, Public Library of Science, vol. 15(6), pages 1-19, June.
    2. Tingting Xiang & Erik Lehnert & Robert E. Jinkerson & Sophie Clowez & Rick G. Kim & Jan C. DeNofrio & John R. Pringle & Arthur R. Grossman, 2020. "Symbiont population control by host-symbiont metabolic interaction in Symbiodiniaceae-cnidarian associations," Nature Communications, Nature, vol. 11(1), pages 1-9, December.
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    Cited by:

    1. Giovanni Scarinci & Jan-Luca Ariens & Georgia Angelidou & Sebastian Schmidt & Timo Glatter & Nicole Paczia & Victor Sourjik, 2024. "Enhanced metabolic entanglement emerges during the evolution of an interkingdom microbial community," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    2. Nils Rädecker & Stéphane Escrig & Jorge E. Spangenberg & Christian R. Voolstra & Anders Meibom, 2023. "Coupled carbon and nitrogen cycling regulates the cnidarian–algal symbiosis," Nature Communications, Nature, vol. 14(1), pages 1-10, December.

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