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Symbiont population control by host-symbiont metabolic interaction in Symbiodiniaceae-cnidarian associations

Author

Listed:
  • Tingting Xiang

    (Carnegie Institution for Science
    University of North Carolina at Charlotte)

  • Erik Lehnert

    (Stanford University School of Medicine)

  • Robert E. Jinkerson

    (University of California)

  • Sophie Clowez

    (Carnegie Institution for Science)

  • Rick G. Kim

    (Carnegie Institution for Science)

  • Jan C. DeNofrio

    (Stanford University School of Medicine)

  • John R. Pringle

    (Stanford University School of Medicine)

  • Arthur R. Grossman

    (Carnegie Institution for Science)

Abstract

In cnidarian-Symbiodiniaceae symbioses, algal endosymbiont population control within the host is needed to sustain a symbiotic relationship. However, the molecular mechanisms that underlie such population control are unclear. Here we show that a cnidarian host uses nitrogen limitation as a primary mechanism to control endosymbiont populations. Nitrogen acquisition and assimilation transcripts become elevated in symbiotic Breviolum minutum algae as they reach high-densities within the sea anemone host Exaiptasia pallida. These same transcripts increase in free-living algae deprived of nitrogen. Symbiotic algae also have an elevated carbon-to-nitrogen ratio and shift metabolism towards scavenging nitrogen from purines relative to free-living algae. Exaiptasia glutamine synthetase and glutamate synthase transcripts concomitantly increase with the algal endosymbiont population, suggesting an increased ability of the host to assimilate ammonium. These results suggest algal growth and replication in hospite is controlled by access to nitrogen, which becomes limiting for the algae as their population within the host increases.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-019-13963-z
    DOI: 10.1038/s41467-019-13963-z
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    Cited by:

    1. 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.
    2. 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.
    3. Kaare-Rasmussen, Jakob O. & Moeller, Holly V. & Pfab, Ferdinand, 2023. "Modeling food dependent symbiosis in Exaiptasia pallida," Ecological Modelling, Elsevier, vol. 481(C).
    4. Dania Nanes Sarfati & Yuan Xue & Eun Sun Song & Ashley Byrne & Daniel Le & Spyros Darmanis & Stephen R. Quake & Adrien Burlacot & James Sikes & Bo Wang, 2024. "Coordinated wound responses in a regenerative animal-algal holobiont," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

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