Molecular insights into the Darwin paradox of coral reefs from the sea anemone Aiptasia

Author:

Cui Guoxin1ORCID,Konciute Migle K.1ORCID,Ling Lorraine2ORCID,Esau Luke3ORCID,Raina Jean-Baptiste4ORCID,Han Baoda5ORCID,Salazar Octavio R.1ORCID,Presnell Jason S.6ORCID,Rädecker Nils178ORCID,Zhong Huawen1,Menzies Jessica1ORCID,Cleves Phillip A.9,Liew Yi Jin1ORCID,Krediet Cory J.10ORCID,Sawiccy Val6,Cziesielski Maha J.1,Guagliardo Paul11ORCID,Bougoure Jeremy11,Pernice Mathieu4ORCID,Hirt Heribert5ORCID,Voolstra Christian R.17ORCID,Weis Virginia M.6ORCID,Pringle John R.2ORCID,Aranda Manuel1ORCID

Affiliation:

1. Red Sea Research Center, Biological and Environmental Sciences and Engineering Division (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal 23955-6900, Saudi Arabia.

2. Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305, USA.

3. Core Labs, King Abdullah University of Science and Technology (KAUST), Thuwal 23955-6900, Saudi Arabia.

4. Climate Change Cluster, University of Technology Sydney, Ultimo, NSW 2007, Australia.

5. DARWIN21, Biological and Environmental Science and Engineering Division (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal 23955-6900, Saudi Arabia.

6. Department of Integrative Biology, Oregon State University, Corvallis, OR 97331, USA.

7. Department of Biology, University of Konstanz, Konstanz 78457, Germany.

8. Laboratory for Biological Geochemistry, School of Architecture, Civil and Environmental Engineering, École Polytechnique Fédérale de Lausanne, Lausanne, Switzerland.

9. Department of Embryology, Carnegie Institution for Science, Baltimore, MD 21218, USA.

10. Department of Marine Science, Eckerd College, St. Petersburg, FL 33711, USA.

11. Centre for Microscopy Characterisation and Analysis, The University of Western Australia, Perth, WA, Australia.

Abstract

Symbiotic cnidarians such as corals and anemones form highly productive and biodiverse coral reef ecosystems in nutrient-poor ocean environments, a phenomenon known as Darwin’s paradox. Resolving this paradox requires elucidating the molecular bases of efficient nutrient distribution and recycling in the cnidarian-dinoflagellate symbiosis. Using the sea anemone Aiptasia, we show that during symbiosis, the increased availability of glucose and the presence of the algae jointly induce the coordinated up-regulation and relocalization of glucose and ammonium transporters. These molecular responses are critical to support symbiont functioning and organism-wide nitrogen assimilation through glutamine synthetase/glutamate synthase–mediated amino acid biosynthesis. Our results reveal crucial aspects of the molecular mechanisms underlying nitrogen conservation and recycling in these organisms that allow them to thrive in the nitrogen-poor ocean environments.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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