Heat stress destabilizes symbiotic nutrient cycling in corals.

Affiliation

Rädecker N(1)(2)(3), Pogoreutz C(4)(3), Gegner HM(4)(5), Cárdenas A(4)(3), Roth F(4)(6)(7), Bougoure J(8), Guagliardo P(8), Wild C(9), Pernice M(10), Raina JB(10), Meibom A(2)(11), Voolstra CR(4)(3).
Author information:
(1)Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal 23955, Saudi Arabia; [Email]
(2)Laboratory for Biological Geochemistry, School of Architecture, Civil and Environmental Engineering, École Polytechnique Fédérale de Lausanne, 1015 Lausanne, Switzerland.
(3)Department of Biology, University of Konstanz, 78457 Konstanz, Germany.
(4)Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal 23955, Saudi Arabia.
(5)Metabolomics Core Technology Platform, Centre for Organismal Studies, University of Heidelberg, 69117 Heidelberg, Germany.
(6)Baltic Sea Centre, Stockholm University, 10691 Stockholm, Sweden.
(7)Tvärminne Zoological Station, University of Helsinki, 10900 Hanko, Finland.
(8)Centre for Microscopy, Characterisation and Analysis, The University of Western Australia, Perth, WA 6009, Australia.
(9)Marine Ecology Department, Faculty of Biology and Chemistry, University of Bremen, 28359 Bremen, Germany.
(10)Climate Change Cluster, Faculty of Science, University of Technology Sydney, Ultimo, NSW 2007, Australia.
(11)Center for Advanced Surface Analysis, Institute of Earth Sciences, Université de Lausanne, 1015 Lausanne, Switzerland.

Abstract

Recurrent mass bleaching events are pushing coral reefs worldwide to the brink of ecological collapse. While the symptoms and consequences of this breakdown of the coral-algal symbiosis have been extensively characterized, our understanding of the underlying causes remains incomplete. Here, we investigated the nutrient fluxes and the physiological as well as molecular responses of the widespread coral Stylophora pistillata to heat stress prior to the onset of bleaching to identify processes involved in the breakdown of the coral-algal symbiosis. We show that altered nutrient cycling during heat stress is a primary driver of the functional breakdown of the symbiosis. Heat stress increased the metabolic energy demand of the coral host, which was compensated by the catabolic degradation of amino acids. The resulting shift from net uptake to release of ammonium by the coral holobiont subsequently promoted the growth of algal symbionts and retention of photosynthates. Together, these processes form a feedback loop that will gradually lead to the decoupling of carbon translocation from the symbiont to the host. Energy limitation and altered symbiotic nutrient cycling are thus key factors in the early heat stress response, directly contributing to the breakdown of the coral-algal symbiosis. Interpreting the stability of the coral holobiont in light of its metabolic interactions provides a missing link in our understanding of the environmental drivers of bleaching and may ultimately help uncover fundamental processes underpinning the functioning of endosymbioses in general.