Metabolomic signatures of corals thriving across extreme reef habitats reveal strategies of heat stress tolerance

Author:

Haydon Trent D.12ORCID,Matthews Jennifer L.2ORCID,Seymour Justin R.2ORCID,Raina Jean-Baptiste2ORCID,Seymour Jamie E.3ORCID,Chartrand Kathryn4ORCID,Camp Emma F.2ORCID,Suggett David J.2ORCID

Affiliation:

1. Center for Genomics and Systems Biology, New York University Abu Dhabi, PO Box 129188, Abu Dhabi, UAE

2. Faculty of Science, Climate Change Cluster, University of Technology Sydney, Ultimo, New South Wales 2007, Australia

3. Division of Tropical Health and Medicine, Australian Institute of Tropical Health and Medicine, James Cook University, Cairns, QLD 4811, Australia

4. Centre for tropical Water and Aquatic Ecosystem Research, James Cook University, Cairns, QLD 4811, Australia

Abstract

Anthropogenic stressors continue to escalate worldwide, driving unprecedented declines in reef environmental conditions and coral health. One approach to better understand how corals can function in the future is to examine coral populations that thrive within present day naturally extreme habitats. We applied untargeted metabolomics (gas chromatography–mass spectrometry (GC–MS)) to contrast metabolite profiles of Pocillopora acuta colonies from hot, acidic and deoxygenated mangrove environments versus those from adjacent reefs. Under ambient temperatures, P. acuta predominantly associated with endosymbionts of the genera Cladocopium (reef) or Durusdinium (mangrove), exhibiting elevated metabolism in mangrove through energy-generating and biosynthesis pathways compared to reef populations. Under transient heat stress, P. acuta endosymbiont associations were unchanged. Reef corals bleached and exhibited extensive shifts in symbiont metabolic profiles (whereas host metabolite profiles were unchanged). By contrast, mangrove populations did not bleach and solely the host metabolite profiles were altered, including cellular responses in inter-partner signalling, antioxidant capacity and energy storage. Thus mangrove P. acuta populations resist periodically high-temperature exposure via association with thermally tolerant endosymbionts coupled with host metabolic plasticity. Our findings highlight specific metabolites that may be biomarkers of heat tolerance, providing novel insight into adaptive coral resilience to elevated temperatures.

Funder

Australian Research Council

Publisher

The Royal Society

Subject

General Agricultural and Biological Sciences,General Environmental Science,General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine

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