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

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.

[1]  D. Suggett,et al.  Experiment Degree Heating Week (eDHW) as a novel metric to reconcile and validate past and future global coral bleaching studies. , 2022, Journal of environmental management.

[2]  T. Hughes,et al.  Emergent properties in the responses of tropical corals to recurrent climate extremes , 2021, Current Biology.

[3]  N. Siboni,et al.  Rapid Shifts in Bacterial Communities and Homogeneity of Symbiodiniaceae in Colonies of Pocillopora acuta Transplanted Between Reef and Mangrove Environments , 2021, Frontiers in Microbiology.

[4]  D. Barshis,et al.  Extending the natural adaptive capacity of coral holobionts , 2021, Nature Reviews Earth & Environment.

[5]  B. Nunn,et al.  Broad scale proteomic analysis of heat-destabilised symbiosis in the hard coral Acropora millepora , 2021, Scientific Reports.

[6]  M. Pujo-Pay,et al.  The Bouraké semi-enclosed lagoon (New Caledonia) – a natural laboratory to study the lifelong adaptation of a coral reef ecosystem to extreme environmental conditions , 2021, Biogeosciences.

[7]  S. Sandin,et al.  Increasing Coral Reef Resilience Through Successive Marine Heatwaves , 2021, Geophysical Research Letters.

[8]  J. M. Deutsch,et al.  Metabolomics of healthy and stony coral tissue loss disease affected Montastraea cavernosa corals , 2021, bioRxiv.

[9]  Wenxu Zhou,et al.  How Symbiodiniaceae meets the challenges of life during coral bleaching , 2021, Coral Reefs.

[10]  R. Gates,et al.  Preconditioning improves bleaching tolerance in the reef‐building coral Pocillopora acuta through modulations in the programmed cell death pathways , 2021, Molecular ecology.

[11]  D. Barshis,et al.  Fast and pervasive transcriptomic resilience and acclimation of extremely heat-tolerant coral holobionts from the northern Red Sea , 2021, Proceedings of the National Academy of Sciences.

[12]  Debolina Sarkar,et al.  Elucidation of trophic interactions in an unusual single-cell nitrogen-fixing symbiosis using metabolic modeling , 2021, PLoS Comput. Biol..

[13]  M. Shokri,et al.  The enhanced expression of heat stress-related genes in scleractinian coral ‘Porites harrisoni’ during warm episodes as an intrinsic mechanism for adaptation in ‘the Persian Gulf’ , 2021, Coral Reefs.

[14]  Ralf J. M. Weber,et al.  Species-Specific Variations in the Metabolomic Profiles of Acropora hyacinthus and Acropora millepora Mask Acute Temperature Stress Effects in Adult Coral Colonies , 2021, Frontiers in Marine Science.

[15]  M. Pernice,et al.  Symbiont shuffling across environmental gradients aligns with changes in carbon uptake and translocation in the reef-building coral Pocillopora acuta , 2021, Coral Reefs.

[16]  C. Wild,et al.  Heat stress destabilizes symbiotic nutrient cycling in corals , 2021, Proceedings of the National Academy of Sciences.

[17]  D. Bhattacharya,et al.  Metabolomic shifts associated with heat stress in coral holobionts , 2021, Science Advances.

[18]  N. Baliga,et al.  Contrasting heat stress response patterns of coral holobionts across the Red Sea suggest distinct mechanisms of thermal tolerance , 2020, Molecular ecology.

[19]  James L. Hench,et al.  Increasing comparability among coral bleaching experiments , 2020, Ecological applications : a publication of the Ecological Society of America.

[20]  M. Kühl,et al.  Divergent expression of hypoxia response systems under deoxygenation in reef‐forming corals aligns with bleaching susceptibility , 2020, Global change biology.

[21]  A. Baker,et al.  Host genotype and stable differences in algal symbiont communities explain patterns of thermal stress response of Montipora capitata following thermal pre-exposure and across multiple bleaching events , 2020, Coral Reefs.

[22]  V. Weis,et al.  The Molecular Language of the Cnidarian-Dinoflagellate Symbiosis. , 2020, Trends in microbiology.

[23]  U. Roessner,et al.  Metabolite pools of the reef building coral Montipora capitata are unaffected by Symbiodiniaceae community composition , 2020, Coral Reefs.

[24]  Danwei Huang,et al.  Gene Expression and Photophysiological Changes in Pocillopora acuta Coral Holobiont Following Heat Stress and Recovery , 2020, Microorganisms.

[25]  A. Baker,et al.  Host genotype and stable differences in algal symbiont communities explain patterns of thermal stress response of Montipora capitata following thermal pre-exposure and across multiple bleaching events , 2020, Coral Reefs.

[26]  D. Barshis,et al.  Standardized short‐term acute heat stress assays resolve historical differences in coral thermotolerance across microhabitat reef sites , 2020, Global change biology.

[27]  A. D. Jones,et al.  Metabolomic signatures of coral bleaching history , 2020, Nature Ecology & Evolution.

[28]  J. Oakeshott,et al.  Heat-evolved microalgal symbionts increase coral bleaching tolerance , 2020, Science Advances.

[29]  Danwei Huang,et al.  The contribution of stress-tolerant endosymbiotic dinoflagellate Durusdinium to Pocillopora acuta survival in a highly urbanized reef system , 2020, Coral Reefs.

[30]  R. Toonen,et al.  Abundance, size, and survival of recruits of the reef coral Pocillopora acuta under ocean warming and acidification , 2020, PloS one.

[31]  F. Houlbrèque,et al.  Corals exhibit distinct patterns of microbial reorganisation to thrive in an extreme inshore environment , 2020, Coral Reefs.

[32]  E. Howells,et al.  Corals in the hottest reefs in the world exhibit symbiont fidelity not flexibility , 2020, Molecular ecology.

[33]  M. V. van Oppen,et al.  Symbiodiniaceae-bacteria interactions: rethinking metabolite exchange in reef-building corals as multi-partner metabolic networks. , 2020, Environmental microbiology.

[34]  C. Drury.  Resilience in reef‐building corals: The ecological and evolutionary importance of the host response to thermal stress , 2019, Molecular ecology.

[35]  H. Cabral,et al.  Oxidative stress on scleractinian coral fragments following exposure to high temperature and low salinity , 2019 .

[36]  David J. Smith,et al.  Coral bleaching patterns are the outcome of complex biological and environmental networking , 2019, Global change biology.

[37]  J. Brandsma,et al.  Lipidome analysis of Symbiodiniaceae reveals possible mechanisms of heat stress tolerance in reef coral symbionts , 2019, Coral Reefs.

[38]  A. Huete,et al.  Mangrove lagoons of the Great Barrier Reef support coral populations persisting under extreme environmental conditions , 2019, Marine Ecology Progress Series.

[39]  S. Palumbi,et al.  Using naturally occurring climate resilient corals to construct bleaching-resistant nurseries , 2019, Proceedings of the National Academy of Sciences.

[40]  Hugh J. M. Warrington,et al.  SymPortal: A novel analytical framework and platform for coral algal symbiont next‐generation sequencing ITS2 profiling , 2019, Molecular ecology resources.

[41]  A. Alfaro,et al.  Itaconic acid inhibits growth of a pathogenic marine Vibrio strain: A metabolomics approach , 2019, Scientific Reports.

[42]  P. Ralph,et al.  Mass coral bleaching of P. versipora in Sydney Harbour driven by the 2015–2016 heatwave , 2019, Coral Reefs.

[43]  M. V. van Oppen,et al.  Relative stability of the Pocillopora acuta microbiome throughout a thermal stress event , 2019, Coral Reefs.

[44]  D. Burkepile,et al.  A global analysis of coral bleaching over the past two decades , 2019, Nature Communications.

[45]  Mrinalini,et al.  Short Term Exposure to Heat and Sediment Triggers Changes in Coral Gene Expression and Photo-Physiological Performance , 2019, Front. Mar. Sci..

[46]  M. V. van Oppen,et al.  Relative stability of the Pocillopora acuta microbiome throughout a thermal stress event , 2019, Coral Reefs.

[47]  M. Shokri,et al.  Extremophile symbionts in extreme environments; a contribution to the diversity of Symbiodiniaceae across the northern Persian Gulf and Gulf of Oman , 2019, Journal of Sea Research.

[48]  U. Roessner,et al.  Partner switching and metabolic flux in a model cnidarian–dinoflagellate symbiosis , 2018, Proceedings of the Royal Society B.

[49]  P. Schmitt‐Kopplin,et al.  Coral metabolite gradients affect microbial community structures and act as a disease cue , 2018, Communications Biology.

[50]  Victoria Barker,et al.  Exceptional Thermal Tolerance of Coral Reefs in American Samoa: a Review , 2018, Current Climate Change Reports.

[51]  Y. Yokoyama,et al.  A simple role of coral-algal symbiosis in coral calcification based on multiple geochemical tracers , 2018, Geochimica et Cosmochimica Acta.

[52]  M. Matz,et al.  Contrasting effects of Symbiodinium identity on coral host transcriptional profiles across latitudes , 2018, Molecular ecology.

[53]  M. Medina,et al.  Intra- and interspecific variation and phenotypic plasticity in thylakoid membrane properties across two Symbiodinium clades , 2018, Coral Reefs.

[54]  David S. Wishart,et al.  MetaboAnalyst 4.0: towards more transparent and integrative metabolomics analysis , 2018, Nucleic Acids Res..

[55]  T. Hughes,et al.  Global warming transforms coral reef assemblages , 2018, Nature.

[56]  A. Alfaro,et al.  Metabolomics Study of Immune Responses of New Zealand Greenshell™ Mussels (Perna canaliculus) Infected with Pathogenic Vibrio sp. , 2018, Marine Biotechnology.

[57]  A. Alfaro,et al.  Metabolomics Study of Immune Responses of New Zealand Greenshell™ Mussels (Perna canaliculus) Infected with Pathogenic Vibrio sp. , 2018, Marine Biotechnology.

[58]  P. Heraud,et al.  Single-Cell Biomolecular Analysis of Coral Algal Symbionts Reveals Opposing Metabolic Responses to Heat Stress and Expulsion , 2018, Front. Mar. Sci..

[59]  David J. Smith,et al.  The Future of Coral Reefs Subject to Rapid Climate Change: Lessons from Natural Extreme Environments , 2018, Front. Mar. Sci..

[60]  S. Palumbi,et al.  Mechanisms of Thermal Tolerance in Reef-Building Corals across a Fine-Grained Environmental Mosaic: Lessons from Ofu, American Samoa , 2018, Front. Mar. Sci..

[61]  U. Roessner,et al.  13C metabolomics reveals widespread change in carbon fate during coral bleaching , 2017, Metabolomics.

[62]  P. Thomé,et al.  Experimentally Induced Bleaching in the Sea Anemone Exaiptasia Supports Glucose as a Main Metabolite Associated with Its Symbiosis , 2017 .

[63]  U. Roessner,et al.  Optimal nutrient exchange and immune responses operate in partner specificity in the cnidarian-dinoflagellate symbiosis , 2017, Proceedings of the National Academy of Sciences.

[64]  S. Palumbi,et al.  Genomic models predict successful coral adaptation if future ocean warming rates are reduced , 2017, Science Advances.

[65]  D. Suggett,et al.  Symbiotic Dinoflagellate Functional Diversity Mediates Coral Survival under Ecological Crisis. , 2017, Trends in ecology & evolution.

[66]  T. Ravasi,et al.  Rapid adaptive responses to climate change in corals , 2017 .

[67]  M. Garren,et al.  Responses of Coral-Associated Bacterial Communities to Local and Global Stressors , 2017, Front. Mar. Sci..

[68]  S. Villas-Bôas,et al.  Differential expression of novel metabolic and immunological biomarkers in oysters challenged with a virulent strain of OsHV‐1 , 2017, Developmental and comparative immunology.

[69]  D. Tchernov,et al.  Physiological and Biogeochemical Responses of Super-Corals to Thermal Stress from the Northern Gulf of Aqaba, Red Sea , 2017, Front. Mar. Sci..

[70]  M. Scheffer,et al.  Coral reefs in the Anthropocene , 2017, Nature.

[71]  David J. Smith,et al.  Reef-building corals thrive within hot-acidified and deoxygenated waters , 2017, Scientific Reports.

[72]  Shaun P. Wilkinson,et al.  Metabolite profiling of symbiont and host during thermal stress and bleaching in the coral Acropora aspera , 2017, Coral Reefs.

[73]  S. Palumbi,et al.  Bacterial community dynamics are linked to patterns of coral heat tolerance , 2017, Nature Communications.

[74]  Y. Loya,et al.  Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change , 2016, Proceedings of the National Academy of Sciences.

[75]  Paul E. Anderson,et al.  Metabolomic signatures of increases in temperature and ocean acidification from the reef-building coral, Pocillopora damicornis , 2016, Metabolomics.

[76]  S. Palumbi,et al.  Gene Networks in the Wild: Identifying Transcriptional Modules that Mediate Coral Resistance to Experimental Heat Stress , 2015, Genome biology and evolution.

[77]  Roman Stocker,et al.  Temperature-induced behavioral switches in a bacterial coral pathogen , 2015, The ISME Journal.

[78]  M. Stat,et al.  Limits to the thermal tolerance of corals adapted to a highly fluctuating, naturally extreme temperature environment , 2015, Scientific Reports.

[79]  Oleg Simakov,et al.  The genome of Aiptasia, a sea anemone model for coral symbiosis , 2015, Proceedings of the National Academy of Sciences.

[80]  S. Palumbi,et al.  Rapid Acclimation Ability Mediated by Transcriptome Changes in Reef-Building Corals , 2015, Genome biology and evolution.

[81]  R. Stocker,et al.  Increased seawater temperature increases the abundance and alters the structure of natural Vibrio populations associated with the coral Pocillopora damicornis , 2015, Front. Microbiol..

[82]  M. Teece,et al.  Taxonomic and Environmental Variation of Metabolite Profiles in Marine Dinoflagellates of the Genus Symbiodinium , 2015, Metabolites.

[83]  B. Humbel,et al.  Subcellular Investigation of Photosynthesis-Driven Carbon Assimilation in the Symbiotic Reef Coral Pocillopora damicornis , 2015, mBio.

[84]  Yohei Matsui,et al.  The cumulative impact of annual coral bleaching can turn some coral species winners into losers , 2014, Global change biology.

[85]  M. Sogin,et al.  Minimum entropy decomposition: Unsupervised oligotyping for sensitive partitioning of high-throughput marker gene sequences , 2014, The ISME Journal.

[86]  S. Palumbi,et al.  Mechanisms of reef coral resistance to future climate change , 2014, Science.

[87]  Matthew S. Burriesci,et al.  Extensive Differences in Gene Expression Between Symbiotic and Aposymbiotic Cnidarians , 2013, G3: Genes, Genomes, Genetics.

[88]  T. Oliver,et al.  Genomic basis for coral resilience to climate change , 2013, Proceedings of the National Academy of Sciences.

[89]  L. Mydlarz,et al.  Variations in Reactive Oxygen Release and Antioxidant Activity in Multiple Symbiodinium Types in Response to Elevated Temperature , 2012, Microbial Ecology.

[90]  Hao Song,et al.  Metabolome Profiling Reveals Metabolic Cooperation between Bacillus megaterium and Ketogulonicigenium vulgare during Induced Swarm Motility , 2011, Applied and Environmental Microbiology.

[91]  Jianguo Xia,et al.  Web-based inference of biological patterns, functions and pathways from metabolomic data using MetaboAnalyst , 2011, Nature Protocols.

[92]  P. Thomé,et al.  Differential stability of photosynthetic membranes and fatty acid composition at elevated temperature in Symbiodinium , 2011, Coral Reefs.

[93]  T. Oliver,et al.  Do fluctuating temperature environments elevate coral thermal tolerance? , 2011, Coral Reefs.

[94]  N. Tuteja,et al.  Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. , 2010, Plant physiology and biochemistry : PPB.

[95]  S. Villas-Bôas,et al.  Analytical platform for metabolome analysis of microbial cells using methyl chloroformate derivatization followed by gas chromatography–mass spectrometry , 2010, Nature Protocols.

[96]  Ning Ma,et al.  BLAST+: architecture and applications , 2009, BMC Bioinformatics.

[97]  M. Holcomb,et al.  Why corals care about ocean acidification : uncovering the mechanism , 2009 .

[98]  Martin Hartmann,et al.  Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities , 2009, Applied and Environmental Microbiology.

[99]  Ray Berkelmans,et al.  The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change , 2006, Proceedings of the Royal Society B: Biological Sciences.

[100]  M. Lesser.  Oxidative stress in marine environments: biochemistry and physiological ecology. , 2006, Annual review of physiology.

[101]  David J. Smith,et al.  Is photoinhibition of zooxanthellae photosynthesis the primary cause of thermal bleaching in corals? , 2005 .

[102]  James H. Brown,et al.  Toward a metabolic theory of ecology , 2004 .

[103]  B. H. Buck,et al.  The Impact of Bleaching on the Metabolic Contribution of Dinoflagellate Symbionts to their Giant Clam Host , 2003 .

[104]  W. Dunlap,et al.  An unusual vitamin E constituent (α-tocomonoenol) provides enhanced antioxidant protection in marine organisms adapted to cold-water environments , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[105]  J. Mcmanus,et al.  Environmental limits to coral reef development: Where do we draw the line? , 1999 .

[106]  S. Coles,et al.  Response of Hawaiian and other Indo-Pacific reef corals to elevated temperature , 1990, Coral Reefs.

[107]  E. Majerová,et al.  A BI-1 mediated cascade improves redox homeostasis during thermal stress and prevents oxidative damage in a preconditioned reef-building coral , 2021 .

[108]  T. Essington,et al.  Management for network diversity speeds evolutionary adaptation to climate change , 2019, Nature Climate Change.

[109]  U. Roessner,et al.  13C metabolomics reveals widespread change in carbon fate during coral bleaching , 2017, Metabolomics.

[110]  R. Gates,et al.  Clade D Symbiodinium in Scleractinian Corals: A “Nugget” of Hope, a Selfish Opportunist, an Ominous Sign, or All of the Above? , 2011 .