Coral geochemical response to uplift in the aftermath of the 2005 Nias-Simeulue earthquake.

On 28 March 2005, the Indonesian islands of Nias and Simeulue experienced a powerful Mw 8.6 earthquake and coseismic uplift and subsidence. In areas of coastal uplift (up to ~ 2.8 m), fringing reef coral communities were killed by exposure, while deeper corals that survived were subjected to habitats with altered runoff, sediment and nutrient regimes. Here we present time-series (2000-2009) of Mn/Ca, Y/Ca and Ba/Ca variability in massive Porites corals from Nias to assess the environmental impact of a wide range of vertical displacement (+ 2.5 m to - 0.4 m). High-resolution LA-ICP-MS measurements show that skeletal Mn/Ca increased at uplifted sites, regardless of reef type, indicating a post-earthquake increase in suspended sediment delivery. Transient and/or long-term increases in skeletal Y/Ca at all uplift sites support the idea of increased sediment delivery. Coral Mn/Ca and Ba/Ca in lagoonal environments highlight the additional influences of reef bathymetry, wind-driven sediment resuspension, and phytoplankton blooms on coral geochemistry. Together, the results show that the Nias reefs adapted to fundamentally altered hydrographic conditions. We show how centuries of repeated subsidence and uplift during great-earthquake cycles along the Sunda megathrust may have shaped the modern-day predominance of massive scleractinian corals on the West Sumatran reefs.

Global warming-related response after bacterial challenge in Astroides calycularis, a Mediterranean thermophilic coral.

A worldwide increase in the prevalence of coral diseases and mortality has been linked to ocean warming due to changes in coral-associated bacterial communities, pathogen virulence, and immune system function. In the Mediterranean basin, the worrying upward temperature trend has already caused recurrent mass mortality events in recent decades. To evaluate how elevated seawater temperatures affect the immune response of a thermophilic coral species, colonies of Astroides calycularis were exposed to environmental (23 °C) or elevated (28 °C) temperatures, and subsequently challenged with bacterial lipopolysaccharides (LPS). Using immunolabeling with specific antibodies, we detected the production of Toll-like receptor 4 (TLR4) and nuclear factor kappa B (NF-kB), molecules involved in coral immune responses, and heat shock protein 70 (HSP70) activity, involved in general responses to thermal stress. A histological approach allowed us to characterize the tissue sites of activation (epithelium and/or gastroderm) under different experimental conditions. The activity patterns of the examined markers after 6 h of LPS stimulation revealed an up-modulation at environmental temperature. Under warmer conditions plus LPS-challenge, TLR4-NF-kB activation was almost completely suppressed, while constituent elevated values were recorded under thermal stress only. An HSP70 up-regulation appeared in both treatments at elevated temperature, with a significantly higher activation in LPS-challenge colonies. Such an approach is useful for further understanding the molecular pathogen-defense mechanisms in corals in order to disentangle the complex interactive effects on the health of these ecologically relevant organisms related to global climate change.

Decline of a distinct coral reef holobiont community under ocean acidification.

BACKGROUND: Microbes play vital roles across coral reefs both in the environment and inside and upon macrobes (holobionts), where they support critical functions such as nutrition and immune system modulation. These roles highlight the potential ecosystem-level importance of microbes, yet most knowledge of microbial functions on reefs is derived from a small set of holobionts such as corals and sponges. Declining seawater pH - an important global coral reef stressor - can cause ecosystem-level change on coral reefs, providing an opportunity to study the role of microbes at this scale. We use an in situ experimental approach to test the hypothesis that under such ocean acidification (OA), known shifts among macrobe trophic and functional groups may drive a general ecosystem-level response extending across macrobes and microbes, leading to reduced distinctness between the benthic holobiont community microbiome and the environmental microbiome. RESULTS: We test this hypothesis using genetic and chemical data from benthic coral reef community holobionts sampled across a pH gradient from CO2 seeps in Papua New Guinea. We find support for our hypothesis; under OA, the microbiome and metabolome of the benthic holobiont community become less compositionally distinct from the sediment microbiome and metabolome, suggesting that benthic macrobe communities are colonised by environmental microbes to a higher degree under OA conditions. We also find a simplification and homogenisation of the benthic photosynthetic community, and an increased abundance of fleshy macroalgae, consistent with previously observed reef microbialisation. CONCLUSIONS: We demonstrate a novel structural shift in coral reefs involving macrobes and microbes: that the microbiome of the benthic holobiont community becomes less distinct from the sediment microbiome under OA. Our findings suggest that microbialisation and the disruption of macrobe trophic networks are interwoven general responses to environmental stress, pointing towards a universal, undesirable, and measurable form of ecosystem changed. Video Abstract.

High response diversity and conspecific density-dependence, not species interactions, drive dynamics of coral reef fish communities.

Species-to-species and species-to-environment interactions are key drivers of community dynamics. Disentangling these drivers in species-rich assemblages is challenging due to the high number of potentially interacting species (the 'curse of dimensionality'). We develop a process-based model that quantifies how intraspecific and interspecific interactions, and species' covarying responses to environmental fluctuations, jointly drive community dynamics. We fit the model to reef fish abundance time series from 41 reefs of Australia's Great Barrier Reef. We found that fluctuating relative abundances are driven by species' heterogenous responses to environmental fluctuations, whereas interspecific interactions are negligible. Species differences in long-term average abundances are driven by interspecific variation in the magnitudes of both conspecific density-dependence and density-independent growth rates. This study introduces a novel approach to overcoming the curse of dimensionality, which reveals highly individualistic dynamics in coral reef fish communities that imply a high level of niche structure.

Gene expression plasticity facilitates acclimatization of a long-lived Caribbean coral across divergent reef environments.

Local adaptation can increase fitness under stable environmental conditions. However, in rapidly changing environments, compensatory mechanisms enabled through plasticity may better promote fitness. Climate change is causing devastating impacts on coral reefs globally and understanding the potential for adaptive and plastic responses is critical for reef management. We conducted a four-year, three-way reciprocal transplant of the Caribbean coral Siderastrea siderea across forereef, backreef, and nearshore populations in Belize to investigate the potential for environmental specialization versus plasticity in this species. Corals maintained high survival within forereef and backreef environments, but transplantation to nearshore environments resulted in high mortality, suggesting that nearshore environments present strong environmental selection. Only forereef-sourced corals demonstrated evidence of environmental specialization, exhibiting the highest growth in the forereef. Gene expression profiling 3.5 years post-transplantation revealed that transplanted coral hosts exhibited profiles more similar to other corals in the same reef environment, regardless of their source location, suggesting that transcriptome plasticity facilitates acclimatization to environmental change in S. siderea. In contrast, algal symbiont (Cladocopium goreaui) gene expression showcased functional variation between source locations that was maintained post-transplantation. Our findings suggest limited acclimatory capacity of some S. siderea populations under strong environmental selection and highlight the potential limits of coral physiological plasticity in reef restoration.

Decadal demographic shifts and size-dependent disturbance responses of corals in a subtropical warming hotspot.

Long-term demographic studies at biogeographic transition zones can elucidate how body size mediates disturbance responses. Focusing on subtropical reefs in eastern Australia, we examine trends in the size-structure of corals with contrasting life-histories and zoogeographies surrounding the 2016 coral bleaching event (2010-2019) to determine their resilience and recovery capacity. We document demographic shifts, with disproportionate declines in the number of small corals and long-term persistence of larger corals. The incidence of bleaching (Pocillopora, Turbinaria) and partial mortality (Acropora, Pocillopora) increased with coral size, and bleached corals had greater risk of partial mortality. While endemic Pocillopora experienced marked declines, decadal stability of Turbinaria despite bleaching, coupled with abundance increase and bleaching resistance in Acropora indicate remarkable resilience of these taxa in the subtropics. Declines in the number of small corals and variable associations with environmental drivers indicate bottlenecks to recovery mediated by inhibitory effects of thermal extremes for Pocillopora (heat stress) and Acropora (heat and cold stress), and stimulatory effects of chlorophyll-a for Turbinaria. Although our study reveals signs of resilience, it foreshadows the vulnerability of subtropical corals to changing disturbance regimes that include marine heatwaves. Disparity in population dynamics suggest that subtropical reefs are ecologically distinct from tropical coral reefs.

Systematic review of the uncertainty of coral reef futures under climate change.

Climate change impact syntheses, such as those by the Intergovernmental Panel on Climate Change, consistently assert that limiting global warming to 1.5 °C is unlikely to safeguard most of the world's coral reefs. This prognosis is primarily based on a small subset of available models that apply similar 'excess heat' threshold methodologies. Our systematic review of 79 articles projecting coral reef responses to climate change revealed five main methods. 'Excess heat' models constituted one third (32%) of all studies but attracted a disproportionate share (68%) of citations in the field. Most methods relied on deterministic cause-and-effect rules rather than probabilistic relationships, impeding the field's ability to estimate uncertainty. To synthesize the available projections, we aimed to identify models with comparable outputs. However, divergent choices in model outputs and scenarios limited the analysis to a fraction of available studies. We found substantial discrepancies in the projected impacts, indicating that the subset of articles serving as a basis for climate change syntheses may project more severe consequences than other studies and methodologies. Drawing on insights from other fields, we propose methods to incorporate uncertainty into deterministic modeling approaches and propose a multi-model ensemble approach to generating probabilistic projections for coral reef futures.

Responses in reef-building corals to wildfire emissions: Heterotrophic plasticity and calcification.

Extreme wildfire events are on the rise globally, and although substantial wildfire emissions may find their way into the ocean, their impact on coral reefs remains uncertain. In a five-week laboratory experiment, we observed a significant reduction in photosynthesis in coral symbionts (Porites lutea) when exposed to fine particulate matter (PM2.5) from wildfires. At low PM2.5 level (2 mg L-1), the changes in δ13C and δ15N values in the host and symbiotic algae suggest reduced autotrophy and the utilization of wildfire particulates as a source of heterotrophic nutrients. This adaptive strategy, characterized by an increase in heterotrophy, sustained some aspects of coral growth (total biomass, proteins and lipids) under wildfire stress. Nevertheless, at high PM2.5 level (5 mg L-1), both autotrophy and heterotrophy significantly decreased, resulting in an imbalanced coral-algal nutritional relationship. These changes were related to light attenuation in seawater and particulate accumulation on the coral surface during PM2.5 deposition, ultimately rendering the coral growth unsustainable. Further, the calcification rates decreased by 1.5 to 1.85 times under both low and high levels of PM2.5, primarily affected by photosynthetic autotrophy rather than heterotrophy. Our study highlights a constrained heterotrophic plasticity of corals under wildfire stress. This limitation may restrict wildfire emissions as an alternative nutrient source to support coral growth and calcification, especially when oceanic food availability or autotrophy declines, as seen during bleaching induced by the warming ocean.

Synergistic response to climate stressors in coral is associated with genotypic variation in baseline expression.

As environments are rapidly reshaped due to climate change, phenotypic plasticity plays an important role in the ability of organisms to persist and is considered an especially important acclimatization mechanism for long-lived sessile organisms such as reef-building corals. Often, this ability of a single genotype to display multiple phenotypes depending on the environment is modulated by changes in gene expression, which can vary in response to environmental changes via two mechanisms: baseline expression and expression plasticity. We used transcriptome-wide expression profiling of eleven genotypes of common-gardened Acropora cervicornis to explore genotypic variation in the expression response to thermal and acidification stress, both individually and in combination. We show that the combination of these two stressors elicits a synergistic gene expression response, and that both baseline expression and expression plasticity in response to stress show genotypic variation. Additionally, we demonstrate that frontloading of a large module of coexpressed genes is associated with greater retention of algal symbionts under combined stress. These results illustrate that variation in the gene expression response of individuals to climate change stressors can persist even when individuals have shared environmental histories, affecting their performance under future climate change scenarios.

Cold-water coral energy reserves and calcification in contrasting fjord environments.

The relationship between energy reserves of cold-water corals (CWCs) and their physiological performance remains largely unknown. In addition, it is poorly understood how the energy allocation to different metabolic processes might change with projected decreasing food supply to the deep sea in the future. This study explores the temporal and spatial variations of total energy reserves (proteins, carbohydrates and lipids) of the CWC Desmophyllum dianthus and their correlation with its calcification rate. We took advantage of distinct horizontal and vertical physico-chemical gradients in Comau Fjord (Chile) and examined the changes in energy reserves over one year in an in situ reciprocal transplantation experiment (20 m vs. 300 m and fjord head vs. mouth). Total energy reserves correlated positively with calcification rates. The fast-growing deep corals had higher and less variable energy reserves, while the slower-growing shallow corals showed pronounced seasonal changes in energy reserves. Novel deep corals (transplanted from shallow) were able to quickly increase both their calcification rates and energy reserves to similar levels as native deep corals. Our study shows the importance of energy reserves in sustaining CWC growth in spite of aragonite undersaturated conditions (deep corals) in the present, and potentially also future ocean.

Host starvation and in hospite degradation of algal symbionts shape the heat stress response of the Cassiopea-Symbiodiniaceae symbiosis.

BACKGROUND: Global warming is causing large-scale disruption of cnidarian-Symbiodiniaceae symbioses fundamental to major marine ecosystems, such as coral reefs. However, the mechanisms by which heat stress perturbs these symbiotic partnerships remain poorly understood. In this context, the upside-down jellyfish Cassiopea has emerged as a powerful experimental model system. RESULTS: We combined a controlled heat stress experiment with isotope labeling and correlative SEM-NanoSIMS imaging to show that host starvation is a central component in the chain of events that ultimately leads to the collapse of the Cassiopea holobiont. Heat stress caused an increase in catabolic activity and a depletion of carbon reserves in the unfed host, concurrent with a reduction in the supply of photosynthates from its algal symbionts. This state of host starvation was accompanied by pronounced in hospite degradation of algal symbionts, which may be a distinct feature of the heat stress response of Cassiopea. Interestingly, this loss of symbionts by degradation was concealed by body shrinkage of the starving animals, resulting in what could be referred to as "invisible" bleaching. CONCLUSIONS: Overall, our study highlights the importance of the nutritional status in the heat stress response of the Cassiopea holobiont. Compared with other symbiotic cnidarians, the large mesoglea of Cassiopea, with its structural sugar and protein content, may constitute an energy reservoir capable of delaying starvation. It seems plausible that this anatomical feature at least partly contributes to the relatively high stress tolerance of these animals in rapidly warming oceans. Video Abstract.

Sponge-derived matter is assimilated by coral holobionts.

Coral reef biodiversity is maintained by a complex network of nutrient recycling among organisms. Sponges assimilate nutrients produced by other organisms like coral and algae, releasing them as particulate and dissolved matter, but to date, only a single trophic link between sponge-derived dissolved matter and a macroalgae has been identified. We sought to determine if sponge-coral nutrient exchange is reciprocal using a stable isotope 'pulse-chase' experiment to trace the uptake of 13C and 15N sponge-derived matter by the coral holobiont for three coral species (Acropora cervicornis, Orbicella faveolata, and Eunicea flexuosa). Coral holobionts incorporated 2.3-26.8x more 15N than 13C from sponge-derived matter and A. cervicornis incorporated more of both C and N than the other corals. Differential isotopic incorporation among coral species aligns with their ecophysiological characteristics (e.g., morphology, Symbiodiniaceae density). Our results elucidate a recycling pathway on coral reefs that has implications for improving coral aquaculture and management approaches.

Environmental Concentrations of Herbicide Prometryn Render Stress-Tolerant Corals Susceptible to Ocean Warming.

Global warming has caused the degradation of coral reefs around the world. While stress-tolerant corals have demonstrated the ability to acclimatize to ocean warming, it remains unclear whether they can sustain their thermal resilience when superimposed with other coastal environmental stressors. We report the combined impacts of a photosystem II (PSII) herbicide, prometryn, and ocean warming on the stress-tolerant coral Galaxea fascicularis through physiological and omics analyses. The results demonstrate that the heat-stress-induced inhibition of photosynthetic efficiency in G. fascicularis is exacerbated in the presence of prometryn. Transcriptomics and metabolomics analyses indicate that the prometryn exposure may overwhelm the photosystem repair mechanism in stress-tolerant corals, thereby compromising their capacity for thermal acclimation. Moreover, prometryn might amplify the adverse effects of heat stress on key energy and nutrient metabolism pathways and induce a stronger response to oxidative stress in stress-tolerant corals. The findings indicate that the presence of prometryn at environmentally relevant concentrations would render corals more susceptible to heat stress and exacerbate the breakdown of coral Symbiodiniaceae symbiosis. The present study provides valuable insights into the necessity of prioritizing PSII herbicide pollution reduction in coral reef protection efforts while mitigating the effects of climate change.

Fatty acid production and associated gene pathways are altered by increased salinity and dimethyl sulfoxide treatments during cryopreservation of Symbiodinium pilosum (Symbiodiniaceae).

The Symbiodinium genus is ancestral among other Symbiodiniaceae lineages with species that are both symbiotic and free living. Changes in marine ecosystems threaten their existence and crucial ecological roles. Cryopreservation offers an avenue for their long-term storage for future habitat restoration after coral bleaching. In our previous study we demonstrated that high salinity treatments of Symbiodiniaceae isolates led to changes in their fatty acid (FA) profiles and higher cell viabilities after cryopreservation. In this study, we investigated the role of increased salinity on FA production and the genes involved in FA biosynthesis and degradation pathways during the cryopreservation of Symbiodinium pilosum. Overall, there was a twofold increase in mass of FAs produced by S. pilosum after being cultured in medium with increased salinity (54 parts per thousand; ppt). Dimethyl sulfoxide (Me2SO) led to a ninefold increase of FAs in standard salinity (SS) treatment, compared to a fivefold increase in increased salinity (IS) treatments. The mass of the FA classes returned to baseline during recovery. Transcriptomic analyses showed an acyl carrier protein gene was significantly upregulated after Me2SO treatment in the SS cultures. Cytochrome P450 reductase genes were significantly down regulated after Me2SO addition in SS treatment preventing FA degradation. These changes in the expression of FA biosynthesis and degradation genes contributed to more FAs in SS treated isolates. Understanding how increased salinity changes FA production and the roles of specific genes in regulating FA pathways will help improve current freezing protocols for Symbiodiniaceae and other marine microalgae.

Algal symbiont diversity in Acropora muricata from the extreme reef of Bouraké associated with resistance to coral bleaching.

Widespread coral bleaching has generally been linked to high water temperatures at larger geographic scales. However, the bleaching response can be highly variable among individual of the same species, between different species, and across localities; what causes this variability remains unresolved. Here, we tracked bleached and non-bleached colonies of Acropora muricata to see if they recovered or died following a stress event inside the semi-enclosed lagoon of Bouraké (New Caledonia), where corals are long-term acclimatized to extreme conditions of temperature, pH and dissolved oxygen, and at a nearby control reef where conditions are more benign. We describe Symbiodiniaceae community changes based on next-generation sequencing of the ITS2 marker, metabolic responses, and energetic reserve measures (12 physiological traits evaluated) during the La Niña warm and rainy summer in 2021. Widespread coral bleaching (score 1 and 2 on the coral colour health chart) was observed only in Bouraké, likely due to the combination of the high temperatures (up to 32°C) and heavy rain. All colonies (i.e., Bouraké and reference site) associated predominantly with Symbiodinaceae from the genera Cladocopium. Unbleached colonies in Bouraké had a specific ITS2-type profile (proxies for Symbiodiniaceae genotypes), while the bleached colonies in Bouraké had the same ITS2-type profile of the reef control colonies during the stress event. After four months, the few bleached colonies that survived in Bouraké (B2) acquired the same ITS2 type profiles of the unbleached colonies in Bouraké. In terms of physiological performances, all bleached corals showed metabolic depression (e.g., Pgross and Rdark). In contrast, unbleached colonies in Bouraké maintained higher metabolic rates and energetic reserves compared to control corals. Our study suggests that Acropora muricata enhanced their resistance to bleaching thanks to specific Symbiodiniaceae associations, while energetic reserves may increase their resilience after stress.

Irradiance driven trophic plasticity in the coral Madracis pharensis from the Eastern Mediterranean.

The distribution of symbiotic scleractinian corals is driven, in part, by light availability, as host energy demands are partially met through translocation of photosynthate. Physiological plasticity in response to environmental conditions, such as light, enables the expansion of resilient phenotypes in the face of changing environmental conditions. Here we compared the physiology, morphology, and taxonomy of the host and endosymbionts of individual Madracis pharensis corals exposed to dramatically different light conditions based on colony orientation on the surface of a shipwreck at 30 m depth in the Bay of Haifa, Israel. We found significant differences in symbiont species consortia, photophysiology, and stable isotopes, suggesting that these corals can adjust multiple aspects of host and symbiont physiology in response to light availability. These results highlight the potential of corals to switch to a predominantly heterotrophic diet when light availability and/or symbiont densities are too low to sustain sufficient photosynthesis, which may provide resilience for corals in the face of climate change.

Coral thermal stress and bleaching enrich and restructure reef microbial communities via altered organic matter exudation.

Coral bleaching is a well-documented and increasingly widespread phenomenon in reefs across the globe, yet there has been relatively little research on the implications for reef water column microbiology and biogeochemistry. A mesocosm heating experiment and bottle incubation compared how unbleached and bleached corals alter dissolved organic matter (DOM) exudation in response to thermal stress and subsequent effects on microbial growth and community structure in the water column. Thermal stress of healthy corals tripled DOM flux relative to ambient corals. DOM exudates from stressed corals (heated and/or previously bleached) were compositionally distinct from healthy corals and significantly increased growth of bacterioplankton, enriching copiotrophs and putative pathogens. Together these results demonstrate how the impacts of both short-term thermal stress and long-term bleaching may extend into the water column, with altered coral DOM exudation driving microbial feedbacks that influence how coral reefs respond to and recover from mass bleaching events.

Physical and cellular impact of environmentally relevant microplastic exposure on thermally challenged Pocillopora damicornis (Cnidaria, Scleractinia).

Microplastic pollution is an increasing threat to coral reefs, which are already strongly challenged by climate change-related heat stress. Although it is known that scleractinian corals can ingest microplastic, little is known about their egestion and how microplastic exposure may impair corals at physiological and cellular levels. In addition, the effects of microplastic pollution at current environmental concentration have been little investigated to date, particularly in corals already impacted by heat stress. In this study, the combined effects of these environmental threats on Pocillopora damicornis were investigated from a physical and cellular perspective. Colonies were exposed to three concentrations of polyethylene microplastic beads (no microplastic beads: [No MP], 1 mg/L: [Low MP]; 10 mg/L: [High MP]), and two different temperatures (25 °C and 30 °C) for 72 h. No visual signs of stress in corals, such as abnormal mucus production and polyp extroflection, were recorded. At [Low MP], beads adhered to colonies were ingested but were also egested. Moreover, thermally stressed colonies showed a lower adhesion and higher egestion of microplastic beads. Coral bleaching was observed with an increase in temperature and microplastic bead concentration, as indicated by a general decrease in chlorophyll concentration and Symbiodiniaceae density. An increase in lipid peroxidation was measured in colonies exposed to [Low MP] and [High MP] and an up-regulation of stress response gene hsp70 was observed due to the synergistic interaction of both stressors. Overall, our findings showed that heat stress still represents the main threat to P. damicornis, while the effect of microplastics on coral health and physiology may be minor, especially at control temperature. However, microplastics could exacerbate the effect of thermal stress on cellular homeostasis, even at [Low MP]. While reducing ocean warming is critical for preserving coral reefs, effective management of emerging threats like microplastic pollution is equally essential.

Effects of bleaching on oxygen dynamics and energy metabolism of two Caribbean coral species.

As mass coral bleaching events become more frequent, it is increasingly important to elucidate the factors underlying coral susceptibility and survival. We measured photosynthesis, respiration, and O2 concentration at the coral tissue surface, Symbiodiniaceae genotypes, and energy metabolic enzyme activities in Agaricia agaricites and Orbicella franksi throughout experimentally-induced thermal bleaching (+3 °C). A. agaricites colonies started to bleach two days into the thermal treatment and were fully bleached between Days 19-31. In contrast, O. franksi colonies only started to bleach on Day 12 and five colonies fully bleached between Days 24-38 while the remining three colonies took up 55 days. Both species experienced decreased photosynthesis and respiration rates as bleaching progressed. As a result, daytime O2 concentration at the coral surface shifted from hyperoxia in unbleached corals to normoxia in partially bleached corals, and to near hypoxia in fully bleached corals. Additionally, nighttime tissue surface O2 concentration shifted from hypoxia to normoxia, likely resulting from decreased symbiotic algae density, respiration, and photosynthates that fuel coral aerobic respiration. Genetic profiling of internal transcribed spacer 2 (ITS2) revealed differences in Symbiodiniaceae clade proportions between control and bleached colonies. Activity levels of energy metabolic enzymes did not significantly vary between control and bleached A. agaricites, but malate dehydrogenase and strombine dehydrogenase activities were significantly higher in bleached O. franksi colonies compared to controls. These differences were driven by the three O. franksi colonies that took the longest to bleach and contained >98 % Durusdinium sp. D1. The shifts in O2 dynamics within the microhabitat of bleached corals may have important implications for the metabolism of the coral holobiont while the changes in Symbiodiniaceae ITS2 profile and the upregulation of energy metabolic enzymes identify a potential factor contributing to bleaching dynamics.

Heat-tolerant intertidal rock pool coral Porites lutea can potentially adapt to future warming.

The growing threat of global warming on coral reefs underscores the urgency of identifying heat-tolerant corals and discovering their adaptation mechanisms to high temperatures. Corals growing in intertidal rock pools that vary markedly in daily temperature may have improved heat tolerance. In this study, heat stress experiments were performed on scleractinian coral Porites lutea from subtidal habitat and intertidal rock pool of Weizhou Island in the northern South China Sea. Thermotolerance differences in corals from the two habitats and their mechanisms were explored through phenotype, physiological indicators, ITS2, 16S rRNA, and RNA sequencing. At the extremely high temperature of 34°C, rock pool P. lutea had a stronger heat tolerance than those in the subtidal habitat. The strong antioxidant capacity of the coral host and its microbial partners was important in the resistance of rock pool corals to high temperatures. The host of rock pool corals at 34°C had stronger immune and apoptotic regulation, downregulated host metabolism and disease-infection-related pathways compared to the subtidal habitat. P. lutea, in this habitat, upregulated Cladocopium C15 (Symbiodiniaceae) photosynthetic efficiency and photoprotection, and significantly increased bacterial diversity and coral probiotics, including ABY1, Ruegeria, and Alteromonas. These findings indicate that rock pool corals can tolerate high temperatures through the integrated response of coral holobionts. These corals may be 'touchstones' for future warming. Our research provides new insights into the complex mechanisms by which corals resist global warming and the theoretical basis for coral reef ecosystem restoration and selection of stress-resistant coral populations.