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1. Symbiont shuffling induces differential DNA methylation responses to thermal stress in the coral Montastraea cavernosa

   https://doi.org/10.1111/mec.16246  

   Rodriguez‐Casariego, Javier A.; Cunning, Ross; Baker, Andrew C.; Eirin‐Lopez, Jose M. (November 2021, Molecular Ecology)

   Abstract Algal symbiont shuffling in favour of more thermotolerant species has been shown to enhance coral resistance to heat‐stress. Yet, the mechanistic underpinnings and long‐term implications of these changes are poorly understood. This work studied the modifications in coral DNA methylation, an epigenetic mechanism involved in coral acclimatization, in response to symbiont manipulation and subsequent heat stress exposure. Symbiont composition was manipulated in the great star coralMontastraea cavernosathrough controlled thermal bleaching and recovery, producing paired ramets of three genets dominated by either their native symbionts (genusCladocopium) or the thermotolerant species (Durusdinium trenchi). Single‐base genome‐wide analyses showed significant modifications in DNA methylation concentrated in intergenic regions, introns and transposable elements. Remarkably, DNA methylation changes in response to heat stress were dependent on the dominant symbiont, with twice as many differentially methylated regions found in heat‐stressed corals hosting different symbionts (Cladocopiumvs.D.trenchii) compared to all other comparisons. Interestingly, while differential gene body methylation was not correlated with gene expression, an enrichment in differentially methylated regions was evident in repetitive genome regions. Overall, these results suggest that changes in algal symbionts favouring heat tolerant associations are accompanied by changes in DNA methylation in the coral host. The implications of these results for coral adaptation, along with future avenues of research based on current knowledge gaps, are discussed in the present work. 

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2. Photosymbiosis reduces the environmental stress response under a heat challenge in a facultatively symbiotic coral

   https://doi.org/10.1038/s41598-024-66057-2  

   Wuitchik, D M; Aichelman, H E; Atherton, K F; Brown, C M; Chen, X; DiRoberts, L; Pelose, G E; Tramonte, C A; Davies, S W (December 2024, Scientific Reports)

   Abstract The symbiosis between corals and dinoflagellates of the family Symbiodiniaceae is sensitive to environmental stress. The oxidative bleaching hypothesis posits that extreme temperatures lead to accumulation of photobiont-derived reactive oxygen species ROS, which exacerbates the coral environmental stress response (ESR). To understand how photosymbiosis modulates coral ESRs, these responses must be explored in hosts in and out of symbiosis. We leveraged the facultatively symbiotic coralAstrangia poculata, which offers an opportunity to uncouple the ESR across its two symbiotic phenotypes (brown, white). Colonies of both symbiotic phenotypes were exposed to three temperature treatments for 15 days: (i) control (static 18 °C), (ii) heat challenge (increasing from 18 to 30 °C), and (iii) cold challenge (decreasing from 18 to 4 °C) after which host gene expression was profiled. Cold challenged corals elicited widespread differential expression, however, there were no differences between symbiotic phenotypes. In contrast, brown colonies exhibited greater gene expression plasticity under heat challenge, including enrichment of cell cycle pathways involved in controlling photobiont growth. While this plasticity was greater, the genes driving this plasticity were not associated with an amplified environmental stress response (ESR) and instead showed patterns of a dampened ESR under heat challenge. This provides nuance to the oxidative bleaching hypothesis and suggests that, at least during the early onset of bleaching, photobionts reduce the host’s ESR under elevated temperatures inA. poculata. 

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3. Heat challenge elicits stronger physiological and gene expression responses than starvation in symbiotic Oculina arbuscula

   https://doi.org/10.1093/jhered/esac068  

   Rivera, Hanny E; Tramonte, Carlos A; Samaroo, Jason; Dickerson, Hayden; Davies, Sarah W (March 2023, Journal of Heredity)

   Zamudio, Kelly (Ed.)

   Heterotrophy has been shown to mitigate coral–algal dysbiosis (coral bleaching) under heat challenge, but the molecular mechanisms underlying this phenomenon remain largely unexplored. Here, we quantified coral physiology and gene expression of fragments from 13 genotypes of symbiotic Oculina arbuscula after a 28-d feeding experiment under (1) fed, ambient (24 °C); (2) unfed, ambient; (3) fed, heated (ramp to 33 °C); and (4) unfed, heated treatments. We monitored algal photosynthetic efficiency throughout the experiment, and after 28 d, profiled coral and algal carbohydrate and protein reserves, coral gene expression, algal cell densities, and chlorophyll-a and chlorophyll-c2 pigments. Contrary to previous findings, heterotrophy did little to mitigate the impacts of temperature, and we observed few significant differences in physiology between fed and unfed corals under heat challenge. Our results suggest the duration and intensity of starvation and thermal challenge play meaningful roles in coral energetics and stress response; future work exploring these thresholds and how they may impact coral responses under changing climate is urgently needed. Gene expression patterns under heat challenge in fed and unfed corals showed gene ontology enrichment patterns consistent with classic signatures of the environmental stress response. While gene expression differences between fed and unfed corals under heat challenge were subtle: Unfed, heated corals uniquely upregulated genes associated with cell cycle functions, an indication that starvation may induce the previously described, milder “type B” coral stress response. Future studies interested in disentangling the influence of heterotrophy on coral bleaching would benefit from leveraging the facultative species studied here, but using the coral in its symbiotic and aposymbiotic states. 

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4. Fast and pervasive transcriptomic resilience and acclimation of extremely heat-tolerant coral holobionts from the northern Red Sea

   https://doi.org/10.1073/pnas.2023298118  

   Savary, Romain; Barshis, Daniel J.; Voolstra, Christian R.; Cárdenas, Anny; Evensen, Nicolas R.; Banc-Prandi, Guilhem; Fine, Maoz; Meibom, Anders (May 2021, Proceedings of the National Academy of Sciences)

   null (Ed.)

   Corals from the northern Red Sea and Gulf of Aqaba exhibit extreme thermal tolerance. To examine the underlying gene expression dynamics, we exposed Stylophora pistillata from the Gulf of Aqaba to short-term (hours) and long-term (weeks) heat stress with peak seawater temperatures ranging from their maximum monthly mean of 27 °C (baseline) to 29.5 °C, 32 °C, and 34.5 °C. Corals were sampled at the end of the heat stress as well as after a recovery period at baseline temperature. Changes in coral host and symbiotic algal gene expression were determined via RNA-sequencing (RNA-Seq). Shifts in coral microbiome composition were detected by complementary DNA (cDNA)-based 16S ribosomal RNA (rRNA) gene sequencing. In all experiments up to 32 °C, RNA-Seq revealed fast and pervasive changes in gene expression, primarily in the coral host, followed by a return to baseline gene expression for the majority of coral (>94%) and algal (>71%) genes during recovery. At 34.5 °C, large differences in gene expression were observed with minimal recovery, high coral mortality, and a microbiome dominated by opportunistic bacteria (including Vibrio species), indicating that a lethal temperature threshold had been crossed. Our results show that the S. pistillata holobiont can mount a rapid and pervasive gene expression response contingent on the amplitude and duration of the thermal stress. We propose that the transcriptomic resilience and transcriptomic acclimation observed are key to the extraordinary thermal tolerance of this holobiont and, by inference, of other northern Red Sea coral holobionts, up to seawater temperatures of at least 32 °C, that is, 5 °C above their current maximum monthly mean. 

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5. Intersection of coral molecular responses to a localized mortality event and ex situ deoxygenation

   https://doi.org/10.1002/ece3.11275  

   Strader, Marie E; Wright, Rachel M; Pezner, Ariel K; Nuttall, Marissa F; Aichelman, Hannah E; Davies, Sarah W (April 2024, Ecology and Evolution)

   Abstract In July 2016, East Bank of Flower Garden Banks (FGB) National Marine Sanctuary experienced a localized mortality event (LME) of multiple invertebrate species that ultimately led to reductions in coral cover. Abiotic data taken directly after the event suggested that acute deoxygenation contributed to the mortality. Despite the large impact of this event on the coral community, there was no direct evidence that this LME was driven by acute deoxygenation, and thus we explored whether gene expression responses of corals to the LME would indicate what abiotic factors may have contributed to the LME. Gene expression of affected and unaffected corals sampled during the mortality event revealed evidence of the physiological consequences of the LME on coral hosts and their algal symbionts from two congeneric species (Orbicella franksiandOrbicella faveolata). Affected colonies of both species differentially regulated genes involved in mitochondrial regulation and oxidative stress. To further test the hypothesis that deoxygenation led to the LME, we measured coral host and algal symbiont gene expression in response to ex situ experimental deoxygenation (control = 6.9 ± 0.08 mg L⁻¹, anoxic = 0.083 ± 0.017 mg L⁻¹) in healthyO. faveolatacolonies from the FGB. However, this deoxygenation experiment revealed divergent gene expression patterns compared to the corals sampled during the LME and was more similar to a generalized coral environmental stress response. It is therefore likely that while the LME was connected to low oxygen, it was a series of interconnected stressors that elicited the unique gene expression responses observed here. These in situ and ex situ data highlight how field responses to stressors are unique from those in controlled laboratory conditions, and that the complexities of deoxygenation events in the field likely arise from interactions between multiple environmental factors simultaneously. 

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