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1. 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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2. Local habitat heterogeneity rivals regional differences in coral thermal tolerance

   https://doi.org/10.1007/s00338-024-02484-x  

   Brown, Kristen_T; Martynek, Marcelina_P; Barott, Katie_L (April 2024, Coral Reefs)

   Abstract Variable temperature regimes that expose corals to sublethal heat stress have been recognized as a mechanism to increase coral thermal tolerance and lessen coral bleaching. However, there is a need to better understand which thermal regimes maximize coral stress hardening. Here, standardized thermal stress assays were used to determine the relative thermal tolerance of three divergent genera of corals (Acropora,Pocillopora,Porites) originating from six reef sites representing an increasing gradient of annual mean diel temperature fluctuations of 1–3 °C day⁻¹. Bleaching severity and dark-acclimated photochemical yield (i.e.,F_v/F_m) were quantified following exposure to five temperature treatments ranging from 23.0 to 36.3 °C. The greatest thermal tolerance (i.e.,F_v/F_meffective dose 50) was found at the site with intermediate mean diel temperature variability (2.2 °C day⁻¹), suggesting there is an optimal priming exposure that leads to maximal thermal tolerance. Interestingly,AcroporaandPocilloporaoriginating from the least thermally variable regimes (< 1.3 °C day⁻¹) had lower thermal tolerance than corals from the most variable sites (> 2.8 °C day⁻¹), whereas the opposite was true forPorites, suggesting divergent responses across taxa. Remarkably, comparisons across global studies revealed that the range in coral thermal tolerance uncovered in this study across a single reef (< 5 km) were as large as differences observed across vast latitudinal gradients (300–900 km). This finding indicates that local gene flow could improve thermal tolerance between habitats. However, as climate change continues, exposure to intensifying marine heatwaves is already compromising thermal priming as a mechanism to enhance coral thermal tolerance and bleaching resistance. 

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3. Positive interactions between corals and damselfish increase coral resistance to temperature stress

   https://doi.org/10.1111/gcb.16480  

   Shantz, Andrew A.; Ladd, Mark C.; Ezzat, Leila; Schmitt, Russell J.; Holbrook, Sally J.; Schmeltzer, Emily; Vega Thurber, Rebecca; Burkepile, Deron E. (October 2022, Global Change Biology)

   Abstract By the century's end, many tropical seas will reach temperatures exceeding most coral species' thermal tolerance on an annual basis. The persistence of corals in these regions will, therefore, depend on their abilities to tolerate recurrent thermal stress. Although ecologists have long recognized that positive interspecific interactions can ameliorate environmental stress to expand the realized niche of plants and animals, coral bleaching studies have largely overlooked how interactions with community members outside of the coral holobiont shape the bleaching response. Here, we subjected a common coral,Pocillopora grandis, to 10 days of thermal stress in aquaria with and without the damselfishDascyllus flavicaudus(yellowtail dascyllus), which commonly shelter within these corals, to examine how interactions with damselfish impacted coral thermal tolerance. Corals often benefit from nutrients excreted by animals they interact with and prior to thermal stress, corals grown with damselfish showed improved photophysiology (F_v/F_m) and developed larger endosymbiont populations. When exposed to thermal stress, corals with fish performed as well as control corals maintained at ambient temperatures without fish. In contrast, corals exposed to thermal stress without fish experienced photophysiological impairment, a more than 50% decline in endosymbiont density, and a 36% decrease in tissue protein content. At the end of the experiment, thermal stress caused average calcification rates to decrease by over 80% when damselfish were absent but increase nearly 25% when damselfish were present. Our study indicates that damselfish‐derived nutrients can increase coral thermal tolerance and are consistent with the Stress Gradient Hypothesis, which predicts that positive interactions become increasingly important for structuring communities as environmental stress increases. Because warming of just a few degrees can exceed corals' temperature tolerance to trigger bleaching and mortality, positive interactions could play a critical role in maintaining some coral species in warming regions until climate change is aggressively addressed. 

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4. Genetic differences in thermal tolerance among colonies of threatened coral Acropora cervicornis: potential for adaptation to increasing temperature

   https://doi.org/10.3354/meps13407  

   Yetsko, K; Ross, M; Bellantuono, A; Merselis, D; Rodriquez-Lanetty, M; Gilg, MR (July 2020, Marine Ecology Progress Series)

   null (Ed.)

   Climate change is resulting in warmer temperatures that are negatively impacting corals. Understanding how much individuals within a population vary in their thermal tolerance and whether this variation is heritable is important in determining whether a species can adapt to climate change. To address this, Acropora cervicornis fragments from 20 genetically distinct colonies collected from the Coral Restoration Foundation Tavernier nursery (Florida, USA) were kept at either ambient (28 ± 1°C) or elevated (32 ± 1°C) temperatures, and mortality was monitored for 26 d. Both broad-sense ( H 2 ) and narrow-sense ( h 2 ) heritability of thermal tolerance were estimated to determine the amount of genetic variation underlying survival to elevated temperature. To understand the physiological basis of thermal tolerance, tissue from both treatments was taken 12 h after the start of the experiment to investigate gene expression at the mRNA and protein level between tolerant and susceptible colonies. Results revealed that this population has considerable total genetic variation in thermal tolerance ( H 2 = 0.528), but low variance in relatedness among colonies prevented us from making any conclusions regarding h 2 . Despite high transcriptomic variability among and within colonies, 40 genes were consistently and significantly different between tolerant and susceptible colonies, and could be potential biomarkers for thermal tolerance should they be verified in a larger sample. Overall, the results suggest that this population has substantial genetic variation for traits that directly impact thermal tolerance; however, their response to projected increases in temperature will depend on more precise estimates of the additive components of this variation ( h 2 ). 

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5. Iron Availability Modulates the Response of Endosymbiotic Dinoflagellates to Heat Stress

   https://doi.org/10.1111/jpy.13078  

   Reich, Hannah_G; Tu, Wan‐Chen; Rodriguez, Irene_B; Chou, Yalan; Keister, Elise_F; Kemp, Dustin_W; LaJeunesse, Todd_C; Ho, Tung‐Yuan (December 2020, Journal of Phycology)

   Warming and nutrient limitation are stressors known to weaken the health of microalgae. In situations of stress, access to energy reserves can minimize physiological damage. Because of its widespread requirements in biochemical processes, iron is an important trace metal, especially for photosynthetic organisms. Lowered iron availability in oceans experiencing rising temperatures may contribute to the thermal sensitivity of reef‐building corals, which rely on mutualisms with dinoflagellates to survive. To test the influence of iron concentration on thermal sensitivity, the physiological responses of cultured symbiotic dinoflagellates (genusBreviolum; family Symbiodiniaceae) were evaluated when exposed to increasing temperatures (26 to 30°C) and iron concentrations ranging from replete (500 pM Fe’) to limiting (50 pM Fe’) under a diurnal light cycle with saturating radiance. Declines in photosynthetic efficiency at elevated temperatures indicated sensitivity to heat stress. Furthermore, five times the amount of iron was needed to reach exponential growth during heat stress (50 pM Fe′ at 26–28°C vs. 250 pM Fe′ at 30°C). In treatments where exponential growth was reached,Breviolum psygmophilumgrew faster thanB.minutum, possibly due to greater cellular contents of iron and other trace metals. The metal composition ofB.psygmophilumshifted only at the highest temperature (30°C), whereas changes inB.minutumwere observed at lower temperatures (28°C). The influence of iron availability in modulating each alga’s response to thermal stress suggests the importance of trace metals to the health of coral‐algal mutualisms. Ultimately, a greater ability to acquire scarce metals may improve the tolerance of corals to physiological stressors and contribute to the differences in performance associated with hosting one symbiont species over another. 

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