The regulation of thermal stress induced apoptosis in corals reveals high similarities in gene expression and function to higher animals

Kvitt, Hagit; Rosenfeld, Hanna; Tchernov, Dan

doi:10.1038/srep30359

Cited by 39 publications

(34 citation statements)

References 31 publications

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“…Despite the loss of lipids and isotopic evidence of reduced heterotrophic carbon input, bleached S. pistillata only showed a trend of declining total energy reserves (p < 0.13) and maintained its biomass (Figures 2D,E). This may be because this species is able to rapidly curb apoptosis and acclimate to sustained thermal stress when exposed to elevated temperatures (Kvitt et al, 2014(Kvitt et al, , 2016. The increase in δ 13 C s and δ 18 O s when bleached (Figures 3A,B) is consistent with decreases in calcification during bleaching due to greater equilibration with seawater DIC when calcification rates drop (McConnaughey, 1989).…”

Section: Stylophora Pistillatasupporting

confidence: 64%

Physiological and Biogeochemical Responses of Super-Corals to Thermal Stress from the Northern Gulf of Aqaba, Red Sea

2017

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Mass coral bleaching is increasing in frequency and severity, leading to the loss of coral abundance and diversity. However, some corals are less susceptible to bleaching than others and can provide a model for identifying the physiological and biogeochemical traits that underlie coral resilience to thermal stress. Corals from Eilat in the Gulf of Aqaba in the northern Red Sea do not bleach unless seawater temperatures are sustained at +6 • C or higher above their average summer maximum. This extreme thermal tolerance qualifies these as super-corals, as most corals bleach when exposed to temperatures that are only +1-2 • C above their thermal maximum. Here, we conducted a controlled bleaching experiment (+6 • C) for 37 days (equivalent to 32 • heating weeks) on three species of corals from Eilat: Stylophora pistillata, Pocillopora damicornis, and Favia favus. To assess the response of the holobiont to thermal stress, the following variables were measured on each coral: endosymbiotic algal cell density, Chlorophyll a, endosymbiotic mitotic cell division, total lipids, protein, carbohydrate, and the stable carbon (δ 13 C) and oxygen (δ 18 O) isotopic composition of the skeleton and the δ 13 C of the animal host tissue and endosymbiotic algae. While all three species appeared visibly bleached, their physiological and biogeochemical responses were species-specific. S. pistillata catabolized lipids but still maintained total energy reserves and biomass. Increases in both skeletal δ 13 C and δ 18 O indicates that calcification declined in this species. P. damicornis was the least affected by bleaching. It maintained its total energy reserves and biomass, and isotopic evidence suggests that it maintained calcification and was not dependent on heterotrophy for meeting metabolic demand when bleached. Finally, F. favus catabolized protein and carbohydrates, and suffered losses in total energy reserves and biomass. Nevertheless, isotopic evidence suggest that photosynthesis and calcification were maintained, and that this species has a high baseline heterotrophic capacity. Thus, just like their non-super-coral conspecific counterparts, maintaining energy reserves Grottoli et al.Response of Super-Corals to Thermal Stress and biomass, and heterotrophic capacity appear to be traits that underlie the thermal tolerance of these super-corals from Eilat. Given the high thermal tolerance of these super-corals, these populations could provide viable seed stock for repopulating coral losses on other reefs.

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Section: Stylophora Pistillatasupporting

confidence: 64%

Physiological and Biogeochemical Responses of Super-Corals to Thermal Stress from the Northern Gulf of Aqaba, Red Sea

2017

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“…Apoptosis has been observed to occur in both coral and algal cells during the very early stages of thermal stress (Dunn et al, 2004;Ainsworth et al, 2008Ainsworth et al, , 2011Strychar and Sammarco, 2009) and initially is localized to the gastrodermal cells that contain symbionts, suggesting that this is triggered through the initial photo-bleaching stage of the bleaching process (Ainsworth et al, 2008(Ainsworth et al, , 2011. While apoptosis is a stress response to cellular damage that results in the removal of host cells, this process increases the potential of the individual coral colony to survive by maximizing resources for the surviving cells and removing sources of ROS (Ainsworth et al, 2011;Tchernov et al, 2011;Kvitt et al, 2016).…”

Section: Coral Thermal Stress Responses and Mhwsmentioning

confidence: 99%

Marine Heatwave Hotspots in Coral Reef Environments: Physical Drivers, Ecophysiological Outcomes, and Impact Upon Structural Complexity

et al. 2019

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A changing climate is driving increasingly common and prolonged marine heatwaves (MHWs) and these extreme events have now been widely documented to severely impact marine ecosystems globally. However, MHWs have rarely been considered when examining temperature-induced degradation of coral reef ecosystems. Here we consider extreme, localized thermal anomalies, nested within broader increases in sea surface temperature, which fulfill the definitive criteria for MHWs. These acute and intense events, referred to here as MHW hotspots, are not always well represented in the current framework used to describe coral bleaching, but do have distinct ecological outcomes, including widespread bleaching, and rapid mass mortality of putatively thermally tolerant coral species. The physical drivers of these localized hotspots are discussed here, and in doing so we present a comprehensive theoretical framework that links the biological responses of the coral photo-endosymbiotic organism to extreme thermal stress and ecological changes on reefs as a consequence of MHW hotspots. We describe how the rapid onset of high temperatures drives immediate heat-stress induced cellular damage, overwhelming mechanisms that would otherwise mitigate the impact of gradually accumulated thermal stress. The warm environment, and increased light penetration of the coral skeleton due to the loss of coral tissues, coupled with coral tissue decay support rapid microbial growth in the skeletal microenvironment, resulting in the widely unrecognized consequence of rapid decay, and degeneration of the coral skeletons. This accelerated degeneration of coral skeletons on a reef scale hinder the recovery of coral populations and increase the likelihood of phase shifts toward algal dominance. We suggest that MHW hotspots, through driving rapid heatinduced mortality, compromise reefs' structural frameworks to the detriment of long term recovery. We propose that MHW hotspots be considered as a distinct class of thermal stress events in coral reefs, and that the current framework used to describe coral bleaching and mass mortality be expanded to include these. We urge further research into how coral mortality affects bioerosion by coral endoliths.

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“…Apoptosis pathway had five highly expressed DE genes; two caspases were up-regulated for Vibrio (CASP7, CASP9), TBA was down-regulated for Vibrio, P53 was up-regulated for aposymbiosis, and BIRC5 was down-regulated for aposymbiosis. Apoptosis has been proposed as a means of removing Symbiodinium during thermal bleaching (Dunn, Schnitzler, & Weis, 2007;Kvitt, Rosenfeld, & Tchernov, 2016;Pernice et al, 2011;Rodriguez-Lanetty et al, 2006) as well as clearing pathogens in the immune response (Fuess et al, 2017;Libro et al, 2013). Caspases are key initiators of apoptosis (McIlwain, Berger, & Mak, 2013).…”

Section: Apoptosis-programmed Cell Deathmentioning

confidence: 99%

Differential gene expression analysis of symbiotic and aposymbiotic Exaiptasia anemones under immune challenge with Vibrio coralliilyticus

Roesel

Vollmer

2019

Ecology and Evolution

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Anthozoans are a class of Cnidarians that includes scleractinian corals, anemones, and their relatives. Despite a global rise in disease epizootics impacting scleractinian corals, little is known about the immune response of this key group of invertebrates. To better characterize the anthozoan immune response, we used the model anemone Exaiptasia pallida to explore the genetic links between the anthozoan–algal symbioses and immunity in a two‐factor RNA‐Seq experiment using both symbiotic and aposymbiotic (menthol‐bleached) Exaiptasia pallida exposed to the bacterial pathogen Vibrio coralliilyticus . Multivariate and univariate analyses of Exaiptasia gene expression demonstrated that exposure to live Vibrio coralliilyticus had strong and significant impacts on transcriptome‐wide gene expression for both symbiotic and aposymbiotic anemones, but we did not observe strong interactions between symbiotic state and Vibrio exposure. There were 4,164 significantly differentially expressed (DE) genes for Vibrio exposure, 1,114 DE genes for aposymbiosis, and 472 DE genes for the additive combinations of Vibrio and aposymbiosis. KEGG enrichment analyses identified 11 pathways—involved in immunity (5), transport and catabolism (4), and cell growth and death (2)—that were enriched due to both Vibrio and/or aposymbiosis. Immune pathways showing strongest differential expression included complement, coagulation, nucleotide‐binding, and oligomerization domain (NOD), and Toll for Vibrio exposure and coagulation and apoptosis for aposymbiosis.

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The regulation of thermal stress induced apoptosis in corals reveals high similarities in gene expression and function to higher animals

Cited by 39 publications

References 31 publications

Physiological and Biogeochemical Responses of Super-Corals to Thermal Stress from the Northern Gulf of Aqaba, Red Sea

Physiological and Biogeochemical Responses of Super-Corals to Thermal Stress from the Northern Gulf of Aqaba, Red Sea

Marine Heatwave Hotspots in Coral Reef Environments: Physical Drivers, Ecophysiological Outcomes, and Impact Upon Structural Complexity

Differential gene expression analysis of symbiotic and aposymbiotic Exaiptasia anemones under immune challenge with Vibrio coralliilyticus

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