Proteomics links the redox state to calcium signalling during bleaching of the scleractinian coral Acropora microphthalma on exposure to high solar irradiance and thermal stress (original) (raw)
Related papers
2010
Background: The success of tropical reef-building corals depends on the metabolic co-operation between the animal host and the photosynthetic performance of endosymbiotic algae residing within its cells. To examine the molecular response of the coral Acropora microphthalma to high levels of solar irradiance, a cDNA library was constructed by PCR-based suppression subtractive hybridisation (PCR-SSH) from mRNA obtained by transplantation of a colony from a depth of 12.7 m to near-surface solar irradiance, during which the coral became noticeably paler from loss of endosymbionts in sun-exposed tissues.
Comparative biochemistry and physiology. Part A, Molecular & integrative physiology, 2015
Mass coral bleaching due to thermal stress represents a major threat to the integrity and functioning of coral reefs. Thermal thresholds vary however between corals, partly as a result of the specific type of endosymbiotic dinoflagellate (Symbiodinium sp.) they harbour. The production of reactive oxygen species (ROS) in corals under thermal and light stress has been recognized as one mechanism that can lead to cellular damage and the loss of their symbiont population (Oxidative Theory of Coral Bleaching). Here, we compared the response of symbiont and host enzymatic antioxidants in the coral species Acropora millepora and Montipora digitata at 28°C and 33°C. A. millepora at 33°C showed a decrease in photochemical efficiency of photosystem II (PSII) and increase in maximum midday excitation pressure on PSII, with subsequent bleaching (declining photosynthetic pigment and symbiont density). M. digitata exhibited no bleaching response and photochemical changes in its symbionts were min...
Marine Pollution Bulletin, 2016
There has been an increase in the scale and frequency of coral bleaching around the world due mainly to changes in sea temperature. This may occur at large scales, often resulting in significant decline in coral coverage. In order to understand the molecular and cellular basis of the everincreasing incidence of coral bleaching, we have undertaken a comparative proteomic approach with the endangered Caribbean coral Acropora palmate. Using two-dimensional gel electrophoresis (2D-GE) and tandem mass spectrometry (MS/MS), we identified 285 and 321 expressed proteins in bleached and unbleached A. palmata colonies, respectively, in southwestern Puerto Rico. Overall the expression level of 38 proteins was significantly different between bleached and unbleached corals. A wide range of proteins was detected and categorized, including transcription factors involved mainly in heat stress/UV responses, immunity, apoptosis, biomineralization, the cytoskeleton, and endo-exophagocytosis. The results suggest that for bleached A. palmate, there was an induced differential protein expression response compared with those colonies that did not bleach under the same environmental conditions.
Coral Reefs, 2016
Rising seawater temperatures pose a significant threat to the persistence of coral reefs. Despite the importance of these systems, major gaps remain in our understanding of how thermal stress and bleaching affect the metabolic networks that underpin holobiont function. We applied gas chromatography-mass spectrometry (GC-MS) metabolomics to detect changes in the intracellular free metabolite pools (polar and semi-polar compounds) of in hospite dinoflagellate symbionts and their coral hosts (and any associated microorganisms) during early-and late-stage thermal bleaching (a reduction of approximately 50 and 70% in symbiont density, respectively). We detected characteristic changes to the metabolite profiles of each symbiotic partner associated with individual cellular responses to thermal, oxidative and osmotic stress, which progressed with the severity of bleaching. Alterations were also indicative of changes to energy-generating and biosynthesis pathways in both partners, with a shift to the increased catabolism of lipid stores. Specifically, in symbiont intracellular metabolite pools, we observed accumulations of multiple free fatty acids, plus the chloroplast-associated antioxidant alpha-tocopherol. In the host, we detected a decline in the abundance of pools of multiple carbohydrates, amino acids and intermediates, in addition to the antioxidant ascorbate. These findings further our understanding of the metabolic changes that occur to symbiont and host (and its associated microorganisms) during thermal bleaching. These findings also provide further insight into the largely undescribed roles of free metabolite pools in cellular homeostasis, signalling and acclimation to thermal stress in the cnidarian-dinoflagellate symbiosis. Keywords Cnidarian Á Symbiodinium Á GC-MS Á Photoinhibition Á Metabolomics Recent advances in the omics fields (genomics, transcriptomics, proteomics and metabolomics) are providing Communicated by Biology Editor Dr. Anastazia Banaszak Electronic supplementary material The online version of this article (
BMC Genomics, 2014
Background: Changes to the environment as a result of human activities can result in a range of impacts on reef building corals that include coral bleaching (reduced concentrations of algal symbionts), decreased coral growth and calcification, and increased incidence of diseases and mortality. Understanding how elevated temperatures and nutrient concentration affect early transcriptional changes in corals and their algal endosymbionts is critically important for evaluating the responses of coral reefs to global changes happening in the environment. Here, we investigated the expression of genes in colonies of the reef-building coral Acropora aspera exposed to short-term sub-lethal levels of thermal (+6°C) and nutrient stress (ammonium-enrichment: 20 μM).
Patterns of Gene Expression in a Scleractinian Coral Undergoing Natural Bleaching
Marine Biotechnology, 2010
Coral bleaching is a major threat to coral reefs worldwide and is predicted to intensify with increasing global temperature. This study represents the first investigation of gene expression in an Indo-Pacific coral species undergoing natural bleaching which involved the loss of algal symbionts. Quantitative real-time polymerase chain reaction experiments were conducted to select and evaluate coral internal control genes (ICGs), and to investigate selected coral genes of interest (GOIs) for changes in gene expression in nine colonies of the scleractinian coral Acropora millepora undergoing bleaching at Magnetic Island, Great Barrier Reef, Australia. Among the six ICGs tested, glyceraldehyde 3-phosphate dehydrogenase and the ribosomal protein genes S7 and L9 exhibited the most constant expression levels between samples from healthy-looking colonies and samples from the same colonies when severely bleached a year later. These ICGs were therefore utilised for normalisation of expression data for seven selected GOIs. Of the seven GOIs, homologues of catalase, C-type lectin and chromoprotein genes were significantly up-regulated as a result of bleaching by factors of 1.81, 1.46 and 1.61 (linear mixed models analysis of variance, P
Molecular Ecology, 2008
The declining health of coral reefs worldwide is likely to intensify in response to continued anthropogenic disturbance from coastal development, pollution, and climate change. In response to these stresses, reef-building corals may exhibit bleaching, which marks the breakdown in symbiosis between coral and zooxanthellae. Mass coral bleaching due to elevated water temperature can devastate coral reefs on a large geographical scale. In order to understand the molecular and cellular basis of bleaching in corals, we have measured gene expression changes associated with thermal stress and bleaching using a complementary DNA microarray containing 1310 genes of the Caribbean coral Montastraea faveolata. In a first experiment, we identified differentially expressed genes by comparing experimentally bleached M. faveolata fragments to control non-heat-stressed fragments. In a second experiment, we identified differentially expressed genes during a time course experiment with four time points across 9 days. Results suggest that thermal stress and bleaching in M. faveolata affect the following processes: oxidative stress, Ca 2+ homeostasis, cytoskeletal organization, cell death, calcification, metabolism, protein synthesis, heat shock protein activity, and transposon activity. These results represent the first medium-scale transcriptomic study focused on revealing the cellular foundation of thermal stress-induced coral bleaching. We postulate that oxidative stress in thermal-stressed corals causes a disruption of Ca 2+ homeostasis, which in turn leads to cytoskeletal and cell adhesion changes, decreased calcification, and the initiation of cell death via apoptosis and necrosis. Annotated differentially expressed genes from a replicate (n = 4) time course experiment (experiment 2) containing four time points. K-means clustering was performed to group genes by common temporal expression patterns. For clusters 1-4 and 7-8, only annotated genes are presented. For clusters 5 and 6, only those annotated genes that show changes in expression between time points are presented. Asterisks denote genes that were also differentially expressed in experiment 1 : *opposite patterns of gene expression, and **similar patterns of gene expression between experiments 1 and 2. All clusters are on the scale of -1 to +1 log 2 ratio (upper scale bar), except for clusters 1 and 3 (denoted by a ^), which are on the scale of -3 to +3 log 2 ratio (lower scale bar).
Scientific Reports
The proliferation of key marine ecological engineers and carbonate producers often relies on their association with photosymbiotic algae. Evaluating stress responses of these organisms is important to predict their fate under future climate projections. Physiological approaches are limited in their ability to resolve the involved molecular mechanisms and attribute stress effects to the host or symbiont, while probing and partitioning of proteins cannot be applied in organisms where the host and symbiont are small and cannot be physically separated. Here we apply a label-free quantitative proteomics approach to detect changes of proteome composition in the diatom-bearing benthic foraminifera Amphistegina gibbosa experimentally exposed to three thermal-stress scenarios. We developed a workflow for protein extraction from less than ten specimens and simultaneously analysed host and symbiont proteomes. Despite little genomic data for the host, 1,618 proteins could be partially assembled and assigned. The proteomes revealed identical pattern of stress response among stress scenarios as that indicated by physiological measurements, but allowed identification of compartment-specific stress reactions. In the symbiont, stress-response and proteolysis-related proteins were up regulated while photosynthesisrelated proteins declined. In contrast, host homeostasis was maintained through chaperone upregulation associated with elevated proteosynthesis and proteolysis, and the host metabolism shifted to heterotrophy. Most marine reef-building organisms such as corals rely on symbiosis with photosynthesizing microalgae. Tropical coral reef ecosystems are one of the structurally most complex and richest hotspots of biodiversity on Earth 1. The symbiotic relationship provides the holobiont with a clear advantage in nutrient-limited settings, but it comes at a cost of lower resilience to perturbations 2,3. Indeed, marine photosymbiotic ecosystems are threatened and decline rapidly due to human activity. Global warming is currently considered as the most damaging factor 4 , inducing bleaching responses in reef organisms, i.e. the loss of photosynthetic microalgae and/or photo-pigments 5,6. Massive bleaching events are reported more frequently, already becoming a regular occurrence 4,7. Ocean warming rarely affects marine ecosystems directly by elevated mean seawater temperature. Instead, heat stress is often induced during episodic heating events. Subsequently, research on thermal tolerance of marine photosymbiotic organisms has shifted from determining thermal limits under constant exposure to the consideration of different thermal stress frequency scenarios. Studies on photosymbiotic corals and large benthic foraminifera (LBF), i.e. photosymbiont-bearing calcifying eukaryotes, have demonstrated that, compared to chronic stress, transient heat-stress events have little immediate impact on these organisms 8-10. On the contrary, variable temperature regimes might even increase their resilience towards warming, because fluctuations may facilitate acclimatization and promote recovery from heat stress events 8,11. The possible energetic costs and
Antioxidant responses to heat and light stress differ with habitat in a common reef coral
Coral Reefs, 2015
Coral bleaching-the stress-induced collapse of the coral-Symbiodinium symbiosis-is a significant driver of worldwide coral reef degradation. Yet, not all corals are equally susceptible to bleaching, and we lack a clear understanding of the mechanisms underpinning their differential susceptibilities. Here, we focus on cellular redox regulation as a potential determinant of bleaching susceptibility in the reef coral Stylophora pistillata. Using slow heating (1°C d-1) and altered irradiance, we induced bleaching in S. pistillata colonies sampled from two depths [5-8 m (shallow) and 15-18 m (deep)]. There was significant depth-dependent variability in the timing and extent of bleaching (loss of symbiont cells), as well as in host enzymatic antioxidant activity [specifically, superoxide dismutase and catalase (CAT)]. However, among the coral fragments that bleached, most did so without displaying any evidence of a host enzymatic antioxidant response. For example, both deep and shallow corals suffered significant symbiont loss at elevated temperature, but only deep colonies exposed to high temperature and high light displayed any up-regulation of host antioxidant enzyme activity (CAT). Surprisingly, this preceded the equivalent antioxidant responses of the symbiont, which raises questions about the source(s) of hydrogen peroxide in the symbiosis. Overall, changes in enzymatic antioxidant activity in the symbionts were driven primarily by irradiance rather than temperature, and responses were similar across depth groups. Taken together, our results suggest that in the absence of light stress, heating of 1°C d-1 to 4°C above ambient is not sufficient to induce a substantial oxidative challenge in S. pistillata. We provide some of the first evidence that regulation of coral enzymatic antioxidants can vary significantly depending on habitat, and, in terms of determining bleaching susceptibility, our results suggest a significant role for the host's differential regulation of cellular redox status. Keywords Coral bleaching Á Cnidarian-dinoflagellate symbiosis Á Symbiodinium Á Stylophora pistillata Á Oxidative stress Á Climate change
Shotgun Proteomic Analysis of Thermally Challenged Reef Corals
Frontiers in Marine Science, 2021
Although coral reef ecosystems across the globe are in decline due to climate change and other anthropogenic stressors, certain inshore reefs of the Upper Florida Keys reef tract have persisted, with some even thriving, under marginalized conditions. To better understand the molecular basis of the thermotolerance displayed by these corals, a laboratory-based temperature challenge experiment that also featured conspecifics from a more stress-susceptible offshore reef was conducted with the common Caribbean reef-builder Orbicella faveolata, and the proteomes of both the coral hosts and their endosymbiotic dinoflagellate communities were profiled in (1) controls, (2) corals that succumbed to high-temperature stress and bleached, and (3) those that instead acclimated to high temperatures ex situ. Proteomic signatures varied most significantly across temperatures, host genotypes, and Symbiodiniaceae assemblages, and the two eukaryotic compartments of this mutualism exhibited distinct pro...