Gene expression under chronic heat stress in populations of the mustard hill coral ( Porites astreoides ) from different thermal environments (original) (raw)
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Thermal and pCO2 Stress Elicit Divergent Transcriptomic Responses in a Resilient Coral
Frontiers in Marine Science, 2016
The oceans are becoming warmer and more acidic as a result of rising atmospheric pCO 2. Transcriptome plasticity may facilitate marine organisms' acclimation to thermal and acidification stress by tailoring gene expression to mitigate the impacts of these stressors. Here, we produce the first transcriptome of the abundant, ubiquitous, and resilient Caribbean reef-building coral Siderastrea siderea, and investigate this corals' transcriptomic response to 95 days of thermal (T = 25, 28, 32 • C) and CO 2-induced acidification (324, 477, 604, 2553 µatm) stress. The S. siderea transcriptome was assembled using RNAseq and then Weighted Gene Correlation Network Analysis was employed to obtain systems-level insights into the coral's stress response. Exposure of the coral to both elevated temperature and acidification elicited strong but divergent transcriptomic responses. Gene Ontology analysis suggests that long-term thermal stress disrupts homeostasis by increasing transcription of protein-coding genes associated with protein catabolism and suppressing transcription of genes involved in responding to environmental stimuli. Both next century (604 µatm) and extreme-high (2553 µatm) pCO 2 stress increased transcription of genes associated with respiration, highlighting the potentially greater energetic requirements of maintaining calcification under high-pCO 2 conditions. Under extreme-high-pCO 2 , increased transcription of H +-transporter genes was observed, consistent with the proposed role of proton transport in facilitating coral calcification under elevated pCO 2. These results suggest that 95 days of exposure to 32 • C seawater elicits a more adverse transcriptomic response (i.e., broad scale reductions in gene expression) than exposure to extreme-high acidification (2553 µatm; i.e., increased expression of genes associated with ion transport) within S. siderea-with the response to extreme warming suggesting cellular shutdown and the response to extreme acidification indicating capacity for acclimation. These results are consistent with the observation that rates of net calcification for the investigated corals were more negatively affected by the prescribed thermal stress than by the prescribed acidification stress. This study demonstrates how transcriptome plasticity may promote coral acclimation to these global change stressors, but that there are limits to the efficacy of this plasticity.
Coral Thermal Tolerance: Tuning Gene Expression to Resist Thermal Stress
PLoS ONE, 2012
The acclimatization capacity of corals is a critical consideration in the persistence of coral reefs under stresses imposed by global climate change. The stress history of corals plays a role in subsequent response to heat stress, but the transcriptomic changes associated with these plastic changes have not been previously explored. In order to identify host transcriptomic changes associated with acquired thermal tolerance in the scleractinian coral Acropora millepora, corals preconditioned to a sub-lethal temperature of 3uC below bleaching threshold temperature were compared to both non-preconditioned corals and untreated controls using a cDNA microarray platform. After eight days of hyperthermal challenge, conditions under which non-preconditioned corals bleached and preconditioned corals (thermal-tolerant) maintained Symbiodinium density, a clear differentiation in the transcriptional profiles was revealed among the condition examined. Among these changes, nine differentially expressed genes separated preconditioned corals from non-preconditioned corals, with 42 genes differentially expressed between control and preconditioned treatments, and 70 genes between non-preconditioned corals and controls. Differentially expressed genes included components of an apoptotic signaling cascade, which suggest the inhibition of apoptosis in preconditioned corals. Additionally, lectins and genes involved in response to oxidative stress were also detected. One dominant pattern was the apparent tuning of gene expression observed between preconditioned and non-preconditioned treatments; that is, differences in expression magnitude were more apparent than differences in the identity of genes differentially expressed. Our work revealed a transcriptomic signature underlying the tolerance associated with coral thermal history, and suggests that understanding the molecular mechanisms behind physiological acclimatization would be critical for the modeling of reefs in impending climate change scenarios.
PLoS ONE, 2013
Background: Understanding the mechanisms by which natural populations cope with environmental stress is paramount to predict their persistence in the face of escalating anthropogenic impacts. Reef-building corals are increasingly exposed to local and global stressors that alter nutritional status causing reduced fitness and mortality, however, these responses can vary considerably across species and populations.
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).
Molecular ecology, 2018
As climate changes, sea surface temperature anomalies that negatively impact coral reef organisms continue to increase in frequency and intensity. Yet, despite widespread coral mortality, genetic diversity remains high even in those coral species listed as threatened. While this is good news in many ways, it presents a challenge for the development of biomarkers that can identify resilient or vulnerable genotypes. Taking advantage of three coral restoration nurseries in Florida that serve as long-term common garden experiments, we exposed over 30 genetically distinct Acropora cervicornis colonies to hot and cold temperature shocks seasonally and measured pooled gene expression responses using RNAseq. Targeting a subset of 20 genes, we designed a high-throughput qPCR array to quantify expression in all individuals separately under each treatment with the goal of identifying predictive and/or diagnostic thermal stress biomarkers. We observed extensive transcriptional variation in the ...
Gene expression biomarkers of heat stress in scleractinian corals: Promises and limitations
Gene expression biomarkers (GEBs) are emerging as powerful diagnostic tools for identifying and characterizing coral stress. Their capacity to detect sublethal stress prior to the onset of signs at the organismal level that might already indicate significant damage makes them more precise and proactive compared to traditional monitoring techniques. A high number of candidate GEBs, including certain heat shock protein genes, metabolic genes, oxidative stress genes, immune response genes, ion transport genes, and structural genes have been investigated, and some genes, including hsp16, Cacna1, MnSOD, SLC26, and Nf-kB, are already showing excellent potential as reliable indicators of thermal stress in corals. In this mini-review, we synthesize the current state of knowledge of scleractinian coral GEBs and highlight gaps in our understanding that identify directions for future work. We also address the underlying sources of variation that have sometimes led to contrasting results between studies, such as differences in experimental setup and approach, intrinsic variation in the expression profiles of different experimental organisms (such as between different colonies or their algal symbionts), diel cycles, varying thermal history, and different expression thresholds. Despite advances in our understanding there is still no universally accepted biomarker of thermal stress, the molecular response of corals to heat stress is still unclear, and biomarker research in Symbiodinium still lags behind that of the host. These gaps should be addressed in future work.
Compartment-specific transcriptomics in a reef-building coral exposed to elevated temperatures
Molecular Ecology, 2014
Although rising ocean temperatures threaten scleractinian corals and the reefs they construct, certain reef corals can acclimate to elevated temperatures to which they are rarely exposed in situ. Specimens of the model Indo-Pacific reef coral Pocillopora damicornis collected from upwelling reefs of Southern Taiwan were previously found to have survived a 36-week exposure to 30°C, a temperature they encounter infrequently and one that can elicit the breakdown of the coral-dinoflagellate (genus Symbiodinium) endosymbiosis in many corals of the Pacific Ocean. To gain insight into the subcellular pathways utilized by both the coral hosts and their mutualistic Symbiodinium populations to acclimate to this temperature, mRNAs from both control (27°C) and high (30°C)-temperature samples were sequenced on an Illumina platform and assembled into a 236 435-contig transcriptome. These P. damicornis specimens were found to be~60% anthozoan and 40% microbe (Symbiodinium, other eukaryotic microbes, and bacteria), from an mRNAperspective. Furthermore, a significantly higher proportion of genes from the Symbiodinium compartment were differentially expressed after two weeks of exposure. Specifically, at elevated temperatures, Symbiodinium populations residing within the coral gastrodermal tissues were more likely to up-regulate the expression of genes encoding proteins involved in metabolism than their coral hosts. Collectively, these transcriptomescale data suggest that the two members of this endosymbiosis have distinct strategies for acclimating to elevated temperatures that are expected to characterize many of Earth's coral reefs in the coming decades.
Diagnostic gene expression biomarkers of coral thermal stress
Molecular Ecology Resources, 2014
Gene expression biomarkers can enable rapid assessment of physiological conditions in situ, providing a valuable tool for reef managers interested in linking organism physiology with large-scale climatic conditions. Here, we assessed the ability of quantitative PCR (qPCR)-based gene expression biomarkers to evaluate (i) the immediate cellular stress response (CSR) of Porites astreoides to incremental thermal stress and (ii) the magnitude of CSR and cellular homeostasis response (CHR) during a natural bleaching event. Expression levels largely scaled with treatment temperature, with the strongest responses occurring in heat-shock proteins. This is the first demonstration of a 'tiered' CSR in a coral, where the magnitude of expression change is proportional to stress intensity. Analysis of a natural bleaching event revealed no signature of an acute CSR in normal or bleached corals, indicating that the bleaching stressor(s) had abated by the day of sampling. Another long-term stress CHR-based indicator assay was significantly elevated in bleached corals, although assay values overall were low, suggesting good prospects for recovery. This study represents the first step in linking variation in gene expression biomarkers to stress tolerance and bleaching thresholds in situ by quantifying the severity of ongoing thermal stress and its accumulated long-term impacts.
Genome Biology and Evolution, 2015
Organisms respond to environmental variation partly through changes in gene expression, which underlie both homeostatic and acclimatory responses to environmental stress. In some cases, so many genes change in expression in response to different influences that understanding expression patterns for all these individual genes becomes difficult. To reduce this problem, we use a systems genetics approach to show that variation in the expression of thousands of genes of reef-building corals can be explained as variation in the expression of a small number of coexpressed "modules." Modules were often enriched for specific cellular functions and varied predictably among individuals, experimental treatments, and physiological state. We describe two transcriptional modules for which expression levels immediately after heat stress predict bleaching a day later. One of these early "bleaching modules" is enriched for sequence-specific DNA-binding proteins, particularly E26 transformation-specific (ETS)-family transcription factors. The other module is enriched for extracellular matrix proteins. These classes of bleaching response genes are clear in the modular gene expression analysis we conduct but are much more difficult to discern in single gene analyses. Furthermore, the ETS-family module shows repeated differences in expression among coral colonies grown in the same common garden environment, suggesting a heritable genetic or epigenetic basis for these expression polymorphisms. This finding suggests that these corals harbor high levels of genenetwork variation, which could facilitate rapid evolution in the face of environmental change.
Nature Communications
As coral reefs struggle to survive under climate change, it is crucial to know whether they have the capacity to withstand changing conditions, particularly increasing seawater temperatures. Thermal tolerance requires the integrative response of the different components of the coral holobiont (coral host, algal photosymbiont, and associated microbiome). Here, using a controlled thermal stress experiment across three divergent Caribbean coral species, we attempt to dissect holobiont member metatranscriptome responses from coral taxa with different sensitivities to heat stress and use phylogenetic ANOVA to study the evolution of gene expression adaptation. We show that coral response to heat stress is a complex trait derived from multiple interactions among holobiont members. We identify host and photosymbiont genes that exhibit lineage-specific expression level adaptation and uncover potential roles for bacterial associates in supplementing the metabolic needs of the coral-photosymbi...