Transcriptomic Changes in Coral Holobionts Provide Insights into Physiological Challenges of Future Climate and Ocean Change (original) (raw)

Major cellular and physiological impacts of ocean acidification on a reef building coral

As atmospheric levels of CO 2 increase, reef-building corals are under greater stress from both increased sea surface temperatures and declining sea water pH. To date, most studies have focused on either coral bleaching due to warming oceans or declining calcification due to decreasing oceanic carbonate ion concentrations. Here, through the use of physiology measurements and cDNA microarrays, we show that changes in pH and ocean chemistry consistent with two scenarios put forward by the Intergovernmental Panel on Climate Change (IPCC) drive major changes in gene expression, respiration, photosynthesis and symbiosis of the coral, Acropora millepora, before affects on biomineralisation are apparent at the phenotype level. Under high CO 2 conditions corals at the phenotype level lost over half their Symbiodinium populations, and had a decrease in both photosynthesis and respiration. Changes in gene expression were consistent with metabolic suppression, an increase in oxidative stress, apoptosis and symbiont loss. Other expression patterns demonstrate upregulation of membrane transporters, as well as the regulation of genes involved in membrane cytoskeletal interactions and cytoskeletal remodeling. These widespread changes in gene expression emphasize the need to expand future studies of ocean acidification to include a wider spectrum of cellular processes, many of which may occur before impacts on calcification.

Early transcriptional changes in the reef-building coral Acropora aspera in response to thermal and nutrient stress

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).

Mediterranean versus Red sea corals facing climate change, a transcriptome analysis

Scientific reports, 2017

The anthropogenic increase in atmospheric CO2 that drives global warming and ocean acidification raises serious concerns regarding the future of corals, the main carbonate biomineralizers. Here we used transcriptome analysis to study the effect of long-term gradual temperature increase (annual rate), combined with lowered pH values, on a sub-tropical Red Sea coral, Stylophora pistillata, and on a temperate Mediterranean symbiotic coral Balanophyllia europaea. The gene expression profiles revealed a strong effect of both temperature increase and pH decrease implying for synergism response. The temperate coral, exposed to a twice as high range of seasonal temperature fluctuations than the Red Sea species, faced stress more effectively. The compensatory strategy for coping apparently involves deviating cellular resources into a massive up-regulation of genes in general, and specifically of genes involved in the generation of metabolic energy. Our results imply that sub-lethal, prolonge...

CORAL RESPONSES TO ANTHROPOGENIC STRESS IN THE TWENTY-FIRST CENTURY: AN ECOPHYSIOLOGICAL PERSPECTIVE

The number of ecophysiological studies involving reef corals has increased markedly over the last 20 years, driven primarily by the concern over the potential effects of anthropogenic change on coral communities. In particular, the evaluation of the effects of global climate change has prompted major research efforts into understanding the consequences of both rising seawater temperatures and ocean acidification on the physiology of corals. In recent years the recognition that corals harbour not only symbiotic algae but also a diverse microbial consortium, which may both influence and be influenced by the physiology of the animal host, has added an extra layer of complexity to this biological system known collectively as the 'coral holobiont'. The present review draws together an extensive literature on ecophysiological responses of the coral holobiont to anthropo-genic change, with specific references to the latest molecular and genetic developments in the field. It also highlights gaps in our basic understanding of coral physiology and draws attention to the value of extreme physical habitats in elucidating the acclimatory and adaptive scope of reef corals to climate change.

Coral physiology and microbiome dynamics under combined warming and ocean acidification

PloS one, 2018

Rising seawater temperature and ocean acidification threaten the survival of coral reefs. The relationship between coral physiology and its microbiome may reveal why some corals are more resilient to these global change conditions. Here, we conducted the first experiment to simultaneously investigate changes in the coral microbiome and coral physiology in response to the dual stress of elevated seawater temperature and ocean acidification expected by the end of this century. Two species of corals, Acropora millepora containing the thermally sensitive endosymbiont C21a and Turbinaria reniformis containing the thermally tolerant endosymbiont Symbiodinium trenchi, were exposed to control (26.5°C and pCO2 of 364 μatm) and treatment (29.0°C and pCO2 of 750 μatm) conditions for 24 days, after which we measured the microbial community composition. These microbial findings were interpreted within the context of previously published physiological measurements from the exact same corals in th...

Coral resilience to ocean acidification and global warming through pH up-regulation

Nature Climate Change, 2012

Rapidly rising levels of atmospheric CO 2 are not only causing ocean warming, but also lowering seawater pH hence the carbonate saturation state of the oceans, on which many marine organisms depend to calcify their skeletons 1,2 . Using boron isotope systematics 3 , we show how scleractinian corals up-regulate pH at their site of calcification such that internal changes are approximately one-half of those in ambient seawater. This species-dependent pH-buffering capacity enables aragonitic corals to raise the saturation state of their calcifying medium, thereby increasing calcification rates at little additional energy cost. Using a model of pH regulation combined with abiotic calcification, we show that the enhanced kinetics of calcification owing to higher temperatures has the potential to counter the effects of ocean acidification. Up-regulation of pH, however, is not ubiquitous among calcifying organisms; those lacking this ability are likely to undergo severe declines in calcification as CO 2 levels increase. The capacity to up-regulate pH is thus central to the resilience of calcifiers to ocean acidification, although the fate of zooxanthellate corals ultimately depends on the ability of both the photosymbionts and coral host to adapt to rapidly increasing ocean temperatures 4 .

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.

Gene Expression Signatures of Energetic Acclimatisation in the Reef Building Coral Acropora millepora

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.

Evaluation of the current understanding of the impact of climate change on coral physiology after three decades of experimental research

Communications Biology

After three decades of coral research on the impacts of climate change, there is a wide consensus on the adverse effects of heat-stress, but the impacts of ocean acidification (OA) are not well established. Using a review of published studies and an experimental analysis, we confirm the large species-specific component of the OA response, which predicts moderate impacts on coral physiology and pigmentation by 2100 (scenario-B1 or SSP2-4.5), in contrast with the severe disturbances induced by only +2 °C of thermal anomaly. Accordingly, global warming represents a greater threat for coral calcification than OA. The incomplete understanding of the moderate OA response relies on insufficient attention to key regulatory processes of these symbioses, particularly the metabolic dependence of coral calcification on algal photosynthesis and host respiration. Our capacity to predict the future of coral reefs depends on a correct identification of the main targets and/or processes impacted by ...

Physiological resilience of a temperate soft coral to ocean warming and acidification

Cell stress & chaperones, 2018

Atmospheric concentration of carbon dioxide (CO) is increasing at an unprecedented rate and subsequently leading to ocean acidification. Concomitantly, ocean warming is intensifying, leading to serious and predictable biological impairments over marine biota. Reef-building corals have proven to be very vulnerable to climate change, but little is known about the resilience of non-reef-building species. In this study, we investigated the effects of ocean warming and acidification on the antioxidant enzyme activity (CAT-catalase, and GST-glutathione S-transferase), lipid peroxidation (using malondialdehyde, MDA-levels as a biomarker) and heat shock response (HSP70/HSC70 content) of the octocoral Veretillum cynomorium. After 60 days of acclimation, no mortalities were registered in all treatments. Moreover, CAT and GST activities, as well as MDA levels, did not change significantly under warming and/or acidification. Heat shock response was significantly enhanced under warming, but high...