Elucidating gene expression adaptation of phylogenetically divergent coral holobionts under heat stress (original) (raw)
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Authorea (Authorea), 2023
Coral reef health is tightly connected to the coral microbiome. Coral bleaching and disease outbreaks have caused an unprecedented loss in coral cover worldwide, particularly correlated to a warming ocean. Coping mechanisms of the coral holobiont under high temperatures are not completely described, but the associated microbial community is a potential source of acquired heat-tolerance. The relationship between stress and stability in the microbiome is key to understanding the role that the coral microbiome plays in thermal tolerance. According to the Anna Karenina Principle (AKP), stress or disease will increase instability and stochasticity among animal microbiomes. Here we investigate whether heat stress results in microbiomes that follow the AKP. We used shotgun metagenomics in an experimental setting to understand the dynamics of microbial taxa and genes in the surface mucous layer (SML) microbiome of the coral Pseudodiploria strigosa under heat treatment. The metagenomes of corals exposed to heat stress showed high similarity, indicating a deterministic and stable response of the coral microbiome to disturbance, in opposition to the AKP. We hypothesize that this stability is the result of a selective pressure towards a coral microbiome that is assisting the holobiont to withstand heat stress. The coral SML microbiome responded to heat stress with an increase in the relative abundance of taxa with probiotic potential, and functional genes for nitrogen and sulfur acquisition. These consistent and specific microbial taxa and gene functions that significantly increased in proportional abundance in corals exposed to heat are potentially beneficial to coral health and thermal resistance.
Warming oceans disrupt the critical endosymbiosis between corals and their photosynthetic dinoflagellate endosymbionts of the family Symbiodiniaceae. Durusdinium trenchii is a heat-tolerant species of Symbiodiniaceae and enhances survival of its coral host, but the basis for tolerance is largely unknown. To identify the underpinnings of heat tolerance and symbiosis, we compared the in hospite and free-living transcriptomes of D. trenchii under stable temperature conditions and acute hyperthermal stress. We discovered that under stable conditions, in hospite cells exhibit lower transcriptional activity than free-living counterparts, suggesting the shutdown of genes uniquely required for a free-living lifestyle. However, under hyperthermal stress the transcriptional response was larger in hospite, indicating an exacerbated stress environment within the host cell. Significantly, we unraveled the molecular signatures of symbiont heat tolerance within the host, which is a critical step t...
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.
Bacterial community dynamics are linked to patterns of coral heat tolerance
Nature communications, 2017
Ocean warming threatens corals and the coral reef ecosystem. Nevertheless, corals can be adapted to their thermal environment and inherit heat tolerance across generations. In addition, the diverse microbes that associate with corals have the capacity for more rapid change, potentially aiding the adaptation of long-lived corals. Here, we show that the microbiome of reef corals is different across thermally variable habitats and changes over time when corals are reciprocally transplanted. Exposing these corals to thermal bleaching conditions changes the microbiome for heat-sensitive corals, but not for heat-tolerant corals growing in habitats with natural high heat extremes. Importantly, particular bacterial taxa predict the coral host response in a short-term heat stress experiment. Such associations could result from parallel responses of the coral and the microbial community to living at high natural temperatures. A competing hypothesis is that the microbial community and coral he...
PLOS ONE, 2015
Tropical reef-building coral stress levels will intensify with the predicted rising atmospheric CO 2 resulting in ocean temperature and acidification increase. Most studies to date have focused on the destabilization of coral-dinoflagellate symbioses due to warming oceans, or declining calcification due to ocean acidification. In our study, pH and temperature conditions consistent with the end-of-century scenarios of the Intergovernmental Panel on Climate Change (IPCC) caused major changes in photosynthesis and respiration, in addition to decreased calcification rates in the coral Acropora millepora. Population density of symbiotic dinoflagellates (Symbiodinium) under high levels of ocean acidification and temperature (Representative Concentration Pathway, RCP8.5) decreased to half of that found under present day conditions, with photosynthetic and respiratory rates also being reduced by 40%. These physiological changes were accompanied by evidence for gene regulation of calcium and bicarbonate transporters along with components of the organic matrix. Metatranscriptomic RNA-Seq data analyses showed an overall down regulation of metabolic transcripts, and an increased abundance of transcripts involved in circadian clock control, controlling the damage of oxidative stress, calcium signaling/homeostasis, cytoskeletal interactions, transcription regulation, DNA repair, Wnt signaling and apoptosis/immunity/ toxins. We suggest that increased maintenance costs under ocean acidification and warming, and diversion of cellular ATP to pH homeostasis, oxidative stress response, UPR and DNA repair, along with metabolic suppression, may underpin why Acroporid species tend not to thrive under future environmental stress. Our study highlights the potential increased energy demand when the coral holobiont is exposed to high levels of ocean warming and acidification.
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.
Understanding the potential for coral adaptation to warming seas is complicated by interactions between symbiotic partners that define stress responses and the difficulties of tracking selection in natural populations. To overcome these challenges, we characterized the contribution of both animal host and symbiotic algae to thermal tolerance in corals that have already experienced considerable warming on par with end-of-century projections for most coral reefs. Thermal responses in Platygyra daedalea corals from the hot Persian Gulf where summer temperatures reach 36°C were compared with conspecifics from the milder Sea of Oman. Persian Gulf corals had higher rates of survival at elevated temperatures (33 and 36°C) in both the nonsymbiotic larval stage (32–49% higher) and the symbiotic adult life stage (51% higher). Additionally, Persian Gulf hosts had fixed greater potential to mitigate oxidative stress (31–49% higher) and their Symbiodinium partners had better retention of photosynthetic performance under elevated temperature (up to 161% higher). Superior thermal tolerance of Persian Gulf vs. Sea of Oman corals was maintained after 6-month acclimatization to a common ambient environment and was underpinned by genetic divergence in both the coral host and symbiotic algae. In P. daedalea host samples, genomewide SNP variation clustered into two discrete groups corresponding with Persian Gulf and Sea of Oman sites. Symbiodinium within host tissues predominantly belonged to ITS2 rDNA type C3 in the Persian Gulf and type D1a in the Sea of Oman contradicting patterns of Sym-biodinium thermal tolerance from other regions. Our findings provide evidence that genetic adaptation of both host and Symbiodinium has enabled corals to cope with extreme temperatures in the Persian Gulf. Thus, the persistence of coral populations under continued warming will likely be determined by evolutionary rates in both, rather than single, symbiotic partners.
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.
Gene expression plasticity and frontloading promote thermotolerance in Pocillopora corals
Ecosystems worldwide are suffering from climate change. Coral reef ecosystems are globally threatened by increasing sea surface temperatures. However, gene expression plasticity provides the potential for organisms to respond rapidly and effectively to environmental changes, and would be favored in variable environments. In this study, we investigated the thermal stress response in Pocillopora coral colonies from two contrasting thermal regimes [more stable seawater temperatures in New Caledonia (South Pacific), more variable in Oman (Persian Gulf)] by exposing them to heat stress. We compared the physiological state, bacterial and Symbionaceae communities (using 16S and ITS2 metabarcoding), and gene expression levels (using RNA-Seq) between control conditions andheat stress (the temperature just below the first signs of compromised health). Colonies from both thermal regimes remained apparently normal and presented open and colored polyps during heat stress, with no change in bacte...