Patterns of Gene Expression in a Scleractinian Coral Undergoing Natural Bleaching

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 < 0.05), respectively. We present these genes as potential coral bleaching response genes. In contrast, three genes, including one putative ICG, showed highly variable levels of expression between coral colonies. Potential variation in microhabitat, gene function unrelated to the stress response and individualised stress responses may influence such differences between colonies and need to be better understood when designing and interpreting future studies of gene expression in natural coral populations.     

Skeletal records of community-level bleaching in Porites corals from Palau

Tropical Pacific sea surface temperature is projected to rise an additional 2–3 °C by the end of this century, driving an increase in the frequency and intensity of coral bleaching. With significant global coral reef cover already lost due to bleaching-induced mortality, efforts are underway to identify thermally tolerant coral communities that might survive projected warming. Massive, long-lived corals accrete skeletal bands of anomalously high density in response to episodes of thermal stress. These “stress bands” are potentially valuable proxies for thermal tolerance, but to date their application to questions of community bleaching history has been limited. Ecological surveys recorded bleaching of coral communities across the Palau archipelago during the 1998 and 2010 warm events. Between 2011 and 2015, we extracted skeletal cores from living Porites colonies at 10 sites spanning barrier reef and lagoon environments and quantified the proportion of stress bands present in each population during bleaching years. Across Palau, the prevalence of stress bands tracked the severity of thermal stress, with more stress bands occurring in 1998 (degree heating weeks = 13.57 °C-week) than during the less severe 2010 event (degree heating weeks = 4.86 °C-week). Stress band prevalence also varied by reef type, as more corals on the exposed barrier reef formed stress bands than did corals from sheltered lagoon environments. Comparison of Porites stress band prevalence with bleaching survey data revealed a strong correlation between percent community bleaching and the proportion of colonies with stress bands in each year. Conversely, annual calcification rates did not decline consistently during bleaching years nor did annually resolved calcification histories always track interannual variability in temperature. Our data suggest that stress bands in massive corals contain valuable information about spatial and temporal trends in coral reef bleaching and can aid in conservation efforts to identify temperature-tolerant coral reef communities.

     

Augmented coral reef monitoring using a stationary reef monitoring system

Coral reef monitoring is a reliable tool to assess the effect of climate change as corals are sensitive to increases in water temperatures between 30 °C and 35 °C resulting in bleaching - a whitening process when the corals lose their color and the reefs begin to die. Existing satellite-based monitoring products facilitate coral bleaching monitoring over large spatial scales, but their use in predicting local scale stress that influences the bleaching severity across reefs is limited. In this paper, we describe a Stationary Reef Monitoring System (SRMS) that monitors the time evolution of coral reefs through the photography of nearby coral clusters. Simultaneously, the SRMS measures and records environmental parameters such as temperature, solar irradiance (PAR), and salinity in the waters surrounding the coral colonies. When deployed in the sea, the SRMS detected a 0.1–0.4 °C variability in temperature between the in situ and satellite datasets. The SRMS uses color photography along with quantitative data on environmental parameters to monitor the health of corals and eliminates the need for physical/visual verification of coral health by a diver. By this approach, one can determine the stress thresholds of corals and identify the vulnerable and resilient reefs so as to prioritize conservation efforts.     

Corals escape bleaching in regions that recently and historically experienced frequent thermal stress

The response of coral-reef ecosystems to contemporary thermal stress may be in part a consequence of recent or historical sea-surface temperature (SST) variability. To test this hypothesis, we examined whether: (i) there was a relationship between the historical frequency of SST variability and stress experienced during the most recent thermal-stress events (in 1998 and 2005–2006) and (ii) coral reefs that historically experienced frequent thermal anomalies were less likely to experience coral bleaching during these recent thermal-stress events. Examination of nine detrended coral δ¹⁸O and Sr/Ca anomaly records revealed a high- (5.7-year) and low-frequency (>54-year) mode of SST variability. There was a positive relationship between the historical frequency of SST anomalies and recent thermal stress; sites historically dominated by the high-frequency mode experienced greater thermal stress than other sites during both events, and showed extensive coral bleaching in 1998. Nonetheless, in 2005–2006, corals at sites dominated by high-frequency variability showed reduced bleaching, despite experiencing high thermal stress. This bleaching resistance was most likely a consequence of rapid directional selection that followed the extreme thermal event of 1998. However, the benefits of regional resistance could come at the considerable cost of shifts in coral species composition.     

The microRNA expression profile in porcine skeletal muscle is changed by constant heat stress

Heat stress has profound effects on animal performance and muscle function, and microRNAs (miRNAs) play a critical role in muscle development and stress responses. To characterize the changes in miRNAs in skeletal muscle responding to heat stress, the miRNA expression profiles of longissimus dorsi muscles of pigs raised under constant heat stress (30 °C; n = 8) or control temperature (22 °C; n = 8) for 21 days were analyzed by Illumina deep sequencing. A total of 58 differentially expressed miRNAs were identified with 30 down‐regulated and 28 up‐regulated, and 63 differentially expressed target genes were predicted by miRNA–mRNA joint analysis. GO and KEGG analyses showed that the genes regulated by differentially expressed miRNAs were enriched in glucose metabolism, cytoskeletal structure and function and stress response. Real‐time PCR showed that the mRNA levels of PDK4, HSP90 and DES were significantly increased, whereas those of SCD and LDHA significantly decreased by heat exposure. The protein levels of CALM1, DES and HIF1α were also significantly increased by constant heat. These results demonstrated that the change in miRNA expression in porcine longissimus dorsi muscle underlies the changes in muscle structure and metabolism in porcine skeletal muscle affected by constant heat stress.     

Coral bleaching response index: a new tool to standardize and compare susceptibility to thermal bleaching

As coral bleaching events become more frequent and intense, our ability to predict and mitigate future events depends upon our capacity to interpret patterns within previous episodes. Responses to thermal stress vary among coral species; however the diversity of coral assemblages, environmental conditions, assessment protocols, and severity criteria applied in the global effort to document bleaching patterns creates challenges for the development of a systemic metric of taxon‐specific response. Here, we describe and validate a novel framework to standardize bleaching response records and estimate their measurement uncertainties. Taxon‐specific bleaching and mortality records (2036) of 374 coral taxa (during 1982–2006) at 316 sites were standardized to average percent tissue area affected and a taxon‐specific bleaching response index (taxon‐BRI) was calculated by averaging taxon‐specific response over all sites where a taxon was present. Differential bleaching among corals was widely variable (mean taxon‐BRI = 25.06 ± 18.44%, ±SE). Coral response may differ because holobionts are biologically different (intrinsic factors), they were exposed to different environmental conditions (extrinsic factors), or inconsistencies in reporting (measurement uncertainty). We found that both extrinsic and intrinsic factors have comparable influence within a given site and event (60% and 40% of bleaching response variance of all records explained, respectively). However, when responses of individual taxa are averaged across sites to obtain taxon‐BRI, differential response was primarily driven by intrinsic differences among taxa (65% of taxon‐BRI variance explained), not conditions across sites (6% explained), nor measurement uncertainty (29% explained). Thus, taxon‐BRI is a robust metric of intrinsic susceptibility of coral taxa. Taxon‐BRI provides a broadly applicable framework for standardization and error estimation for disparate historical records and collection of novel data, allowing for unprecedented accuracy in parameterization of mechanistic and predictive models and conservation plans.     

Climate‐change refugia in the sheltered bays of Palau: analogs of future reefs

Coral bleaching and mortality are predicted to increase as climate change‐induced thermal‐stress events become more frequent. Although many studies document coral bleaching and mortality patterns, few studies have examined deviations from the expected positive relationships among thermal stress, coral bleaching, and coral mortality. This study examined the response of >30,000 coral colonies at 80 sites in Palau, during a regional thermal‐stress event in 2010. We sought to determine the spatial and taxonomic nature of bleaching and examine whether any habitats were comparatively resistant to thermal stress. Bleaching was most severe in the northwestern lagoon, in accordance with satellite‐derived maximum temperatures and anomalous temperatures above the long‐term averages. Pocillopora populations suffered the most extensive bleaching and the highest mortality. However, in the bays where temperatures were higher than elsewhere, bleaching and mortality were low. The coral‐community composition, constant exposure to high temperatures, and high vertical attenuation of light caused by naturally high suspended particulate matter buffered the corals in bays from the 2010 regional thermal‐stress event. Yet, nearshore reefs are also most vulnerable to land‐use change. Therefore, nearshore reefs should be given high conservation status because they provide refugia for coral populations as the oceans continue to warm.     

The effect of species and colony size on the bleaching response of reef-building corals in the Florida Keys during the 2005 mass bleaching event

Understanding the variation in coral bleaching response is necessary for making accurate predictions of population changes and the future state of reefs in a climate of increasing thermal stress events. Individual coral colonies, belonging to inshore patch reef communities of the Florida Keys, were followed through the 2005 mass bleaching event. Overall, coral bleaching patterns followed an index of accumulated thermal stress more closely than in situ temperature measurements. Eight coral species (Colpophyllia natans, Diploria strigosa, Montastraea cavernosa, M. faveolata, Porites astreoides, P. porites, Siderastrea siderea, and Stephanocoenia intersepta), representing >90% of the coral colonies studied, experienced intense levels of bleaching, but responses varied. Bleaching differed significantly among species: Colpophyllia natans and Diploria strigosa were most susceptible to thermal stress, while Stephanocoenia intersepta was the most tolerant. For colonies of C. natans, M. faveolata, and S. siderea, larger colonies experienced more extensive bleaching than smaller colonies. The inshore patch reef communities of the Florida Keys have historically been dominated by large colonies of Montastraea sp. and Colpophyllia natans. These results provide evidence that colony-level differences can affect bleaching susceptibility in this habitat and suggest that the impact of future thermal stress events may be biased toward larger colonies of dominant reef-building species. Predicted increases in the frequency of mass bleaching and subsequent mortality may therefore result in significant structural shifts of these ecologically important communities.     

Coral microbiome diversity reflects mass coral bleaching susceptibility during the 2016 El Niño heat wave

Repeat marine heat wave‐induced mass coral bleaching has decimated reefs in Seychelles for 35 years, but how coral‐associated microbial diversity (microalgal endosymbionts of the family Symbiodiniaceae and bacterial communities) potentially underpins broad‐scale bleaching dynamics remains unknown. We assessed microbiome composition during the 2016 heat wave peak at two contrasting reef sites (clear vs. turbid) in Seychelles, for key coral species considered bleaching sensitive (Acropora muricata, Acropora gemmifera) or tolerant (Porites lutea, Coelastrea aspera). For all species and sites, we sampled bleached versus unbleached colonies to examine how microbiomes align with heat stress susceptibility. Over 30% of all corals bleached in 2016, half of which were from Acropora sp. and Pocillopora sp. mass bleaching that largely transitioned to mortality by 2017. Symbiodiniaceae ITS2‐sequencing revealed that the two Acropora sp. and P. lutea generally associated with C3z/C3 and C15 types, respectively, whereas C. aspera exhibited a plastic association with multiple D types and two C3z types. 16S rRNA gene sequencing revealed that bacterial communities were coral host‐specific, largely through differences in the most abundant families, Hahellaceae (comprising Endozoicomonas), Rhodospirillaceae, and Rhodobacteraceae. Both Acropora sp. exhibited lower bacterial diversity, species richness, and community evenness compared to more bleaching‐resistant P. lutea and C. aspera. Different bleaching susceptibility among coral species was thus consistent with distinct microbiome community profiles. These profiles were conserved across bleached and unbleached colonies of all coral species. As this pattern could also reflect a parallel response of the microbiome to environmental changes, the detailed functional associations will need to be determined in future studies. Further understanding such microbiome‐environmental interactions is likely critical to target more effective management within oceanically isolated reefs of Seychelles.