Gene expression of Pocillopora damicornis coral larvae in response to acidification and ocean warming.

OBJECTIVES: The endosymbiosis with Symbiodiniaceae is key to the ecological success of reef-building corals. However, climate change is threatening to destabilize this symbiosis on a global scale. Most studies looking into the response of corals to heat stress and ocean acidification focus on coral colonies. As such, our knowledge of symbiotic interactions and stress response in other stages of the coral lifecycle remains limited. Establishing transcriptomic resources for coral larvae under stress can thus provide a foundation for understanding the genomic basis of symbiosis, and its susceptibility to climate change. Here, we present a gene expression dataset generated from larvae of the coral Pocillopora damicornis in response to exposure to acidification and elevated temperature conditions below the bleaching threshold of the symbiosis. DATA DESCRIPTION: This dataset is comprised of 16 samples (30 larvae per sample) collected from four treatments (Control, High pCO2, High Temperature, and Combined pCO2 and Temperature treatments). Freshly collected larvae were exposed to treatment conditions for five days, providing valuable insights into gene expression in this vulnerable stage of the lifecycle. In combination with previously published datasets, this transcriptomic resource will facilitate the in-depth investigation of the effects of ocean acidification and elevated temperature on coral larvae and its implication for symbiosis.

Rapid shifts in thermal reaction norms and tolerance of brooded coral larvae following parental heat acclimation.

Thermal priming of reef corals can enhance their heat tolerance; however, the legacy effects of heat stress during parental brooding on larval resilience remain understudied. This study investigated whether preconditioning adult coral Pocillopora damicornis to high temperatures (29°C and 32°C) could better prepare their larvae for heat stress. Results showed that heat-acclimated adults brooded larvae with reduced symbiont density and shifted thermal performance curves. Reciprocal transplant experiments demonstrated higher bleaching resistance and better photosynthetic and autotrophic performance in heat-exposed larvae from acclimated adults compared to unacclimated adults. RNA-seq revealed strong cellular stress responses in larvae from heat-acclimated adults that could have been effective in rescuing host cells from stress, as evidenced by the widespread upregulation of genes involved in cell cycle and mitosis. For symbionts, a molecular coordination between light harvesting, photoprotection and carbon fixation was detected in larvae from heat-acclimated adults, which may help optimize photosynthetic activity and yield under high temperature. Furthermore, heat acclimation led to opposing regulations of symbiont catabolic and anabolic pathways and favoured nutrient translocation to the host and thus a functional symbiosis. Notwithstanding, the improved heat tolerance was paralleled by reduced light-enhanced dark respiration, indicating metabolic depression for energy saving. Our findings suggest that adult heat acclimation can rapidly shift thermal tolerance of brooded coral larvae and provide integrated physiological and molecular evidence for this adaptive plasticity, which could increase climate resilience. However, the metabolic depression may be maladaptive for long-term organismal performance, highlighting the importance of curbing carbon emissions to better protect corals.

Ocean acidification elicits differential bleaching and gene expression patterns in larval reef coral Pocillopora damicornis under heat stress.

The successful dispersal of coral larvae is vital to the population replenishment and reef recovery and resilience. Despite that this critical early stage is susceptible to ocean warming and acidification, little is known about the responses of coral larvae to warming and acidification across different biological scales. This study explored the influences of elevated temperature (29 °C versus 33 °C) and pCO2 (500 µatm versus 1000 µatm) on brooded larvae of Pocillopora damicornis at the organismal, cellular and gene expression levels. Heat stress caused bleaching, depressed light-enhanced dark respiration, photosynthesis and autotrophy, whereas high pCO2 stimulated photosynthesis. Although survival was unaffected, larvae at 33 °C were ten-times more likely to settle than those at 29 °C, suggesting reduced capacity to disperse and differentiate suitable substrate. Remarkably, heat stress induced greater symbiont loss at ambient pCO2 than at high pCO2, while cell-specific pigment concentrations of symbionts at 33 °C increased twofold under ambient pCO2 relative to high pCO2, suggesting pCO2-dependent bleaching patterns. Considerable increases in activities of host antioxidants superoxide dismutase (SOD) and catalase (CAT) at 33 °C indicated oxidative stress, whereas lipid peroxidation and caspase activities were contained, thereby restraining larval mortality at 33 °C. Furthermore, the coral host mounted stronger transcriptional responses than symbionts. High pCO2 stimulated host metabolic pathways, possibly because of the boosted algal productivity. In contrast, host metabolic processes and symbiont photosystem genes were downregulated at 33 °C. Interestingly, the upregulation of extracellular matrix genes and glycosaminoglycan degradation pathway at 33 °C was more evident under ambient pCO2 than high pCO2, suggesting compromised host tissue integrity that could have facilitated symbiont expulsion and bleaching. Our results provide insights into how coral larvae respond to warming and acidification at different levels of biological organization, and demonstrate that ocean acidification can mediate thermal bleaching and gene expression in coral larvae under heat stress.

Light availability regulated by particulate organic matter affects coral assemblages on a turbid fringing reef.

Recently, increasing evidence suggests that reef-building corals exposed to elevated suspended solids (SS) are largely structured by changes in underwater light availability (ULA). However, there are few direct and quantitative observations in situ support for this hypothesis; in particular, the contribution of SS to the diffuse attenuation coefficient of the photosynthetically active radiation (Kd-PAR) variations is not yet fully understood. Here, we investigated the variations in ULA, the structure of coral assemblages, and the concentration and composition of SS on the Luhuitou fringing reef, Sanya, China. Light attenuation was rapid (Kd-PAR: 0.60 ± 0.39 m-1) resulting in a shallow euphotic depth (Zeu-PAR) (<11 m). Benthic PAR showed significant positive correlations with branching and corymbose corals (e.g. Acropora spp.), while massive and encrusting species (e.g. Porites spp.) dominated the coral communities and showed no significant correlations with PAR. These results indicate that the depth range available for coral growth is shallow and the tolerance to low-light stress differs among coral species. Notably, Kd-PAR showed no significant correlations with the grain size fractions of SS, whereas significant positive correlations were found with its organic fraction content, demonstrating that the light attenuation of SS is mainly regulated by particulate organic matter (POM). Intriguingly, our isotopic evidence revealed that POM concentration contributed the most to changes in Kd-PAR, with its source being slightly less important. Combined, our results highlight ULA regulated by POM is an important factor in contributing to changes in coral assemblages on inshore turbid reefs, and reducing the input of terrestrial materials, especially POM, is an effective measure to alleviate the low-light stress on sensitive coral species.

Zonal macroalgae blooms influenced by different aquaculture discharges in the Xuwen fringing reef, southern China.

Reef-building corals are experiencing major impacts from climate change and increasing anthropogenic activities worldwide. Coral reef degradation is associated with the loss of coral species abundance and diversity, followed by an ecological imbalance that commonly occurs with a shift from coral- to macroalgae-dominated community states. The species composition of the bloom-forming macroalgae in the Xuwen National Coral Reef Reserve, southern China, and the associated drivers affecting the composition remain unclear. We investigated the relationship between zonal macroalgae blooms and different aquaculture discharges in this coral reef in March 2016. The structure of macroalgae communities varied greatly among the three study sites, with green and brown algae dominating the high-level pond aquaculture discharge zone; red, green and brown algae dominating the tidal flat aquaculture discharge zone; and green and brown algae dominating in the enclosure aquaculture discharge zone. A significant amount of variation in the structure and composition of the macroalgae community was explained by temperature, total suspended solids (TSS), chlorophyll a (Chla) and dissolved inorganic nutrients (DIN), while temperature and TSS had a significant relationship with these variables. Our findings highlight the negative effects of aquaculture sewage discharges on the health of coral reefs, and we recommend effective and integrated management of anthropogenic sewage discharge into coral reefs.

Changes in physiological performance and protein expression in the larvae of the coral Pocillopora damicornis and their symbionts in response to elevated temperature and acidification.

Climate change causes ocean warming and acidification, which threaten coral reef ecosystems. Ocean warming and acidification cause bleaching and mortality, and decrease calcification in adult corals, leading to changes in the composition of coral communities; however, their interactive effects on coral larvae are not comprehensively understood. To examine the underlying molecular mechanisms of larval responses to elevated temperature and pCO2, we examined the physiological performance and protein expression profiles of Pocillopora damicornis at two temperatures (29 and 33 °C) and pCO2 levels (500 and 1000 µatm) for 5 d. Extensive physiological and proteomic changes were observed in coral larvae. The results indicated a significant decrease in net photosynthesis (PNET) and autotrophic capability (PNET/RD) of larvae exposed to elevated temperature but a marked increase in PNET and PNET/RD of larvae exposed to high pCO2 levels. Elevated temperature significantly reduced endosymbiont densities by 70% and photochemical efficiency, indicating that warming impaired host-symbiont symbiosis. Expression of photosynthesis-related proteins, the photosystem (PS) I reaction center subunits IV and XI as well as oxygen-evolving enhancer 1, was downregulated at higher temperatures in symbionts, whereas expression of the PS I iron­sulfur center protein was increased under high pCO2 conditions. Furthermore, expression of phosphoribulokinase (involved in the Calvin cycle) and phosphoenolpyruvate carboxylase (related to the C4 pathway) was downregulated in symbionts under thermal stress; this finding suggests reduced carbon fixation at high temperatures. The abundance of carbonic anhydrase-associated proteins, which are predicted to exert biochemical roles in dissolved inorganic carbon transport in larvae, was reduced in coral host and symbionts at high temperatures. These results elucidate potential mechanisms underlying the responses of coral larvae exposed to elevated temperature and acidification and suggest an important role of symbionts in the response to warming and acidification.

Impact of Ocean Warming and Acidification on Symbiosis Establishment and Gene Expression Profiles in Recruits of Reef Coral Acropora intermedia.

The onset of symbiosis and the early development of most broadcast spawning corals play pivotal roles in recruitment success, yet these critical early stages are threatened by multiple stressors. However, molecular mechanisms governing these critical processes under ocean warming and acidification are still poorly understood. The present study investigated the interactive impact of elevated temperature (∼28.0°C and ∼30.5°C) and partial pressure of carbon dioxide (pCO2) (∼600 and ∼1,200 µatm) on early development and the gene expression patterns in juvenile Acropora intermedia over 33 days. The results showed that coral survival was >89% and was unaffected by high temperature, pCO2, or the combined treatment. Notably, high temperature completely arrested successful symbiosis establishment and the budding process, whereas acidification had a negligible effect. Moreover, there was a positive exponential relationship between symbiosis establishment and budding rates (y = 0.0004e6.43x, R = 0.72, P < 0.0001), which indicated the importance of symbiosis in fueling asexual budding. Compared with corals at the control temperature (28°C), those under elevated temperature preferentially harbored Durusdinium spp., despite unsuccessful symbiosis establishment. In addition, compared to the control, 351 and 153 differentially expressed genes were detected in the symbiont and coral host in response to experimental conditions, respectively. In coral host, some genes involved in nutrient transportation and tissue fluorescence were affected by high temperature. In the symbionts, a suite of genes related to cell growth, ribosomal proteins, photosynthesis, and energy production was downregulated under high temperatures, which may have severely hampered successful cell proliferation of the endosymbionts and explains the failure of symbiosis establishment. Therefore, our results suggest that the responses of symbionts to future ocean conditions could play a vital role in shaping successful symbiosis in juvenile coral.