Adaptation to Bleaching: Are Thermotolerant Symbiodiniaceae Strains More Successful Than Other Strains Under Elevated Temperatures in a Model Symbiotic Cnidarian?
ABSTRACT: The ability of some symbiotic cnidarians to resist and better withstand stress factors that cause bleaching is a trait that is receiving increased attention. The adaptive bleaching hypothesis postulates that cnidarians that can form a stable symbiosis with thermotolerant Symbiodiniaceae strains may cope better with increasing seawater temperatures. We used polyps of the scyphozoan, Cassiopea xamachana, as a model system to test symbiosis success under heat stress. We sought to determine: (1) if aposymbiotic C. xamachana polyps could establish and maintain a symbiosis with both native and non-native strains of Symbiodiniaceae that all exhibit different tolerances to heat, (2) whether polyps with these newly acquired Symbiodiniaceae strains would strobilate (produce ephyra), and (3) if thermally tolerant Symbiodiniaceae strains that established and maintained a symbiosis exhibited greater success in response to heat stress (even if they are not naturally occurring in Cassiopea). Following recolonization of aposymbiotic C. xamachana polyps with different strains, we found that: (1) strains Smic, Stri, Slin, and Spil all established a stable symbiosis that promoted strobilation and (2) strains Bmin1 and Bmin2 did not establish a stable symbiosis and strobilation did not occur. Strains Smic, Stri, Slin, and Spil were used in a subsequent bleaching experiment; each of the strains was introduced to a subset of aposymbiotic polyps and once polyp tissues were saturated with symbionts they were subjected to elevated temperatures - 32°C and 34°C - for 2 weeks. Our findings indicate that, in general, pairings of polyps with Symbiodiniaceae strains that are native to Cassiopea (Stri and Smic) performed better than a non-native strain (Slin) even though this strain has a high thermotolerance. This suggests a degree of partner specificity that may limit the adaptive potential of certain cnidarians to increased ocean warming. We also observed that the free-living, non-native thermotolerant strain Spil was relatively successful in resisting bleaching during experimental trials. This suggests that free-living Symbiodiniaceae may provide a supply of potentially "new" thermotolerant strains to cnidarians following a bleaching event.
Project description:The ability of corals and other cnidarians to survive climate change depends partly on the composition of their endosymbiont communities. The dinoflagellate family Symbiodiniaceae is genetically and physiologically diverse, and one proposed mechanism for cnidarians to acclimate to rising temperatures is to acquire more thermally tolerant symbionts. However, cnidarian-dinoflagellate associations vary in their degree of specificity, which may limit their capacity to alter symbiont communities. Here, we inoculated symbiont-free polyps of the sea anemone Exaiptasia pallida (commonly referred to as 'Aiptasia'), a model system for the cnidarian-dinoflagellate symbiosis, with simultaneous or sequential mixtures of thermally tolerant and thermally sensitive species of Symbiodiniaceae. We then monitored symbiont success (relative proportional abundance) at normal and elevated temperatures across two to four weeks. All anemones showed signs of bleaching at high temperature. During simultaneous inoculations, the native, thermally sensitive Breviolum minutum colonized polyps most successfully regardless of temperature when paired against the non-native but more thermally tolerant Symbiodinium microadriaticum or Durusdinium trenchii. Furthermore, anemones initially colonized with B. minutum and subsequently exposed to S. microadriaticum failed to acquire the new symbiont. These results highlight how partner specificity may place strong limitations on the ability of certain cnidarians to acquire more thermally tolerant symbionts, and hence their adaptive potential under climate change.
Project description:Corals rely on a symbiosis with dinoflagellate algae (Symbiodinium spp.) to thrive in nutrient poor tropical oceans. However, the coral-algal symbiosis can break down during bleaching events, potentially leading to coral death. While genome-wide expression studies have shown the genes associated with the breakdown of this partnership, the full conglomerate of genes responsible for the establishment and maintenance of a healthy symbiosis remains unknown. Results from previous studies suggested little transcriptomic change associated with the establishment of symbiosis. In order to elucidate the transcriptomic response of the coral host in the presence of its associated symbiont, we utilized a comparative framework. Post-metamorphic aposymbiotic coral polyps of Orbicella faveolata were compared to symbiotic coral polyps 9 days after metamorphosis and the subsequent differential gene expression between control and treatment was quantified using cDNA microarray technology. Coral polyps exhibited differential expression of genes associated with nutrient metabolism and development, providing insight into pathways turned as a result of symbiosis driving early polyp growth. Furthermore, genes associated with lysosomal fusion were also upregulated, suggesting host regulation of symbiont densities soon after infection. Overall design: RNA from 3 control and 3 infected polyp samples were hybridized in a 3-replicate pooled reference (6 total hyb's)
Project description:Reef-building corals switch endosymbiotic algae of the genus Symbiodinium during their early growth stages and during bleaching events. Clade C Symbiodinium algae are dominant in corals, although other clades - including A and D - have also been commonly detected in juvenile Acroporid corals. Previous studies have been reported that only molecular data of Symbiodinium clade were identified within field corals. In this study, we inoculated aposymbiotic juvenile polyps with cultures of clades C1 and D Symbiodinium algae, and investigated the different effect of these two clades of Symbiodinium on juvenile polyps. Our results showed that clade C1 algae did not grow, while clade D algae grew rapidly during the first 2 months after inoculation. Polyps associated with clade C1 algae exhibited bright green fluorescence across the body and tentacles after inoculation. The growth rate of polyp skeletons was lower in polyps associated with clade C1 algae than those associated with clade D algae. On the other hand, antioxidant activity (catalase) of corals was not significantly different between corals with clade C1 and clade D algae. Our results suggested that clade D Symbiodinium algae easily form symbiotic relationships with corals and that these algae could contribute to coral growth in early symbiosis stages.
Project description:Cassiopea xamachana jellyfish are an attractive model system to study metamorphosis and/or cnidarian-dinoflagellate symbiosis due to the ease of cultivation of their planula larvae and scyphistomae through their asexual cycle, in which the latter can bud new larvae and continue the cycle without differentiation into ephyrae. Then, a subsequent induction of metamorphosis and full differentiation into ephyrae is believed to occur when the symbionts are acquired by the scyphistomae. Although strobilation induction and differentiation into ephyrae can be accomplished in various ways, a controlled, reproducible metamorphosis induction has not been reported. Such controlled metamorphosis induction is necessary for an ensured synchronicity and reproducibility of biological, biochemical, and molecular analyses. For this purpose, we tested if differentiation could be pharmacologically stimulated as in Aurelia aurita, by the metamorphic inducers thyroxine, KI, NaI, Lugol's iodine, H2O2, indomethacin, or retinol. We found reproducibly induced strobilation by 50 ?M indomethacin after six days of exposure, and 10-25 ?M after 7 days. Strobilation under optimal conditions reached 80-100% with subsequent ephyrae release after exposure. Thyroxine yielded inconsistent results as it caused strobilation occasionally, while all other chemicals had no effect. Thus, indomethacin can be used as a convenient tool for assessment of biological phenomena through a controlled metamorphic process in C. xamachana scyphistomae.
Project description:Snorkelers in mangrove forest waters inhabited by the upside-down jellyfish Cassiopea xamachana report discomfort due to a sensation known as stinging water, the cause of which is unknown. Using a combination of histology, microscopy, microfluidics, videography, molecular biology, and mass spectrometry-based proteomics, we describe C. xamachana stinging-cell structures that we term cassiosomes. These structures are released within C. xamachana mucus and are capable of killing prey. Cassiosomes consist of an outer epithelial layer mainly composed of nematocytes surrounding a core filled by endosymbiotic dinoflagellates hosted within amoebocytes and presumptive mesoglea. Furthermore, we report cassiosome structures in four additional jellyfish species in the same taxonomic group as C. xamachana (Class Scyphozoa; Order Rhizostomeae), categorized as either motile (ciliated) or nonmotile types. This inaugural study provides a qualitative assessment of the stinging contents of C. xamachana mucus and implicates mucus containing cassiosomes and free intact nematocytes as the cause of stinging water.
Project description:Climate change threatens coral survival by causing coral bleaching, which occurs when the coral's symbiotic relationship with algal symbionts (Symbiodiniaceae) breaks down. Studies on thermal adaptation focus on symbionts because they are accessible both in vitro and in hospite. However, there is little known about the physiological and biochemical response of adult corals (without Symbiodiniaceae) to thermal stress. Here we show acclimatization and/or adaptation potential of menthol-bleached aposymbiotic coral Platygyra verweyi in terms of respiration breakdown temperature (RBT) and malate dehydrogenase (MDH) enzyme activity in samples collected from two reef sites with contrasting temperature regimes: a site near a nuclear power plant outlet (NPP-OL, with long-term temperature perturbation) and Wanlitong (WLT) in southern Taiwan. Aposymbiotic P. verweyi from the NPP-OL site had a 3.1?°C higher threshold RBT than those from WLT. In addition, MDH activity in P. verweyi from NPP-OL showed higher thermal resistance than those from WLT by higher optimum temperatures and the activation energy required for inactivating the enzyme by heat. The MDH from NPP-OL also had two times higher residual activity than that from WLT after incubation at 50?°C for 1?h. The results of RBT and thermal properties of MDH in P. verweyi demonstrate potential physiological and enzymatic response to a long-term and regular thermal stress, independent of their Symbiodiniaceae partner.
Project description:This study provides the first observation that umbrellar tissue can lead to the formation of virtually all body structures in jellyfish of the order Rhizostomeae. The regeneration process was observed in two specimens of the upside-down jellyfish Cassiopea xamachana Bigelow, 1892, one housed at the Vienna Zoo, Austria and the other in a laboratory at the University of São Paulo, Brazil. The process was triggered by an injury and ended with the formation of two new sets of body structures. Our observation offers evidence that C. xamachana has a hidden regenerative capacity exceeding that previously recorded.
Project description:Thermal stress drives the bleaching of reef corals, during which the endosymbiotic relationship between Symbiodiniaceae microalgae and the host breaks down. The endosymbiont communities are known to shift in response to environmental disturbances, but how they respond within and between colonies during and following bleaching events remains unclear. In 2016, a major global-scale bleaching event hit countless tropical reefs. Here, we investigate the relative abundances of Cladocopium LaJeunesse & H.J.Jeong, 2018 and Durusdinium LaJeunesse, 2018 within and among Pachyseris speciosa colonies in equatorial Singapore that are known to host both these Symbiodiniaceae clades. Bleached and unbleached tissues from bleaching colonies, as well as healthy colonies, during and following the bleaching event were sampled and analyzed for comparison. The nuclear ribosomal internal transcribed spacer (ITS) regions were separately amplified and quantified using a SYBR Green-based quantitative polymerase chain reaction (qPCR) method and Illumina high-throughput sequencing. We found Cladocopium to be highly abundant relative to Durusdinium. The relative abundance of Durusdinium, known to be thermally tolerant, was highest in post-bleaching healthy colonies, while bleached and unbleached tissues from bleaching colonies as well as tissue from healthy colonies during the event had depressed proportions of Durusdinium. Given the importance of Durusdinium for thermal tolerance and stress response, it is surprising that bleached tissue showed limited change over healthy tissue during the bleaching event. Moreover, colonies were invariably dominated by Cladocopium during bleaching, but a minority of colonies were Durusdinium-dominant during non-bleaching times. The detailed characterization of Symbiodiniaceae in specific colonies during stress and recovery will provide insights into this crucial symbiosis, with implications for their responses during major bleaching events.
Project description:Coral reefs are threatened by global warming, which disrupts the symbiosis between corals and their photosynthetic symbionts (Symbiodiniaceae), leading to mass coral bleaching. Planktonic diazotrophs or dinitrogen (N2)-fixing prokaryotes are abundant in coral lagoon waters and could be an alternative nutrient source for corals. Here we incubated untreated and bleached coral colonies of Stylophora pistillata with a 15N2-pre-labelled natural plankton assemblage containing diazotrophs. 15N2 assimilation rates in Symbiodiniaceae cells and tissues of bleached corals were 5- and 30-fold higher, respectively, than those measured in untreated corals, demonstrating that corals incorporate more nitrogen derived from planktonic diazotrophs under bleaching conditions. Bleached corals also preferentially fed on Synechococcus, nitrogen-rich picophytoplanktonic cells, instead of Prochlorococcus and picoeukaryotes, which have a lower cellular nitrogen content. By providing an alternative source of bioavailable nitrogen, both the incorporation of nitrogen derived from planktonic diazotrophs and the ingestion of Synechococcus may have profound consequences for coral bleaching recovery, especially for the many coral reef ecosystems characterized by high abundance and activity of planktonic diazotrophs.
Project description:Increasing ocean temperatures have widespread consequences for coral reefs, one of which is coral bleaching. We analyzed a global network of associations between coral species and Symbiodiniaceae for resistance to temperature stress and robustness to perturbations. Null networks were created by changing either the physiological parameters of the nodes or the structures of the networks. We developed a bleaching model in which each link, association, is given a weight based on temperature thresholds for specific host-symbiont pairs and links are removed as temperature increases. Resistance to temperature stress was determined from the response of the networks to the bleaching model. Ecological robustness, defined by how much perturbation is needed to decrease the number of nodes by 50%, was determined for multiple removal models that considered traits of the hosts, symbionts, and their associations. Network resistance to bleaching and robustness to perturbations differed from the null networks and varied across spatial scales, supporting that thermal tolerances, local association patterns, and environment play an important role in network persistence. Networks were more robust to attacks on associations than to attacks on species. Although the global network was fairly robust to random link removals, when links are removed according to the bleaching model, robustness decreases by about 20%. Specific environmental attacks, in the form of increasing temperatures, destabilize the global network of coral species and Symbiodiniaceae. On a global scale, the network was more robust to removals of links with susceptible Symbiodiniaceae than it was to removals of links with susceptible hosts. Thus, the symbionts convey more stability to the symbiosis than the hosts when the system is under an environmental attack. However, our results also provide evidence that the environment of the networks affects robustness to link perturbations. Our work shows that ecological resistance and robustness can be assessed through network analysis that considers specific biological traits and functional weaknesses. The global network of associations between corals and Symbiodiniaceae and its distribution of thermal tolerances are non-random, and the evolution of this architecture has led to higher sensitivity to environmental perturbations.