Symbiodinium clade content drives host transcriptome more than thermal stress in the coral Montastraea faveolata part 2
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ABSTRACT: A mutualistic relationship between reef-building corals and endosymbiotic algae (Symbiodinium spp.) forms the basis for the existence of coral reefs. Genotyping tools for Symbiodinium spp. have added a new level of complexity to studies concerning cnidarian growth, nutrient acquisition, and stress. For example, the response of the coral holobiont to thermal stress is connected to the host-Symbiodinium genotypic combination, as different partnerships can have different bleaching susceptibilities. If, and to what extent, differences in algal symbiont clade contents can exert effects on the coral host transcriptome is currently unknown. In this study, we monitored algal physiological parameters and profiled the coral host transcriptional responses in acclimated, thermally stressed, and recovered coral fragments using a custom cDNA gene expression microarray. Combining these analyses with results from algal and host genotyping revealed a striking symbiont effect on both the acclimated coral host transcriptome and the magnitude of the thermal stress response. This is the first study that links coral host transcriptomic patterns to the clade content of their algal symbiont community. Our data provide a critical step to elucidating the molecular basis of the apparent variability seen among different coral-algal partnerships.
Project description:Given the overwhelming evidence that symbiont genotypes differentially affect host processes such as growth, bleaching susceptibility, and nutrient acquisition, we set out to measure gene expression differences in fragments of Montastraea faveolata harboring two different clades of Symbiodinium. On the reefs near Puerto Morelos, México, colonies of M. faveolata are known to shift algal symbiont clade with depth, often associating with clade A at the top, clade B in the middle, and clade C near the bottom of the colony. By measuring photosynthetic efficiency and gene expression in control and heat-stressed fragments containing either clade B, clade C, or a mix of both, we found that: 1) the algal response to thermal stress is due to both host and algal factors; 2) fragments of M. faveolata express different genes in response to sub-bleaching thermal stress depending on algal genotype; 3) the overall effect of heat stress on coral gene expression is less significant than the effect of housing different zooxanthellae types. Overall, we present convincing evidence that different Symbiodinium clades may be functionally distinct, which in turn, greatly influences host gene expression.
Project description:This SuperSeries is composed of the following subset Series: GSE12809: Symbiodinium clade content drives host transcriptome more than thermal stress in the coral Montastraea faveolata (part 1) GSE15253: Symbiodinium clade content drives host transcriptome more than thermal stress in the coral Montastraea faveolata (part 2) Refer to individual Series
Project description:The emergence of genomic tools for reef-building corals and symbiotic anemones comes at a time when alarming losses in coral cover are being observed worldwide. These tools hold great promise in elucidating novel and unforeseen cellular processes underlying the successful mutualism between corals and their algal endosymbionts (Symbiodinium spp.). Since thermal stress triggers a breakdown in the symbiosis (coral bleaching), measuring the transcriptomic response to thermal stress-induced bleaching offers an extraordinary view of the cellular processes specific to coral-algal symbioses. In the present study, we utilized a cDNA microarray containing 2,059 genes of the Caribbean Elkhorn coral Acropora palmata to identify genes differentially expressed upon thermal stress. Fragments from four separate colonies were exposed to elevated temperature (3˚C increase) for two days, and samples were frozen for microarray analysis after 24 and 48 hours. Fragments experienced a 60% reduction in algal cell density after two days. 204 genes were differentially expressed in samples collected one day after thermal stress; in samples collected after two days, 104 genes. Annotations of the differentially expressed genes indicate a conserved cellular stress response in A. palmata involving: 1) growth arrest; 2) chaperone activity; 3) nucleic acid stabilization and repair; and 4) the removal of damaged macromolecules. Other differentially expressed processes include sensory perception, metabolite transfer between host and symbiont, nitric oxide signaling, and modifications to the actin cytoskeleton and extracellular matrix. The results are also compared to those from a previous coral microarray study of thermal stress in Montastraea faveolata.
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.
Project description:Coral reefs are declining globally. Temperature anomalies disrupt coral-algal symbioses at the molecular level, causing bleaching and mortality events. In terrestrial mutualisms, diversity in pairings of host and symbiont individuals (genotypes) results in ecologically and evolutionarily relevant stress response differences. The extent to which such intraspecific diversity provides functional variation in coral-algal systems is unknown. Here we assessed functional diversity among unique pairings of coral and algal individuals (holobionts). We targeted six genetically distinct Acropora palmata coral colonies that all associated with a single, clonal Symbiodinium ‘fitti’ strain in a natural common garden. No other species of algae or other strains of S. ‘fitti’ could be detected in host tissues. When colony branches were experimentally exposed to cold stress, host genotype influenced the photochemical efficiency of the symbiont strain, buffering the stress response to varying degrees. Gene expression differences among host individuals with buffered vs. non-buffered symbiont responses included biochemical pathways that mediate iron availability and oxygen stress signaling—critical components of molecular interactions with photosynthetic symbionts. Spawning patterns among hosts reflected symbiont performance differences under stress. These data are some of the first to indicate that genetic interactions below the species level affect coral holobiont performance. Intraspecific diversity serves as an important but overlooked source of physiological variation in this system, contributing raw material available to natural selection. Note: in the final publication, only ambient and cold treatments are discussed, but there was an additional hot treatment for each genotype at 34C. Most colonies expired after 6 hours, so PAM data could not be collected. The microarray data from 3.5 hours are included here.
Project description:Coral reefs are based on the symbiotic relationship between corals and photosynthetic dinoflagellates of the genus Symbiodinium. We followed gene expression of coral larvae of Acropora palmata and Montastraea faveolata after exposure to Symbiodinium strains that differed in their ability to establish symbioses. We show that the coral host transcriptome remains almost unchanged during infection by competent symbionts, but is massively altered by symbionts that fail to establish symbioses. Our data suggest that successful coral-algal symbioses depend mainly on the symbionts' ability to enter the host in a stealth manner rather than a more active response from the coral host.
Project description:Coral reefs are based on the symbiotic relationship between corals and photosynthetic dinoflagellates of the genus Symbiodinium. We followed gene expression of coral larvae of Acropora palmata and Montastraea faveolata after exposure to Symbiodinium strains that differed in their ability to establish symbioses. We show that the coral host transcriptome remains almost unchanged during infection by competent symbionts, but is massively altered by symbionts that fail to establish symbioses. Our data suggest that successful coral-algal symbioses depend mainly on the symbionts' ability to enter the host in a stealth manner rather than a more active response from the coral host. Acropora palmata Samples: Three biological replicates of pooled larvae from each species and condition (i.e. untreated control, inoculated with competent Symbiodinium strain, inoculated with incompetent Symbiodinium strain) for both time points were hybridized against a pooled reference. Pooled references were constructed by combining equal amounts of aRNA from all control samples from A. palmata. References were labeled with Cy3, samples with Cy5. Montastraea faveolata Samples: Three biological replicates of pooled larvae from each species and condition (i.e. untreated control, inoculated with competent Symbiodinium strain, inoculated with incompetent Symbiodinium strain) for both time points were hybridized against a pooled reference. Pooled references were constructed by combining equal amounts of aRNA from all control samples from M. faveolata. References were labeled with Cy3, samples with Cy5. Symbiodinium sp. CassKB8: competent strain Symbiodinium sp. EL1: incompetent strain Symbiodinium sp. Mf1.05b: competent strain
Project description:The emergence of genomic tools for reef-building corals and symbiotic anemones comes at a time when alarming losses in coral cover are being observed worldwide. These tools hold great promise in elucidating novel and unforeseen cellular processes underlying the successful mutualism between corals and their algal endosymbionts (Symbiodinium spp.). Since thermal stress triggers a breakdown in the symbiosis (coral bleaching), measuring the transcriptomic response to thermal stress-induced bleaching offers an extraordinary view of the cellular processes specific to coral-algal symbioses. In the present study, we utilized a cDNA microarray containing 2,059 genes of the Caribbean Elkhorn coral Acropora palmata to identify genes differentially expressed upon thermal stress. Fragments from four separate colonies were exposed to elevated temperature (3ËC increase) for two days, and samples were frozen for microarray analysis after 24 and 48 hours. Fragments experienced a 60% reduction in algal cell density after two days. 204 genes were differentially expressed in samples collected one day after thermal stress; in samples collected after two days, 104 genes. Annotations of the differentially expressed genes indicate a conserved cellular stress response in A. palmata involving: 1) growth arrest; 2) chaperone activity; 3) nucleic acid stabilization and repair; and 4) the removal of damaged macromolecules. Other differentially expressed processes include sensory perception, metabolite transfer between host and symbiont, nitric oxide signaling, and modifications to the actin cytoskeleton and extracellular matrix. The results are also compared to those from a previous coral microarray study of thermal stress in Montastraea faveolata. The field experiment was performed at the Smithsonian Tropical Research Instituteâs Bocas del Toro field station in Panamá during September and October 2006. Four colonies of A. palmata were sampled from two separate reefs 21 km apart (two colonies from Isla Solarte â 9o19â56.78â N and 82o12â54.65â W, and two colonies from Cayos Zapatillas â 9o15â08.79â N and 82o02â24.63â W). Each colony was broken into six fragments using a hammer and chisel. For each colony, three fragments were placed in a control aquarium, and three fragments were placed in an experimental aquarium fitted with two 200-Watt aquarium heaters, such that each colony was represented by a pair of aquaria (total of three control and three heated aquaria, all 75-liter). The three control aquaria were placed in one large fiberglass pond with continuous water flow, and the three experimental aquaria were placed in another large pond. All aquaria were exposed to shaded ambient light, and each aquarium was a closed system (but contained a pump to generate continuous water flow). Fragments were kept at a depth of ~25cm. HOBO Pendant Temperature/Light Data Loggers (Onset Corp UA-002-64) recorded temperature and light data every three minutes. These data loggers are not designed to measure photosynthetically active radiation (PAR â 400-700nm), as only ~30% of the measured light is in the range of PAR. For this reason, relative light levels in the aquaria are reported (expressed as the percentage of the average 10am to 2pm light intensity measured on a reef ~4m deep in Bocas del Toro (9o22â68.4â N and 82o18â24.6â W) during September and October 2007). Light intensity differed slightly between the four aquaria fitted with HOBOs (control aquaria 1 â 43%; control aquaria 2 â 46%; heated aquaria 1 â 35%; and heated aquaria 2 â 34% of reef light). After an acclimation period of four days at the natural temperature of the seawater system (mean temperature = 30.29±0.07oC), a fragment from each control and experimental aquaria was sampled (t0C and t0H). After time zero sampling, the heaters in each of the experimental aquaria were turned on. The temperatures of the experimental aquaria increased to ca. 32oC over three hours. The mean temperature of the control aquaria during the entire experiment was 29.74±0.03oC, and the mean temperature of the heated aquaria was 32.72±0.32oC. Control and experimental fragments were sampled again one day (1dC and 1dH) and two days (2dC and 2dH) after turning on the heaters. Heated fragments from one of the colonies (col3) showed extreme bleaching after one day of thermal stress. The remaining fragment of col3 was removed at this time to avoid fouling of the water due to death. Thus, there are four replicates for t0C, t0H, 1dC, and 1dH, and three replicates for 2dC and 2dH. All samples were taken at night. Fragments were frozen in liquid nitrogen. We employed a reference design where all control and heat-stressed samples were compared to a pooled reference aRNA sample composed of aRNA from the four t0C fragments. Since all RNA samples were compared to the reference sample, direct comparisons of gene expression across all time points and conditions can be performed.