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Location-specific responses to thermal stress in larvae of the reef-building coral Montastraea faveolata

ABSTRACT: The potential to adapt to a changing climate depends in part upon the standing genetic variation present in wild populations. In corals, the dispersive larval phase is particularly vulnerable to the effects of environmental stress. Larval survival and response to stress during dispersal and settlement will play a key role in the persistence of coral populations. To test the hypothesis that larval transcription profiles reflect population specific responses to thermal stress, symbiont-free gametes of the scleractinian coral Montastraea faveolata were collected from Florida and Mexico and raised under normal and elevated temperatures. These populations have been shown to exchange larvae frequently enough to prevent significant differentiation of neutral loci. Differences among thousands of genes were simultaneously characterized using microarrays, allowing investigation of gene expression patterns among wild populations under stressful environmental conditions. Results show site-specific signatures of gene expression in larvae of a reef-building coral from different parts of its range (despite low genetic divergence), and reveal both local and general components of stress response during later stages of larval development. These results provide evidence of site-specific variation in the face of gene flow, which may represent functional genetic variation in different subpopulations, and support the idea that coral host genomes may indeed house the adaptive potential needed to deal with changing environmental conditions.

ORGANISM(S): Orbicella faveolata

PROVIDER: GSE19998 | GEO | 2010/06/23

SECONDARY ACCESSION(S): PRJNA120165

REPOSITORIES: GEO

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Project description:The potential to adapt to a changing climate depends in part upon the standing genetic variation present in wild populations. In corals, the dispersive larval phase is particularly vulnerable to the effects of environmental stress. Larval survival and response to stress during dispersal and settlement will play a key role in the persistence of coral populations. To test the hypothesis that larval transcription profiles reflect population specific responses to thermal stress, symbiont-free gametes of the scleractinian coral Montastraea faveolata were collected from Florida and Mexico and raised under normal and elevated temperatures. These populations have been shown to exchange larvae frequently enough to prevent significant differentiation of neutral loci. Differences among thousands of genes were simultaneously characterized using microarrays, allowing investigation of gene expression patterns among wild populations under stressful environmental conditions. Results show site-specific signatures of gene expression in larvae of a reef-building coral from different parts of its range (despite low genetic divergence), and reveal both local and general components of stress response during later stages of larval development. These results provide evidence of site-specific variation in the face of gene flow, which may represent functional genetic variation in different subpopulations, and support the idea that coral host genomes may indeed house the adaptive potential needed to deal with changing environmental conditions. The experimental setup followed a reference design, i.e. all samples were hybridized against the same pool made up of equal amounts of RNA from all samples collected in Mexico. For samples from Mexico we used three technical replicates for each treatment temperature, for samples from Florida three biological replicates were used for each treatment temperature, except for the high temperature samples at day two where only two replicates were available due to high larval mortality at that temperature. Common reference samples were labeled with Cy3, temperature treatment samples with Cy5. Microarrays for M. faveolata contained 1,314 coding sequences, of which 43% had functional annotations as determined by homology to known genes.

Project description:Coral populations have declined worldwide largely due to increased sea surface temperatures. Recovery of coral populations depends in part upon larval recruitment. Many corals reproduce during the warmest time of year when further increases in temperature can lead to low fertilization rates of eggs and high larval mortality. Microarray experiments were designed to capture and assess variability in the thermal stress responses of Acropora palmata larvae from Puerto Rico. Transcription profiles showed a striking acceleration of normal developmental gene expression patterns with increased temperature. The transcriptional response to heat suggested rapid depletion of larval energy stores via peroxisomal lipid oxidation and included key enzymes that indicated the activation of the glyoxylate cycle. High temperature also resulted in expression differences in key developmental signalling genes including the conserved WNT pathway that is critical for pattern formation and tissue differentiation in developing embryos. Expression of these and other important developmental and thermal stress genes such as ferritin, heat shock proteins, cytoskeletal components, cell adhesion and autophagy proteins also varied among larvae derived from different parent colonies. Disruption of normal developmental and metabolic processes will have negative impacts on larval survival and dispersal as temperatures rise. However, it appears that variation in larval response to high temperature remains despite the dramatic population declines. Further research is needed to determine whether this variation is heritable or attributable to maternal effects. Hybridization followed a dual channel loop design using two biological replicates (dye-swapped) from each treatment that maximized power to detect differential expression in contrasts between temperatures and batches (within time-points) as well as the amount of data obtained from each slide (Simon and Dobbin 2003). A total of 18 arrays on two 12 plex slides were used (Table S1). Additional samples from other sub-batches (b3/b4) were included in the microarray experiment but are not used in this analysis. Each array measures the expression level of 135,185 genes from the elkhorn coral (Acropora palmata) transcriptome (Polato et al. 2011). Two 60-mer probes were designed for each contig (n = 85,260), and a single probe was designed for each singleton sequence (n = 45,390). Two additional probes each were developed for sequences associated with annotation information relating to calcium metabolism and stress response (n = 4,798). Replicate probes for individual sequences from the assembled transcriptome were not identical; rather they represented multiple different 60-mer sequences from the original template.

Project description:In this study, we examined the very early transcriptional response of aposymbiotic coral larval host (still not engaged in symbiosis) to hyperthermal stress. This experimental setting provided a scenario and opportunity to study the direct effect of environmental stressors on the host cell per se. Using a cDNA microarray constructed for Acropora millepora and Q-RT-PCR assays, we identified a number of genes that were significantly up- and down-regulated with increase of seawater temperature. Down-regulation of several key component of DNA/RNA metabolism was detected implying inhibition of this cellular metabolic process, however the down-regulation of overall protein synthesis was not simple and random, which suggest that the response to stress is a more complicated adjustment to the metabolic needs of the cell. We identified four significant outcomes during the very early hours of the transcriptional response to hyperthermal stress in coral larvae. First, molecular chaperones responded to hyperthermal stress by increasing their expression as expected, but the response was immediate and extremely rapid during the first 3 hours of heat exposure. Secondly, elevated temperature triggers down-regulation of a fluorescent protein homolog, DsRed-type FP, suggesting that this gene might be used as a potential molecular marker for monitoring hyperthermal stress in nature. Thirdly, the downregulation of a coral mannose-binding lectin under hyperthermal stress might compromise the coral immune defense and bring about susceptibility to pathogenic diseases. And lastly, an absence in the response of oxidative stress genes in aposymbiotic coral larvae during the early hours to hyperthermal stress suggest that the up-regulation of cnidarian host oxidative stress genes reported during thermal stress in algal/host symbiosis might be triggered directly by ROS generated by photosynthetic-dysfunctionally algal endosymbionts that diffuse into host cells, as very little ROS seems to be produced by the host cells from thermal-associated host cellular damage.

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Location-specific responses to thermal stress in larvae of the reef-building coral Montastraea faveolata

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