Dual‐compartmental transcriptomic + proteomic analysis of a marine endosymbiosis exposed to environmental change

Mayfield, Anderson B.; Wang, Yu Bin; Chen, Chii Shiarng; Chen, Shu Hwa; Lin, Chung Yen

doi:10.1111/mec.13896

Cited by 41 publications

(72 citation statements)

References 28 publications

(34 reference statements)

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“…Whether or not these generally high levels of expression of genes encoding stress proteins indicates that these corals were indeed stressed at the time of sampling or were, alternatively, better prepared for future environmental changes (as discussed in the Introduction), remains to be determined. Furthermore, little congruency between mRNA and protein expression was documented for another reef-building pocilloporid [40]; therefore, it is possible that the respective proteins may show entirely different expression patterns.…”

Section: Discussionmentioning

confidence: 99%

Identifying corals displaying aberrant behavior in Fiji’s Lau Archipelago

2017

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Given the numerous threats against Earth’s coral reefs, there is an urgent need to develop means of assessing reef coral health on a proactive timescale. Molecular biomarkers may prove useful in this endeavor because their expression should theoretically undergo changes prior to visible signs of health decline, such as the breakdown of the coral-dinoflagellate (genus Symbiodinium) endosymbiosis. Herein 13 molecular- and physiological-scale biomarkers spanning both eukaryotic compartments of the anthozoan-Symbiodinium mutualism were assessed across 70 pocilloporid coral colonies sampled from reefs of Fiji’s easternmost province, Lau. Eleven colonies were identified as outliers upon employment of a detection method based partially on the Mahalanobis distance; these corals were hypothesized to have been displaying aberrant sub-cellular behavior with respect to their gene expression signatures, as they were characterized not only by lower Symbiodinium densities, but also by higher levels of expression of several stress-targeted genes. Although these findings could suggest that the sampled colonies were physiologically compromised at the time of sampling, further studies are warranted to state conclusively whether these 11 scleractinian coral colonies are more stress-prone than nearby conspecifics that demonstrated statistically normal phenotypes.

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Section: Discussionmentioning

confidence: 99%

Identifying corals displaying aberrant behavior in Fiji’s Lau Archipelago

2017

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“…The source of balancing selection is unclear, as there is no discernable association of the haplotype frequencies with genetic or current environmental PCs (P > 0.15, Table S5). However, sacsin has been shown to be significantly upregulated when exposed to elevated temperatures in the laboratory, in multiple coral species from the genus Acropora and Pocillipora [45][46][47][48] , indicating that variation in the gene is plausibly associated with heat response in natural populations.…”

Section: Introductionmentioning

confidence: 99%

Population genetics of the coralAcropora millepora: Towards a genomic predictor of bleaching

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et al. 2019

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Although reef-building corals are rapidly declining worldwide, responses to bleaching vary both within and among species. Because these inter-individual differences are partly heritable, they should in principle be predictable from genomic data. Towards that goal, we generated a chromosome-scale genome assembly for the coral Acropora millepora. We then obtained whole genome sequences for 237 phenotyped samples collected at 12 reefs distributed along the Great Barrier Reef, among which we inferred very little population structure. Scanning the genome for evidence of local adaptation, we detected signatures of long-term balancing selection in the heat-shock co-chaperone sacsin. We further used 213 of the samples to conduct a genome-wide association study of visual bleaching score, incorporating the polygenic score derived from it into a predictive model for bleaching in the wild. These results set the stage for the use of genomics-based approaches in conservation strategies.

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“…Of the 38 DEPs uncovered at the two-week sampling time, only 4 were associated with an mRNA in which a congruent temperature treatment difference was documented; all were of Symbiodinium origin (Table 2). In all cases, mRNA and protein expression were higher in samples of the high temperature treatment, and the overall congruency of 10.5% (4/38) was significantly higher than that of a temperature experiment with S. hystrix (Mayfield et al, 2016c): 2% (2-sample proportion test p<0.01). Congruency also differed significantly between compartments (2-sample proportion test p<0.05): 0% for the host (0/15 molecules showed a congruent response between mRNA and protein.)…”

Section: Resultsmentioning

confidence: 71%

“…For instance, if mRNA expression of a gene was significantly higher in samples of the C2 treatment relative to the H2 treatment, and the respective DEP was sequenced from the C2 2D gel, the mRNA and protein-level findings would be said to be congruent. Two-sample proportion tests were used to determine whether congruency differed significantly across compartments, as well as between this study and one featuring S. hystrix (Mayfield et al, 2016c).…”

Section: Methodsmentioning

confidence: 99%

“…Although protein homeostasis may indeed be ultimately implicated in coral acclimation to high temperatures, it is possible that the proteins encoded by the differentially expressed genes (DEGs) uncovered in the aforementioned transcriptomic analysis did not actually differ in expression between corals incubated at the control and high temperature treatments. In fact, the degree of congruency between mRNA and protein expression was markedly low in another pocilloporid, Seriatopora hystrix, exposed to either stable (26°C) or variable temperatures (23-29°C over a 6-hr period) for seven days (Mayfield et al, 2016c). Only 2 of the 167 differentially expressed proteins (DEPs) were associated with an mRNA that was also differentially expressed between treatments.…”

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Supplemental Information 2: Peptide Sequences for the Differentially Expressed Proteins (DEPs) Identified at the Four-Week Samp

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Although most reef-building corals live near the upper threshold of their thermotolerance, some scleractinians are resilient to temperature increases. For instance, Pocillopora acuta specimens from an upwelling habitat in Southern Taiwan survived a 9-month experimental exposure to 30°C, a temperature hypothesized to induce stress. To gain a greater understanding of the molecular pathways underlying such high-temperature acclimation, the protein profiles of experimental controls incubated at 27°C were compared to those of conspecific P. acuta specimens exposed to 30°C for two, four, or eight weeks, and differentially expressed proteins (DEPs) were removed from the protein gels and sequenced with mass spectrometry. Sixty unique DEPs were uncovered across both eukaryotic compartments of the P. acuta-dinoflagellate (genus Symbiodinium) mutualism, and Symbiodinium were more likely to up-regulate protein expression in response to high temperature exposure than the coral hosts in which they resided at the 2-week sampling time. Furthermore, different cellular pathways were affected by elevated temperature exposure in each compartment; Symbiodinium tended to up-regulate the expression of proteins involved in the cellular stress response, whereas the differentially expressed host coral proteome featured numerous proteins involved in cytoskeletal structure, immunity, and metabolism. These proteome-scale data suggest that the coral host and its intracellular dinoflagellates have differing cellular strategies for acclimating to elevated temperatures.PeerJ Preprints | https://doi.org/10.7287/peerj.preprints.3252v1 | CC BY 4.0 Open Access | rec AbstractAlthough most reef-building corals live near the upper threshold of their thermotolerance, some scleractinians are resilient to temperature increases. For instance, Pocillopora acuta specimens from an upwelling habitat in Southern Taiwan survived a nine-month experimental exposure to 30°C, a temperature hypothesized to induce stress. To gain a greater understanding of the molecular pathways underlying such high-temperature acclimation, the protein profiles of experimental controls incubated at 27°C were compared to those of conspecific P. acuta specimens exposed to 30°C for two, four, or eight weeks, and differentially expressed proteins (DEPs) were removed from the protein gels and sequenced with mass spectrometry. Sixty unique DEPs were uncovered across both eukaryotic compartments of the P. acuta-dinoflagellate (genus Symbiodinium) mutualism, and Symbiodinium were more likely to up-regulate protein expression in response to high temperature exposure than the coral hosts in which they resided at the twoweek sampling time. Furthermore, different cellular pathways were affected by elevated temperature exposure in each compartment; Symbiodinium tended to up-regulate the expression of proteins involved in the cellular stress response, whereas the differentially expressed host coral proteome featured numerous proteins involved in cytoskeletal structure, immunity, and metabolism. The...

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Dual‐compartmental transcriptomic + proteomic analysis of a marine endosymbiosis exposed to environmental change

Cited by 41 publications

References 28 publications

Identifying corals displaying aberrant behavior in Fiji’s Lau Archipelago

Identifying corals displaying aberrant behavior in Fiji’s Lau Archipelago

Population genetics of the coralAcropora millepora: Towards a genomic predictor of bleaching

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