Title: Gene expression response under thermal stress in two Hawaiian corals is dominated by ploidy and genotype
Abstract Transcriptome data are frequently used to investigate coral bleaching; however, the factors controlling gene expression in natural populations of these species are poorly understood. We studied two corals,Montipora capitataandPocillopora acuta, that inhabit the sheltered Kāne'ohe Bay, Hawai'i.M. capitatacolonies in the bay are outbreeding diploids, whereasP. acutais a mixture of clonal diploids and triploids. Populations were sampled from six reefs and subjected to either control (no stress), thermal stress, pH stress, or combined pH and thermal stress treatments. RNA‐seq data were generated to test two competing hypotheses: (1) gene expression is largely independent of genotype, reflecting a shared treatment‐driven response (TDE) or, (2) genotype dominates gene expression, regardless of treatment (GDE). Our results strongly support the GDE model, even under severe stress. We suggest that post‐transcriptional processes (e.g., control of translation, protein turnover) modify the signal from the transcriptome, and may underlie the observed differences in coral bleaching sensitivity via the downstream proteome and metabolome. more »« less
Williams, Amanda; Chiles, Eric N.; Conetta, Dennis; Pathmanathan, Jananan S.; Cleves, Phillip A.; Putnam, Hollie M.; Su, Xiaoyang; Bhattacharya, Debashish
(, Science Advances)
null
(Ed.)
Understanding the response of the coral holobiont to environmental change is crucial to inform conservation efforts. The most pressing problem is “coral bleaching,” usually precipitated by prolonged thermal stress. We used untargeted, polar metabolite profiling to investigate the physiological response of the coral species Montipora capitata and Pocillopora acuta to heat stress. Our goal was to identify diagnostic markers present early in the bleaching response. From the untargeted UHPLC-MS data, a variety of co-regulated dipeptides were found that have the highest differential accumulation in both species. The structures of four dipeptides were determined and showed differential accumulation in symbiotic and aposymbiotic (alga-free) populations of the sea anemone Aiptasia ( Exaiptasia pallida ), suggesting the deep evolutionary origins of these dipeptides and their involvement in symbiosis. These and other metabolites may be used as diagnostic markers for thermal stress in wild coral.
Understanding the response of the coral holobiont to environmental change is crucial to inform conservation efforts. The most pressing problem is “coral bleaching,” usually precipitated by prolonged thermal stress. We used untargeted, polar metabolite profiling to investigate the physiological response of the coral species Montipora capitata and Pocillopora acuta to heat stress. Our goal was to identify diagnostic markers present early in the bleaching response. From the untargeted UHPLC-MS data, a variety of co-regulated dipeptides were found that have the highest differential accumulation in both species. The structures of four dipeptides were determined and showed differential accumulation in symbiotic and aposymbiotic (alga-free) populations of the sea anemone Aiptasia (Exaiptasia pallida), suggesting the deep evolutionary origins of these dipeptides and their involvement in symbiosis. These and other metabolites may be used as diagnostic markers for thermal stress in wild coral.
Abstract Coral bleaching, precipitated by the expulsion of the algal symbionts that provide colonies with fixed carbon is a global threat to reef survival. To protect corals from anthropogenic stress, portable tools are needed to detect and diagnose stress syndromes and assess population health prior to extensive bleaching. Here, medical grade Urinalysis strips, used to detect an array of disease markers in humans, were tested on the lab stressed Hawaiian coral species,Montipora capitata(stress resistant) andPocillopora acuta(stress sensitive), as well as samples from nature that also includedPorites compressa. Of the 10 diagnostic reagent tests on these strips, two appear most applicable to corals: ketone and leukocytes. The test strip results fromM. capitatawere explored using existing transcriptomic data from the same samples and provided evidence of the stress syndromes detected by the strips. We designed a 3D printed smartphone holder and image processing software for field analysis of test strips (TestStripDX) and devised a simple strategy to generate color scores for corals (reflecting extent of bleaching) using a smartphone camera (CoralDX). Our approaches provide field deployable methods, that can be improved in the future (e.g., coral-specific stress test strips) to assess reef health using inexpensive tools and freely available software.
Williams, Amanda; Pathmanathan, Jananan S.; Stephens, Timothy G.; Su, Xiaoyang; Chiles, Eric N.; Conetta, Dennis; Putnam, Hollie M.; Bhattacharya, Debashish
(, PeerJ)
Background Corals, which form the foundation of biodiverse reef ecosystems, are under threat from warming oceans. Reefs provide essential ecological services, including food, income from tourism, nutrient cycling, waste removal, and the absorption of wave energy to mitigate erosion. Here, we studied the coral thermal stress response using network methods to analyze transcriptomic and polar metabolomic data generated from the Hawaiian rice coral Montipora capitata . Coral nubbins were exposed to ambient or thermal stress conditions over a 5-week period, coinciding with a mass spawning event of this species. The major goal of our study was to expand the inventory of thermal stress-related genes and metabolites present in M. capitata and to study gene-metabolite interactions. These interactions provide the foundation for functional or genetic analysis of key coral genes as well as provide potentially diagnostic markers of pre-bleaching stress. A secondary goal of our study was to analyze the accumulation of sex hormones prior to and during mass spawning to understand how thermal stress may impact reproductive success in M. capitata . Methods M. capitata was exposed to thermal stress during its spawning cycle over the course of 5 weeks, during which time transcriptomic and polar metabolomic data were collected. We analyzed these data streams individually, and then integrated both data sets using MAGI (Metabolite Annotation and Gene Integration) to investigate molecular transitions and biochemical reactions. Results Our results reveal the complexity of the thermal stress phenome in M. capitata , which includes many genes involved in redox regulation, biomineralization, and reproduction. The size and number of modules in the gene co-expression networks expanded from the initial stress response to the onset of bleaching. The later stages involved the suppression of metabolite transport by the coral host, including a variety of sodium-coupled transporters and a putative ammonium transporter, possibly as a response to reduction in algal productivity. The gene-metabolite integration data suggest that thermal treatment results in the activation of animal redox stress pathways involved in quenching molecular oxygen to prevent an overabundance of reactive oxygen species. Lastly, evidence that thermal stress affects reproductive activity was provided by the downregulation of CYP-like genes and the irregular production of sex hormones during the mass spawning cycle. Overall, redox regulation and metabolite transport are key components of the coral animal thermal stress phenome. Mass spawning was highly attenuated under thermal stress, suggesting that global climate change may negatively impact reproductive behavior in this species.
Price, James T; McLachlan, Rowan H; Jury, Christopher P; Toonen, Robert J; Wilkins, Michael J; Grottoli, Andréa G
(, PLOS ONE)
Keshavmurthy, Shashank
(Ed.)
The plasticity of some coral-associated microbial communities under stressors like warming and ocean acidification suggests the microbiome has a role in the acclimatization of corals to future ocean conditions. Here, we evaluated the acclimatization potential of coral-associated microbial communities of four Hawaiian coral species (Porites compressa,Porites lobata,Montipora capitata, andPocillopora acuta) over 22-month mesocosm experiment. The corals were exposed to one of four treatments: control, ocean acidification, ocean warming, or combined future ocean conditions. Over the 22-month study, 33–67% of corals died or experienced a loss of most live tissue coverage in the ocean warming and future ocean treatments while only 0–10% died in the ocean acidification and control. Among the survivors, coral-associated microbial communities responded to the chronic future ocean treatment in one of two ways: (1) microbial communities differed between the control and future ocean treatment, suggesting the potential capacity for acclimatization, or (2) microbial communities did not significantly differ between the control and future ocean treatment. The first strategy was observed in bothPoritesspecies and was associated with higher survivorship compared toM.capitataandP.acutawhich exhibited the second strategy. Interestingly, the microbial community responses to chronic stressors were independent of coral physiology. These findings indicate acclimatization of microbial communities may confer resilience in some species of corals to chronic warming associated with climate change. However,M.capitatagenets that survived the future ocean treatment hosted significantly different microbial communities from those that died, suggesting the microbial communities of the survivors conferred some resilience. Thus, even among coral species with inflexible microbial communities, some individuals may already be tolerant to future ocean conditions. These findings suggest that coral-associated microbial communities could play an important role in the persistence of some corals and underlie climate change-driven shifts in coral community composition.
Chille, Erin_E, Stephens, Timothy_G, Misri, Deeksha, Strand, Emma_L, Putnam, Hollie_M, and Bhattacharya, Debashish. Gene expression response under thermal stress in two Hawaiian corals is dominated by ploidy and genotype. Ecology and Evolution 14.7 Web. doi:10.1002/ece3.70037.
Chille, Erin_E, Stephens, Timothy_G, Misri, Deeksha, Strand, Emma_L, Putnam, Hollie_M, & Bhattacharya, Debashish. Gene expression response under thermal stress in two Hawaiian corals is dominated by ploidy and genotype. Ecology and Evolution, 14 (7). https://doi.org/10.1002/ece3.70037
Chille, Erin_E, Stephens, Timothy_G, Misri, Deeksha, Strand, Emma_L, Putnam, Hollie_M, and Bhattacharya, Debashish.
"Gene expression response under thermal stress in two Hawaiian corals is dominated by ploidy and genotype". Ecology and Evolution 14 (7). Country unknown/Code not available: Wiley Blackwell (John Wiley & Sons). https://doi.org/10.1002/ece3.70037.https://par.nsf.gov/biblio/10576939.
@article{osti_10576939,
place = {Country unknown/Code not available},
title = {Gene expression response under thermal stress in two Hawaiian corals is dominated by ploidy and genotype},
url = {https://par.nsf.gov/biblio/10576939},
DOI = {10.1002/ece3.70037},
abstractNote = {Abstract Transcriptome data are frequently used to investigate coral bleaching; however, the factors controlling gene expression in natural populations of these species are poorly understood. We studied two corals,Montipora capitataandPocillopora acuta, that inhabit the sheltered Kāne'ohe Bay, Hawai'i.M. capitatacolonies in the bay are outbreeding diploids, whereasP. acutais a mixture of clonal diploids and triploids. Populations were sampled from six reefs and subjected to either control (no stress), thermal stress, pH stress, or combined pH and thermal stress treatments. RNA‐seq data were generated to test two competing hypotheses: (1) gene expression is largely independent of genotype, reflecting a shared treatment‐driven response (TDE) or, (2) genotype dominates gene expression, regardless of treatment (GDE). Our results strongly support the GDE model, even under severe stress. We suggest that post‐transcriptional processes (e.g., control of translation, protein turnover) modify the signal from the transcriptome, and may underlie the observed differences in coral bleaching sensitivity via the downstream proteome and metabolome.},
journal = {Ecology and Evolution},
volume = {14},
number = {7},
publisher = {Wiley Blackwell (John Wiley & Sons)},
author = {Chille, Erin_E and Stephens, Timothy_G and Misri, Deeksha and Strand, Emma_L and Putnam, Hollie_M and Bhattacharya, Debashish},
}
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