Differential Responses of the Coral Host and Their Algal Symbiont to Thermal Stress

Leggat, William; Seneca, François O.; Wasmund, Kenneth; Ukani, Lubna; Yellowlees, David; Ainsworth, Tracy D.

doi:10.1371/journal.pone.0026687

Cited by 141 publications

(160 citation statements)

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“…A recent study by Wright et al (2015) also found differential expression of genes related to oxidative stress and translation in diseased tissues. In comparison, transcriptomic adjustment in Symbiodinium was marginal, i.e., only few genes were regulated but with pronounced fold-changes, which aligns with previous stress studies (Leggat et al, 2011;Baumgarten et al, 2013;Libro et al, 2013;Barshis et al, 2014). WPD microbiomes have been shown to reflect increased bacterial diversity compared to healthy consortia in 16S based surveys (Sunagawa et al, 2009;Roder et al, 2014a,b).…”

Section: Discussion All Holobiont Compartments Respond To Coral Diseasesupporting

confidence: 86%

Metatranscriptome analysis of the reef-building coral Orbicella faveolata indicates holobiont response to coral disease

et al. 2015

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White Plague Disease (WPD) is implicated in coral reef decline in the Caribbean and is characterized by microbial community shifts in coral mucus and tissue. Studies thus far have focused on assessing microbial communities or the identification of specific pathogens, yet few have addressed holobiont response across metaorganism compartments in coral disease. Here, we report on the first metatranscriptomic assessment of the coral host, algal symbiont, and microbial compartment in order to survey holobiont structure and function in healthy and diseased samples from Orbicella faveolata collected at reef sites off Puerto Rico. Our data indicate holobiont-wide as well as compartment-specific responses to WPD. Gene expression changes in the diseased coral host involved proteins playing a role in innate immunity, cytoskeletal integrity, cell adhesion, oxidative stress, chemical defense, and retroelements. In contrast, the algal symbiont showed comparatively few expression changes, but of large magnitude, of genes related to stress, photosynthesis, and metal transport. Concordant with the coral host response, the bacterial compartment showed increased abundance of heat shock proteins, genes related to oxidative stress, DNA repair, and potential retroelement activity. Importantly, analysis of the expressed bacterial gene functions establishes the participation of multiple bacterial families in WPD pathogenesis and also suggests a possible involvement of viruses and/or phages in structuring the bacterial assemblage. In this study, we implement an experimental approach to partition the coral holobiont and resolve compartment-and taxa-specific responses in order to understand metaorganism function in coral disease.

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Section: Discussion All Holobiont Compartments Respond To Coral Diseasesupporting

confidence: 86%

Metatranscriptome analysis of the reef-building coral Orbicella faveolata indicates holobiont response to coral disease

et al. 2015

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“…DeSalvo et al, 2008;Bay et al, 2009;Császár et al, 2009;Reyes-Bermudez et al, 2009;Voolstra et al, 2009;DeSalvo et al, 2010;Portune et al, 2010;Starcevic et al, 2010;Hoogenboom et al, 2011;Kenkel et al, 2011;Leggat et al, 2011;Levy et al, 2011), generating a wealth of potentially interesting findings with regard to the molecular capacity of corals to acclimate to changes they may face over the Site of origin (SO), temperature treatment (TT) and interaction effects were deemed statistically significant at P<0.05 and, in such cases, are denoted by a tick. Only response variables for which significant differences were detected have been included..…”

Section: Methodological Quality Controlmentioning

confidence: 99%

The effects of a variable temperature regime on the physiology of the reef-building coralSeriatopora hystrix: results from a laboratory-based reciprocal transplant

Mayfield

Chan

Putnam

et al. 2012

Journal of Experimental Biology

104

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SUMMARYTo understand the effects of global climate change on reef-building corals, a thorough investigation of their physiological mechanisms of acclimatization is warranted. However, static temperature manipulations may underestimate the thermal complexity of the reefs in which many corals live. For instance, corals of Houbihu, Taiwan, experience changes in temperature of up to 10°C over the course of a day during spring-tide upwelling events. To better understand the phenotypic plasticity of these corals, a laboratory-based experiment was conducted whereby specimens of Seriatopora hystrix from an upwelling reef (Houbihu) and conspecifics from a non-upwelling reef (Houwan) were exposed to both a stable seawater temperature (26°C) regime and a regime characterized by a 6°C fluctuation (23-29°C) over a 12h period for 7days. A suite of physiological and molecular parameters was measured in samples of both treatments, as well as in experimental controls, to determine site of origin (SO) and temperature treatment (TT) responses. Only chlorophyll a (chl a) concentration and growth demonstrated the hypothesized trend of higher levels when exposed to a TT that mimicked SO conditions. In contrast, chl a, maximum dark-adapted quantum yield of photosystem II (F v /F m ), and Symbiodinium ribulose-1,5-bisphosphate carboxylase/oxygenase (rbcL), photosystem I (psI, subunit III) and phosphoglycolate phosphatase (pgpase) mRNA expression demonstrated significant TT effects. Specifically, levels of these response variables were higher in samples exposed to a variable temperature regime, suggesting that S. hystrix may acclimate to fluctuating temperatures by increasing its capacity for photosynthesis.Supplementary material available online at http://jeb.biologists.org/cgi/content/full/215/23/4183/DC1 Key words: acclimation, coral reef, endosymbiosis, gene expression, photosynthesis, Symbiodinium. susceptible to impact by unexpected environmental variability, and results must always be interpreted conservatively.With this in mind, by conducting a laboratory-based reciprocal transplant (LBRT) study, we took advantage of the thermally unique and dynamic environments of southern Taiwan in order to gain insight into how a common reef-building scleractinian, Seriatopora hystrix Dana 1846, acclimates to changes in seawater temperature. Coral colonies were collected from both Houbihu, a reef within Nanwan Bay that experiences episodic summer upwelling (Putnam et al., 2010), and Houwan, a reef on the western side of the Hengchun Peninsula that does not experience this phenomenon, and specimens from each site were incubated at either stable (26°C) or variable (23-29°C over a 12h period) temperature for 7days. This laboratory-based approach was also utilized in place of a reciprocal transplant in situ because of the multitude of other abiotic parameters (e.g. nutrient and dissolved oxygen levels) that are affected by upwelling events in Taiwan (Chen et al., 2004); while the physiological response to upwelling is indeed a worthy avenue ...

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“…Severe bleaching leaves corals covered with translucent tissue, allowing the white skeleton to show through and, without their algal partners, corals can become more vulnerable to other threats and stressors, such as starvation and disease (Gates et al, 1992). Although a large number of studies have documented strong gene expression changes associated with bleaching conditions, little is known about whether these patterns are part of the bleaching reaction itself or part of the heat stress response that is seen in most animals, plants and fungi (Barshis et al, 2013;Bay and Palumbi, 2015;Dixon et al, 2015;Leggat et al, 2011;Meyer et al, 2009;Pinzon et al, 2015;Rose et al, 2015;RuizJones andPalumbi, 2014, 2015;Seneca and Palumbi, 2015). Most transcriptomics projects are based on slurries of tissue from corals and so information concerning specificity in cell expression is lost.…”

Section: Introductionmentioning

confidence: 99%

The cell specificity of gene expression in the response to heat stress in corals

Traylor-Knowles

Rose

Palumbi

2017

Journal of Experimental Biology

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Previous transcriptional studies in heat-stressed corals have shown that many genes are responsive to generalized heat stress whereas the expression patterns of specific gene networks after heat stress show strong correlations with variation in bleaching outcomes. However, where these specific genes are expressed is unknown. In this study, we employed in situ hybridization to identify patterns of spatial gene expression of genes previously predicted to be involved in general stress response and bleaching. We found that tumor necrosis factor receptors (TNFRs), known to be strong responders to heat stress, were not expressed in gastrodermal symbiont-containing cells but were widely expressed in specific cells of the epidermal layer. The transcription factors AP-1 and FosB, implicated as early signals of heat stress, were widely expressed throughout the oral gastrodermis and epidermis. By contrast, a G protein-coupled receptor gene (GPCR) and a fructose bisphosphate aldolase C gene (aldolase), previously implicated in bleaching, were expressed in symbiont-containing gastrodermal cells and in the epidermal tissue. Finally, chordin-like/kielin (chordin-like), a gene highly correlated to bleaching, was expressed solely in the oral gastrodermis. From this study, we confirm that heat-responsive genes occur widely in coral tissues outside of symbiont-containing cells. Joint information about expression patterns in response to heat and cell specificity will allow greater dissection of the regulatory pathways and specific cell reactions that lead to coral bleaching.

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Differential Responses of the Coral Host and Their Algal Symbiont to Thermal Stress

Cited by 141 publications

References 59 publications

Metatranscriptome analysis of the reef-building coral Orbicella faveolata indicates holobiont response to coral disease

Metatranscriptome analysis of the reef-building coral Orbicella faveolata indicates holobiont response to coral disease

The effects of a variable temperature regime on the physiology of the reef-building coralSeriatopora hystrix: results from a laboratory-based reciprocal transplant

The cell specificity of gene expression in the response to heat stress in corals

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