Complex Diel Cycles of Gene Expression in Coral-Algal Symbiosis

Levy, Oren; Kaniewska, Paulina; Alon, Shahar; Eisenberg, Eli; Karako-Lampert, Sarit; Bay, Line K.; Reef, Ruth; Rodríguez-Lanetty, Mauricio; Miller, David J.; Høegh-Guldberg, Ove

doi:10.1126/science.1196419

Cited by 114 publications

(150 citation statements)

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“…These hemoproteins may function as post-translationally activated redox-regulated nitrite reductases that could mediate the NO response to cause cnidarian bleaching. Separate from the hemoproteins of metabolism and photosynthesis, these oxygen-binding globins may serve additionally as O 2 sensors to activate cellular defense pathways by regulating the transcription of protective oxygen-responsive genes (95), particularly those factors activated in response to hypoxia (96), an usual condition of coral tissues during dark respiration (18). Expressed also are the ubiquitous ferritin intracellular iron storage proteins providing iron homeostasis in heme metabolism (Table IV).…”

Section: Discussionmentioning

confidence: 99%

A Profile of an Endosymbiont-enriched Fraction of the Coral Stylophora pistillata Reveals Proteins Relevant to Microbial-Host Interactions

Weston

Dunlap

Shick

et al. 2012

Molecular & Cellular Proteomics

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This study examines the response of Symbiodinium sp. endosymbionts from the coral Stylophora pistillata to moderate levels of thermal "bleaching" stress, with and without trace metal limitation. Using quantitative high throughput proteomics, we identified 8098 MS/MS events relating to individual peptides from the endosymbiontenriched fraction, including 109 peptides meeting stringent criteria for quantification, of which only 26 showed significant change in our experimental treatments; 12 of 26 increased expression in response to thermal stress with little difference affected by iron limitation. Surprisingly, there were no significant increases in antioxidant or heat stress proteins; those induced to higher expression were generally involved in protein biosynthesis. An outstanding exception was a massive 114-fold increase of a viral replication protein indicating that thermal stress may substantially increase viral load and thereby contribute to the etiology of coral bleaching and disease. In the absence of a sequenced genome for Symbiodinium or other photosymbiotic dinoflagellate, this proteome reveals a plethora of proteins potentially involved in microbial-host interactions. This includes photosystem proteins, DNA repair enzymes, antioxidant enzymes, metabolic redox enzymes, heat shock proteins, globin hemoproteins, proteins of nitrogen metabolism, and a wide range of viral proteins associated with these endosymbiont-enriched samples. Also present were 21 unusual peptide/protein toxins thought to originate from either microbial consorts or from contamination by coral nematocysts. Of particular interest are the proteins of apoptosis, vesicular transport, and endo/exocytosis, which are discussed in context of the cellular processes of coral bleaching. Notably, the protein complement provides evidence that, rather than being expelled by the host, stressed endosymbionts may mediate their own departure.

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Section: Discussionmentioning

confidence: 99%

A Profile of an Endosymbiont-enriched Fraction of the Coral Stylophora pistillata Reveals Proteins Relevant to Microbial-Host Interactions

Weston

Dunlap

Shick

et al. 2012

Molecular & Cellular Proteomics

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“…Physiological tuning of coral metabolism to light has been studied for several years. The expression of genes and proteins linked to cellular redox states, division rates of both endoderm cells and symbionts, and rates of calcification all show diel periodicity (Wilkerson et al, 1983;Fitt, 2000;Levy et al, 2006;Levy et al, 2011;Tambutté et al, 2011). The potential role of light-driven pHi variation in contributing to regulation of coral cell physiology is worthy of future research.…”

Section: Discussionmentioning

confidence: 99%

The influence of photosynthesis on host intracellular pH in scleractinian corals

Laurent

Tambutté

et al. 2012

Journal of Experimental Biology

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SUMMARYThe regulation of intracellular pH (pHi) is a fundamental aspect of cell physiology that has received little attention in studies of reef-building corals and symbiotic cnidarians. Here, we investigated the hypothesis that dynamic changes in the pHi of coral host cells are controlled by the photosynthetic activity of the coralʼs dinoflagellate symbionts. Using live cell imaging and the pHsensitive dye SNARF-1, we tracked pH in symbiont-containing and symbiont-free cells isolated from the reef coral Stylophora pistillata. We characterised the response of coral pHi in the presence of a photosynthetic inhibitor, the dynamics of coral pHi during light exposure and how pHi values vary on exposure to a range of irradiance levels lying within the coralʼs photosynthesis-irradiance response curve. Our results demonstrate that increases in coral pHi are dependent on photosynthetic activity of intracellular symbionts and that pHi recovers under darkness to values that match those of symbiont-free cells. Furthermore, we show that the timing of the pHi response is governed by irradiance level and that pHi increases to irradiancespecific steady-state values. Minimum steady-state pHi values of 7.05±0.05 were obtained under darkness and maximum values of 7.46±0.07 were obtained under saturating irradiance. As changes in pHi often affect organism homeostasis, there is a need for continued research into acid/base regulation in symbiotic corals. More generally, these results represent the first characterization of photosynthesis-driven pHi changes in animal cells. Supplementary material available online at

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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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Complex Diel Cycles of Gene Expression in Coral-Algal Symbiosis

Cited by 114 publications

References 10 publications

A Profile of an Endosymbiont-enriched Fraction of the Coral Stylophora pistillata Reveals Proteins Relevant to Microbial-Host Interactions

A Profile of an Endosymbiont-enriched Fraction of the Coral Stylophora pistillata Reveals Proteins Relevant to Microbial-Host Interactions

The influence of photosynthesis on host intracellular pH in scleractinian corals

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

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