Prolonged exposure to elevated CO2 promotes growth of the algal symbiont <i>Symbiodinium muscatinei</i> in the intertidal sea anemone <i>Anthopleura elegantissima</i>

Towanda, Trisha; Thuesen, Erik V.

doi:10.1242/bio.2012521

Cited by 33 publications

(65 citation statements)

References 69 publications

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“…This alkalinisation demonstrates the capacity of Symbiodinium cells to strongly buffer the external environmental pH signal, probably due to a fertilising effect on photosynthesis in these normally CO 2 -limited algae (Nimer et al, 1999). An increase in photosynthetic productivity after CO 2 addition has also been observed in other symbiotic associations, most notably in the temperate sea anemones Anemonia viridis (Suggett et al, 2012) and Anthopleura elegantissima (Towanda and Thuesen, 2012), and the benthic foraminiferan Marginopora vertebralis (Uthicke and Fabricius, 2012). The application of DCMU (a photosynthetic inhibitor) reversed the increase in pH i , confirming that the change was a direct consequence of photosynthesis, as the inhibited photosynthetic machinery of the symbionts is not able to ameliorate the increasing H + concentration (Fig.…”

Section: The Journal Of Experimental Biologysupporting

confidence: 57%

Intracellular pH and its response to CO2-driven seawater acidification in symbiotic versus non-symbiotic coral cells

Gibbin

Putnam

Davy

et al. 2014

Journal of Experimental Biology

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Regulating intracellular pH (pH i ) is critical for optimising the metabolic activity of corals, yet the mechanisms involved in pH regulation and the buffering capacity within coral cells are not well understood. Our study investigated how the presence of symbiotic dinoflagellates affects the response of pH i to P CO2 -driven seawater acidification in cells isolated from Pocillopora damicornis. Using the fluorescent dye BCECF-AM, in conjunction with confocal microscopy, we simultaneously characterised the pH i response in host coral cells and their dinoflagellate symbionts, in symbiotic and non-symbiotic states under saturating light, with and without the photosynthetic inhibitor DCMU. Each treatment was run under control (pH 7.8) and CO 2 -acidified seawater conditions (decreasing pH from 7.8 to 6.8). After 105 min of CO 2 addition, by which time the external pH (pH e ) had declined to 6.8, the dinoflagellate symbionts had increased their pH i by 0.5 pH units above control levels when in the absence of DCMU. In contrast, in both symbiotic and non-symbiotic host coral cells, 15 min of CO 2 addition (0.2 pH unit drop in pH e ) led to cytoplasmic acidosis equivalent to 0.3-0.4 pH units irrespective of whether DCMU was present. Despite further seawater acidification over the duration of the experiment, the pH i of non-symbiotic coral cells did not change, though in host cells containing a symbiont cell the pH i recovered to control levels when photsynthesis was not inhibited. This recovery was negated when cells were incubated with DCMU. Our results reveal that photosynthetic activity of the endosymbiont is tightly coupled with the ability of the host cell to recover from cellular acidosis after exposure to high CO 2 /low pH.

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Section: The Journal Of Experimental Biologysupporting

confidence: 57%

Intracellular pH and its response to CO2-driven seawater acidification in symbiotic versus non-symbiotic coral cells

Gibbin

Putnam

Davy

et al. 2014

Journal of Experimental Biology

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“…Indeed, the acoel worm Symsagittifera roscoffensis entering in symbiosis with the microalgae Tetraselmis convolutae shows a remarkable symbiosis stability even at a very low pH level (up to pH 6) [86]. In a second example, the sea anemone Anthopleura elegantissima / Symbiodinium muscatinei photosymbiosis, high p CO 2 level (pH 8.08 and pH 7.35) induces a higher rate of photosynthesis and mitotic index of the algae compared to pH 8.1 [87]. Under such conditions the cnidarian host received more of their respiratory carbon from the symbiont that under the actual pH condition [87].…”

Section: Discussionmentioning

confidence: 99%

“…In a second example, the sea anemone Anthopleura elegantissima / Symbiodinium muscatinei photosymbiosis, high p CO 2 level (pH 8.08 and pH 7.35) induces a higher rate of photosynthesis and mitotic index of the algae compared to pH 8.1 [87]. Under such conditions the cnidarian host received more of their respiratory carbon from the symbiont that under the actual pH condition [87]. These results taking together confirmed the hypothesis that photosymbiosis could be resistant to high p CO 2 , and that the negative effect of this high p CO 2 could be the results of indirect impact at other levels (hypothesis proposed in [86]).…”

Section: Discussionmentioning

confidence: 99%

Genes Related to Ion-Transport and Energy Production Are Upregulated in Response to CO2-Driven pH Decrease in Corals: New Insights from Transcriptome Analysis

et al. 2013

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Since the preindustrial era, the average surface ocean pH has declined by 0.1 pH units and is predicted to decline by an additional 0.3 units by the year 2100. Although subtle, this decreasing pH has profound effects on the seawater saturation state of carbonate minerals and is thus predicted to impact on calcifying organisms. Among these are the scleractinian corals, which are the main builders of tropical coral reefs. Several recent studies have evaluated the physiological impact of low pH, particularly in relation to coral growth and calcification. However, very few studies have focused on the impact of low pH at the global molecular level. In this context we investigated global transcriptomic modifications in a scleractinian coral (Pocillopora damicornis) exposed to pH 7.4 compared to pH 8.1during a 3-week period. The RNAseq approach shows that 16% of our transcriptome was affected by the treatment with 6% of upregulations and 10% of downregulations. A more detailed analysis suggests that the downregulations are less coordinated than the upregulations and allowed the identification of several biological functions of interest. In order to better understand the links between these functions and the pH, transcript abundance of 48 candidate genes was quantified by q-RT-PCR (corals exposed at pH 7.2 and 7.8 for 3 weeks). The combined results of these two approaches suggest that pH≥7.4 induces an upregulation of genes coding for proteins involved in calcium and carbonate transport, conversion of CO2 into HCO3 − and organic matrix that may sustain calcification. Concomitantly, genes coding for heterotrophic and autotrophic related proteins are upregulated. This can reflect that low pH may increase the coral energy requirements, leading to an increase of energetic metabolism with the mobilization of energy reserves. In addition, the uncoordinated downregulations measured can reflect a general trade-off mechanism that may enable energy reallocation.

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“…However, non-calcifying Anthozoans, such as sea anemones, have received less attention (Towanda & Thuesen, 2012). Anemonia viridis is a temperate Mediterranean species, which occurs naturally throughout Levante Bay.…”

Section: Introductionmentioning

confidence: 99%

Trace element profiles of the sea anemoneAnemonia viridisliving nearby a natural CO₂vent

Horwitz

Borell

Fine

et al. 2014

PeerJ

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Ocean acidification (OA) is not an isolated threat, but acts in concert with other impacts on ecosystems and species. Coastal marine invertebrates will have to face the synergistic interactions of OA with other global and local stressors. One local factor, common in coastal environments, is trace element contamination. CO2 vent sites are extensively studied in the context of OA and are often considered analogous to the oceans in the next few decades. The CO2 vent found at Levante Bay (Vulcano, NE Sicily, Italy) also releases high concentrations of trace elements to its surrounding seawater, and is therefore a unique site to examine the effects of long-term exposure of nearby organisms to high pCO2 and trace element enrichment in situ. The sea anemone Anemonia viridis is prevalent next to the Vulcano vent and does not show signs of trace element poisoning/stress. The aim of our study was to compare A. viridis trace element profiles and compartmentalization between high pCO2 and control environments. Rather than examining whole anemone tissue, we analyzed two different body compartments—the pedal disc and the tentacles, and also examined the distribution of trace elements in the tentacles between the animal and the symbiotic algae. We found dramatic changes in trace element tissue concentrations between the high pCO2/high trace element and control sites, with strong accumulation of iron, lead, copper and cobalt, but decreased concentrations of cadmium, zinc and arsenic proximate to the vent. The pedal disc contained substantially more trace elements than the anemone’s tentacles, suggesting the pedal disc may serve as a detoxification/storage site for excess trace elements. Within the tentacles, the various trace elements displayed different partitioning patterns between animal tissue and algal symbionts. At both sites iron was found primarily in the algae, whereas cadmium, zinc and arsenic were primarily found in the animal tissue. Our data suggests that A. viridis regulates its internal trace element concentrations by compartmentalization and excretion and that these features contribute to its resilience and potential success at the trace element-rich high pCO2 vent.

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Prolonged exposure to elevated CO2 promotes growth of the algal symbiont Symbiodinium muscatinei in the intertidal sea anemone Anthopleura elegantissima

Cited by 33 publications

References 69 publications

Intracellular pH and its response to CO2-driven seawater acidification in symbiotic versus non-symbiotic coral cells

Intracellular pH and its response to CO2-driven seawater acidification in symbiotic versus non-symbiotic coral cells

Genes Related to Ion-Transport and Energy Production Are Upregulated in Response to CO2-Driven pH Decrease in Corals: New Insights from Transcriptome Analysis

Trace element profiles of the sea anemoneAnemonia viridisliving nearby a natural CO₂vent

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Prolonged exposure to elevated CO2 promotes growth of the algal symbiont Symbiodinium muscatinei in the intertidal sea anemone Anthopleura elegantissima

Cited by 33 publications

References 69 publications

Intracellular pH and its response to CO2-driven seawater acidification in symbiotic versus non-symbiotic coral cells

Intracellular pH and its response to CO2-driven seawater acidification in symbiotic versus non-symbiotic coral cells

Genes Related to Ion-Transport and Energy Production Are Upregulated in Response to CO2-Driven pH Decrease in Corals: New Insights from Transcriptome Analysis

Trace element profiles of the sea anemoneAnemonia viridisliving nearby a natural CO2vent

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Product

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Trace element profiles of the sea anemoneAnemonia viridisliving nearby a natural CO₂vent