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Host Coenzyme Q Redox State Is an Early Biomarker of Thermal Stress in the Coral Acropora millepora.

Lutz A, Raina JB, Motti CA, Miller DJ, van Oppen MJ - PLoS ONE (2015)

Bottom Line: The current consensus is that this phenomenon results from enhanced production of harmful reactive oxygen species (ROS) that disrupt the symbiosis between corals and their endosymbiotic dinoflagellates, Symbiodinium.The results show that the responses of the two antioxidant systems occur on different timescales: (i) the redox state of the Symbiodinium PQ pool remained stable until twelve days into the experiment, after which there was an abrupt oxidative shift; (ii) by contrast, an oxidative shift of approximately 10% had occurred in the host CoQ pool after 6 days of thermal stress, prior to significant changes in any other physiological parameter measured.Host CoQ pool oxidation is thus an early biomarker of thermal stress in corals, and this antioxidant pool is likely to play a key role in quenching thermally-induced ROS in the coral-algal symbiosis.

View Article: PubMed Central - PubMed

Affiliation: AIMS@JCU, James Cook University, Townsville, Queensland, Australia; Australian Institute of Marine Science, Townsville, Queensland, Australia; Comparative Genomics Centre and Department of Molecular and Cell Biology, James Cook University, Townsville, Queensland, Australia; ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland, Australia.

ABSTRACT
Bleaching episodes caused by increasing seawater temperatures may induce mass coral mortality and are regarded as one of the biggest threats to coral reef ecosystems worldwide. The current consensus is that this phenomenon results from enhanced production of harmful reactive oxygen species (ROS) that disrupt the symbiosis between corals and their endosymbiotic dinoflagellates, Symbiodinium. Here, the responses of two important antioxidant defence components, the host coenzyme Q (CoQ) and symbiont plastoquinone (PQ) pools, are investigated for the first time in colonies of the scleractinian coral, Acropora millepora, during experimentally-induced bleaching under ecologically relevant conditions. Liquid chromatography-mass spectrometry (LC-MS) was used to quantify the states of these two pools, together with physiological parameters assessing the general state of the symbiosis (including photosystem II photochemical efficiency, chlorophyll concentration and Symbiodinium cell densities). The results show that the responses of the two antioxidant systems occur on different timescales: (i) the redox state of the Symbiodinium PQ pool remained stable until twelve days into the experiment, after which there was an abrupt oxidative shift; (ii) by contrast, an oxidative shift of approximately 10% had occurred in the host CoQ pool after 6 days of thermal stress, prior to significant changes in any other physiological parameter measured. Host CoQ pool oxidation is thus an early biomarker of thermal stress in corals, and this antioxidant pool is likely to play a key role in quenching thermally-induced ROS in the coral-algal symbiosis. This study adds to a growing body of work that indicates host cellular responses may precede the bleaching process and symbiont dysfunction.

No MeSH data available.


Related in: MedlinePlus

Effects of thermal stress on physiological parameters of the scleractinian coral Acropora millepora.Images of representative coral nubbins demonstrating the visual difference in Symbiodinium cell densities within A. millepora tissues under control (27°C) (A—B) and thermal stress (32°C) (C—D) conditions at day 17 (end of experiment). Scale bars = 1 mm. Thermal stress effects on (E) Symbiodinium density; (F) photosystem II photochemical efficiency; (G) plastoquinone (%PQH2) and (H) coenzyme Q (%CoQH2) pool redox states; (I) total plastoquinone concentration (PQ + PQH2) per Symbiodinium cell and (J) total coenzyme Q concentration (CoQ + CoQH2) per coral surface area over the course of the experiment. All data points are means ± 95% CI; * indicate significant differences between control and treatment at p < 0.05; n = 6–12 (see Table 1 for details).
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pone.0139290.g002: Effects of thermal stress on physiological parameters of the scleractinian coral Acropora millepora.Images of representative coral nubbins demonstrating the visual difference in Symbiodinium cell densities within A. millepora tissues under control (27°C) (A—B) and thermal stress (32°C) (C—D) conditions at day 17 (end of experiment). Scale bars = 1 mm. Thermal stress effects on (E) Symbiodinium density; (F) photosystem II photochemical efficiency; (G) plastoquinone (%PQH2) and (H) coenzyme Q (%CoQH2) pool redox states; (I) total plastoquinone concentration (PQ + PQH2) per Symbiodinium cell and (J) total coenzyme Q concentration (CoQ + CoQH2) per coral surface area over the course of the experiment. All data points are means ± 95% CI; * indicate significant differences between control and treatment at p < 0.05; n = 6–12 (see Table 1 for details).

Mentions: A. millepora colony fragments exposed to hyperthermal stress (32°C) showed clear symptoms of bleaching, when compared to ambient (27°C) treatment controls (Fig 2A–2D). In the thermal stress treatment group, Symbiodinium cell densities were reduced by 25.7% after five days and by 82.4% at the end of the experiment (Fig 2E). No significant changes were observed in cellular chlorophyll concentrations (a and c2) during the experiment (mean = 29.6 ± 4.5 pg cell−1; p = 0.46). Mortality was low; of the 24 colony fragments used, only two of the 12 exposed to thermal stress showed signs of necrosis, patchy tissue sloughing and algal overgrowth. No further data were collected for these fragments after day 13 and 15, respectively, when symptoms of mortality were first observed. PSII photochemical efficiency (FV/FM ± 95% confidence interval (CI)) remained stable in control colonies (mean = 0.68 ± 0.1) but declined markedly in the 32°C treatment group concomitant with the loss of Symbiodinium cells after day 9 (Fig 2F; p < 0.001; Table 1). The declining trend of FV/FM was observable from the third day after heating commenced; however, FV/FM did not differ significantly from control samples until day five (t-test; F1,278 = 10.683; p = 0.0012). TEM images showed no impact on the Symbiodinium thylakoid membrane or cell wall structure in the first seven days of the experiment; however, disintegrated internal organelles were observed in 7% of the cells examined (total 1502). After five days exposure to 32°C (t = 12 d), all of the remaining Symbiodinium cells exhibited both structurally compromised thylakoid membranes and widespread disintegration of organelles in the cytoplasm (Fig 3). While damage to internal structures was apparent, cell walls appeared intact and no fragmented symbiont cells were observed.


Host Coenzyme Q Redox State Is an Early Biomarker of Thermal Stress in the Coral Acropora millepora.

Lutz A, Raina JB, Motti CA, Miller DJ, van Oppen MJ - PLoS ONE (2015)

Effects of thermal stress on physiological parameters of the scleractinian coral Acropora millepora.Images of representative coral nubbins demonstrating the visual difference in Symbiodinium cell densities within A. millepora tissues under control (27°C) (A—B) and thermal stress (32°C) (C—D) conditions at day 17 (end of experiment). Scale bars = 1 mm. Thermal stress effects on (E) Symbiodinium density; (F) photosystem II photochemical efficiency; (G) plastoquinone (%PQH2) and (H) coenzyme Q (%CoQH2) pool redox states; (I) total plastoquinone concentration (PQ + PQH2) per Symbiodinium cell and (J) total coenzyme Q concentration (CoQ + CoQH2) per coral surface area over the course of the experiment. All data points are means ± 95% CI; * indicate significant differences between control and treatment at p < 0.05; n = 6–12 (see Table 1 for details).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4591267&req=5

pone.0139290.g002: Effects of thermal stress on physiological parameters of the scleractinian coral Acropora millepora.Images of representative coral nubbins demonstrating the visual difference in Symbiodinium cell densities within A. millepora tissues under control (27°C) (A—B) and thermal stress (32°C) (C—D) conditions at day 17 (end of experiment). Scale bars = 1 mm. Thermal stress effects on (E) Symbiodinium density; (F) photosystem II photochemical efficiency; (G) plastoquinone (%PQH2) and (H) coenzyme Q (%CoQH2) pool redox states; (I) total plastoquinone concentration (PQ + PQH2) per Symbiodinium cell and (J) total coenzyme Q concentration (CoQ + CoQH2) per coral surface area over the course of the experiment. All data points are means ± 95% CI; * indicate significant differences between control and treatment at p < 0.05; n = 6–12 (see Table 1 for details).
Mentions: A. millepora colony fragments exposed to hyperthermal stress (32°C) showed clear symptoms of bleaching, when compared to ambient (27°C) treatment controls (Fig 2A–2D). In the thermal stress treatment group, Symbiodinium cell densities were reduced by 25.7% after five days and by 82.4% at the end of the experiment (Fig 2E). No significant changes were observed in cellular chlorophyll concentrations (a and c2) during the experiment (mean = 29.6 ± 4.5 pg cell−1; p = 0.46). Mortality was low; of the 24 colony fragments used, only two of the 12 exposed to thermal stress showed signs of necrosis, patchy tissue sloughing and algal overgrowth. No further data were collected for these fragments after day 13 and 15, respectively, when symptoms of mortality were first observed. PSII photochemical efficiency (FV/FM ± 95% confidence interval (CI)) remained stable in control colonies (mean = 0.68 ± 0.1) but declined markedly in the 32°C treatment group concomitant with the loss of Symbiodinium cells after day 9 (Fig 2F; p < 0.001; Table 1). The declining trend of FV/FM was observable from the third day after heating commenced; however, FV/FM did not differ significantly from control samples until day five (t-test; F1,278 = 10.683; p = 0.0012). TEM images showed no impact on the Symbiodinium thylakoid membrane or cell wall structure in the first seven days of the experiment; however, disintegrated internal organelles were observed in 7% of the cells examined (total 1502). After five days exposure to 32°C (t = 12 d), all of the remaining Symbiodinium cells exhibited both structurally compromised thylakoid membranes and widespread disintegration of organelles in the cytoplasm (Fig 3). While damage to internal structures was apparent, cell walls appeared intact and no fragmented symbiont cells were observed.

Bottom Line: The current consensus is that this phenomenon results from enhanced production of harmful reactive oxygen species (ROS) that disrupt the symbiosis between corals and their endosymbiotic dinoflagellates, Symbiodinium.The results show that the responses of the two antioxidant systems occur on different timescales: (i) the redox state of the Symbiodinium PQ pool remained stable until twelve days into the experiment, after which there was an abrupt oxidative shift; (ii) by contrast, an oxidative shift of approximately 10% had occurred in the host CoQ pool after 6 days of thermal stress, prior to significant changes in any other physiological parameter measured.Host CoQ pool oxidation is thus an early biomarker of thermal stress in corals, and this antioxidant pool is likely to play a key role in quenching thermally-induced ROS in the coral-algal symbiosis.

View Article: PubMed Central - PubMed

Affiliation: AIMS@JCU, James Cook University, Townsville, Queensland, Australia; Australian Institute of Marine Science, Townsville, Queensland, Australia; Comparative Genomics Centre and Department of Molecular and Cell Biology, James Cook University, Townsville, Queensland, Australia; ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland, Australia.

ABSTRACT
Bleaching episodes caused by increasing seawater temperatures may induce mass coral mortality and are regarded as one of the biggest threats to coral reef ecosystems worldwide. The current consensus is that this phenomenon results from enhanced production of harmful reactive oxygen species (ROS) that disrupt the symbiosis between corals and their endosymbiotic dinoflagellates, Symbiodinium. Here, the responses of two important antioxidant defence components, the host coenzyme Q (CoQ) and symbiont plastoquinone (PQ) pools, are investigated for the first time in colonies of the scleractinian coral, Acropora millepora, during experimentally-induced bleaching under ecologically relevant conditions. Liquid chromatography-mass spectrometry (LC-MS) was used to quantify the states of these two pools, together with physiological parameters assessing the general state of the symbiosis (including photosystem II photochemical efficiency, chlorophyll concentration and Symbiodinium cell densities). The results show that the responses of the two antioxidant systems occur on different timescales: (i) the redox state of the Symbiodinium PQ pool remained stable until twelve days into the experiment, after which there was an abrupt oxidative shift; (ii) by contrast, an oxidative shift of approximately 10% had occurred in the host CoQ pool after 6 days of thermal stress, prior to significant changes in any other physiological parameter measured. Host CoQ pool oxidation is thus an early biomarker of thermal stress in corals, and this antioxidant pool is likely to play a key role in quenching thermally-induced ROS in the coral-algal symbiosis. This study adds to a growing body of work that indicates host cellular responses may precede the bleaching process and symbiont dysfunction.

No MeSH data available.


Related in: MedlinePlus