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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

Schematic diagram of electron transfer reactions using the coenzyme Q (CoQ) pool in the coral mitochondrial and plasma membrane electron transport.Respiratory “linear” electron flows (black arrows) proceed from NADH in the mitochondrial matrix to H2O via the CoQ pool and the enzyme complexes I, II, III, and IV, forming ubiquinol (CoQH2) as an intermediary product. The electron flows via complexes I, III and IV occur (mostly) via tunnelling or micro-diffusion of CoQ/CoQH2 in I-II-IV supercomplexes rather than via the larger mobile CoQ pool [72]. “Non-linear” electron flows (dark blue arrows) proceed from electron donors (e.g. NAD(P)H) via several quinone dehydrogenases to the CoQ pool, and to H2O from CoQH2 via AOX. Plasma membrane electron transport occurs from NAD(P)H to H2O via one or more type of NAD(P)H-CoQ reductases, the plasma membrane CoQ pool and Ecto-NOX. CoQH2 ROS scavenging occurs continuously in O2 metabolism primarily via chain breaking of lipid peroxidation (LPO) caused by O2•− and H2O2. Abbreviations: AOX, alternative oxidase; cyt-c, cytochrome c; DHAP, dihydroxyacetone phosphate; DHO, dihydroorotate; DHODH, dihydroorotate dehydrogenase; Ecto-NOX, external quinone oxidase; ETFred/ox, reduced/oxidised electron-transferring-flavoprotein; ETFDH, electron-transferring-flavoprotein dehydrogenase reduced/oxidised; Ecto-NOX, external quinone oxidase; GPDH, glycerol-3-phosphate dehydrogenase; G-3-P, glycerol-3-phosphate; H2O2, hydrogen peroxide; LPO, lipid peroxidation; pmNDH/mNDH, plasma membrane/mitochondrial NAD(P)H dehydrogenases; OA, orotate; O2•−, superoxide.
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pone.0139290.g004: Schematic diagram of electron transfer reactions using the coenzyme Q (CoQ) pool in the coral mitochondrial and plasma membrane electron transport.Respiratory “linear” electron flows (black arrows) proceed from NADH in the mitochondrial matrix to H2O via the CoQ pool and the enzyme complexes I, II, III, and IV, forming ubiquinol (CoQH2) as an intermediary product. The electron flows via complexes I, III and IV occur (mostly) via tunnelling or micro-diffusion of CoQ/CoQH2 in I-II-IV supercomplexes rather than via the larger mobile CoQ pool [72]. “Non-linear” electron flows (dark blue arrows) proceed from electron donors (e.g. NAD(P)H) via several quinone dehydrogenases to the CoQ pool, and to H2O from CoQH2 via AOX. Plasma membrane electron transport occurs from NAD(P)H to H2O via one or more type of NAD(P)H-CoQ reductases, the plasma membrane CoQ pool and Ecto-NOX. CoQH2 ROS scavenging occurs continuously in O2 metabolism primarily via chain breaking of lipid peroxidation (LPO) caused by O2•− and H2O2. Abbreviations: AOX, alternative oxidase; cyt-c, cytochrome c; DHAP, dihydroxyacetone phosphate; DHO, dihydroorotate; DHODH, dihydroorotate dehydrogenase; Ecto-NOX, external quinone oxidase; ETFred/ox, reduced/oxidised electron-transferring-flavoprotein; ETFDH, electron-transferring-flavoprotein dehydrogenase reduced/oxidised; Ecto-NOX, external quinone oxidase; GPDH, glycerol-3-phosphate dehydrogenase; G-3-P, glycerol-3-phosphate; H2O2, hydrogen peroxide; LPO, lipid peroxidation; pmNDH/mNDH, plasma membrane/mitochondrial NAD(P)H dehydrogenases; OA, orotate; O2•−, superoxide.

Mentions: CoQ/CoQH2 is present (in varying quantities) in all intracellular membranes of every animal with the highest concentrations found in the mitochondrial membranes at the primary site of ROS production [32, 70]. In eukaryotes, CoQ redox processes are relatively complex (Fig 4; for relevant enzymes identified in Acropora sp. see S1 Table). Within mitochondrial membranes, CoQH2 is continuously regenerated by the respiratory chain (complex I, II and alternative NAD(P)H dehydrogenases) [71] and other mitochondrial enzymes (glycerol-3-phosphate dehydrogenase, electron-transferring flavoprotein dehydrogenase, dihydroorotate dehydrogenase; [72]). In other membranes, several enzymes catalyse CoQ reduction including a NADH-cytochrome b5 reductase [73] and a distinct, unresolved NADPH-CoQ reductase [74]. Interestingly, a cytosolic NAD(P)H:quinone reductase (NQO1; formerly DT-diaphorase) [75]–the most studied CoQ reducing enzyme–appears to be absent in cnidarians along with other NQO genes [76].


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)

Schematic diagram of electron transfer reactions using the coenzyme Q (CoQ) pool in the coral mitochondrial and plasma membrane electron transport.Respiratory “linear” electron flows (black arrows) proceed from NADH in the mitochondrial matrix to H2O via the CoQ pool and the enzyme complexes I, II, III, and IV, forming ubiquinol (CoQH2) as an intermediary product. The electron flows via complexes I, III and IV occur (mostly) via tunnelling or micro-diffusion of CoQ/CoQH2 in I-II-IV supercomplexes rather than via the larger mobile CoQ pool [72]. “Non-linear” electron flows (dark blue arrows) proceed from electron donors (e.g. NAD(P)H) via several quinone dehydrogenases to the CoQ pool, and to H2O from CoQH2 via AOX. Plasma membrane electron transport occurs from NAD(P)H to H2O via one or more type of NAD(P)H-CoQ reductases, the plasma membrane CoQ pool and Ecto-NOX. CoQH2 ROS scavenging occurs continuously in O2 metabolism primarily via chain breaking of lipid peroxidation (LPO) caused by O2•− and H2O2. Abbreviations: AOX, alternative oxidase; cyt-c, cytochrome c; DHAP, dihydroxyacetone phosphate; DHO, dihydroorotate; DHODH, dihydroorotate dehydrogenase; Ecto-NOX, external quinone oxidase; ETFred/ox, reduced/oxidised electron-transferring-flavoprotein; ETFDH, electron-transferring-flavoprotein dehydrogenase reduced/oxidised; Ecto-NOX, external quinone oxidase; GPDH, glycerol-3-phosphate dehydrogenase; G-3-P, glycerol-3-phosphate; H2O2, hydrogen peroxide; LPO, lipid peroxidation; pmNDH/mNDH, plasma membrane/mitochondrial NAD(P)H dehydrogenases; OA, orotate; O2•−, superoxide.
© Copyright Policy
Related In: Results  -  Collection

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

pone.0139290.g004: Schematic diagram of electron transfer reactions using the coenzyme Q (CoQ) pool in the coral mitochondrial and plasma membrane electron transport.Respiratory “linear” electron flows (black arrows) proceed from NADH in the mitochondrial matrix to H2O via the CoQ pool and the enzyme complexes I, II, III, and IV, forming ubiquinol (CoQH2) as an intermediary product. The electron flows via complexes I, III and IV occur (mostly) via tunnelling or micro-diffusion of CoQ/CoQH2 in I-II-IV supercomplexes rather than via the larger mobile CoQ pool [72]. “Non-linear” electron flows (dark blue arrows) proceed from electron donors (e.g. NAD(P)H) via several quinone dehydrogenases to the CoQ pool, and to H2O from CoQH2 via AOX. Plasma membrane electron transport occurs from NAD(P)H to H2O via one or more type of NAD(P)H-CoQ reductases, the plasma membrane CoQ pool and Ecto-NOX. CoQH2 ROS scavenging occurs continuously in O2 metabolism primarily via chain breaking of lipid peroxidation (LPO) caused by O2•− and H2O2. Abbreviations: AOX, alternative oxidase; cyt-c, cytochrome c; DHAP, dihydroxyacetone phosphate; DHO, dihydroorotate; DHODH, dihydroorotate dehydrogenase; Ecto-NOX, external quinone oxidase; ETFred/ox, reduced/oxidised electron-transferring-flavoprotein; ETFDH, electron-transferring-flavoprotein dehydrogenase reduced/oxidised; Ecto-NOX, external quinone oxidase; GPDH, glycerol-3-phosphate dehydrogenase; G-3-P, glycerol-3-phosphate; H2O2, hydrogen peroxide; LPO, lipid peroxidation; pmNDH/mNDH, plasma membrane/mitochondrial NAD(P)H dehydrogenases; OA, orotate; O2•−, superoxide.
Mentions: CoQ/CoQH2 is present (in varying quantities) in all intracellular membranes of every animal with the highest concentrations found in the mitochondrial membranes at the primary site of ROS production [32, 70]. In eukaryotes, CoQ redox processes are relatively complex (Fig 4; for relevant enzymes identified in Acropora sp. see S1 Table). Within mitochondrial membranes, CoQH2 is continuously regenerated by the respiratory chain (complex I, II and alternative NAD(P)H dehydrogenases) [71] and other mitochondrial enzymes (glycerol-3-phosphate dehydrogenase, electron-transferring flavoprotein dehydrogenase, dihydroorotate dehydrogenase; [72]). In other membranes, several enzymes catalyse CoQ reduction including a NADH-cytochrome b5 reductase [73] and a distinct, unresolved NADPH-CoQ reductase [74]. Interestingly, a cytosolic NAD(P)H:quinone reductase (NQO1; formerly DT-diaphorase) [75]–the most studied CoQ reducing enzyme–appears to be absent in cnidarians along with other NQO genes [76].

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