Coenzyme Q and plastoquinone pool redox states in the coral-Symbiodinium symbiosis

Lutz, Adrian (2013) Coenzyme Q and plastoquinone pool redox states in the coral-Symbiodinium symbiosis. PhD thesis, James Cook University.

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Abstract

Widespread mass coral bleaching events have been consistently linked to higher than usual summer temperatures, caused by global climate change, in combination with high solar irradiance. Although the cellular aetiology leading to the loss of Symbiodinium cells via exocytosis and apoptosis is still debated, coral bleaching caused by thermal and irradiance stress is generally attributed to oxidative damage resulting from the excessive formation of reactive oxygen species (ROS). The production of ROS is tightly linked to the electron transport chains (ETC) of photosynthesis and respiration and the performance of the coral and Symbiodinium antioxidant defences. Two antioxidant defence components directly linked to the ETCs are the pools of the prenylquinones coenzyme Q (CoQ; ubiquinone) and plastoquinone (PQ) and their respective reduced (antioxidant) forms ubiquinol (CoQH2) and plastoquinol (PQH2). The pools of these redox carriers play indispensable roles in electron transport – CoQ/CoQH2 in the mitochondrial ETC and PQ/PQH2 in the photosynthetic ETC – and also have an important antioxidant function within mitochondrial, cellular and thylakoid membranes. Consequently, shifts in the proportion of reduced to oxidised prenylquinones (the CoQ and PQ pool redox states) have been used to infer oxidative stress and antioxidant activity in vertebrates and higher plants. Little is known about the sizes or redox states of these pools of prenylquinones in the coral-Symbiodinium symbiosis, as neither have so far been directly measured.

Taking advantage of the high sensitivity and specificity of liquid chromatography-mass spectrometry (LC-MS) quantification, I assessed the roles that these prenylquinone pools play in antioxidant defence of coral and Symbiodinium. I discuss shifts of the CoQ and PQ pool redox states in response to irradiance, heat and cold stress and in the context of the coral bleaching stress response. First, I developed a novel technique for reliable and accurate quantification of CoQ/CoQH2 in the coral host and PQ/PQH2 in Symbiodinium, enabling analysis of the CoQ and PQ pool redox states in symbio without the need for separation of the two symbiosis partners. This technique enabled the first study of diurnal variation in coral CoQ and symbiont PQ pool redox states in the coral Acropora millepora (Ehrenberg, 1834). Subsequently, the CoQ and PQ pool redox states were monitored in A. millepora during a 17-day heat stress experiment during which a coral bleaching response was induced. Finally, the CoQ and PQ pool redox states were monitored during both natural and experimentally induced cold bleaching events in the intertidal coral Acropora aspera (Dana, 1846).

I found that in A. millepora both the CoQ pool in the coral and the PQ pool in Symbiodinium are continuously maintained in a highly reduced state at a level comparable to vertebrates and higher plants, implying that these prenylquinone pools have antioxidant functions in coral and Symbiodinium. Furthermore, while the CoQ pool in the coral host was unaffected by daily exposure to high light intensities, the PQ pool exhibited significant oxidative shifts in response to midday solar irradiation maxima. Symbiodinium from A. millepora contained a proportionally large non-photoactive PQ pool (> 90 % of total pool size), which likely represents an acclimatory response to the high light environment of the host coral and provides further evidence for a significant antioxidant scavenging activity of the PQ pool.

Quantification of the CoQ and PQ pool responses to heat stress in A. millepora demonstrated that the CoQ pool was significantly oxidised prior to both measurable loss of Symbiodinium cells from the host and prior to major photoinhibition of photosystem II (PSII). The PQ pool redox state, on the other hand, remained unaffected by hyperthermal stress until PSII photochemical efficiency was severely impaired at the end of the experiment. In contrast to the effect of elevated temperatures and high irradiance in A. millepora, low temperature was associated with an increase in the PQ redox state in Symbiodinium hosted by A. aspera. Chlorophyll fluorescence induction kinetics supported the hypothesis that increases in PQH2 are linked to over-reduction of the photosynthetic electron transport chain. These observations are consistent with models for cold stress in higher plants and macro-algae which predict over-reduction of the photosynthetic ETC and the PQ pool. Acute cold stress did not significantly affect the redox state of the coral host CoQ pool, suggesting that, at least during acute exposure, low temperatures cause only limited oxidative stress within the coral host.

Taken together my results clearly imply that, as in some other eukaryotes, the CoQ and PQ pools have important functions in antioxidant defence in coral and Symbiodinium, and the redox states of these prenylquinone pools are significantly shifted in response to environmental insults that are associated with oxidative damage such as irradiance, heat and cold stress. Most importantly, my results provide the necessary baselines for future comparison of CoQ and PQ pool redox states in response to different stressors and among different coral species and Symbiodinium types.

Item ID: 31441
Item Type: Thesis (PhD)
Keywords: prenylquinones; coenzyme Q; plastoquinone; Symbiodinium cell loss; Acropora millepora; Acropera aspera; antioxidant defence; redox states; coral Symbiodinium symbiosis; response to stressors
Date Deposited: 27 Feb 2014 01:08
FoR Codes: 06 BIOLOGICAL SCIENCES > 0606 Physiology > 060602 Animal Physiology - Cell @ 33%
06 BIOLOGICAL SCIENCES > 0606 Physiology > 060601 Animal Physiology - Biophysics @ 34%
06 BIOLOGICAL SCIENCES > 0608 Zoology > 060808 Invertebrate Biology @ 33%
SEO Codes: 97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 100%
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