Mitochondria in actively swimming ectotherms ROS consumers instead of producers?

dabele [ at ]


Antarctic marine ectotherms look back on several million years of adaptation to constant extreme cold temperatures. Most endemic species are cold stenothermal, with low and not thermally compensated metabolic rates, low scope for activity and narrow windows of thermal tolerance. Critical warming of the environment causes an exponential acceleration of mitochondrial oxygen demand in ectotherms and as many of them, especially small aquatic invertebrates, rely considerably (up to 50 %) on oxygen surface diffusion, the metabolic stress response to heat will increase surface oxygen flux to tissues. Elevated tissue oxygen flux under heat stress or during and after exhaustive exercise causes a necessity to buffer the tissue redox potential, because of an elevated probability of reactive oxygen species (ROS) formation. Basic ROS-buffering is achieved by the glutathione system and a significantly more oxidized glutathione redox ratio is found in marine ectotherms, when compared to higher organisms. The ratio of reduced to oxidized glutathione which is conserved at 10 : 1 in mammalian tissues comes down to 4 : 1 in fish and can be even more oxidized in marine bivalves, possibly in line with the decrement in oxygen consumption. Moreover, a pronounced necessity for oxygen redox buffering obviously characterizes polar animals, their tissues being equipped with double to 4-fold glutathione concentrations, compared to con-generic temperate water species.Mitochondria have been described as the major cellular ROS producers, especially under physiological stress. While we were able to detect a net production of ROS in mitochondria isolated from metabolically low tuned infaunal marine bivalves and worms, ROS release from mitochondria that we isolated from more active or higher evolved epibenthic animals, scallops and benthic fish, was null under all experimental conditions. It is conceivable that these mitochondria prevent ROS release into the cells, due to considerable antioxidant potential of the matrix. Higher mitochondrial volume densities and subsarcolemnal localization found in many polar species, may not only decrease diffusion distances of oxygen inside the cells but help to control the local dioxygen concentration and even mop up extra-mitochondrially produced ROS, rendering them innoxious and preventing initiation of lipid radical chain reactions.The question arises, whether especially in these more highly evolved epibenthic marine ectotherms, mitochondria may function as an extension of the basal antioxidant system (glutathione and antioxidant enzymes). A control of extra-mitochondrial ROS levels could be important to enable onset of stress signalling. In animals, many forms of stress converge into a state of functional hypoxia and ischemia. The physiological response is triggered as po2 dependent ROS formation by cytosolic NADPH-dependent oxidases ceases, enabling the stabilization of the hypoxia inducible transcription factor (HIF). We found first evidence that HIF may be involved in metabolic re-organisation during heat and cold stress in polar and North Sea fish. Higher oxygen flux under heat stress increases the probability of ROS formation and might hamper HIF stabilization. The enzymatic ROS quenching defence system of Antarctic ectotherms is optimised to function at low temperatures within the thermal envelope of the animals. Our hypothesis is that mitochondrial ROS quenching activity might substitute fading enzymatic antioxidant activity under heat stress and support HIF-induced metabolic re-organization (= hypoxic ventilatory slow down, HIF-related, erythropoesis & expression and activation of anaerobic enzymes and transporters).

Item Type
Conference (Invited talk)
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Event Details
Invited Introductory lecture, 12th Biennial Meeting of the Society for Free Radical Research, SFRR 2004, Buenos Aires, Argentina..
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Abele, D. (2004): Mitochondria in actively swimming ectotherms ROS consumers instead of producers? , Invited Introductory lecture, 12th Biennial Meeting of the Society for Free Radical Research, SFRR 2004, Buenos Aires, Argentina. .

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