Abstract
The mitochondrial alternative oxidase, AOX, present in most eukaryotes apart from vertebrates and insects, catalyzes the direct oxidation of ubiquinol by oxygen, by‐passing the terminal proton‐motive steps of the respiratory chain. Its physiological role is not fully understood, but it is proposed to buffer stresses in the respiratory chain similar to those encountered in mitochondrial diseases in humans. Previously, we found that the ubiquitous expression of AOX from Ciona intestinalis in Drosophila perturbs the development of flies cultured under low‐nutrient conditions (media containing only glucose and yeast). Here we tested the effects of a wide range of nutritional supplements on Drosophila development, to gain insight into the physiological mechanism underlying this developmental failure. On low‐nutrient medium, larvae contained decreased amounts of triglycerides, lactate, and pyruvate, irrespective of AOX expression. Complex food supplements, including treacle (molasses), restored normal development to AOX‐expressing flies, but many individual additives did not. Inhibition of AOX by treacle extract was excluded as a mechanism, since the supplement did not alter the enzymatic activity of AOX in vitro. Furthermore, antibiotics did not influence the organismal phenotype, indicating that commensal microbes were not involved. Fractionation of treacle identified a water‐soluble fraction with low solubility in ethanol, rich in lactate and tricarboxylic acid cycle intermediates, which contained the critical activity. We propose that the partial activation of AOX during metamorphosis impairs the efficient use of stored metabolites, resulting in developmental failure.
Highlights
Animals have evolved a wide variety of physiological mechanisms to tailor their development and feeding behavior to the nature and availability of food resources
In an earlier series of experiments, we found that flies expressing the alternative oxidase AOX from the tunicate Ciona intestinalis failed to complete development when reared on a low‐nutrient agar medium containing only yeast and glucose (Saari et al, 2018)
Since activated AOX is known to facilitate tricarboxylic acid (TCA) cycle reactions and decrease reactive oxygen species (ROS) production, and to result in less adenosine triphosphate (ATP) synthesis, developmental failure could result from multiple, nonexclusive causes
Summary
Animals have evolved a wide variety of physiological mechanisms to tailor their development and feeding behavior to the nature and availability of food resources. Since activated AOX is known to facilitate TCA cycle reactions and decrease ROS production, and to result in less ATP synthesis, developmental failure could result from multiple, nonexclusive causes This might explain why the addition of either glucose or yeast to the low‐nutrient medium failed to improve the developmental outcome for AOX‐expressing flies. We found that L3 (wandering‐ stage) larvae reared on the low‐nutrient medium are deficient in specific stored nutrients, regardless of genotype Together, these results imply that AOX‐expressing flies are unable to make proper use of this depleted metabolic store, so as to complete development. We identified a specific set of metabolites as the most likely candidates to rectify this deficiency, enabling AOX‐expressing flies to fully undergo metamorphosis
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More From: Journal of Experimental Zoology Part A: Ecological and Integrative Physiology
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