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9. Intrinsic Mechanisms Underlying Hypoxia-Tolerant Mitochondrial Phenotype During Hypoxia-Reoxygenation Stress in a Marine Facultative Anaerobe, the Blue Mussel Mytilus edulis

Author

Sokolov, Eugene P., Adzigbli, Linda, Markert, Stephanie, Bundgaard, Amanda, Fago, Angela, Becher, Dörte, Hirschfeld, Claudia, and Sokolova, Inna M.

Subjects
mitochondria, supercomplexes, proteomics, posttranslational modification (PTM), oxidative stress, bioenergetics, bivalve, respiration
Abstract

Hypoxia is common in marine environments and a major stressor for marine organisms inhabiting benthic and intertidal zones. Several studies have explored the responses of these organisms to hypoxic stress at the whole organism level with a focus on energy metabolism and mitochondrial response, but the instrinsic mitochondrial responses that support the organelle’s function under hypoxia and reoxygenation (H/R) stress are not well understood. We studied the effects of acute H/R stress (10 min anoxia followed by 15 min reoxygenation) on mitochondrial respiration, production of reactive oxygen species (ROS) and posttranslational modifications (PTM) of the proteome in a marine facultative anaerobe, the blue mussel Mytilus edulis. The mussels’ mitochondria showed increased OXPHOS respiration and suppressed proton leak resulting in a higher coupling efficiency after H/R stress. ROS production decreased in both the resting (LEAK) and phosphorylating (OXPHOS) state indicating that M. edulis was able to prevent oxidative stress and mitochondrial damage during reoxygenation. Hypoxia did not lead to rearrangement of the mitochondrial supercomplexes but impacted the mitochondrial phosphoproteome including the proteins involved in OXPHOS, amino acid- and fatty acid catabolism, and protein quality control. This study indicates that mussels’ mitochondria possess intrinsic mechanisms (including regulation via reversible protein phosphorylation) that ensure high respiratory flux and mitigate oxidative damage during H/R stress and contribute to the hypoxia-tolerant mitochondrial phenotype of this metabolically plastic species.

Published
2021

15. Mitochondrial capacity and reactive oxygen species production during hypoxia and reoxygenation in the ocean quahog, Arctica islandica

Author

Steffen, Jennifer B. M., Haider, Fouzia, Sokolov, Eugene P., Bock, Christian, Sokolova, Inna M., Steffen, Jennifer B. M., Haider, Fouzia, Sokolov, Eugene P., Bock, Christian, and Sokolova, Inna M.

Abstract

Oxygen fluctuations are common in marine waters, and hypoxia– reoxygenation (H–R) stress can negatively affect mitochondrial metabolism. The long-lived ocean quahog, Arctica islandica, is known for its hypoxia tolerance associated with metabolic rate depression, yet the mechanisms that sustain mitochondrial function during oxygen fluctuations are not well understood. We used top-down metabolic control analysis (MCA) to determine aerobic capacity and control over oxygen flux in the mitochondria of quahogs exposed to short-term hypoxia (24 h <0.01% O2) and subsequent reoxygenation (1.5 h 21% O2) compared with normoxic control animals (21% O2). We demonstrated that flux capacity of the substrate oxidation and proton leak subsystems were not affected by hypoxia, while the capacity of the phosphorylation subsystem was enhanced during hypoxia associated with a depolarization of the mitochondrial membrane. Reoxygenation decreased the oxygen flux capacity of all three mitochondrial subsystems. Control over oxidative phosphorylation (OXPHOS) respiration was mostly exerted by substrate oxidation regardless of H–R stress, whereas control by the proton leak subsystem of LEAK respiration increased during hypoxia and returned to normoxic levels during reoxygenation. During hypoxia, reactive oxygen species (ROS) efflux was elevated in the LEAK state, whereas it was suppressed in the OXPHOS state. Mitochondrial ROS efflux returned to normoxic control levels during reoxygenation. Thus, mitochondria of A. islandica appear robust to hypoxia by maintaining stable substrate oxidation and upregulating phosphorylation capacity, but remain sensitive to reoxygenation. This mitochondrial phenotype might reflect adaptation of A. islandica to environments with unpredictable oxygen fluctuations and its behavioural preference for low oxygen levels.

Published
2021

26. Effects of mechanical disturbance and salinity stress on bioenergetics and burrowing behavior of the soft-shell clam Mya arenaria.

Author

Haider, Fouzia, Sokolova, Inna M., and Sokolov, Eugene P.

Subjects
CLAMS, FISH bioenergetics, ANIMAL burrowing, MYA arenaria, SALINITY, BIOTURBATION, PHYSIOLOGICAL stress, PHYSIOLOGY, ANIMAL behavior
Abstract

Bioturbation of sediments by burrowing organisms plays a key role in the functioning of coastal ecosystems. Burrowing is considered an energetically expensive activity, yet the energy costs of burrowing and the potential impacts of multiple stressors (such as salinity stress and wave action) on bioenergetics and burrowing performance of marine bioturbators are not well understood. We investigated the effects of mechanical disturbance and salinity stress on the burrowing behavior, aerobic capacity and energy expense of digging in a common marine bioturbator, the soft-shell clam Mya arenaria from the Baltic Sea (control salinity 15). Mya arenaria showed large individual variability in the burrowing efficiency, with an average of ~7% of the body energy reserves used per burial. Clams with higher mitochondrial capacity and lower energy expenditure per burial showed higher endurance. Acclimation for 3-4 weeks to low (5) or fluctuating (5-15) salinity reduced the burrowing speed and the number of times the clams can rebury but did not affect the mitochondrial capacity of the whole body or the gill. Acclimation to the fluctuating salinity shifted the predominant fuel use for burrowing from proteins to lipids. Our data indicate that the reduced burrowing performance of clams under the salinity stress is not due to the limitations of energy availability or aerobic capacity but must involve other mechanisms (such as impaired muscle performance). The reduction in the burrowing capacity of clams due to salinity stress may have important implications for survival, activity and ecological functions of the clams in shallow coastal ecosystems. [ABSTRACT FROM AUTHOR]

Published
2018
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36. Temperature-dependent effects of cadmium and purine nucleotides on mitochondrial aconites from a marine ectotherm, Crassostrea virginica: a role of temperature in oxidative stress and allosteric enzyme regulation.

Author

Cherkasov, Anton A., Overton Jr., Robert A., Sokolov, Eugene P., and Sokolova, Inna M.

Subjects
CADMIUM, TEMPERATURE, PURINE nucleotides, OXIDATIVE stress, COLD-blooded animals, BIVALVES
Abstract

Temperature and heavy metals such as cadmium (Cd) are important environmental stressors that can strongly affect mitochondrial function of marine poikilotherms. In this study, we investigated the combined effects of temperature (20°C and 30°C) and Cd stress on production of reactive oxygen species (ROS) and oxidative stress in a marine poikilotherm Crassostrea virginica (the eastern oyster) using mitochondrial aconitase as a sensitive biomarker of oxidative damage. We also assessed potential involvement of mitochondrial uncoupling proteins (UCPs) in antioxidant protection in oyster mitochondria using purine nucleotides (GDP, ATP and ADP) as specific inhibitors, and free fatty acids as stimulators, of UCPs. Our results show that exposure to Cd results in elevated ROS production and oxidative damage as indicated by aconitase inactivation which is particularly pronounced at elevated temperature. Unexpectedly, oyster mitochondrial aconitase was inhibited by physiologically relevant levels of ATP (IC50=1.93 and 3.04 mmol l-1 at 20°C and 30°C, respectively), suggesting that allosteric regulation of aconitase by this nucleotide may be involved in regulation of the tricarboxylic acid flux in oysters. Aconitase was less sensitive to ATP inhibition at 30°C than at 20°C, consistent with the elevated metabolic flux at higher temperatures. ADP and GDP also inhibited mitochondrial aconitase but at the levels well above the physiological concentrations of these nucleotides (6-11 mmol l-1). Our study shows expression of at least three UCP isoforms in C. virginica gill tissues but provides no indication that UCPs protect mitochondrial aconitase from oxidative inactivation in oysters. Overall, the results of this study indicate that temperature stress exaggerates toxicity of Cd leading to elevated oxidative stress in mitochondria, which may have important implications for survival of poikilotherms in polluted environments during seasonal warming and/or global climate change, and suggest a novel temperature-dependent mechanism of allosteric regulation of TCA flux in oyster mitochondria. [ABSTRACT FROM AUTHOR]

Published
2007
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38. Mitochondrial performance of a continually growing marine bivalve, Mytilus edulis, depends on body size

Author

Sukhotin, Alexey, Kovalev, Anton, Sokolov, Eugene, and Sokolova, Inna M.

Abstract

Allometric decline of mass-specific metabolic rate with increasing body size in organisms is a well-documented phenomenon. Despite a long history of research, the mechanistic causes of metabolic scaling with body size remain under debate. Some hypotheses suggest that intrinsic factors such as allometry of cellular and mitochondrial metabolism may contribute to the organismal-level metabolic scaling. The aim of our present study was to determine the metabolic allometry at the mitochondrial level using a continually growing marine ectotherm, the mussel Mytilus edulis, as a model. Mussels from a single cohort that considerably differed in body size were selected, implying faster growth in the larger specimens. We determined the body mass-dependent scaling of the mitochondrial proton leak respiration, respiration in the presence of ADP indicative of the oxidative phosphorylation (OXPHOS), and maximum activity of the mitochondrial electron transport system (ETS) and cytochrome coxidase (COX). Respiration was measured at normal (15°C), and elevated (27°C) temperatures. The results demonstrated a pronounced allometric increase in both proton leak respiration and OXPHOS activity of mussel mitochondria. Mussels with faster growth (larger body size) showed an increase in OXPHOS rate, proton leak respiration rate, and ETS and COX activity (indicating an overall improved mitochondrial performance) and higher respiratory control ratio (indicating better mitochondrial coupling and potentially lower costs of mitochondrial maintenance at the same OXPHOS capacity) compared with slower growing (smaller) individuals. Our data show that the metabolic allometry at the organismal level cannot be directly explained by mitochondrial functioning.

Published
2020
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