Effects of temperature and cadmium exposure on the mitochondria of oysters (Crassostrea virginica) exposed to hypoxia and subsequent reoxygenation

Abstract

SUMMARYIntertidal bivalves are commonly exposed to multiple stressors including periodic hypoxia, temperature fluctuations and pollution, which can strongly affect energy metabolism. We used top-down control and elasticity analyses to determine the interactive effects of intermittent hypoxia, cadmium (Cd) exposure and acute temperature stress on mitochondria of the eastern oyster Crassostrea virginica. Oysters were acclimated at 20°C for 30days in the absence or presence of 50gl -1 Cd and then subjected to a long-term hypoxia (6days at <0.5% O 2 in seawater) followed by normoxic recovery. Mitochondrial function was assessed at the acclimation temperature (20°C), or at elevated temperature (30°C) mimicking acute temperature stress in the intertidal zone. In the absence of Cd or temperature stress, mitochondria of oysters showed high resilience to transient hypoxia. In control oysters at 20°C, hypoxia/reoxygenation induced elevated flux capacity of all three studied mitochondrial subsystems (substrate oxidation, phosphorylation and proton leak) and resulted in a mild depolarization of resting mitochondria. Elevated proton conductance and enhanced capacity of phosphorylation and substrate oxidation subsystems may confer resistance to hypoxia/reoxygenation stress in oyster mitochondria by alleviating production of reactive oxygen species and maintaining high aerobic capacity and ATP synthesis rates during recovery. Exposure to environmental stressors such as Cd and elevated temperatures abolished the putative adaptive responses of the substrate oxidation and phosphorylation subsystems, and strongly enhanced proton leak in mitochondria of oysters subjected to hypoxia/reoxygenation stress. Our findings suggest that Cd exposure and acute temperature stress may lead to the loss of mitochondrial resistance to hypoxia and reoxygenation and thus potentially affect the ability of oysters to survive periodic oxygen deprivation in coastal and estuarine habitats.

Hypoxia-cadmium interactions on rainbow trout (Oncorhynchus mykiss) mitochondrial bioenergetics: attenuation of hypoxia-induced proton leak by low doses of cadmium

“…Although the cellular targets and toxic effects of Cd are numerous, the mitochondrion is arguably the most important target site of its toxic action. In this regard, extant literature indicates that several aspects of the three mitochondrial subsystems -phosphorylation, substrate oxidation and proton leak -are impacted by Cd (Kesseler and Brand, 1994;Belyaeva and Korotkov, 2003;Cannino et al, 2009;Kurochkin et al, 2011;Adiele et al, 2012;Ivanina et al, 2012).…”

Effects of intermittent hypoxia on oxidative stress and protein degradation in molluscan mitochondria

“…scallops) (Ivanina et al, 2016(Ivanina et al, , 2012Kurochkin et al, 2008). Clams show a notably greater mitochondrial tolerance to H/R stress compared with oysters and especially scallops, as indicated by their ability to upregulate the activity of the ETS and oxidative phosphorylation capacity during hypoxia and subsequent reoxygenation (Ivanina et al, 2016(Ivanina et al, , 2012Kurochkin et al, 2008).…”

“…scallops) (Ivanina et al, 2016(Ivanina et al, , 2012Kurochkin et al, 2008). Clams show a notably greater mitochondrial tolerance to H/R stress compared with oysters and especially scallops, as indicated by their ability to upregulate the activity of the ETS and oxidative phosphorylation capacity during hypoxia and subsequent reoxygenation (Ivanina et al, 2016(Ivanina et al, , 2012Kurochkin et al, 2008). Oysters also showed an upregulation of ETS activity during H/R stress (albeit to a lesser degree than clams), whereas in scallops, H/R stress led to a suppression of the ETS activity, collapse of the oxidative phosphorylation capacity, and a decrease in the mitochondrial membrane potential (Ivanina et al, 2016).…”

“…Highly tolerant hard clams that can survive for weeks in anoxic and sulfidic sediments (Altieri, 2008;Kraeuter and Castagna, 2001;Savage, 1976) show the highest levels of mitochondrial protection, indicated by the constitutively high activity of mitoproteases, strong anticipatory induction of antioxidants during anoxia and hypoxia and lack of accumulation of the oxidative lesions in mitochondria during intermittent hypoxia. Similarly, hypoxia-tolerant intertidal oysters that can survive several days to weeks without oxygen (Ivanina et al, 2010(Ivanina et al, , 2012VaquerSunyer and Duarte, 2008) achieve mitochondrial protection by upregulating mitochondrial antioxidants and/or mitoproteases during H/R or A/R stress. In scallops, suppression of ATPdependent protease activity during intermittent anoxia or hypoxia is associated with accumulation of oxidatively damaged proteins and is not alleviated by the high baseline activity of antioxidants.…”

“…However, some animals such as diving birds and mammals or intertidal invertebrates can undergo frequent H/R cycles without any apparent tissue damage. Recent studies showed that hypoxia-tolerant organisms (such as fish and mollusks) maintain mitochondrial integrity during H/R via rapid functional reorganization of mitochondria that upregulates activity of the electron transport system (ETS) and suppresses ATP wastage in hypoxia (Ivanina et al, 2016(Ivanina et al, , 2012Kurochkin et al, 2009). Mitochondrial tolerance to H/R stress in hypoxia-tolerant organisms also requires that the oxidative damage is prevented and/or repaired during the H/R cycles.…”