Effects of acclimation temperature and cadmium exposure on cellular energy budgets in the marine molluskCrassostrea virginica: linking cellular and mitochondrial responses

Abstract

SUMMARY In order to understand the role of metabolic regulation in environmental stress tolerance, a comprehensive analysis of demand-side effects (i.e. changes in energy demands for basal maintenance) and supply-side effects (i.e. metabolic capacity to provide ATP to cover the energy demand) of environmental stressors is required. We have studied the effects of temperature (12, 20 and 28°C) and exposure to a trace metal, cadmium (50 μg l–1), on the cellular energy budget of a model marine poikilotherm, Crassostrea virginica (eastern oysters), using oxygen demand for ATP turnover, protein synthesis, mitochondrial proton leak and non-mitochondrial respiration in isolated gill and hepatopancreas cells as demand-side endpoints and mitochondrial oxidation capacity, abundance and fractional volume as supply-side endpoints. Cadmium exposure and high acclimation temperatures resulted in a strong increase of oxygen demand in gill and hepatopancreas cells of oysters. Cd-induced increases in cellular energy demand were significant at 12 and 20°C but not at 28°C,possibly indicating a metabolic capacity limitation at the highest temperature. Elevated cellular demand in cells from Cd-exposed oysters was associated with a 2–6-fold increase in protein synthesis and, at cold acclimation temperatures, with a 1.5-fold elevated mitochondrial proton leak. Cellular aerobic capacity, as indicated by mitochondrial oxidation capacity,abundance and volume, did not increase in parallel to compensate for the elevated energy demand. Mitochondrial oxidation capacity was reduced in 28°C-acclimated oysters, and mitochondrial abundance decreased in Cd-exposed oysters, with a stronger decrease (by 20–24%) in warm-acclimated oysters compared with cold-acclimated ones (by 8–13%). These data provide a mechanistic basis for synergism between temperature and cadmium stress on metabolism of marine poikilotherms. Exposure to combined temperature and cadmium stress may result in a strong energy deficiency due to the elevated energy demand on one hand and a reduced mitochondrial capacity to cover this demand on the other hand, which may have important implications for surviving seasonally and/or globally elevated temperatures in polluted estuaries.

Interactive effects of metal pollution and temperature on metabolism in aquatic ectotherms: implications of global climate change

“…Within the thermal tolerance range, a rise in temperature results in a proportional increase in different aspects of the standard metabolic rate, including costs of protein synthesis, ATP turnover, mitochondrial proton leak and nonmitochondrial respiration (Cherkasov et al 2006a). Beyond the tolerance range at the pejus and upper critical temperatures, some cellular maintenance costs (especially costs of mitochondrial maintenance due to the proton leak) may increase disproportionately at the expense of other cellular functions (Pörtner 2001).…”

“…the amount of metabolic energy required for the basal maintenance and survival of the individual) (Sibly & Calow 1989, Calow & Forbes 1998; however, unlike temperature, metal exposures typically lead to a disproportionate increase in the aspects of cell metabolism responsible for cellular detoxification and repair (Sibly & Calow 1989, Calow & Forbes 1998, Cherkasov et al 2006a, Ivanina et al 2008a). Our studies showed that both protein synthesis rate and oxygen consumption required to cover the costs of protein synthesis increased in eastern oysters Crassostrea virginica exposed to Cd (Cherkasov et al 2006a, Ivanina et al 2008a). An increase in the cellular protein synthesis in metal-exposed oysters was associated with an elevated expression of cellular protection proteins, such as metallothioneins, P-glycoproteins and heat shock proteins (Ivanina & Sokolova 2008, Ivanina et al 2008a.…”

“…Metallothionein synthesis may account for up to 5% of the total metabolic rate in metal-challenged organisms (Barber et al 1990). Given that total protein synthesis typically accounts for 10 to 20% of the standard metabolic rate (Hand & Hardewig 1996, Cherkasov et al 2006a, metallothionein and HSP synthesis may represent a significant additional cost to the organism, diverting energy from essential functions such as growth, reproduction and immunity toward metal detoxification and damage repair.…”

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

“…Elevated temperature led to an increase in mitochondrial respiration and the flux through the three studied mitochondrial subsystems in oysters, as is typical for ectotherm mitochondria (Abele et al, 2002;Blier and Guderley, 1993;Chamberlin, 2004b;Cherkasov et al, 2006a;Sokolova, 2004).…”

“…This suggests that in addition to the direct effects of Cd present in the cytosol and mitochondria, there are also slight but persistent shifts in the properties of oyster mitochondria induced by long-term Cd exposure that can contribute to the disturbance of energy metabolism in Cd-exposed oysters (Cherkasov et al, 2006a;Sokolova et al, 2004;Sokolova et al, 2005b). The molecular mechanisms of these shifts are currently unknown but may involve ROS-induced damage to mitochondrial enzymes due to the prooxidant effects of Cd (Cherkasov et al, 2007a;Valko et al, 2005;Wang et al, 2004).…”