Cadmium effects on mitochondrial function are enhanced by elevated temperatures in a marine poikilotherm,Crassostrea virginicaGmelin(Bivalvia: Ostreidae)

Abstract

SUMMARY Marine intertidal mollusks, such as oysters, are exposed to multiple stressors in estuaries, including varying environmental temperature and levels of trace metals, which may interactively affect their physiology. In order to understand the combined effects of cadmium and elevated temperature on mitochondrial bioenergetics of marine mollusks, respiration rates and mitochondrial volume changes were studied in response to different cadmium levels (0–1000 μmol l–1) and temperatures (15, 25 and 35°C) in isolated mitochondria from the eastern oyster Crassostrea virginica acclimated at 15°C. It was found that both cadmium and temperature significantly affect mitochondrial function in oysters. Elevated temperature had a rate-enhancing effect on state 3 (ADP-stimulated) and states 4 and 4+ (representative of proton leak) respiration, and the rate of temperature-dependent increase was higher for states 4 and 4+ than for state 3 respiration. Exposure of oyster mitochondria to 35°C resulted in a decreased respiratory control and phosphorylation efficiency (P/O ratio)compared to that of the acclimation temperature (15°C), while an intermediate temperature (25°C) had no effect. Cadmium exposure did not lead to a significant volume change in oyster mitochondria in vitro. Low levels of cadmium (1–5 μmol l–1) stimulated the rate of proton leak in oyster mitochondria, while not affecting ADP-stimulated state 3 respiration. In contrast, higher cadmium levels (10–50 μmol l–1) had little or no effect on proton leak, but significantly inhibited state 3 respiration by 40–80% of the control rates. Elevated temperature increased sensitivity of oyster mitochondria to cadmium leading to an early inhibition of ADP-stimulated respiration and an onset of complete mitochondrial uncoupling at progressively lower cadmium concentrations with increasing temperature. Enhancement of cadmium effects by elevated temperatures suggests that oyster populations subjected to elevated temperatures due to seasonal warming or global climate change may become more susceptible to trace metal pollution, and vice versa.

Top-down control analysis of the cadmium effects on molluscan mitochondria and the mechanisms of cadmium-induced mitochondrial dysfunction

“…Mitochondria were isolated from oyster gills using a method modified from Sokolova (65). Gills are an appropriate tissue for studying the effects of Cd stress because they represent the major sites of metal uptake and are among the first tissues to encounter environmental fluctuations in Cd levels (68).…”

“…Mitochondrial respiration and membrane potential were measured simultaneously in a water-jacketed, temperature-stabilized four-port chamber (World Precision Instruments, Sarasota, FL) in the presence or absence of Cd (34 M total Cd added as CdCl2 or 12.5 M free Cd 2ϩ ; see below) and in the presence or absence of a mitochondrially targeted ROS scavenger, MitoVitE (10 M). We used 12.5 M free Cd, which is within the range of the intracellular Cd levels found in Cd-exposed oysters (65,68, and references therein) and is similar to experimental Cd concentrations used in earlier studies (18,19,65).…”

“…Because of the central role of mitochondria in critical cellular processes such as bioenergetics, redox signaling, and cell death, Cdinduced mitochondrial damage has long-ranging consequences for cellular function, energy homeostasis, and whole-organism performance and survival. Previous studies have shown that Cd suppresses respiration and leads to the partial uncoupling, as well as elevated rates of reactive oxygen species (ROS) production in animal and plant mitochondria (11,13,14,18,23,35,65, and references therein). Several mechanisms have been proposed to explain effects of Cd on mitochondrial bioenergetics, including inhibition of electron transport chain (ETC), oxidative damage to mitochondrial enzymes and opening of the mitochondrial permeability pore (1,23,52,73).…”

Alteration of mitochondrial efficiency affects oxidative balance, development and growth in frog (Rana temporaria) tadpoles

“…In this sense, the plasticity of mitochondrial energy transduction efficiency strongly varies in a phylogenetic manner and in response to environmental factors, such as season, diet and temperature (Heise et al, 2003;Sokolova, 2004;Sommer and Portner, 2004;Brand, 2005;Emel'Yanova et al, 2007;Robert and Bronikowski, 2010). However, according to the above-mentioned theory of limited resources, evolutionary force should have optimized the ATP/O ratio toward better efficiency of the mitochondrial energy transduction system in order to maximize individual fitness.…”

Tolerancia a la anoxia y defensas antioxidantes en el mejillon verde Perna viridis (Linneus, 1758) bajo exposicion aguda al cadmio

“…Tales niveles de Cd presentes en mejillones y en su entorno crean expectativas sobre las estrategias bioquímicas de defensa en organismos contaminados, en especial en su adaptación a sobrevivir a la anoxia. Distintos estudios han considerado que el Cd puede provocar daños a nivel molecular en los organismos marinos en bajas concentraciones, conllevando a alteraciones en el trasporte a través de las membranas biológicas (Dailianis & Kaloyianni, 2004), actividad enzimática (Canesi et al, 1998;Nusetti et al, 2010), producción energética (Sokolova, 2004) y daños oxidativos (Prakash & Jagannatha-Roa, 1995;Rajkumar & Milton, 2011).…”