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Temperature-dependence of mitochondrial function and production of reactive oxygen species in the intertidal mud clam Mya arenaria

D. Abele^1,*, K. Heise¹, H. O. Pörtner¹ and S. Puntarulo²

¹ Alfred Wegener Institut for Polar and Marine Research, Columbusstraße, 27568 Bremerhaven, Germany
² Physical Chemistry, School of Pharmacy and Biochemistry, University of Buenos Aires, Buenos Aires, Argentina

View larger version (25K): [in a new window]   Fig. 1. Comparison of the respiratory coupling ratios (RCR) at different temperatures of isolated mantle mitochondria from Mya arenaria determined from the rates of state 3 and state 4 respiration (RCR 3/4; grey columns) and from the rates of state 3 respiration and respiration in the presence of oligomycin (RCR 3/4+; hatched columns); N=7-15. RCR 3/4, P=0.27 (Kruskal—Wallis ANOVA), RCR3/4+, P=0.12 (ANOVA). Values are means ± S.D.

View larger version (18K): [in a new window]   Fig. 2. Temperature-dependence of (A) the rate of state 3 respiration (diamonds) and the difference between the rates of state 3 and state 4+ respiration (circles) and (B) the rate of state 4 respiration (triangles) and state 4+ respiration (squares) of mantle mitochondria from Mya arenaria. ABT, Arrhenius break temperature. * indicates values that are significantly different from values at the lower temperature; N=8-18. *1 for state 3 and state 3 minus state 4+: P<0.01; *2 for state 3: P=0.023; *3 for state 4 and state 4+: P<0.01. (All ANOVA, ANCOVA; Newman—Keuls test.) Values are means ± S.D.

View larger version (8K): [in a new window]   Fig. 3. Dependence of ADP/O ratios of Mya arenaria mantle mitochondria on temperature; N=7-16; P<0.01 (ANOVA; Newman—Keuls test). a indicates values significantly different from the value at 5°C (means ± S.D.).

View larger version (22K): [in a new window]   Fig. 4. Temperature dependence of total reactive oxygen species (ROS) formation in Mya arenaria mantle mitochondria under state 3 conditions (grey columns) and under state 4+ conditions (hatched columns); N=6-7. Values are means ± S.D. State 3, P<0.01 (Kruskal—Wallis ANOVA); state 4+, P=0.062 (ANCOVA) and P=0.032 (Newman—Keuls test), ABT, Arrhenius break temperature. * indicates values significantly different from values at the 5°C lower experimental temperature in state 4+.

View larger version (28K): [in a new window]   Fig. 5. Temperature-dependence of percentage of total oxygen converted to hydrogen peroxide (% of O2 as H2O2) by Mya arenaria mantle mitochondria under state 3 conditions (grey columns) and under state 4+ conditions (hatched columns). N=5-7. Values are means ± S.D. state 3, P=0.16 (ANOVA), state 4+, P=0.72 (ANOVA). The line indicates a significant difference between state 3 and state 4+; P<0.01; N=107.

View larger version (43K): [in a new window]   Fig. 6. Malonedialdehyde (MDA) concentrations and AOX (catalase and superoxide dismutase, SOD) activities in Mya arenaria tissues after experimental warming of live animals. Experimental groups: t-1, stepwise warming to 18 °C; t-2, stepwise warming to 25 °C (1 °C per day), t-3, direct transfer from 10 to 25 °C (heat stress); c-1 to c-3, respective controls kept at constant 10 °C for the same time as the `temperature groups'. Measurements were taken at 20 °C (B,C) and at the respective maintenance temperature (incub-T) (D,E). (A) malonedialdehyde concentrations (MDA) in mantle tissue, (B,D) catalase mantle tissue, (C,E) SOD gill tissue. Data are means ± S.D. from 4-10 animals, *P<0.05, **P<0.01, values significantly different from controls.

View larger version (23K): [in a new window]   Fig. 7. Temperature profiles of antioxidant enzyme activities in Mya arenaria in vitro (units mg fresh mass). (A) Catalase in mantle tissues, (B) superoxide dismutase in gill tissues. Values are means ± S.D., N=5-8. **Values at 18 and 22 °C in B are significantly different from those at all other temperatures (P<0.01).

View larger version (133K): [in a new window]   Fig. 8. Confocal image of mitochondrial clustering in Mya arenaria mantle cells. Staining with MitoTracker green FM (Molecular Probes). Mitochondria (stained yellow) are located periferal and around the nucleus. Scale bar, 10 µm.