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First published online June 7, 2004
Journal of Experimental Biology 207, 2529-2538 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.01050

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Seasonality of energetic functioning and production of reactive oxygen species by lugworm (Arenicola marina) mitochondria exposed to acute temperature changes

Martina Keller¹, Angela Maria Sommer², Hans O. Pörtner¹ and Doris Abele^1,*

¹ Alfred Wegener Institute for Polar and Marine Research, Columbusstrasse 27568 Bremerhaven, Germany
² International University Bremen, Campus Ring 1, 28759 Bremen, Germany

View larger version (17K): [in a new window]   Fig. 1. Measurement of mitochondrial ROS production using homovanillic acid (HVA) as fluorophore in a peroxidase-catalysed reaction. Data interval, 0.02·min. M, start of measurement by addition of mitochondrial isolate to the buffer solution; 1, basal fluorescence of HVA suspension; HRP, addition of horseradish peroxidase; S, sodium succinate addition induces state 2; ADP addition induces state 3; `break' indicates the change of slope caused by the transition to state 4 after complete phosphorylation of ADP; O, oligomycin addition starts state 4+; dotted arrow, calibration with H2O2.

View larger version (15K): [in a new window]   Fig. 2. Temperature dependence of mitochondrial respiration in body wall tissue of Arenicola marina winter (A) and pre-spawning summer (B) animals. Data are means ± S.D.; N=5–10 isolations. Black bars, 10°C; hatched bars, 1°C. All 10°C values differ significantly from the values at 1°C (P<0.001); *All 1°C values are significantly different from the 10°C measurement in summer animals (P<0.001); significantly different from summer animals at the same experimental temperature and in the same respiratory state (P<0.014) (ANOVA; Newman–Keuls test).

View larger version (19K): [in a new window]   Fig. 3. Temperature dependence of mitochondrial H2O2 formation in body wall tissue of Arenicola marina winter (A) and summer (B) animals. Data are means ± S.D. of 5–10 mitochondrial isolations. Black bars, 10°C; hatched bars, 1°C. State 3 values were significantly lower in winter than in summer mitochondria at both temperatures; H2O2 formation at 10°C differs significantly from formation at 1°C (P<0.001), except of the 10°C value of the winter animals. State 4 and 4+ values at both temperatures differ significantly from state 3 (P<0.01) and with season (P<0.001), as well as between temperatures (P<0.01). (ANOVA; Newman–Keuls test).

View larger version (13K): [in a new window]   Fig. 4. Correlation between respiration rates in states 3 and 4+ and the membrane potential in states 3 and 4+ of body wall tissue mitochondria of Arenicola marina (data from winter and summer animals at 1 and 10°C), N=7–10; (ANOVA; Pearson correlation). Regression equations: MP (for state 3) vs O2: f(x)=0.35x–18.38 (r2=0.83, P<0.005, N=7); MP (for state 4+) vs O2: f(x)=0.09x–9.73 (r2=0.71, P<0.001, N=10), where MP = membrane potential and O2 = rate of oxygen production.

View larger version (17K): [in a new window]   Fig. 5. H2O2 formation vs membrane potential in state 4+ respiration in mitochondrial isolates from A. marina winter (white triangles) and summer (black triangles) animals. Data are means ± S.D. from 1–3 isolations per point assayed at 10°C.

View larger version (18K): [in a new window]   Fig. 6. Seasonal development of oxygen consumption of A. marina whole animals (solid line) and gametes (dotted line) adapted from Schöttler (1989). Bars depict oxygen consumption of mitochondrial isolated from winter and summer animals collected from the German Wadden Sea (dark bars) in this study and (light bars) by Sommer and Pörtner (2004). Scaling of the data is the same for all mitochondrial isolates (nmol O mg min-1 protein-1), but distinct (µmol O2 h-1 g-1 fresh mass) for whole animal oxygen consumption (solid line) and coelomic fluid (gamete oxygen consumption, dotted line; after Schöttler, 1989) (µmol O2 h-1 g fresh mass-1).

View larger version (15K): [in a new window]   Fig. 7. State 4+ respiration vs membrane potential in state 4+ in mitochondrial isolates from A. marina winter (white triangles) and summer animals (black triangles). Data are means ± S.D. from 1–3 isolations per point assayed at 10°C. Circles are data from Brookes et al. (1998) for Xenopus toad and rainbow trout.