The influence of seasonal and acute temperature changes on mitochondrial functions were studied in isolated mitochondria of the eurythermal lugworm

The lugworm Arenicola marina is one of the most successful species on intertidal mudflats and is highly adaptable to various abiotic stress factors in its changeable environment. This applies not only to oxygen partial pressure and salinity, but also to temperature, which varies greatly around the annual mean of 10°C in the North Sea. Thus, intertidal lugworm populations of the Wadden Sea can be exposed to short periods of ice cover in January and February, whereas in summer the sediment can warm to 20°C at the depths where the burrows are located. Lugworms from the North Sea intertidal flats start gamete production in late March, which leads to an elevated energy demand throughout the summer. Ripe gametes are ejected in a brief spawning event during the second half of September (Schöttler, 1989). The elevated energy demand for gamete production in both sexes leads to a vast increase of whole animal oxygen consumption during summer, until some weeks before the spawning. Pre-spawning oxygen demand is therefore elevated in excess of a rising demand due to the higher summer temperatures, and exacerbates susceptibility to anoxia. Warming exacerbates the formation of reactive oxygen species (ROS) in marine invertebrates (Abele et al., 1998a,b, 2001). These oxygen free radicals arise largely but not exclusively from the mitochondria (Abele et al., 2002; Heise et al., 2003), known as major ROS producers under pathophysiological conditions and in ageing animals (Sastre et al., 2000; St-Pierre et al., 2002). Additional ROS originate from several enzymatic oxidase reactions (for a review, see Storey, 1996). If stress-induced production of active oxygen species is not adequately counterbalanced by cellular antioxidants, mainly catalase, superoxide dismutase and the glutathione system, oxidative damage of lipids, proteins and nucleic acids ensues (Halliwell and Gutteridge, 1989; Lenaz, 1998; Duval et al., 2002). As important ROS producers, mitochondria are prone to become immediate targets for ROS-induced molecular damage. This leads to disturbance of mitochondrial energetic functioning in a primary assault (Yan et al., 1997; Brand, 2000), whereas slowly accumulating damage of the mitochondrial DNA causes mitochondrial degeneration and enhances the process of cellular ageing (Sastre et al., 2000; StPierre et al., 2002). Mitochondrial ROS production depends on the magnitude of membrane potential (∆Ψ) in isolated mitochondria (Korshunov et al., 1997; Brand, 2000), and not so much on the rate of electron transport. The ∆Ψ-threshold value for significant ROS production is just above state 3 ∆Ψ level (Korshunov et al., 1997) and, indeed, most investigations The Journal of Experimental Biology 207, 2529-2538 Published by The Company of Biologists 2004 doi:10.1242/jeb.01050